*Click Here* and Character List will appear to your left.

Below I discuss briefly major characters in the order in which they will be encountered when mentioned at the branching points of the phylogeny and in family characterizations. The emphasis in this section is on providing entries both to the general morphological literature, but especially to articles where there is much information on variation of a single character; I sometimes also give an indication of how good the sampling is. Definitions of the characters mentioned here and of related features are provided in the Glossary. Note, however, that these characters and the "states" I use in describing the variation within them should not simply be converted into data for phylogenetic analysis. Some, for example, fruit types, are logically connected with the nature of the gynoecium, others, such as fruit types themselves, seedling morphology, pollen, testa and tegmen types, might each yield a dozen or dozens of more or less individually varying characters. Furthermore, in these and many other characters the states we talk about may well be arbitrarily delimited. This does not necessarily mean that they are useless, but it does mean that they do not necessarily refer to anything "real" in the world. It should also be remembered that because the same term is used for features of two plants, it cannot be assumed that this entails a hypothesis that the structures in the two organisms had a common evolutionary origin, i. e., that they are homologous under one definition of the term. However, if botanical terms were reformulated so as to refer only to synapomorphies (shared derived features), changes in the terms we use would be almost innumerable and botanical discourse would become nigh on impossible. Although an indication of how useful a character is systematically - i.e., how much it varies, and its general pattern of variation - is sometimes given, it will soon become clear that in general, even if a feature is an apomorphy for a clade in one part of the tree, it will vary elsewhere (e.g. Stebbins 1951). Finally, it should be remembered that ecological and systematic definitions of characters of flowers, fruits and seeds in particular may be at odds; the definitions and circumscriptions adopted will depend on the purpose of the study. See also the Plant Ontology Consortium.

There are of course many other features mentioned in individual family characterisations. For these, general distributions may be unknown or not really of much interest because the feature is varying in a phylogenetically informative fashion only locally, although I try to provide context for mention of features where necessary.

I cannot emphasize enough the value of much older literature, especially that from ca 1870-1920. There one can find surveys of various aspects of plant anatomy and morphology for individual characters or for plant groups that have never been improved since, and I mention such work frequently. Of course, not all of this literature is helpful - it can be difficult to understand, one has to be careful about the names used, etc. - but in all too many cases it still provides most of the information we have. Work in which the evolution of individual organs or organ systems are discussed outside any immediate phylogenetic context, but rather from the point of view of particular a priori theories of plant morphology, are much less easy to use. Kaplan (2001) concisely summarized the different approaches of the great practitioners in the far from monolithic German tradition; the meticulous and comprehensive surveys of various aspects of plant form by Hofmeister (e.g. 1851), von Goebel (e.g. 1932), Troll (e.g. 1969, 1971) and the like have never been equalled - and in the four volumes of Kaplan (1997) much of this and subsequent literature is synthesized (see also Kaplan 2001). The task is to put their findings in a phylogenetic context... I have also necessarily relied much on the secondary literature, for instance, there is much information in Engler (1900-onwards) and Engler and Prantl (1887-1915; Ed. 2, 1924-onwards - cited under individual authors), Airy Shaw (1966), Hutchinson (1973), Cronquist (1981), Goldberg (1986, see also 2003), Mabberley (2007), Takhtajan (1997: beware of typographical errors!, 2009), and N. Smith et al. (2004). The meticulously-documented series of papers that make up the Generic Flora of the Southeastern United States (ed. C. E. Wood Jr.) and of course the monumental series of volumes edited by Kubitzki and others (1993a onwards) have been invaluable; contributions to these two endeavours are cited individually. Much information is summarized in Rolf Dahlgren's diagrams (e.g. Dahlgren 1975a) and is included in recent large-scale phylogenies (e.g. Hufford 1992: Rosidae; Nandi et al. 1998: all flowering plants). Zomlefer (1994) was helpful, especially early on. Information on many characters mentioned below is taken from these references and also from the general references mentioned at the beginning of each character group; this is definitely not the best method of documentation (see Introduction).


Plant architecture. Hallé et al. (1978) list a number of architectural models, growth patterns based on variation in a number of growth characters and to which plants may be assigned (see also Hallé 2004; Millet 2012; esp. Bell & Bryan 2008). These are rarely mentioned here except in passing since they are not often constant in taxa of any size and the general approach is typological; a large number of "models" could be named if the variation discussed by Hallé et al. (1978) were applied consistently. However, the individual characters that Hallé et al. (1978) discuss, e.g., ortho- and plagiotropy (the latter in particular comes in various flavours), continuous and discontinuous (rythmic) and monopodial and sympodial growth, are mentioned below. Thinking of plant growth in terms of these variables is very helpful, much more so than thinking of models per se (see also Barthélémy & Caraglio 2007).

Poorter et al. (2006) analyse architectural s. l. traits in moist Bolivian forests, finding four functional groups there. León Enriquez et al. (2008) examined variation in plant models in the context of phylogeny in Phyllanthaceae, and found that whether growth was rythmic or continuous correlated well with the major clades recognized, while growth characters vary in an interesting way within Fagraea (Wong & Sugumaran 2012).

How are the growth patterns that result in these architectural models produced? Costes et al. (2008) show how growth form of trees can be generated given the careful specification of appropriate starting variables. Prusinkiewicz and Barbier de Reuille (2010: p. 2125) discuss tree form from the point of view of "a competitive, self-organizing process through which branching forms emerge", contrasting this with an approach that emphasizes a "precisely controlled genetic program which determines their development" of Hallé and Oldeman (1978, p. 74) (see also Palubicki et al. 2009; also leaf insertion, form, and venation, inflorescence morphology, etc., below). "Models" are the result of the interaction on internal variables (hormones, nutrient flow, etc.) with the external environment.

Habit/life form classifications are ways of looking at whole plant morphology in the context of ecology and function. Habit is indicated in a very general fashion in the characterizations. For an interesting survey and categorization of plant life forms that emphasizes the position of resting buds, see Raunkiaer (1934); du Rietz (1931) is another approach to categorizing growth forms. Ellenberg and Mueller-Dombois (1967) provide a key to a revised Raunkiaer system, Barkman (1988) a more recent discussion of growth forms and phenology, while von Willert et al. (1990) suggest that the term growth form refers more to architectural features of the plant (see Plant Architecture above). The growth of monocots, predominantly a perennial herbaceous group, can be interpreted as variation on a basically sympodial theme (Holttum 1955).

Groover (2005) discussed the multiple derivations of the herbaceous life form from the woody, and the reverse; the latter transition can often be detected by the presence of distinctive details of xylem anatomy (see e.g. Carlquist 2009; Lens et al. 2012) and is mentioned under individual families. For a survey of epiphytes, see Madison (1977), Kress (1986a), Gentry and Dodson (1987), and Zotz (2013: numbers partly based on The Plant List, so beware!); see Benzing (1990) for a general discussion about vascular epiphytes. Schuettpelz (2007) and Dubuiosson et al. (2009) discusses epiphytism in ferns; there the sometimes long-lived gametophyte can be particularly important. For a summary of carnivorous plants and of plants with sticky glandular hairs that some have suspected of being carnivorous, see e.g. Chase et al. (2009c) and Schlauer (2010). For a survey of lianes - of which there are 5,000-10,000 species - see e.g. Gentry (1991), Caballé (1993), and Schnitzer and Bongers (2002), Rowe and Speck (2005), also Schnitzer and Bongers (2002) for their ecology, and for general information, see Putz and Mooney (1991) and Feild and Isnard (2013) and references. Much has been written on succulent plants, often focusing on those that are drought avoiders, although succulence is also associated with salt tolerance (Ogburn & Edwards 2010) and also with the epiphytic habit. Ogburn and Edwards (2010) note how hard it is to define succulence clearly - Tillandsia usneoides is ecophysiologically, even if not morphologically, a succulent. For a survey of succulent plants in general, see also von Willert et al. (1990), Eggli and Nyffeler (2009) and Nyffeler and Eggli (2010b). Procheŝ et al. (2006) noted the richness of the geophytic flora in the Cape region of South Africa, while at the same time they observed how hard it was to define a geophyte... For the bizarre leaf morphologies of plants from Namaqualand, see Vogel and Müller-Doblies (2011).

Leake (1994; see also Imhof 2007; Merckx et al. 2009b; Merckx & Freudenstein 2010) surveyed the biology of echlorophyllous myco-heterotrophic plants, observing that they were commonest in monocots, although also occuring in broad-leaved angiosperms, while echlorophyllous parasites are known from broad-leaved angiosperms alone (for the latter, see Barkman et al. 2007) and also in Parasitaxus (Podocarpaceae) (see Fay et al. 2010 for a good general account). The association of myco-heterotrophy with monocots may be connected with the absence of secondary thickening there, a thick cortex, lack of primary root, etc. (Imhof 2010). Note that myco-heterotrophic and parasitic plants often lack stomata and are otherwise distinctive anatomically; they often have flowers with parietal placentation, many ovules with sometimes long funicles, small seeds, little endosperm, an undifferentiated embryo, etc. The floral morphology of some parasitic plants in particular is often very difficult to relate to that of their putative photosynthetic relatives, while the vegetative morphology of all echlorophyllous plants is much reduced and modified.

Both parasitic and myco-heterotrophic plants have a distinctive physiology, too. In the case of myco-heterotrophic plants, much work has been carried out recently to establish the direction of flow of nutrients between the fungus, the echlorophyllous myco-heterotroph, and other plants with which the fungus may have a mycorrhizal association (see Merckx et al. 2009b for references). Glomeromycota are often involved in myco-heterotrophic relationships in tropical echlorophyllous plants other than Ericaceae and Orchidaceae, and details of the nutrient exchange between the two partners may be different from these other situations when ectomycorrhizal fungi, often basidiomycetes, are involved (Franke et al. 2006; Courty et al. 2011). Being a parasite often seems to entail having a high rate of transpiration both day and night, and if they do have stomata, these are often permanently open (Stewart and Press 1990).

For general literature on parasitic plants see Kuijt (1969: still useful), the Parasitic Plants Website (Nickrent 1998 onwards, a great deal of information), and also Heide-Jørgensen (2008), while images of both parasitic and myco-heterotrophic taxa may also be found at the Parasitic Plants Website. Intermediates of both conditions occur. Thus Orobanchaceae are noted for including both hemi- and holoparasitic plants and Santalales include all intermediates between holoparasites and free-living plants. All Orchidaceae are more or less mycotrophic, and a number lack chlorophyll entirely and are myco-heterotrophic (see also Dioscoreales). More details on parasitic and myco-heterotrophic associations are to be found under the families involved.

Dessication tolerance. This is basically a physiological character; see Lüttge et al. (2011) for a review. A relatively few plants, usually more or less herbaceous, show various degrees of dessication tolerance, some being known as "resurrection plants", examples being Myrothamnaceae, many Velloziaceae, and perhaps surprisingly also Linderniaceae and Gesneriaceae (Burtt 1998; Alpert & Oliver 2002; Proctor & Pence 2002; Dickie & Pritchard 2002; Porembski 2011). A number of plants have seeds that can tolerate dessication, also surviving very high temperatures, that is, they are anhydrobiotes (Mertens et al. 2008), and genes involved in dessication tolerance in adults of at least some flowering plants seem be derived from those that give dessication tolerance to propagules, not other stress-tolerance genes (Fisher 2008). Some of the genes involved in seed development and maturation, the LEC1- type HAP3 genes, are inductively expressed under drought stress in non-seed plants like lycophytes and ferns - and of course the seed dries out during the maturation phase (Xie et al. 2008).

Ant-Plant relationships. Plants in which there is a close relationship between ant and plant, loosely linked under the term myrmecophytism, are widely scattered phylogenetically (see Davidson & McKey 1993 [ground-dwelling epiphytes] and Davidson & Epstein 1989 [epiphytic myrmecophytes] for general accounts; Webber et al. 2007 for clarification of the kinds of relationships involved). It has recently become clear that fungi are frequently an obligate third party in this relationship (Defossez et al. 2009).

Mycorrhizae. For the evolution and ecological significance of mycorrhizae, see Malloch et al. (1980), Read et al. (2000), etc., and for an account with a summary of the distributions of the main mycorrhizal types within angiosperms, see Brundrett (2002, 2004), Wang and Qiu (2006), and especially Brundrett (2009, see also 2008 for updated online resource), F. A. Smith and Smith (1997), S. E. Smith and Read (1997), and Landis et al. (2002). Akhmetzhanova et al. (2012) is a database conaining information of mycorrhizal type, etc., in some 3,000 species in the old U.S.S.R., and Brundrett (2004; see also Peterson & Massicotte 2004) offers a classification of mycorrhizal types based on anatomical criteria regulated by the host plant. Mycorrhizal development is intimately connected with fine root thickness, branching, the development of root hairs, etc., although correlations are by no means absolute (Baylis 1975; St John, 1980; Schweiger et al. 1995) and plants can have at first sight bewildering complexes of root morphologies and fungal associations (e.g. Gao & Yang 2010). Species can have both mycorrhizal types (e.g. Frioni et al. 1997; Akhmetzhanova et al. 2012). Although families, etc., may be assigned a particular mycorrhizal status, this usually represents merely the condition most common for that taxon.

Ectomycorrhizae form a Hartig net of hyphae investing the rootlets and penetrating between the cortical cells; the hyphae are septate and are not intracellular - with the exceptions of the distinctive ectomycorrhizae of Ericaceae and Orchidaceae. Bruns and Shefferson (2004) provide a convenient summary of taxa with ectomycorrhizae, but more detail will often be found here (see e.g. Ducousso et al. 2008 and references); sometimes the fungus-root association results in the formation of tuberculate structures (Smith & Pfister 2009). Although basidiomycetes are frequent ectomycorrhizal associates, Pezizales (ascomycetes) are also quite common (Tedersoo 2006, ascomycetes with an hypogeous life style are derived from them). Ectomycorrhizae are common in Fagales, which dominate in temperate woodland, but they are also notable in caesalpinioids in African Miombo vegetation, Dipterocarpaceae in dipterocarp forests in Malesia, etc. Ectomycorrhizae - along with endomycorrhizae - also occur in plants like Graffenrieda emarginata (Melastomataceae) that grows in tropical montane environments (Haug et al. 2004 and references).

Endomycorrhizae, or vesicular-arbuscular mycorrhizae, are formed by an association of Glomeromycota (Schüßler et al. 2001) with land plants - indeed, Glomeromycota are found only in association with plants, whether sporophyte or gametophyte. There is evidence of such mycorrhizae in the fossil record from the Silurian/early Devonian ca 400 million years ago, but this association has almost certainly arisen - and been lost - a number of times (e.g. Baylis 1975; Redecker et al. 2000b; Duckett et al. 2006). Thus although plants of the first pectinations of the liverwort clade are associated with Glomales (Kottke & Nebel 2005), this association may subsequently have been lost (Duckett et al. 2006b), indeed, in some cases the fungus involved may have moved to the liverwort from a tracheophyte (Ligrone et al. 2007). Within Jungermanniopsida, Porellales lack fungus associations, but within Jungermanniales associations with ascomycetes are very old, more than 250 million years (Pressel et al. 2008). Glomeromycota are involved in some myco-heterotrophic relationships in tropical echlorophyllous plants, although in plants with a similar life style in Ericaceae and Orchidaceae basidiomycetes are the fungal partner; details of the nutrient flow between fungus and angiosperm may differ (see above). Glomus itself is probably paraphyletic (or worse: Redecker et al. 2000a; Schwarzott et al. 2001) and Glomeromycota seem to be a very ancient asexual group (Pawlowska & Taylor 2004) whose basic genetic structure is not well understood (Rodriguez et al. 2004).

In vesicular-arbuscular mycorrhizae the aseptate hyphae are intracellular, often forming vesicles or branching structures called arbuscules within the cells (when the latter alone are formed, an arbuscular mycorrhiza may result). In a few taxa, root nodules are formed, and these are modified lateral roots, occuring in 2-3 longitudinal series opposite the protoxylem poles - similar to the root branchlets of Proteoid roots and actinorrhizal nodules (Duhoux et al. 2001; Schwendemann et al. 2011 for literature). Baylis (1975; see also St John 1980) emphasized the prevalence of mycorrhizal magnolioid roots in plants included in the magnoliid clade here, such roots were coarsely branched and rarely less than 0.5 mm across; they often lacked or had only a few root hairs, and these were small, less than 100 x 15-20 µm. Since such roots are also known from Griselinia (Apiales) and Liquidambar (Saxifragales: Baylis 1975), their overall distribution is unclear, but Comas et al. (2012) have recently reexamined factors like root density, biomass, and root diameter in the context of angiosperm evolution, suggesting that root diameter has greatly decreased within the angiosperm clade.

For phylogenetic aspects of vesicular-arbuscular mycorrhizal associations, see also Trappe (1987). The two main mycorrhizal variants described there, the Paris and Arum types (see also Gallaud 1905; Dickson et al. 2007) show little association with higher-level groupings, except perhaps when Asparagales are compared with Liliales (Smith & Smith 1997); the Paris type may be under-recorded. Note also that both types are known from several families and there are intermediate morphologies (Dickson et al. 2007). Thus it has been suggested that these mycorrhizal types be discarded, emphasis being better placed on the morphological and physiological details of the association (Brundrett 2004), but some think that the types are indeed useful enough (Dickson et al. 2007). Interestingly, in mycotrophic plants, the pattern of fungal infestation seems always to be a variant of the Paris type of endomycorrhiza, with well developed intracellular hyphae (Imhof 2007 and references). In addition to variation in details of intra-plant fungal infestation, there is also variation in the proportion/amount of fungal biomass inside the plant compared to that outside the plant that is linked with the taxonomy of the fungus (Maherali & Klironomos 2007).

Aquatic plants, hardly surprisingly, lack mycorrhizae, as do parasitic plants (Trappe 1987; Radhika & Rodrigues 2007 and references for records, also de Marins et al. 2009; for a convenient summary, see Brundrett 2008), although there may be infraspecific variation in some taxa depending on whether growth is in marshy or drier conditions (Bristow 1975). The frequent absence of mycorrhizae in Caryophyllales, Proteales, etc., is systematically interesting. In, say, the tundra habitat there are a number of plants that take up substantial amounts of amino acids directly from the soil, but the ability to do this is not obviously correlated either with mycorrhizal status or taxonomy. In such habitats a number of Cyperaceae, which usually lack mycorrhizae (but c.f. Muthukumar et al. 2004), take up N predominantly in an organic form, but other species in the family take it up in an inorganic form (Raab et al. 1999).

Endophytic fungi are found in a number of flowering plants, perhaps particularly in Poaceae (q.v.) and Ericaceae (e.g. Petrini 1986 and other references in this volume; Saikkonen et al. 2004 and references), although they are probably pervasive in angiosperms (Herre et al. 2005: tropical plants). Indeed, Arnold et al. (2001) found 418 morphospecies of endophytes in only 83 leaves of two species of tropical trees (Ouratea [Olacaceae], Heisteria {Erythropalaceae]). The effect of endophytes on their hosts is little understood, Poaceae being something of an exception (Schardl 2010 and references). Endophytes of Poaceae seem to have evolved from an insect pathogen (e.g. Spatafora et al. 2007; Vega et al. 2009) and they may protect the plant against pathogens, as well as affect the water balance of seedlings, the branching of the root, the palatability of leaves and fruits, etc. (Arnold & Engelbrecht 2007 and Sasan & Bidochka 2012 and references). They may also be involved in the synthesis of metabolites previously attributed to the plant host, and the angiosperm-endophyte partnership has even been likened to a chimaera (Herre et al. 2005; see also Markert et al. 2008: Wink 2008). Endophytes may be either vertically or horizontally transmitted - via the seed or other plant propagules or via spores. Arnold (2008) provides a convenient entry into the literature.

Another set of associations between plant and insect - although other organisms may be involved, too - result in the distinctive outgrowths evident as galls (see Redfern 2011 for a good introduction). Cecidomyiidae (dipterans), the most speciose gall formers (Yukawa & Rohfritsch 2005), are worldwide in distribution but show no particular pattern of host associations. Cynipidae (hymenopterans) are north temperate in distribution and do show an association with particular plant groups (Stone et al. 2009; Redfern 2011), while psyllids (jumping plant lice, hemipterans) are particularly common in Australia (Fernandes & Price 1991; Crespi et al. 2004; Espiritó-Santo & Fernandes 2007; Raman et al. 2005). In general, gall-inducing insects are commonest on sclerophyllous plants growing on poor soils in warm climates between 25 and 45o N and S, or perhaps more generally in species-rich communities, whether dry or wet, but not necessarily in tropical climates (Price et al. 1998; Yukawa & Rohfritsch 2005; Redfern 2011).

For rusts and their hosts, see OTHER at the end of this page.

Nitrogen fixation. Angiosperms that can fix nitrogen in association with bacteria are uncommon, yet are found almost exclusively in a group of four orders, the N-fixing clade (Fabales, Rosales, Cucurbitales, Fagales), where the association has evolved several times. Jeong et al. (1999) and Clawson et al. (2004) discuss this association in the context of the evolution of Frankia, the bacterium most commonly involved outside the Fabaceae, and within Fabaceae (q.v.) themselves, there may have been several acquisitions of the ability to nodulate, very different bacteria being involved. A few land plants - hornworts, the water fern Azolla, cycads, and Gunnera (Gunnerales) have established a relationship with the N-fixing cyanobacterium Nostoc (Adams et al. 2006 for a summary).


For some formulae, etc., see the Glossary.

Hegnauer (1962 onwards) remains the source of information, Siegler (1998) is also invaluable, and Gershenzon and Mabry (1983) can still be read with profit. Kite et al. (2000) provided a useful survey of the distribution of some chemicals in the monocots, while Strauss and Zangerl (2002) summarise the diversity of the major classes of compounds involved in chemical defence in angiosperms (see also Waterman 2005, also the insect-plant and fungus-plant relationships mentioned at the end of this page - secondary metabolites are commonly involved here, too).

Note that sampling for chemical characters may be spotty (although still often better than that for many embryological characters?), indeed, sophisticated screening methods are leading to the detection of some classes of secondary metabolites in families from which they had not been recorded (Lapcík 2007). Indeed, it can be very difficult to say that a compound is really absent: Is an alkaloid present at 0.000001% concentration present or not (Waterman 2007, q.v. for the problems facing chemical systematics)? Furthermore, the part of the plant sampled may well affect the metabolites that are detected (e.g. Webber & Miller 2008 and references; Ferreres et al. 1996). Almost all authors rightly emphasize the importance of the pathways by which compounds are produced, and apparently distinctive substances like napthoquinones can have quite diverse biosynthetic origins, conversely, furanocoumarins in Ficus (Moraceae), Apiaceae and Rutaceae - quite unrelated - are produced by the same pathway (Berenbaum 1983 and references; Pichersky & Lewinsohn 2011: convergent evolution at various levels; Maia et al. 2012: parallel evolution and pollination cues). Unfortunately, systematic surveys of plant groups for single classes of compounds are now out of fashion unlesss they are of obvious biological interest, like glucosinolates.

Pichersky and Lewinsohn (2011) estimated that there were probably far more than 200,000 secondary/specialized metabolites to be found in "plants", any one species having 3,000-8,000 such compounds. The diversity of phytochemicals known is in part understandable because it appears, for example, to be very easy for the sugar donor specificity of the enzymes which conjugate flavonoids with sugars to change (Noguchi et al. 2009). Individual terpene synthases may have many products, and there are several terpene synthases (Davis & Croteau 2000) - as an example, gamma-humulene synthase of Abies grandis can generate 52 different sesquiterpenes (Degenhardt et al. 2009). Genes involved in the biosynthesis of particular defence compounds tend to cluster on the same chromosome (Takos & Rook 2012).

As a final wrinkle, there is increasing evidence that some important secondary compounds of plants are in fact synthesised by endophytic fungal or bacterial associates of the plant (e.g. Tan & Zou 2001; Gunatilaka 2006 [both surveys]; Markert et al. 2008; Wink 2008); families like Convolvulaceae, Celastraceae and especially Fabaceae and Poaceae are distinctive in this regard. Sporadic associations between plant and fungus/microbe, and/or horizontal transfer of genes from bacteria, may also go some way towards understanding the pattern of distribution of secondary metabolites, the presence of the metabolite in a particular organism then depending on regulation of these genes (Wink 2008, 2013). Indeed, secondary metabolites like terpenoids and quinolizidine alkaloids are produced more or less exclusively in mitochondria and/or chloroplasts - i.e. in bacteria whose association with plants is of very long standing (Wink 2008; see also Davis & Croteau 2000 for terpenoid synthesis). Other metabolites may be Finally, alkaloids and other noxious compounds may move from host to associated (hemi)parasite (Cabezas et al. 2009).

The distribution of a number of these secondary metabolites are of systematic and/or functional interest. In general, chemical characters are like others in terms of their value in understanding phylogenetic relationships; some, like the presence of glucosinolates, are very valuable, many others, much less so. Still others - presence of ellagic acid is an example - show fairly restricted distributions, but are still very variable in terms of presence/absence (e.g. D. Soltis et al. 2005b). Monocots in general have a less diverse secondary chemistry than do other angiosperms.

Acetylenes. Acetylenes are relatively uncommon in flowering plants (see Bohlmann et al. 1973 for a survey, etc.), although they are notably common in some families in Asterales and Apiales, where they seem to substitute for iridoids.

Alkaloids. For a general introduction, see Hegnauer (1988; Aniszewski 2007). Alkaloids are extremely diverse (some 12,000 different kinds are known), and, complicating the issue, similar alkaloids can be formed via different biosynthetic pathways. Alkaloids can be classified according to the nature of the skeleton nucleus that they have, some of which are mentioned below. For a survey of the structure and distribution of isoquinoline alkaloids, see Buck (1987) and Bentley (1998), while Liscombe et al. (2005) put the origin of these alkaloids in a phylogenetic context. Detection of the activity of (S)norcolaurine synthase, the gateway to benzylisoquinoline synthesis, may suggest that these alkaloids will be found in groups in which they are not currently known, e.g. Chloranthaceae. For the synthesis of benzylisoquinoline alkaloids in the opium poppy (they are synthesised in the sieve tubes!), see Bird et al. (2003); these are normally, but not always, derived from tyrosine. For pyrrolizidine alkaloids, which are concentrated in a few plant groups and are only sporadic elsewhere, see Hartmann and Witte (1995), Hartmann and Ober (2000), Ober and Hartmann (2000), Anke et al. (2004), Reimann et al. (2004) and Hartmann and Ober (2008); they are used by insects both in defence and for pheromones. The distribution of some distinctive alkaloid types such as the erythrina (Erythrina, Cocculus) and homoerythrina (Phelline, Dysoxylum, Schelhammera, some conifers) alkaloids is very scattered. For the distribution of calystegines (tropane alkaloids) see Dräger (2004), for that of ergot alkaloids, see Gröger and Floss (1998), and for that of indolizidine and quinolizidine alkaloids, see Michael (2008).

Aluminium accumulation. Useful surveys of aluminium accumulation are found in Chenery (1948), Webb (1954), Kukachka and Miller (1980), and Jansen et al. (2002b, 2004a, c). Broadley et al. (2001) and Cappa and Pilon-Smits (2014) summarize patterns of hyperaccumulation of heavy metals (e.g. nickel, manganese, etc.) and other unusual elements in angiosperms (see also Baker & Brooks 1989). Freeman et al. (2009) and others advance hypotheses for its advantages to the plant.

Anthraquinones may be synthesised from polyacetates or shikimic acid. Overall, little detail seems to be known about this, but the broad patterns of variation are interesting (Jensen 1992 for a survey).

For calcium oxalate crystals, see below under anatomy.

There are over characterised 500 cardiac glycosides involved in plant protection; they are scattered over a variety of plant groups, and belong to two main classes, cardenolides and bufadienolides (see Singh & Rastogi 1970; Agrawal et al. 2012 for literature). For resistance to cardenolides in herbivorous insects in which there is convergence at the amino acid level, see Dobler et al. (2012).

Some information on the distribution of chelidonic acid is taken from Ramstad (1953).

Coumarins are involved in plant defense, some 800 different kinds being known from about 80 families (see also Berenbaum 1983).

Cyanogenetic pathways - see the surveys by Saupe (1981) and Lechtenberg and Nahrstedt (1999) and comments by Hegnauer (1977, 1986), also Seigler and Brinker (1993) and Miller et al. (2006). Some 60 different kinds of cyanogenic compounds are known from about 130 families; the distribution of some, e.g. the cyclopentenoid cyanhydrin glycosides, is of particular interest (see Malpighiales, families near Achariaceae), and these are derived from the non-protein amino acid 2-(2-cyclopentenyl)glycine (e.g. Spencer & Seigler 1985b; Webber & Miller 2008). Cyanogenic compounds are stored as ß-glycosides and are activated by a ß-glycosidase; ß-glucosidases activate both the "cyanide bomb" and the "glucosinolate bomb", and the topology of an (abbreviated) tree produced by a phylogenetic analysis of the enzyme sequence is similar to that of other trees of angiosperms (Morant et al. 2008). For an example of the interactions of cyanogenic host and herbivorous insect (which can also synthesize the cyanogenic compounds itself), see e.g. Zagrobelny and Møller (2011).

Ethereal oils are more or less volatile and aromatic; they are often terpenes of some sort. They may be found in idioblasts, i.e. specialized cells, as in basal angiosperms, and leaf blades, tepals, etc., containing ethereal oil cells may be punctate when a light is shone through them.

Fats, whether saturated or unsaturated, and their corresponding fatty acids (see also polyacetylenes below) are widespread, and are often important components of seeds. Petroselenic (cis-6-octadecenoic) acid has a distribution of considerable systematic interest (see Garryales and Apiales in particular: Kleiman & Spencer 1982 for a survey) and there are other distinctive fatty acids that have distributions that appear to be of systematic interest (Badami & Patil 1981).

For unlignified cells walls with UV-fluorescent ferulic and coumaric acids, see Harris and Hartley (1980) and Rudall and Caddick (1994).

Flavonoids. For general information about flavonoids, see Giannasi (1988), Bohm (1988), and Harborne and Baxter (1999), for minor flavonoids, see Bohm (1988), for isoflavonoids in particular (often phytoalexins), see Reynaud et al. (2005), Mackova et al. (2006) and Lapcík (2007), for biflavonoids, Geiger and Quinn (1975), and for flavonoid distribution in monocots, Williams and Harborne (1988). As Stafford (1990: p. 9) notes, "the use of duplicate or triplicate names for the same group of flavonoids is an unfortunate aspect of flavonoid nomenclature". Hegnauer (1986) suggests that flavonoids are of little use when looking at higher-level relationships. Anthocyanins are common flavonoid pigments, and when found in leaves they are usually red, perhaps protecting the young leaf (Manetas 2006: insect herbivores cannot see red, and if they are green, they contrast with leaf color).

Mustard oils, glucosinolates, are uncommon in flowering plants and are largely restricted to Brassicales (see also Putranjivaceae - Malpighiales: Fahey et al. 2001 for a summary). For details of glucosinolates and their distribution, see Fahey et al. (2001); some 120 or more different glucosinolates are known. They are broken down by the enzyme thioglucoside glucohydrolase (myrosinase) into glucose and aglucones, which automatically rearrange into a isothiocyanates, mustard oils, which have a R-N=C=S arrangement (see Cyanogenetic pathways above for ß-glucosidases), but the aglucones can also be converted into nitriles, thiocyanates, etc. (Halkier & Gershenzon 2006; Burow et al. 2009; Winde & Wittstock 2011). Note that some of the more unexpected records of glucosinolates, e.g. in Phytolaccaceae and Pittosporaceae, are reported by Daxenbichler et al. (1981), however, there are no vouchers and the reports must be considered suspect (J. E. Rodman pers. comm.; Mithen et al. 2010 for Brassicales). For the ecological and agricultural implications of glucosinolates, see e.g. Courtney (1986), Chew (1988), Brown and Morra (1997) and Rask et al. (2000), and for herbivores that are attracted to mustard oils, see Host-plant preferences below.

Gums, non-crystalline mixtures of sugars and organic acids, are scattered in angiosperms, being notably common in Fabaceae, where they are often found in the seeds (Nair 1995).

Hemicelluloses, see polysaccharides.

Iridoids. Data are taken mainly from Bate-Smith et al. (1975), Hegnauer and Kooiman (1978), Bate-Smith (1984), Fredericksen et al. (1999), and especially Jensen (1991, 1992, 1999) and Jensen et al. (1975b) and other papers from his laboratory. Iridoids are formed from two C5 isopentane (isoprene) units. They are cyclic C10 compounds, often (always?) with O in one ring; they are formed in two main ways; they may be route I (secoridoids) or route II (carboxylated and decarboxylated iridoids: see the Glossary for their structures). Although a very useful character, presence/absence of iridoids may vary in closely related taxa (e.g. Jensen et al. 1975b). (Note that Inouye and Uesato [1986] questioned a classification of iridoids that was based on their biosynthetic pathways.) Iridoids are produced by the mevalonate pathway, and although polyacetylenes have a very different origin, being derived from their corresponding fatty acids, in families or groups of families of asterids one of these two classes of compounds may dominate to the exclusion of the other. Families that contain iridoids are largely asterids, although there are a few records from Saxifragales, etc.; all told, some 600 different structures are known. For further details of possible evolutionary pathways of iridoids, see Albach et al. (2001a). As glycosides, many have distinctive, often adverse, physiological effects on mammals, micro-organisms, etc. (see also Dobler et al. 2011); Bowers (1988) summarises aspects of the relationships between iridoids, plants and insects and Nishida (2002) gives examples of insects that sequester the compound. See also Host-plant preferences below.

Isoprene. Plants can produce substantial amounts of isoprene, a gas that playsan important rols in atmospheric chemistry. Sharkey et al. (2013) discuss the evolution of isoprene synthase genes; Kesselmeier and Staudt (1999) provide a convenient summary of the distribution, etc., of the gas.

Latex is mentioned only when it occurs (see also laticifers, below). Gutta has the trans- configuration of isoprene units, and is distinguished from latex in the strict sense, which has the cis- configuration, in the descriptions. See Konno (2011) for aspects of the chemistry of latex.

For plant lectins, a group of haemagglutinating proteins, see Vandenborre et al. (2011).

Lignans and neolignans. Lignans are ß,ß'(8-8')-linked dimers of cinnamic acid residues or their biogenetic equivalents (diaryl propanoids), and are widespread, although they apparently do not occur in monocots. They are also found in gymnosperms. Neolignans, more directly linked, or at least with other than ß,ß' links, are found especially in magnoliids (monomeric allyl- and propenylphenols are also found in the groups where they occur). For definitions (which are not consistent, and depend either on structure or on biosynthetic pathway), distribution, etc., see McRae and Towers (1984), Bedigian et al. (1985), Whiting (1985: structure) and Ayres and Loike (1990).

Lignins are complex and still poorly understood but major components of secondary cell walls. Their composition is of considerable interest, and under certain conditions they yield substantial amounts of aromatic aldehydes - various combinations of vanillin, syringaldehyde, and p-hydroxybenzaldehyde. In particular, the Mäule reaction, in which a reddish colour is obtained after treatment of the plant sample with potassium permanganate, then dilute hydrochloric acid, and then ammonia, signifies presence of syringaldehyde, derived from sinapyl alcohol (Gibbs 1957 for an early but fairly comprehensive survey). The occurrence (or otherwise) of this reaction is correlated with fairly major taxonomic groups; note that vascular tissue may not always be stained - and even when it is, primary xylem is not always stained.

For the monolignols/phenyl propanoid units/phenol units/glycosides of the three major types of lignin see the coniferyl (MIG)/guaiacyl (G-lignin)/vanillyl/coniferin; sinapyl (MIS)/syringyl (S-lignin)/syringyl/syringin; and p-coumaryl MIH)/p-hydroxyphenyl (H-lignin)/p-hydroxyl/? lignins. Conventionally, distinctions are drawn between G lignin, found in conifers, also tree ferns, G + S lignin, found in many angiosperms, but also elsewhere, and G + S + H lignin, found in monocots, but the situation is not that simple. There are two hydroxycinnamyl alcohols - usually not considered to be be monolignols - that can also be involved: 5-hyroxyconiferyl alcohols can be found in angiosperm lignis, while caffeyl alcohol has recently been found in the seed coats of some Orchidaceae (Vanilla) and Cactaceae (Chen et al. 2012). There are also a number of minor lignin components found, for example, in conifers and grasses; there is more variation in the three major "types" than commonly thought - certainly, they are not restricted to the major plant groups they nominally characterize; and there can even be substantial variation ontogenetically and/or in different parts of the plant. For instance, in Eucalyptus globulosus, the order of monolignol deposition is H, G, and then S (Rencoret et al. 2010), while the lignins of the bark and wood of Betula pendula differ (Logan & Thomas 1985; see also Lewis & Yamamoto 1990; Boerjan et al. 2002). H-lignin is somewhat restricted, being absent from broad-leaved angiosperms - at least from magnoliids and eudicots (Towers & Gibbs 1953), where syringyl units are particularly common. Finally, syringyl lignin is also found in Selaginella, where its synthetic pathway is different from that in angiosperms (Weng et al. 2011).

For a general discussion on details of the synthesis of lignin precursors, see Li et al. (2001), Weng and Chapple (2010), and Weng et al. (2010), and for discussion on the distribution of lignin types and synthesis of lignins, see Logan and Thomas (1985), Whetten et al. (1998), Harris (2005), Weng et al. (2010), Guo et al. (2010), Li and Chapple (2010), and Espiñeira et al. (2010, 2011). Note that syringyl (S) lignin is also found in some lycophytes, e.g. Selaginella, and in other vascular plants, but it is (?always) synthesised in a way different from that of similar lignin in flowering plants, while at least some red algae can produce lignin-like substances (Martone et al. 2009).

Fructose is a kind of monosaccharide that is sometimes stored by the plant; families in which storage fructose polysaccharides like inulin have been detected are listed by Pollard and Amuti (1981) - these are mentioned only when they occur reasonably consistently within a family. Thus they are not mentioned in Cornaceae, where they occur only in a few species of Cornus, but not others, nor in Melianthaceae, where they are reported only in trace amounts. For the distribution of stem fructans in monocots, see Pollard (1982); for fructans in general, see Meier and Read (1982).

The metabolic pathway of nicotinic acid in tissue culture may be of systematic significance, although at some 50 species the sampling is poor (see Willeke et al. 1979). Gymnosperms and all flowering plants except asterids metabolise nicotinic acid into trigonelline.

Non-protein amino acids are mentioned only when they are abundant, as in families like Fabaceae and Cucurbitaceae; they are quite widely distributed, and some 600 different forms are known, over 300 in flowering plants (see Rosenthal 1982 for the compounds, etc., Hunt 1991 for some other literature; Huang et al. 2011).

Oligosaccharides, containing three to ten sugar units, include raffinose, a prominent component of the translocate; it is synthesized in the phloem and actively loaded via the symplast into the phloem (e.g. see Davidson et al. 2010, also sugar transport below); the disaccharide sucrose is the commonest component of the translocate (see also

polyols below.

Phenols are widespread. Hydroxycinnamic acids such as caffeic acid, p-coumaric, ferulic and sinapic acids and their derivatives are widespread, and the distributions of disaccharide esters of caffeic acid and related compounds are particular interest (Mølgaard & Ravn 1988). The distribution of caffeic acid itself, perhaps involved in plant defence, seems to be of some systematic interest. It is especially common in herbaceous groups, and is produced from cinnamic acid; proanthocyanidins or non-hydrolyzable tannins (see below under tannin) are also produced from cinnamic acid and tend to show an inverse distribution.

Phorbol esters are diterpenes, often with a toxic effect (Evans & Taylor 1983 for distribution; Evans & Edwards 1987 for physiological effects [for which also see other papers in volume 94 of the Botanical Journal of the Linnean Society]).

Photosynthetic pathways. There are three main pathways by which carbon is incorporated into the organism or, perhaps more accurately, is initially captured prior to being incorporated into metabolic cycles, the C3 and C4 pathways and CAM (Crassulacean Acid Metabolism). C3 and C4 pathways may occur in the same organism (Surridge 2002; Sage 2004 for references), as may C3 photosynthesis and CAM (Martin et al. 2012). It is thus perhaps not surprising that distinctive photosynthetic pathways - let alone their subtypes - are rarely constant in major taxa and have evolved in parallel many times. However, C4 and CAM are particularly common in core Caryophyllales, Poales in general and Bromeliaceae (CAM), Poaceae and Cyperaceae (C4) in particular, and the CAM is common in succulents and epiphytes (e.g. see Sage et al. 1999; Sage et al. 2012 for the C4 pathway). For the evolutionary inter-relationships of the three types of photosynthetic mechanisms, see West-Eberhard et al. (2011 and references) and Edwards and Ogburn (2012).

For a general survey of C4 photosynthesis, see the papers in Sage and Monson (1999), also Sage et al. (2012) and Kellogg (2013). Although particularly common in Poaceae, it occurs other families, especially Cyperaceae, Amaranthaceae and other Caryophyllales and Euphorbia subgenus Chamaesyce (Osmond et al. 1980; Sage et al. 1999; Muhaidat et al. 2007). C4 photosynthesis is usually found in plants growing in rather hot, also dry and saline conditions, but it is sometimes found in plants growing in decidedly cooler conditions (e.g. Wang et al. 2008). It includes several morphological and enzymatic variants (see esp. Poaceae), although some kind of Kranz anatomy with enlarged bundle sheath cells and closely-spaced veins is typical (Sage et al. 2012). In submerged monocots and a few terrestrial dicots there is C4 photosynthesis without Kranz anatomy and the spatial segregation of organelles (Boykin et al. 2008 and references). That C3 and C4 pathways may occur in the same organism (Surridge 2002; Sage 2004 for references) may facilitate the reversals that have happened (Kadereit et al. 2012). The spatial separation of the different parts of the C4 photosynthetic cycle may occur at the scale of the cytoplasm and chloroplast within a single cell, as well as in different cells organized as distinct tissues (see also Bowes et al. 2002; Voznesenskaya et al. 2003), and more examples of separation at the subcellular scale continue to be reported. McKown and Dengler (2010) discuss the distinctive vein patterning in C4 plants. As Kadereit et al. (2012) emphasize, there is unlikely to be a single ecological explanation for the origin of this syndrome (Sage et al. 2012), and there are perhaps intermediate (see Kellogg 2013) species with C2 photosynthesis in which there is concentration in enlarged bundle sheath cells of the CO2 produced by photorespiration by the decarboxylation of glycine (Vogan et al. 2007; Sage et al. 2011, 2012).

CAM is especially common in epiphytes, plants of arid areas, and sometimes in aquatic plants (for the latter, see Keeley 1998). It, too, has a number of variants and there are intermediates between C3 photosynthesis and CAM; seedlings of CAM plants seem to have C3 photosynthesis. For literature on CAM, see Winter & Smith 1996; Sayed 2001; Keeley & Rundell 2003; Lüttge 2004, 2005; Silvera et al. 2010b); Herppich (2004) wonders exactly for what it might be an adaptation...

Phytoalexins, antifungal or antimicrobial substances produced by plants following infection, are very variable chemically. However, some families (Cucurbitaceae, Rosaceae) seem rarely to produce them, others (Brassicaceae) produce chemically very distinctive phytoalexins, while in yet others (Fabaceae) there is some infrafamilial systematic information in the type of phytoalexin produced (Harborne 1999).

It might seem that phytochrome behaviour is perhaps of interest phylogenetically; very limited evidence suggests that Pr is converted to Pfr, and then in core Caryophyllales, Pfr undergoes light-dependent decay, while in broad-leaved angiosperms it reverts to Pr in a thermal dark reaction (Kendrick & Hillman 1971). However, Sarah Mathews (pers. comm.) observes that light-dependent decay of Pfr is very widespread indeed in angiosperms.

Polyacetylenes (more accurate;y acetyleneic compounds) are often derived from their corresponding fatty acids; they have a C C triple bund, but are by no means always polymers. In asterids either polyacetlyenes or iridoids dominate to the exclusion of the other even although they are biosynthetically unrelated; exceptionally, the two may co-occur, as in Torricellia angulata (Torricelliaceae: see Pan et al. 2006; Liang et al. 2009). For an entry into the literature, see Minto and Blacklock (2008).

Polyols are linear reduced forms of monosaccharides that are carbon transporters in the phloem of a few families. They are particularly loaded into the phloem under stress conditions caused by drought or high sodium chloride, although the families which are recorded as having them - Celastraceae, Apiaceae, Oleaceae, Plantaginaceae, etc. - are not particularly notable components of vegetation that is habitually water- or salt-stressed (see Pommerrenig et al. 2007 for the physiological literature). Mannitol is a polyol that is particularly common in groups like Oleaceae, but the systematic significance of its distribution is unclear (see Stoop et al. 1996). In others plants sorbitol or dulcitol (galactitol) predominate (see Reidel et al. 2009; Turgeon 2010a; Fu et al. 2011 for details of phloem loading). Root-parasitic plants commonly have mannitol as the main sugar alcohol (Noiraud et al. 2001)

Primary cell wall polysaccharides show potentially interesting variation within vascular plants (see Domozych et al. 2010: cell wall composition in land plants and their immediate relatives; Silva et al. 2011: variation in ferns). Poaceae and perhaps a large part of the asterid I clade differ in xyloglucan hemicellulose composition from other angiosperms and gymnosperms, and Poaceae have a generally different hemicellulose/pectin composition from other seed plants (O'Neill & York 2003; Hsieh & Harris 2012). (1->3),(1->4)-ß-D-glucans are found in many, but not all, Poales (Smith & Harris 1999; Trethewey et al. 2005). There may also be variation in primary wall structure and composition at deeper levels in the land plants (Nothnagel & Nothnagel 2007; Hsieh & Harris 2012). Finally, the orientation of cellulose microfibrils in the outer epidermal walls of the elongation zone in roots varies (Kerstens & Verbelen 2002: ANITA grade and gymnosperms not studied). However, sampling in such studies generally leaves something to be desired. For amyloid/hemicelluloses/other polysaccharides in vegetative parts of the plant, see also Meier and Reid (1982), for those in seeds, whether cotyledons or endosperm, see below.

Quaternary Ammonium Compounds such as glycine betaine commonly occur in plants growing in saline habitats, and are probably involved in maintaining the osmotic balance of cells and organelles (Rhodes & Hanson 1993). Tertiary sulfonium compounds may also be involved. However, details of the distribution of glycine betaine and related compounds are still not well understood, and they are also common in many Lamiaceae (Blunden et al. 1996) and Convolvulaceae - families with vanishingly few halophytic members.

Resins and substances either similar to or confused with them are quite widespread in plants; for their distribution, see see Nair (1995), and for a readable summary, Langenheim (2002).

Saponins. Previously defined as compounds that produced soap-like foams when shaken with water, they are now characterized as being derived from the 30-carbon oxidosqualene (this contains 6 isoprene units) to which glycosyl residues are attached (Vincken et al. 2007, who also provide a classification of saponins). By and large, the distributions of saponins with particular skeletons seems to be of little systematic interest (Vincken et al. 2007).

Sesquiterpene lactones a subclass of C15 terpenoids (= sesquiterpenoids, sesquiterpenes), bitter-tasting and toxic, sometimes with allelopathic effects (Abdelgaleil & Hashinaga 2007), that are derived via the mevalonate pathway from three C5 isopentenyl pyrophosphate units.

Steroids, compounds characterized by a nucleus of 17 carbon atoms in the form of four fused rings, three containing six carbon atoms and one containing five; derived from triterpenoids. For phytoecdysteroids, perhaps protecting plants against herbivorous insects by affecting moulting, etc., of the latter, see Lafont et al. (1991).

For suberin, see Bernards (2002).

The sugar that is the main non-structural or storage carbohydrate in the plant varies. Although usually glucans, polymers of glucose, predominate, in some plants fructans are found (for the latter, see also fructose oligosaccharides above. The distribution of plants with fructans is of systematic interest (for taxa involved, see e.g. Pollard & Amuti 1981; Hendry & Wallace 1993), even if not circumscribing a broadly delimited Liliales (c.f. Pollard 1982). It has been suggested that fructan accumulation is associated with low temperatures (taxa accumulating fructans are rare in the tropics), and is involved in osmoregulation and cell growth by expansion - perhaps seasonality in general is an important trigger (Hendry 1993; Hendry & Wallace 1993; Livingston III et al. 2009). Note that the taxa storing fructans are a rather heterogeneous group ecologically (a number of Ericales, Poaceae-Poöideae [but not all], a number of Asterales, etc.). Zimmermann and Ziegler (1975) list sugars - Oligosaccharides - and sugar alcohols - see polyols above - found in exudates from sieve tubes (for the latter, see also Noiraud et al. 2001); in many plants the disaccharide sucrose is the main component.

Sulphated/sulfated compounds are particularly common in plants growing in saline habitats, e.g. Juncaginaceae and relatives (Alismatales) and Frankeniaceae/Polygonaceae and relatives (Caryophyllales).

Tannins are either condensed and non-hydrolyzable, proanthocyanidins of flavonoid origin (see Dixon et al. 2005) or hydrolyzable, and here caffeic acid and in particular gallic acid are the building blocks. The two kinds of tannins are not chemically immediately related, and although the vague terms "tannins" and "tanniniferous" occur in some of the characterisations, the more specific non-hydrolyzable and hydrolyzable tannins are to be preferred. Proanthocyanidins/condensed tannins are synthesised in the chloroplasts, whence they move into vacuoles (Brillouet et al. 2013). They and caffeic acid tend to be alternatives and the latter is especially common in herbaceous taxa, e.g. the asterid I and II groups (Mølgaard 1985 and Mølgaard & Ravn 1986, which see for more details than have been incorporated here). The immediate precursor for both galloyl and ellagitannins is pentagalloylated glucose (1,2,3,4,6-pentagalloyl glucose), and although the derivation of gallotannins from this and their biogenetic relationships are fairly well understood, those of ellagitannins is still unclear (Niemetz & Gross 2005). Ellagic acid, basically two units of gallic acid, is easily detected and its distribution was much commented on in the 1900s. Early surveys by Bate-Smith (1962: phenolics in general) and Bate-Smith and Metcalfe (1957: non-hydrolyzable tannins) are still useful; Bate-Smith (1983) discussed the distribution of galloyl esters. Okuda et al. (2000) reviewed the distribution of various types of hydrolyzable tannins in the context of Cronquistian relationships; ellagic acid is uncommon in the asterid I + II clade. Barbehenn and Constabel (2011) summarized the role of tannins in general in herbivore defence.

Terpenoids are a diverse and ecologically important group of compounds (e.g. Harborne & Tomas-Barberan 1991) made up of isoprene building blocks (see Bohlmann et al. 1998; Davis & Croteau 2000 for early steps in synthesis, inc. cyclization). Well over 30,000 different kinds are known, with over 15,000 structures known from land plants alone; Davis and Croteau (2000) and Degenhardt et al. (2009) discuss how terpene skeletal diversity in plants is generated. Isoprene (2-methyl-1,3-butadiene) is a hemiterpenoid released in immense amounts by many woody plants (but isoprene production seems to vary infragenerically in a systematically interesting fashion, as in Quercus: Harley et al. 1999) that can have direct effects on biotic interactions between plants and insects, for instance, affecting herbivory (Loivamäki et al. 2008). Two isoprene units make up monoterpenes, three make up sequiterpenes, etc. Terpenoids are related to steroids (see above), etc.


For definitions, etc., see the Glossary.

Metcalfe and Chalk (1950; 2nd edition, 1979 onwards, incomplete) provide information on general anatomy, although characters like nodal structure are rarely mentioned in the first edition; the recent Atlas of Stem Anatomy by Schweingruber et al. (2011, 2013) is full of magnificent illustrations. Much classical literature remains useful (see e.g. Thouvenin 1890; Beauvisage 1920; Watari 1939 for taxa that used to be placed in Saxifragaceae). Gregory (1994) is a good bibliography with the more important contributions conveniently indicated, Dickison (2000) is a very accessible introduction to general plant anatomy, and Carlquist (2001) has recently updated his survey of comparative plant anatomy (see also Carlquist 1988b); Esau (1977) is still very useful. Herendeen et al. (1999b) surveyed wood anatomical features in basal angiosperms and compared their findings to the classical evolutionary trends (see below); Carlquist (2012) provided a extensive critical survey of monocot vessel and tracheid morphology and their use in phylogeny. Wheeler et al. (1989) provide a useful survey of terms used in wood anatomy, InsideWood: An Internet Accessible Wood Anatomy Database is a developing resource for information about wood anatomy, also identification, etc., while Baas and Wheeler (2011) discuss some of the literature bearing on the functional and phylogenetic implications of features of wood anatomy, an area where debate remains lively.

For a summary of some ideas about the evolution of angiosperm wood, see Carlquist (2012c). Carlquist (e.g. 1988, 1998b, 1998c) has repeatedly emphasized the linkage between features of wood anatomy and the environment. For this reason, and also because many characters have states whose limits need justification, especially in the context of angiosperm-wide surveys such as this, wood anatomical features must be interpreted with caution (for wood anatomy and cladistic characters, see Herendeen & Miller 2000; Rosell et al. 2007). Indeed, Olson et al. (2011, see also Olson & Rosell 2012) note that thinking of anatomical features as being linked directly to the environment may skew our perspective; features such as vessel diameter may be more immediately connected to e.g. plant height, rather than being selected for independently. However, I have been cautiously adding some features of wood anatomy to the characterizations.

Gross Root Morphology. There is a considerable amount of variation in fine details of root morphology. For instance, roots may be aggregated and form cluster roots, as in many Proteaceae and a few other groups (Shane & Lambers 2005); plants with cluster roots are generally not mycorrhizal (see above). Baylis (1975) described the stout (over 0.5 mm across) and often almost hairless endomycorrhizal roots that he noted were common in magnoliid families in particular, and at the other extreme are the hair roots common in Ericaceae that are barely wider than a root hair (their vascular tissue may consist of a vessel, a sieve tube and a companion cell). However, there is no general survey of fine root morphology/anatomy, although Comas et al. (2012) note the reduction of fine root diameter in angiosperms. The apical meristems of the roots of some monocots, especially those like Pandanus with aerial roots (but see also Rhizophoraceae?) may be very large (Gill & Tomlinson 1975), but I know of no surveys of root meristem size.

In some plants, especially Cactaceae and Proteaceae, the apical meristems of cluster or other ephemeral roots, or even the radicle, constitutively abort (Shishkova et al. 2008, 2013). In the nitrogen-fixing clade there are nodules with a variety of morphologies (see e.g. Corby 1988; Gualtieri & Bisseling 2000; Vessey et al. 2004); N-fixing taxa may also form root clusters of varying morphologies (Lambers et al. 2006, 2012b). Vegetative buds may sometimes develop on roots (Peterson 1975); plants that can do this may be pernicious weeds...

Mention is often made in the literature, especially in that dealing with monocots, of adventitious roots, which implies a rather haphazard and contingent origin. However, in such plants the radicle is often at best poorly developed, and the development of further roots from the stem, usually at or immediately below the nodes, is normal; the use of the qualifier "adventitious" is to be discouraged (see Mangin 1882 for a survey; Barlow 1986; Groff & Kaplan 1988). Aerial roots are quite common, and often help in the attachment of climbers to their hosts, or in support, but they may also be thorny and have a variety of other functions (see Gill & Tomlinson 1975 for a survey).

For a general survey of the anatomy of primary roots, see von Guttenberg (1968).

Root apical meristem. Details of the organization of the root apical meristem are known for relatively few plants, but whether or not the tiers of initials are closed, i.e. are clonally distinct, open, with the fate of the derivatives of the apical cells not being immediately obvious, or intermediate-open, with some more or less intermediate condition, may be of systematic significance (Groot et al. 2004). The character has been placed on the tree, as much to draw attention to it as anything else; monocots are notably variable. Heimsch and Seago (2008) provide a recent summary of the information about root meristems; patterns of development are difficult to interpret (see also Charbonnier & Vallade 2011). In broad-leaved angiosperms, the root cap is made up of gravity-sensing columella and peripheral root cap cells. Cells of the outer layers of the root cap, the border cells, finally become detached from the cap, although they may remain attached because of mucilage secreted by columella cells. These cells detach either individually, the common condition, or in rows, as in Brassicaceae (Driouich et al. 2006), although sampling of this feature is very poor.

Root epidermis development. Whether or not the epidermis of the root develops from the proto-epidermal layer that makes up the inner layer of the root cap or from the outer layer of the cortex varies at about the same level as root hair development (Clowes 2000). The inner layer of the root cap is lost completely in monocots (and Nymphaeaceae), the epidermis then developing from the cortex, although the inner layer of the root cap remains attached in broad-leaved angiosperms (van Tieghem & Douliot 1888). Monocots - in particular, perhaps, although close to angiosperms-as-a-whole (Damus et al. 1997) - may have distinctively-thickened cells in the exodermis (see also below: root hair development), and there the development of a velamen is quite widespread, if sporadic (von Guttenberg 1968 for literature).

Root hair development normally occurs from epidermal cells that are just like cells that do not have hairs, that is, there are no distinctive trichoblasts. However, in Arabidopsis and relatives hairs develop at the proximal ends of distinctive trichoblast cells (Schiefelbein et al. 1997), the trichoblasts developing from epidermal cells that are situated above the radial walls of cortical cells; these trichoblasts are in vertical files (Pemberton et al. 2001; Dolan & Costa 2001).

Root hair development in monocots differs substantially from that of most other flowering plants. In monocots trichoblasts, large, densely staining cells that give rise to root hairs, alternate with their sister cells, the smaller atrichoblasts, and both of these cells are differentiated from other epidermal cells. Trichoblasts are usually the proximal cell of the trichoblast/atrichoblast pair (i.e. they are nearer the root apex), and these pairs occur in vertical files, although there is infrafamilial variation in this proximal position (e.g. Poaceae, Hydrocharitaceae: check). Within grasses, whether or not the division resulting in the trichoblast/atrichoblast pair is asymmetric or not, and, if it is symmetric, whether or not subsequent development of the two cells is equal, both vary (Kim & Dolan 2011 and references). In some monocots, especially those with a velamen, hypodermal cells may also be dimorphic (e.g. Kauff et al. 2000), and root hairs may develop from these cells and push up through the overlying cells. There seems to be a relationship between the development of these cutinized root hairs from outer cortical cells and the absence of secondary growth in the root (Pinkerton 1936); there is usually no secondary growth in monocot roots (see Carlquist 2012a for the odd exception).

Root hairs are found in most species, although not often in myco-heterotrophic plants (von Guttenberg 1968) and aquatic plants. The roots of some plants may be clothed in exceptionally long and dense root hairs, and the result is what are called dauciform roots (Shane et al. 2005). Such features are of both systematic and physio-ecological interest (see also Lambers et al. 2006; Shishkova et al. 2008; Brundrett 2008, 2009). In experimental conditions, at least, long and dense (more cortical cells, smaller epidermal cells) root hairs develop when iron and phosphorous are in low supply (Ma et al. 2001; López-Bucio et al. 2003). Note that some fungi associated with plants can stimulate root hair development by the production of auxin-like compounds (Contreras-Cornejo et al. 2009). Furthermore, species of Kobresia may have dauciform roots as well as form ectomycorrhizal and perhaps other fungal associations (Gao & Yang 2010 and references; see also above under mycorrhizae.

In a number of monocots in particular, ?mostly grasses, there are prominent rhizosheaths. These are made up of mucilage from root cap cells, root cap cells, soil particles, bacteria, etc., all anchored to root hairs and surrounding the root; the rhizosheath may occupy a volume up to 16 times greater than that of the root (McCulley 1995).

Root stele. The stele or vascular tissue in the root is central, and the xylem forms a solid mass, although it is sometimes medullated, perhaps especially in monocots. However, the root stele of a number of broad-leaved angiosperms, e.g. Mimusops (Sapotaceae) and the primary roots of Clusiaceae and Dipterocarpaceae is medullated, while that of some monocots, e.g. sapromycotrophic taxa, some Alismatales, Sisyrynchium, etc., is not medullated (van Tieghem & Douliot 1888; von Guttenberg 1968). The proportion of the root occupied by the stele varies considerably, and in a small study it was found to occupy 20-48% of the area in carnivorous plants (and was sometimes medullated), usually rather less than 34% in other plants (Adamec et al. 2006). Tracheids, and sometimes also phloem, are to be found scattered in the pith in some monocots (von Guttenberg 1968).

In broad-leaved angiosperms there are commonly two to five xylem poles (thus they are di- to pentarch) alternating with phloem poles. Diarch and tetrarch, etc., taxa commonly occur in the same family, but some larger groups (e.g. Rosales, possibly Brassicales) are overwhelmingly diarch. Lateral roots arise on the xylem radii except when the roots are diarch, and then they arise on either side of the xylem poles, but in Pittosporaceae and their relatives origination in this distinctive position is found in taxa that are other than diarch (van Tieghem & Douliot 1888; von Guttenberg 1968). Monocots are more often polyarch (even the primary roots are not diarch), and in a number - but not all - of Poales the lateral roots arise opposite the phloem poles (van Tieghem & Douliot 1888). However, there is substantial intra-individual variation in the number of xylem poles, especially in lateral roots, with increases and decreases occuring along the length of the one root (Torrey & Walllace 1975).

Shoot apical meristem. Hagemann (1967), Kaplan and Cooke (1997) and Bowman and Eshed (2000) discuss the basic organization of the apical meristem. In angiosperms the apex of the stem is covered by layers of cells, the tunica, in which cell division is predominantly in an anticlinal direction. The tunica surrounds the corpus, a central mass of cells in which the plane of cell division is not so restrained. This construction pattern is responsible for the distinctive variegation patterns in many taxa (e.g. Tilney-Basset 1986). Tunica-corpus construction may be a synapomorphy for angiosperms and a parallelism with Araucaria and Gnetales (Johnson 1951; Fagerlind 1954; Pohlheim 1971; also Gifford 1954 for angiosperms; Evert 2006 for gymnosperm meristems). Although details of organization of the shoot apical meristem are known for relatively few plants, the numbers of corpus layers may perhaps be of some systematic interest (Bowman & Eshed 2000). Tissues in monocot leaves often come from three types of cells (Stewart & Dermen 1979), but a 1-layered tunica is somewhat more common there than in other angiosperms. The tunica may be up to four cell layers thick (Gifford 1950;Brown et al. 1957; Jouannic et al. 2011 for literature and information).

There is considerable variation in the size of apical meristems, and stem meristems of Cactaceae seem substantially wider than those of other angiosperms: 400-1500 µm across in cacti, versus often less than 325 µm across, although up to 528 µm in Phoenix canariensis (but lepidocaryoid palms have slender stems and small apices) and almost as big in Nymphaeaceae. Within both polysporangiates and gymnosperms there is also considerable variation in meristem size, and in the gymnosperms the shoot apices of Cycadales are notably larger than the rest - 500-3,300 µm across, versus <400 µm (Gifford 1954; Clowes 1961; also references in Gifford & Corson 1971; Jouannic et al. 2011). Pachycaul plants in general have wide meristems (see also Staff 1968). I do not know of any recent surveys of meristem size.

In the primary stem vascular system there can be separate bundles (an eusetele), a (pseudo)siphonostele, with the vascular tissue forming an apparently complete cylinder, or a complete cylinder. However, Benzing (1967b) suggests that there is no sharp difference between siphonosteles and eusteles in angiosperms, moreover, the use of such terms may be inappropriate when describing the vascular system there (Benzing 1967a; Namboodiri & Beck 1968c; Howard 1979a). The angiosperm primary vascular system can often be interpreted as a series of sympodially-branching bundles, and this reflects the initial development of the vascular system; the stimulus for its initiation is basipetal auxin movement from the apex of the primordium, so finally linking up with existing stele (). Beck et al. (1982) suggested that there is a correlation in broad-leaved angiosperms between closed primary stelar patterns (with anastomoses between sympodia) and distichous or opposite phyllotaxy and between open patterns (the sympodia are separate) and spiral phyllotaxis; within-family variation in details of stelar construction may be quite extensive (Jensen 1968). Note that interpretation of the primary vasculature in terms of axial or foliar theories yields very different results (Al-Turki et al. 2003) - and of course the theories suggest very different pathways for the evolution of the plant body. See Schmid (1982; also Namboodiri & Beck 1968a, b; Beck et al. 1982) for a discussion of stelar variation and terminology in both angiosperms and gymnosperms. See also below for nodal anatomy.

Cortical and medullary bundles, vascular bundles independent of leaf traces that run in the cortex and pith respectively of broad-leaved angiosperms, are mentioned only when they occur, see Col (1904) for an early discussion and summary of information. They can be confused with especially early diverging vascular traces, as in Hasseltia (Salicaceae).

In monocot stems the vascular bundles are usually scattered, and I mention their arrangement only when they are in rings.

In general, cauline vascular bundles are collateral, with xylem to the center of the stem and phloem to the outside. Variants of this are interesting, and are mentioned when they occur; this variation is often reflected in the general arrangement of tissue types in the vascular bundles of the petiole and midrib. In monocot rhizomes in particular, but not in the annual stems, the scattered bundles are frequently amphivasal, i.e., they consist of phloem entirely surrounded by xylem (Jeffrey 1917; Arber 1925).

Details of the initiation of endodermis and pericycle, etc. differ across seed plants (Stewart & Tomescu 2009), but the systematic significance of this variation is unclear.

The endodermis consists of one or a few layers of cells that surrounds the central stele and sometimes also vascular tissue elsewhere. In the root the endodermis is often marked by a single layer of cells with Casparian bands, but such clearly-developed endodermes are uncommon in above-ground stems and even more so in the leaf. However, it may occur there, perhaps especially in herbaceous taxa, although Bonnetia (Bonnetiaceae), woody, also has a foliar endodermis (see Gutenberg 1943; Metcalf & Chalk 1979; Lersten 1997 for references). In the stem a ring of starch-containing cells (the starch sheath) may be found in this endodermal position, although casparian bands may develop when the stem is placed underground (Van Fleet 1961). Details of the distribution and nature of cauline and foliar endodermes in particular may be of systematic significance, see also Alseuosmiaceae, etc.

The pericycle is the outermost part of the stele and is made up of a single layer of cells. In the roots of at least some angiosperms, this layer early differentiates into cells that can subsequently divide and initiate lateral roots and those that cannot (Parizot et al. 2008). There are often lignified fibers immediately external/peripheral to the phloem in the stem, the so-called pericyclic sheath. This sheath is sometimes absent, or it may be made up of sclereids. Gibson (1993) discussed the need to distinguish between fibers that are derived from phloic tissue and those that are extra-phloic in origin (see also Blyth 1958), indeed, the stem endodermis is absent in gymnosperms and woody angiosperms, so recognizing a pericycle becomes even harder. Although simple presence/absence and nature (if present) of this sclerified sheath may be of systematic interest, as in Schlegliaceae, Dipsacales, etc., distinguishing between its different origins may also be of value.

Unlignified cell wall fluorescence is caused by the presence of ferulic and/or coumaric acids. Unlignified walls of most angiosperms do not fluoresce, and only those taxa with fluorescence are mentioned (data largely from Hartley & Harris 1981). Other information on the composition of primary cell walls, especially in monocots, is given by Smith and Harris (1999) and Harris (2000).

Iqbal (1995) and Spicer and Groover (2010) provide an entry into the literature on plant cambia, or lateral meristems (secondary thickening meristems), and the cells that differentiate from them. Hagemann and Gleissberg (1996) discuss the difference between marginal blastozones in angiosperm leaves and meristems. There are two main kinds of lateral meristems or cambia, cork cambia and vascular cambia.

The products of cork cambium (or phellogen), are cork or phellem to the outside and a little phelloderm to the inside; together the three make up the periderm. There is variation in the tissues produced as the cork cambium differentiates, when the cambium is first produced (see e.g. Möller 1882; Esau 1965; Edwards & Donoghue 2006), and, perhaps most importantly from a systematic point of view (Weiss 1890), where it is first initiated. Cork cambium occurs widely in broad-leaved angiosperms and in gymnosperms. In the stem it tends to be either superficial, the common condition in angiosperms, being initiated at or immediately below the epidermis (I have not distinguished between these positions), or deep-seated, being initiated deep in the cortex, inside the pericycle, or even in the phloem (for still invaluable surveys, see Möller 1882 [much information on gymnosperms]; Douliot 1889, also Kuhla 1987; Waisel 1995; etc.). Initiation in the cortex is also quite common and there is of course no absolute distinction to be made between the superficial and deep-seated positions. Czaja (1934) discusses the cork of several taxa that have cork wings on the young stem, although such variation is not of systematic significance at this level. A polyderm is a distinctive cambial derivative that is rather infrequently found, but whose distribution often seems to be of systematic significance (Mylius 1913 for a survey); the cambial cells cut off alternating layers of cork and endodermal cells.

In broad-leaved angiosperms, cork cambium position in the stem and root of the same plant commonly differs, the cork cambium in the roots usually being deep-seated (see Peterson 1975; Waisel & Liphschitz 1975; Esau 1977; Fahn 1990). However, in plants with aerial roots of various kinds the cork cambium may be superficial (von Guttenberg 1968); thus Clusieae, alone of Clusiaceae, are often epiphytic and have superficial cork cambium in their roots, but the cork cambium is deep seated in Clusiella, a Clusia look-alike that recent work has placed in Calophyllaceae. However, detailed information on the initiation of cork cambium in the roots is hard to come by.

The cork cambium in the stem of monocots is also usually superficial, although records are few (Thompson 1976); of course, the aerial stems of many monocots are more or less short-lived and lack any secondary thickening at all (see below). In monocots the cork cambium in the root, when developed, is usually to be found just under the exodermis, i.e. in a rather superficial position (Philipp 1923; Arber 1925; Tomlinson et al. 2011); again, many monocot roots are quite short-lived, so the function of any cork cambium is not obvious. Etagenkork, suberised cells that are not produced by a cork cambium, are also to be found in some monocots.

The vascular cambium is the other main type of lateral meristem. In extant vascular plants other than lignophytes, a vascular cambium is found only in some Ophioglossaceae, although unifacial cambia are known from a few other taxa (Spicer & Groover 2010). In angiosperms, whether or not a vascular cambium develops, and the nature of its products, are both of considerable interest. Vascular bundles in which cambium does not develop are described as being closed; if a cambium develops, normally at the interface between the phloem and xylem, they are open.

Climbers in particular, especially lianas, often show distinctive growth with anomalous patterns of secondary thickening, the number of cambia, their position, and the nature of the tissue they produce, varying (e.g. Obaton 1960; Carlquist 1991b; Caballé 1993; Rowe & Speck 2005; Angyalossy et al. 2012). Carlquist (2004, see also 2007b, 2013) studied the secondary tissue of Nyctaginaceae in detail, and suggested that there, at least, the use of the term "included phloem" was inappropriate; several taxa that had been described as having included phloem in fact have successive cambia. In plants with such cambia, a so-called master cambium produces conjunctive tissue adaxially. In this tissue new vascular cambia develop producing phloem externally and xylem internally. Each successive cambium and its products are surrounded by a narrow layer of conjunctive tissue, hence the phloem is not completely included or enclosed by xylem tissue (see also Carlquist 2010). Successive cambia are common in climbing Caryophyllales, but they are also found even in non-climbing members such as Phytolaccaceae. Robert et al. (2011) note that in such cambia, often found in plants that are under some kind of water stress, both xylem and phloem are organized in a three-dimensional network. See Feild et al. (2012 and references) for more functional/biomechanical aspects of liane anatomy, also above.

In this site the term interxylary phloem is used to describe the situation when phloem islands cut off internally by a vascular cambium are completely surrounded by xylem cut off by that same cambium (see Carlquist 2013 for a list of taxa with this), and internal phloem (= intraxylary phloem) the situation where phloem is found internally to the xylem in the primary stem (this latter condition is commonly associated with the presence of bicollateral vascular bundles in the leaves). The terms "interxylary phloem" and "intraxylary phloem" are confusing and should not normally be used.

For primary thickening/primary thickening meristems/sustained primary growth of the stem in particular, see Boke (1954), Waterhouse and Quinn (1978), Stevenson (1980), etc. In broad-leaved angiosperms - primarily herbaceous plants, annuals and perennials - increase in width of the stem towards the base may be by expansion of cortical or medullary tissue, whether or not also in association with secondary growth (Troll & Rauh 1950); secondary growth can more or less mask this expansion. Monocots (?all) have a primary thickening meristem (Rudall 1991a for a summary), perhaps located in the pericycle-endodermis area (de Menezes et al. 2005). Details of its origin and the tissues to which it gives rise vary; the endodermis may produce radial files of cortical cells, while procambial strands are of pericyclic origin. However, de Menezes et al. (2011) have suggested that there was in fact no distinct primary thickening meristem in monocots; this may bear on the nature of monocot secondary thickening (see above).

A normal vascular cambium is absent in monocots, although there may be traces of cambial activity in the bundles (Stant 1970 and references). In some monocots a meristem develops that cuts off tissue to the inside; separate vascular bundles embedded in ground tissue differentiate in this tissue. This type of secondary thickening is scattered in Asparagales (Rudall 1995b for records and literature) and has also been reported from Eriocaulaceae (Poales: Scatena et al. 2005), and it was compared with the primary thickening meristem of cycads, although development in the first is primatily centripetal and in the second, centrifugal (Stevenson 1980). Vascular cambium in monocot roots is extremely uncommon, although it is reported from Dracaeana (Asparagaceae-Nolinoideae), but not in other monocots with secondary thickening in the stem (Arber 1925; Carlquist 2012).

A number of taxa are secondarily woody. Secondary woodiness is sporadic in origin, sometimes being connected with the insular habitat, and paedomorphosis may also be involved. It can usually be recognized by plotting length-on-age curves for the vessel elements. If these curves are flat or decrease, then secondary woodiness is likely, but if they gradually increase, then woodiness is probably primary (see Carlquist 2009 and references; Dulin & Kirchoff 2010). In addition, ray cells (see below) are predominantly upright, not horizontal.

Reaction wood. The amount and to a certain extent the anatomy of the xylem produced at the branch-stem junction - called the reaction wood - varies, although in some taxa it may not be produced at all. Although it is often suggested that angiosperms and gymnosperms differ in the nature of their reaction wood, angiosperms producing cellulose-rich tension wood on the adaxial side of the branch and gymnosperms lignin-rich compression wood on the abaxial side, a summary of the information available for angiosperms (Höster & Liese 1966; see also Fisher & Stevenson 1981; Aiso et al. 2013) suggests that this is a gross oversimplification (see also Westing 1965, 1968 and Timell 1986 for gymnosperms). Tension wood cells also have gelatinous fibers immediately internal to the cell wall. These fibres contain pectic mucilages and arabinogalactan proteins and may generate the active contraction force of such wood (Bowling & Vaughan 2008), and they are also found in tendrils and in the stems of twining climbers (Bowling & Vaughn 2009).

Data on cambium storying are taken mostly from Carlquist (1988b); if not mentioned, the cambium is unstoried. One or both the kinds of cambial initials (ray, fusiform) may be storied, but only rarely are ray initials alone storied, as perhaps in Lauraceae (Paul van Rijckevorsel [pers. comm.] noted problems with this character).

There is a vast literature on tracheary (vessels and tracheids) morphology, especially the nature of scalariform perforation plates of vessels (e.g. the number of bars in the plates), the width of vessels and tracheids, the nature of their pitting, etc., although there is surprisingly little on vessel length (Jacobsen et al. 2012). The nature of the vessel perforations and other elements of tracheary morphology were treated as being of very great phylogenetic importance throughout much of the twentieth century, variation in individual features being described as evolutionary "trends" and similarities in tracheary tissues being particularly important when determining relationships (e.g. Bailey & Tupper 1918; Bailey 1944; Cheadle 1944; Cheadle & Tucker 1961). The trends were supposed to proceed tracheids only -> scalariform perforation plates with many -> few bars -> simple perforation plates; the cells also became shorter and wider and the end wall less oblique, etc. (e.g. Tippo 1938; Bailey 1944, 1954). I have not tried to fit all the details of variation in vessel and tracheid morphology to the trees. Certainly the evolutionary significance of this variation may be considerably less than was thought, thus Olson et al. (2012, 2013) noted that vessel diameter was strongly linked with stem diameter. However, the Baileyan trends are more or less evident in the fossil record (Wheeler & Baas 1991). Herendeen et al. (1999b) noted that there was polymorphism in perforation type (scalariform/simple) in no fewer than 54 families of broad-leaved angiosperms, although it was uncommon in five of these.

Note that whether plants like Amborella and Trochodendrales have vessels is unclear; it opartly depends of the definition of vessels, and also of "having vessels". Hetero-mycotrophic monocots lack vessels, and this is clearly a secondary absence (Cronquist 2012b). The distribution of tracheids in protoxylem (common) and metaxylem (much less common) in broad-leaved angiosperms is detailed by Bierhorst and Zamora (1965).

Pit membrane remnants are turning out to be quite common in broad-leaved angiosperms (e.g. Aextoxicaceae, Bruniaceae, Hydrangeaceae, families near Ericaceae, Schisandraceae, Quintiniaceae, Rousseaceae), and in monocots, but the functional and systematic significance of this feature is unclear (e.g. see Schneider & Carlquist 2003, 2004a; Carlquist & Schneider 2004). Indeed, the distinction between vessels and tracheids is not always that sharp (e.g. Feild et al. 2000b; Hacke et al. 2007; Carlquist & Schneider 2009; Carlquist 2012a), fibrils across the plate being closer or more distant and breakdown more or less evident. Similarly, whether pits have tori may not always be easy to recognize (Rabaey et al. 2006; for the functional significance of tori, see Pittermann et al. 2010).

For information on the nature of the vessel element perforation plates in broad-leaved angiosperms, see Bierhorst and Zamora (1965), for those in monocots, see Wagner (1977, sampling needs to be extended/newer literature integrated) and Carlquist (2012). There has been discussion whether vessels in monocots and those in other angiosperms arose independently (e.g. Cheadle 1942; Cheadle 1953; c.f. Carlquist 2012a), and given the morphology of vessels in Nymphaeales (Carlquist & Schneider 2009), perhaps the same question may be asked of broad-leaved angiosperms - or perhaps the question as phrased, or the implications behind it, are really not that important. The distribution of vessels in the monocot plant body, whether in the stems, roots, etc., may be of systematic interest (Cheadle 1944 and references; Wagner 1977; but see Carlquist 2012a).

Some information is included about the presence of vascular tracheids and wood fibers, and the presence and distribution of xylem parenchyma (see Hess 1950), but these features are neither treated consistently nor mentioned for all families.

Pits. Vascular pits are in general quite variable in morphology and arrangement, although the distinction between some of the pit "types", such as bordered and non-bordered pits is arbitrary. It is thus hardly surprising that Herendeen et al. (1999b) noted that bordered pit presence/absence varies in some 45 families of broad-leaved angiosperms. The nature of intervascular pitting may be of systematic interest, but I have not included many details of this character. Hacke et al. (2004) describe how the torus-margo pit membranes of gymnosperms function; their absence may be an angiosperm apomorphy (see also Sperry & Hacke 2004). However, a torus, sometimes lignified, occurs occasionally in angiosperms (e.g. Coleman et al. 2004), and its distribution there may be of systematic interest. Vestured pits have close and minute sculpturing of the surface of the cell wall in the pit, and their distribution is of systematic interest (e.g. Jansen et al. 1998, 2001). Nearly all taxa with vestured pits - perhaps ca 30% of all woody flowering plants and ca 50% of woody species in tropical lowland forests - have vessels with simple perforation plates, and vestured pits may promote the functioning of these vessels (Jansen et al. 2003, 2004b; Baas et al. 2003). Jansen et al. (2004b) noted that vestured pits were most likely to be found in plants growing in deserts or tropical seasonal woodlands. Scalariform perforation plates are most frequently found in taxa growing in cooler climates (Jansen et al. 2004b: context?). Carlquist (2010) also discussed how vestured pits might function.

Wood fluorescence. Data are taken largely from a survey of some 10,600 species summarized in Avella et al. (1988). I am unclear as to the significance of this character.

Details of vascular ray "types" are rarely mentioned, partly because it is difficult to reconcile the definitions of the terms as they have been used over the years (see Kribs 1935, 1959), partly because of the typology involved, and partly because it can be difficult even to define what a ray is (Carlquist 2003). Systematically interesting information in this feature is probably best recorded in descriptive terms, i.e., describing the morphology of the cells involved, the width of the rays, etc.; the short discussion by Chalk (1983) is particularly useful. Particularly distinctive rays are found in some Malvaceae (e.g. Chattaway 1933a, b). Ray width in both xylem and phloem may vary considerably. Broad phloem and xylem rays are a valuable field character for identifying families, and when the phloem rays are wide, tangential cuts of the phloem show a net-like arrangement of the paler-coloured, anastomosing rays (Keller 1996). More precise indication of ray width can provide systematically interesting information (see Herendeen et al. 1999b for some "basal" angiosperms and relatives).

Phloem. For a good survey of phloem micromorphology, etc., see papers in Behnke and Sjolund (1990). In gymnosperms sieve cells are involved in carbohydrate transfer. These cells are at least sometimes notably long (Jensen et al. 2012) and nucleated, although the nucleus degenerates and becomes pycnotic. The sieve pores are distinctive. They are narrow, and are traversed by endoplasmic reticulum (ER), and they join to form a cavity in the region of the middle lamella (e.g. Behnke 1990a; Iqbal 1995). These sieve cells are associated with Strasburger cells (albuminous cells) which, although closely linked functionally with the sieve cell, are not formed from the same mother cell. In angiosperms sieve tubes carry out the same function as sieve cells; they have rather wider pores that lack ER and the mature cells lack nuclei (the nucleus usually becomes chromalytic and disappears). Sieve tubes are usually closely associated with nucleated companion cells that are derived from the same immediate mother cell (see Behnke 1986 for literature and definitions; Botha 2013). For microfilament-rich peripheral phloem cells, perhaps restricted to extant gymnosperms, see Pesacreta (2009).

An important set of characters is found in the structure and composition of sieve tube plastids. Data on the ultrastructural morphology of these plastids, in particular, their starch and/or proteinaceous inclusions, are taken from the work of Behnke (e.g. 1969, 1981b, 1989, 1990a, 1994a, 2001; summaries in Benhke 1972, 1974, 1975, 1981a, 1981c, 1991a, 2000). Angiosperm plastids usually include starch grains alone, and this is the primitive condition for the clade. However, in very nearly all monocots the plastid inclusions are cuneate protein crystals alone while in core Caryophyllales there are peripheral protein fibres; Pistia (Araceae) is the only monocot known to have starch-containing plastids (Behnke 1995). There are many other less striking variants with various combinations of starch and protein, and these may characterize smaller clades such as [Erythroxylaceae + Rhizophoraceae] (c.f. Behnke 1988b), whilst the absence of both starch and protein is common in parasitic groups, and also in Rosales, [Malpighiaceae + Elatinaceae], etc. The sizes of the starch grains and fine details of the protein crystals in the plastids may provide still more evidence of relationships, although I have not always included this information. All told, this character complex is of considerable systematic significance, yet the function of these plastids, and so the evolutionary significance of the variation they show, is unclear (Tratt et al. 2009).

P-proteins are proteins in mature sieve elements of angiosperms that vary in origin (the come from the nucleus or elsewhere) and appearance (aggregated [non-dispersed] or not, shape of aggregations, fibrillar or tubular) and also behaviour, e.g. changing their morphology when the turgor of the sieve tube changes, as in Fabaceae-Faboideae (Knoblauch et al. 2001; Peters et al. 2008, 2010; Knoblauch & van Bel 1998). Information on this character, varying mostly in broad-leaved angiosperms, was obtained largely from Behnke (1981a, 1991b); P-proteins are absent from non-angiosperms and at least some monocots, e.g. Poaceae, but they are present in e.g. Iridaceae (Evert et al. 1973; Tóth & Sjölund 1994; Sabnis & Sabnis 1995). Callose is also deposited very quickly over the pores of sieve plates when phloem is damaged (Mullendore et al. 2010: Parre & Geitmann 2005: mechanical properties of callose), and both callose deposition and protein bodies that can reverse their shape (e.g. Peters et al. 2008, 2010) may be involved in the plugging of sieve plate pores. How the pores are plugged may depend on whether the phloem is exposed to bright light or there is mechanical damage (Knoblauch & van Bel 1999). Gymnosperms lack P-proteins, and there the pores may be plugged by the swelling of the ER that traverses them (e.g. Shulz 1992). However, the role of protein agglomerations in modulating phloem flow is unclear; they do not seem to affect it in Arabidopsis thaliana, at least (Froelich et al. 2012). All in all, sieve tube flow is poo rly understood (Jensen et al. 2012).

There is little variation in other aspects of sieve tube morphology that is easily usable at higher levels. Sometimes sieve tubes or sieve cells have substantially thickened, lamellate and nacreous secondary walls; these seem to be sporadically distributed, although within gymnosperms they may be restricted to Pinaceae (see Behnke 1990b: cycads, etc.; Schulz 1990b: conifers; Evert 1990b: "dicots"; Eletheriou 1990b: monocots). Zahur (1956) described substantial variation in many characters, albeit it seems to be overlapping (Iqbal & Zahur 1995 list trends of specialization). Zahur (1956) found a weak correlation between presence of secondary septae and sympetalous families, but his data show variation within orders. Turgeon et al. (2001; see also Gamalei 1991) summarise variation in companion cell anatomy and delimit a number of "types" in the minor veins of leaves. Type I or open phloem probably has symplastic connections between bundle sheath and phloem, there being 10-100 plasmodesmata/mm2 between bundle sheath and companion cells, while Type II or closed phloem probably has apoplastic connections, there being only <10 plasmodesmata/mm2 (see also Batashev et al. 2013).

Recent work suggests that there is unexpected variation in phloem tissue that is connected to differentiation of function within the phloem. For example, within commelinid monocots, and especially Poales, some sieve tubes lack companion cells, are notably thick-walled, and seem to be involved in short distance transport of not very concentrated sugars (Botha 2013). The phloem system in Cucurbitaceae is very complex. Fischer (1884) early noted that those Cucurbitaceae that had bicollateral vascular bundles also have extrafascicular phloem (EFP) strands in the cortex outside the sclerenchymatous ring. The sieve tubes of the EFP system differ in morphology from those of the fascicular phloem, although they may be similar to cells in the peripheral part of the latter (Crafts 1932). The composition of EFP and fascicular phloem exudate is very different: Fascicular phloem exudate is rich in sugars and unidentified proteins, etc., EFP exudate contains P-proteins, amino acids, protein synthesizing machinery, and various secondary metabolites, but little sugar (Zhang et al. 2010). The EFP system is involved more in plant defence, and Gaupels et al. (2012) even thought that ecologically EFP exudate was like latex (see also Tallamy 1985; Konno 2011; Gaupels & Ghirado 2013). In both these systems aphids are able to distinguish between sieve tubes that have more concentrated sugars and those that do not.

There is interesting variation in how sugars are translocated within the plant that is linked both with details of phloem anatomy and with phsyiology. Intermediary cells in phloem tissue are characterized by having numerous plasmodesmata that branch in the outer part of the walls adjacent to the bundle sheath cells. There seems to be a correlation between the presence of intermediary cells and the presence of raffinose and stachyose in the translocate; sucrose is the most common form in which carbohydrates are translocated. However, whether or not such characters are more or less constant within families is not obvious (see Lamiales), and the link between type of carbohydrate translocated and details of phloem anatomy is not entirely clear (see also Goggin et al. 2001; Turgeon & Ayre 2005). However, there are interesting correlations between how sugars move into the phloem, plant habit, and climate (see e.g. Rennie & Turgeon 2009; Turgeon 2010b; Fu et al. 2011; Davidson et al. 2011, also the Garryales page). Unfortunately, how sugars move into the phloem in gymnosperms is unknown (Liesche et al. 2011), and I do not know how sugars are transported in monocots. Zimmermann and Ziegler (1975) list sugars and sugar alcohols found in exudates from sieve tubes in broad-leaved angiosperms; the transport of raffinose family oligosaccharides is involved in a particularly distinctive sugar tranport mechanism.

Stratified phloem, secondary phloem in which there are bands of fibres alternating with ordinary phloem tissue, is well developed in groups like Malvales, Annonaceae, etc. It is easy to recognize using a hand lens, or even with the naked eye, in phloroglucinol-stained hand sections. Plants with such phloem typically have bark that can be pulled off in long strips and which is often used for making paper-type products.

Transfer cells, metabolically very active cells with more or less labyrinthine intrusions of the walls, occur in various parts of the plant (Gunning et al. 1970; Pate & Gunning 1972), e.g. the heads of the glandular hairs in insectivorous plants, associated with phloem in vascular bundles (they are one type of companion cell), especially in the xylem and at the nodes, and in seeds (see below).

The stem, node and leaf are part of a continuum (see especially Howard 1974, 1979a), and to understand nodal anatomy serial sections of the stem, leaf base, and petiole should be examined together. For information about nodal anatomy see especially Sinnott (1914), Dormer (1946), Marsden and Bailey (1955), Bailey (1956), Balfour and Philipson (1962), Cutler and Gregory (1998), Howard (1970, 1974), Beck et al. (1982), and Metcalfe (1987). Note that the behavior of protoxylem strands in the young stem may not correlate with node type (e.g. Beck 1962; Kumari 1963; Benzing 1967a, b; Gibson 1994), and treating flowering plants as if they had a modified siphonostele (see above) may obscure information (Keating 2000). In particular, although I refer to "leaf gaps" in these pages, Beck et al. (1982) and Namboodiri and Beck (1968c) in particular argue that this is inappropriate when talking about the steles of seed plants given the basic sympodial construction of the primary vascular system. However, when looking at nodal anatomy in stems with some secondary thickening, it is impossible to see that the ring of vascular tissue originally consisted of sympodia, the separate bundles going to the leaf originally being traces from these sympodia. In the descriptions I use formulae like 1:1, 5:5, etc.; the first number is the number of gaps, the second is the number of traces or separate vascular bundles leaving the gaps as seen in cross sections at or near the nodal region. These gaps are often recognizable as interruptions in the vascular cylinder formed by the early stages of secondary thickening. Split laterals occur in some taxa with opposite leaves and are single traces that send branches to both leaves (e.g. Howard 1970). They are designated by formulae like "1:1 + split laterals" in the characterizations; this means that each leaf has a three bundles entering the base, one from the central bundle (the "1:1" part), and one from each of the split laterals. Related flank-bridges and variants are found in some Dipsacales and Rubiaceae (e.g. Neubauer 1982), etc.

The basic nodal condition for seed plants as a whole may be 1:1, although some have argued for 1:2 (Kumari 1963; Namboodiri & Beck 1968c). Gymnosperm nodal anatomy is also described in terms of gaps and traces (e.g. Namboodiri & Beck 1968a, b for information), although at the very least the behaviour of the traces can be unexpected from an angiosperm perspective, as with the girdling traces of the foliage leaves in Cycadales. Within Pinales (for example) 1:2 nodes occur only (but not always) in taxa with opposite leaves (Namboodiri & Beck 1968a, b; see also below).

Leaves with stipules usually have trilacunar nodes and often have blades with serrate margins (Sinnott & Bailey 1914). Celastraceae, with their unilacunar nodes, stipules, and more or less serrate blades, seem to be an important exception, however, their stipules can be the most evanescent of structures (see also some Myrtales), while both Perrottetia and Bhesa, recently removed from Celastraceae (and now in Huerteales and Malpighiales respectively), have more complex nodes - and much more obvious stipules, especially in Bhesa. Rosaceae tend to have 3:3 or more complex nodes, and are generally stipulate; the estipulate Spiraea has 1:1 nodes. There is a similar relationship between the normally trilacunar and stipulate Elaeocarpaceae that also include the unilacunar, estipulate Tremandra and its relatives, and also within the small family Surianaceae; I do not know the nodal anatomy of estipulate species of Euphorbia subgenus Esula. Lateral traces of trilacunar nodes often form wing bundles in the petioles, and branches from them may innervate stipules, when present. However, most Rubiaceae, a family characterized by its conspicuous interpetiolar stipules, have unilacunar nodes, but lateral bundles immediately split off and form a vascular ring around the stem, and it is from this ring that the stipules are innervated (e.g. Majumdar & Pal 1958). Finally, broad-leaved angiosperms with sheathing leaf bases and also those with compound leaves usually have multilacunar nodes (Sinnott & Bailey 1914), whether or not they also have stipules. See also below, under stipules.

In aquatic angiosperms like Nymphaeales nodal anatomy is very complex, with a vascular plexus forming at the nodes and the internodal vascular tissue being very distinctive, even if ultimately the vasculature of the leaves can be interpreted in conventional angiospermous terms (c.f. Schneider 1980; Moseley et al. 1984). Although many asterids, especially Lamiales, etc., are commonly reported as having 1:1 nodes, Neubauer (e.g. 1977, 1978) emphasized that there the single trace often divided immediately into three or more (e.g. see Linderniaceae, Scrophulariaceae, also Cordia [Boraginaceae]). Nodal anatomy may repay attention in Gesneriaceae, and perhaps more generally in Lamiales, also in Melastomataceae, Primulaceae, etc..

For the nodal anatomy of cotyledons, see Bailey (1956). Nodal vascularisation of cotyledons and foliage leaves of the one plant may differ (e.g. Stone 1970), but aside fron this there can be quite extensive variation in nodal anatomy even within an individual and especially in the context of heteroblastic leaf development and plants with anisophyllous leaves (see e.g. Post 1958; Howard 1970; Dengler & Donnelly 1987; Dengler et al. 1989) - and this also applies to the primary vascular organization as a whole. Cotyledons often have 1:2 nodal anatomy (Thomas 1907; Bailey 1956), whatever the nodal anatomy of the later leaves; this may be connected with the fact that cotyledons are opposite (c.f. gymnosperms!). Note that there can be quite a lot of variation at the cotyledonary node, too; it may be multilacunar in Juglandaceae, or 4:3 in some Magnoliaceae (with split laterals, e.g. Sugiyama 1976a).

Gross patterns of nodal anatomy are often easy to confirm in the field using a razor blade or sharp knife and a hand lens, and so can help in identification. Thus the 1:1 nodes of Celastraceae clearly differ from the 3:3 nodes common in Malpighiales and with which Celastraceae can otherwise be confused vegetatively.

Monocot leaves usually have entire margins and broad bases into which several bundles proceed, but Sinnott and Bailey (1914) noted that in the petiolate Potamogeton and Smilax there was a tendency for three main bundles to enter the leaf base (see also Colomb 1887). Details of nodal vasculature are not generally recorded for monocots.

Aerenchyma is developed in aquatic plants both in the roots (Seago et al. 2005) and also elsewhere (Jung et al. 2008 for a convenient summary); the mode of formation of the aerenchyma varies.

Various tissues in the plant contain distinctive secretions. Latex is generally found in laticifers, rarely in isolated cells. Laticifers may be unarticulated, branched or unbranched but not anastomosing syncytia that originate from single cells in the embryo. Articulated laticifers, generally associated with the phloem, are often anastomosing tubes that develop from cells whose common walls have broken down. Laticifers in the broad sense contain secretions other than latex in the strict sense (see Hagel et al. 2008 [distribution of laticiferous taxa displayed on a Dahlgrenogram...] and Agrawal & Konno 2009 for summaries).

Taxa like Rutaceae and Myrtaceae have glands, schizogenous cavities often containing distinctive secondary metabolites (see also below). Truly lysigenous glands appear not to occur in plants, reports of such structures seeming to refer to artifacts of preparation (Turner et al. 1998; Turner 1999). Cells containing ethereal oils and those with mucilage are similar in their early development, as in basal angiosperms (Bakker 1992). The main differences between the two is that oil cells often have a suberised layer between cellulose layers and plastids secrete the oil, while mucilage cells lack the suberised layer and mucilage is usually secreted in Golgi vesicles.

Gregory and Baas (1989; see also Dickinson 2000) provide a useful survey of mucilage cells, while Matthews and Endress (2006b) emphasize the distinctive nature of a type of mucilage cell with thickened inner periclinal wall and distinct cytoplasm. They catalogue the distributions of this and of other kinds of mucilage cells.

Sclereids (sclerenchymatous idioblasts) found free in the cortex, the mesophyll of the lamina, or elsewhere are variable in morphology; several sclereid types have been named. Sclereids are mentioned when they are common in a family (Rao 1991 for a survey), although those occuring only in the pith are rarely mentioned. Sclereids intergrade morphologically with fibers, very elongated and unbranched lignified cells. Cells of the tracheidal transfusion tissue in gymnosperm leaves may sometimes look very sclereidal, as in Sciadopitys (Hu & Yao 1981). Distinctive sclereids of various kinds, including tracheoidal cells, may be associated with vein endings; such sclereids are rarely mentioned below because they are of significance at lower levels. Leaf blades with sclereids may be punctate when a light is shone through the leaf, and even fibrous tissue is often evident, either in such transmitted light or in surface view.

Cristarque cells are distinctive cells with U-shaped lignification and with calcium oxalate crystals or druses. They are mentioned only in those taxa from which they have been reported. They often occur in the cortex, whether of the stem or the petiole.

Calcium oxalate may crystallize in distinctive forms such as raphides (needle-like crystals), styloids (narrowly oblong crystals), crystal sand (very small crystals that appear granular), or single rhomboid crystals little longer than broad. Calcium oxalate crystals are usually in the form of druses, irregular aggregations of more or less radially arranged crystals, but then their presence is not mentioned; crystals of any sort are rarely entirely absent. Two or more forms of crystal may occur in the one plant, e.g. druses and raphides occur together in some Araceae. Raphides can sometimes be seen in herbarium material when using a dissecting microscope if the tissue containing them is cut. The raphide sacs containing bundles of raphides are then evident as small white patches, and these may be visible on the cut surface of fresh material as it dries out. Individual raphide crystals vary in details of their morphology, e.g. shape in transverse section (Horner & Wagner 1995), and are especially common in monocots. Not only does the crystal form of calcium oxalate vary, but also the particular tissues in which the crystals accumulate, and the combination of the two can be of systematic interest, as in the Apiaceae-Araliaceae area (Rompel 1895; Burtt 1991; Liu et al. 2006). Many data are taken from Metcalfe and Chalk (1950); Prychid and Rudall (1999, 2000) provide surveys for monocots, Lersten and Horner (2005) discuss styloid morphology and distribution, and Franceschi and Horner (1980) review the subject from a more physiological perspective.

Calcium oxalate may crystallize as whewellite or calcium oxalate monohydrate [CaC2O4.H2O - COM] or weddellite, calcium oxalate dihydrate [CaC2O4.2H2O - COD], the latter being the less common form (Monje & Baran 2002), although I do not know what the general distributions of these forms are (but see Cactaceae). Hartl et al. (2007) suggest that more attention be paid to this variation when discussing crystal morphology. Vacuolar crystal formation associated with membranes and also paracrystalline bodies with widely spaced subunits occur in eudicots, while in monocots there are no membrane complexes and the paracrystalline bodies have closely spaced subunits (Horner & Wagner 1995; Evert 2006).

A few taxa produce soluble, rather than crystalline, oxalate, whether as potasssium oxalate or oxalic acid itself (hence the pleasingly sharp taste of some Polygonaceae and Oxalidaceae).

Some taxa show little or no accumulation of oxalate in any form (Hodgkinson 1977; Zindler-Frank 1976), conversely, in Cactaceae calcium oxalate can represent the bulk of the plant body. Little is known about why oxalate accumulates, or accumulates in one form rather than another. Raphides have certainly been implicated in protection of the plant against herbivores (see Araceae, Onagraceae, etc.), and there may be connections between oxalate metabolism, the type of carbon fixation, the aquatic habit, etc., thus Franceschi and Nakata (2005) suggest that oxalate formation is connected with calcium regulation, plant protection, and metal detoxification.

Cystoliths are moderately common and their morphology and distribution is quite often of systematic interest. They are concretions of calcium carbonate developing on an intrusion of the cell wall, silica may also be involved; the cells containing cystoliths are known as lithocysts. Cystoliths can sometimes be seen in the leaf blade when it is held up to the light, as in Acanthaceae and Urticaceae; they can also be visualized in spodograms, basically what remains after the leaf is calcined (e.g. Bigalke 1933).

Crystalline Silica (SiO2) is sometimes present, either in the wood of families like Chrysobalanaceae, or in the leaf, as in many Poales. It may be present as sand, or as larger, more organized bodies of distinctive shapes. Presence or absence of silica bodies, where they are deposited in the plant, and the morphology of the silica bodies provide especially valuable characters in the monocots (see Prychid et al. 2003b for a summary). Silica-containing cells or other parts of plants are commonly preserved in the fossil record, where they are called phytoliths (see Piperno 2006 for a good summary); phytoliths are especially important in archaeology. Currie and Perry (2007) provide an introduction to the biochemistry of silica. Silica can wear down the mouthparts of animals that feed on plants containing it, but it can also have negative physiological effects (see Massey & Hartley 2006, 2009; Massey et al. 2007a, b).

Ma and Takahashi (2002) and Hodson et al. (2005) summarize the literature on silicon concentrations in plants and Cooke and Leishman (2011a) summarise its physiology; Westbrook et al. (2009) looked at the SiO2 concentration in the leaves of a number of neotropical taxa. Although most broad-leaved angiosperms and non-commelinid monocots have low concentrations of silicon while commelinids have high concentrations, some commelinids, including members of Commelinales and Juncaceae sampled (but see conflicting information in Hodson et al. 2005), also have low concentrations, but these groups also lack SiO2 bodies.

Petiole anatomy has been recorded rather sporadically. Radford et al. (1974) describe and name some of the main variants, although other sets of terms for describing petiole vasculature have also been proposed (e.g. Watari 1939; see also Howard 1979b). Col (1904) is a source for information in several groups. Families like Clusiaceae show great variation in this feature, and it is usually of systematic significance at levels lower than those emphasized here. However, Kim et al. (2003) have recently drawn attention to variation in how much adaxial surface is evident in petioles; when there is none the petiole bundles form a circle, or there is a single annular bundle, in both cases without any adaxial bundles (the "wing bundles" of the descriptions). The petiolar vasculature of taxa that have a clear adaxial petiolar surface is variable. Vascular bundles in the petioles of monocots are usually scattered, although sometimes they form a ring; only the latter feature is recorded.

A number of features of leaf construction/anatomy vary within the lignophytes. These include whether the vein endings are free or form a dense reticulum, the density of the venation of the leaf, and whether or not the smaller veins are transcurrent, that is, joined to the leaf surfaces by echlorophyllous tissue. These features all have considerable physiological significance.

Epidermis. There is much variation in features associated with the epidermis, even if there has been a tendency to be typological when describing their variation; see the Cuticle Database Project (Barclay et al. 2012) for numerous images.

Epidermal cells may contain silica bodies (see above) or their walls may be lignified. In many monocots, but not, apparently, in Helobiae - members of Alismatales here (Löv 1926; Metcalfe 1960), there are bulliform cells, large, thin-walled cells often of the adaxial epidermis, that help cause curling and uncurling of the leaf blade as its turgor changes; subepidermal cells may be involved as well or alone (Löv 1926; Linsbauer 1930). Of course, many Alismatales are more or less aquatic. Epidermal cell shape is usually of little interest at the genus level and above.

Stomatal type. The stomatal "types" mentioned in the characterizations are largely those delimited by Van Cotthem (1970: slightly modified by Baranova 1983, see also Baranova 1987; Wilkinson 1979), however, there is much disagreement in the literature over stomatal morphology, even that of smaller families - partly this is because there is considerable variation in this set of features. Thus stomatal "type" is variable, even when definable, but further confusing the issue is the tendency for each author to use a different set of terms or to interpret a particular configuration of cells in a different way (Prabhakar 2004 is a recent effort to develop a synonymy). Carpenter (2005) introduced nine new types in an exhaustive study of stomatal variation in the ANITA grade, but the forty four types recognized by Patel in 1979, but largely ignored since, is probably the record. Paliwal (1969) introduced Sanskrit terms like "chatushsahkoshik" (= tetraperigenous), but alack, without success. As Payne (1970) observed when introducing his helicocytic and allocytic stomatal types, what may seem to be a distinct stomatal type to one person can be considered a mere modification of an existing type to another person. Baranova (1987) is a useful guide through the nomenclatural chaos. She, too, noted "The distinctions among these types, although conceptually useful, are often difficult to draw. We should not let the necessity to categorize the diversity among stomatotypes obscure the fact that variation is continuous." (Baranova 1987: 64). Members of the ANITA grade, and also of a number of fossil groups, show considerable intra-individual variation in stomatal morphology (e.g. Upchurch 1984). Illustrations in Conover (1991) are useful for ascertaining stomatal morphology of some monocot groups. Inclusions in the guard cells may be of systematic interest (see Tiemann 1988). However, the literature on stomatal morphology is huge, and I have looked at rather little of it...

The patterning of cells around hair bases, epidermal oil cells, etc., can be described using the same set of terms as are used for stomata, even if the idea that all these structures are "homologous" seems unlikely (c.f. Carpenter 2006).

Even aside from problems with recognition of stomatal types, there is the issue of relating the morphology of mature stomata to their development. Payne (1979) surveyed stomatal ontogeny across embryophytes from a developmental point of view. A distinction has been made between mesogenous/syndetocheilic and perigenous/haplocheilic stomata, in the former the subsidiary cells are produced from the same cell (meristemoid, initial) that gives rise to the guard cell initials, in the latter, they are not. However, there can be variation within an individual in this (Taylor et al. 2009; Rudall et al. 2012), for instance, Paliwal and Bhandari (1962) found that stomata on the flowers of Magnolia were haplocheilic while those on the leaves were syndetocheilic. Indeed, the two sets of terms are not exact synonyms, and the syndetocheilic/haplocheilic pair may be best abandoned (e.g. Rudall et al. 2013 and references) and the mesogenous/perigenous pair need to be redefined (see Payne 1979 for some apposite comments). Peterson et al. (2010) looked at stomatal development from a molecular point of view. Fryns-Claessens and van Cotthem (1973) provide a classification of ontogeny-based stomatal types, and Pole (2010) attempted to integrate morphology of the adult stomata with development, at least in part, in his study of the epidermis of Australian Sapindaceae. Stebbins and Khush (1961) provide an early stomatal survey for monocots, although Tomlinson (1974a; see also Rudall 2000) qualified their account, emphasizing the importance of understanding stomatal development. In general, stomatal morphology may not be a very accurate guide to stomatal development (Paliwal & Bhandari 1962; Tomlinson 1970; Rudall et al. 2013; etc.).

Stomatal orientation also varies. In monocots with parallel leaf venation (see below), stomata are usually oriented with the long axes of their apertures parallel to that of the blade, however, in those monocots with reticulate venation orientation is often random (Conover 1983). Elsewhere, random orientation is common, although there are exceptions. Butterfass (1987) summarises information on taxa that have tranversely-oriented stomata. As to stomatal distribution, stomata are usually found on the abaxial side of the blade, but in plants growing in the full sun and with rapidly-fluctuating water conditions, and early successional or marshy conditions, hence often in plants with CAM or C4 photosynthesis, they occur on both surfaces (amphistomatic); there is quite often infraspecific variation in this feature (Metcalfe & Chalk 1950; Mott et al. 1982 for a survey). Isobifacial and unifacial leaves in monocots have been much discussed (see below).

Cuticle waxes. Data are taken from Barthlott and his coworkers (e.g. Fehrenbach & Barthlott 1988; Ditsch & Barthlott 1994, 1997; Barthlott et al. 2003). Barthlott et al. (1998) standardized the terms used in describing wax crystals, and noted that unoriented platelets, often with more or less irregular margins, are common; indeed, their distribution at and above the familial level seems of little systematic significance. Thus although Fehrenbach and Barthlott (1988) included Dichroa (here Hydrangeaceae-Cornales), Francoa (Francoaceae-Geraniales), Vahlia, as well as Penthorum (Penthoraceae) and Saxifragaceae s. str. in their Saxifragaceae in a survey of cuticle waxes, but no significant differences between the species in these very different groups were noted. Below I usually mention only other forms assumed by the waxes and their chemical composition (for which, see Meusel et al. 1994, 1999; Barthlott et al. 2003). In general, wax crystalloid type shows some correlation with higher taxa in monocots (e.g. Barthlott & Fröhlich 1983), but even there the distinctive types are often disconcertingly sporadic in their occurrence. Amyrins, triterpene-type compounds, are found in the epicuticular waxes of a number of families, and in Asteraceae, Apocynaceae and Boraginaceae they are used by chrysomelid leaf beetles as defence compounds (Termonia et al. 2002).

Wax crystals, cuticular folds (Barthlott & Ehler 1977) and trichomes (Barthlott et al. 2003) rarely occur together on the one plant, with wax crystals predominating in "basal" angiosperms (but they seem to provide little information of systematic interest in the ANITA grade) and monocots, while a well-developed indumentum - and conversely poorly-developed wax crystals - predominate for example in Lamiales, Solanales, and Asterales (Pierce et al. 2001 for Bromeliaceae; Agrawal et al. 2009c for the trade-off). There can be a change from wax-no hairs to no wax-hairs within the ontogeny of an individual plant (maize - Takacs et al. 2012).

Hair type. Only particularly distinctive hair types are mentioned, and these rarely suggest relationships between families, although they are quite useful at rather lower levels. Hair types have the same problems as stomatal morphology, etc.: "Because of the intergradations between trichome types, and also in consequence of the use of imprecise and varied morphological and histological terms, it is often difficult, from the voluminous published descriptions that exist, to determine exactly what type of trichome is being discussed, unless there is an illustration." (Theobald et al. 1979, p. 41) - not to mention the ambiguity of terms like "pubescence". For terminology, see Payne (1978), Hewson (1988), Stearn (1992), etc. Pearl bodies, small multicellular hairs, seems to function as food bodies (see e.g. O'Dowd 1982) and are found in e.g. Indigofera (Fabaceae-Faboideae), Vitaceae, etc.


Understanding basic plant morphology is not simple, indeed, the vegetative body in particular of plants like Podostemaceae and Utricularia (Lentibulariaceae) is difficult to understand using the conventional distinctions between stem, root, and leaf (e.g. Rutishauser 2005 and references). Still extremely useful are general studies such as those of Arber (1925) for monocots and Arber (1920) and Sculthorpe (1967) for aquatic plants, while Goebel (1931, 1932) and especially Troll (1935-1971) remain without equal; Bell and Bryan (1991, 2008) provide an attractive short but comprehensive survey of plant morphology while Cronk (2009) reviews plant morphology in the context of gene expression and control. The importance of floral morphology for systematics has been much emphasized in the past, yet vegetative characters are mentioned below where possible, especially in the thumb-nail sketches of families - here Hallé, Oldeman and Tomlinson (1978), Keller (1994, 1996, 2004), van Balgooy (1997, 1998, 2001) and Schatz (2001) have been valuable sources of information. Vegetative characters are often most useful in a more local context, identifying members of the local flora; for identification using vegetative characters, see e.g. Keller (1996), van Balgooy (1997, 1998, 2001), Schatz (2001), Rejmánek and Brewer (2001), Spichiger et al. (2005), and others.

The Vegetative Body.

For definitions, etc., see the Glossary.

There may be leaves - or more generally metamers or construction units - with quite sharply different morphologies and functions on the one plant; this is the phenomenon known as heteroblasty. Such leaves may have quite different forms (bud scales, expanded leaves), internodes may be elongated or not, etc. (Zotz et al. 2011 for a review). Heterophylly, environment-induced changes in leaf form of plants, phenotypic plasticity in leaf development, is particularly striking in many emergent aquatic plants (Zotz et al. 2011).

More or less distinct and organized (i.e. with leaves evident) axillary buds are found in the axils of most or all leaves in nearly all angiosperms, but in gymnosperms their distribution is much more erratic (e.g. Namboodiri & Beck 1968a; Fink 1984). However, in some conifers in which most leaves appear to lack axillary buds there are persistently meristematic but not otherwise morphologically recognizable areas in the leaf axils that will produce organized axillary shoots on damage of the apex of the shoot, etc. (Namboodiri & Beck 1968a; Fink 1984; Burrows 1999). Organized axillary buds are absent in cycads, and indeed they are in general rare outside seed plants (Stevenson 2010). In angiosperms, the number of axillary buds, and their arrangement (collateral, superposed) may be of interest. The development of the prophyll(s) of axillary buds may be precocious, as in some species of Aristolochia and Bignoniaceae-Bignonieae; they can then be confused with stipules. In some Myrtaceae, especially Eucalyptus, there are epicormic strands that enable regeneration after fire (Burrows 2002; see Meier et al. 2012 for a review of epicormic buds), and preventitious buds also occur in some trees (Fink 1983).

The vegetative bud< can be perulate (scaly) or "naked", that is, lacking morphologically modified leaves enclosing the apex; see Henry (1846) and Lubbock (1899) for classic accounts of variation in buds. Information on this character is only sometimes mentioned. Lamina vernation (see below) is best observed at the bud stage or when the leaves are beginning to unfold.

Branching. Branching is not always simply axillary (Fisher 1978), and in some cases, e.g. Solanaceae-Solanoideae, it can be difficult to understand how the plant is put together. A number of aquatic Alismatales show vegetative bifurcation of the vegetative axes, perhaps precocious axillary branching, but strictly dichotomous branching is very rare in seed plants, occuring only in Hyphaene (Arecaceae), Strelitzia (Strelitziaceae), and a few other examples, mostly (?all) monocots (e.g. Wilder 1975; Fisher 1976; Tillich 1998 for references). Particularly robust and quickly-developing axillary shoots may displace the the terminal bud/inflorescence/shoot, the result being that the erstwhile terminal structures appear to arise opposite leaves and the axillary shoot appears to be terminal; the terminal bud/inflorescence/shoot is described as having been evicted.

Keller (1996, see also 1994) distinguished between immediate branching, with branches coming from the current flush, and delayed branching, with branches developed on the previous flush. This is close to the distinction between prolepsis and syllepsis, whether branches develop from the shoot with (prolepsis) or without (syllepsis) evident rest. Buds developing from the axils of the last pair of leaves of the previous flush (e.g. Clusia, Garcinia) present problems for such distinctions, since they may grow out simultaneously with the elongation of the main axis, but after a period of rest. Branching in vines and annuals may also depart from any family norm, furthermore, branching behavior on sucker shoots or young plants may differ from that elsewhere on the plant, especially the canopy. Immediate/sylleptic branching is relatively rare in temperate taxa, but may occur in the local representatives of otherwise largely tropical families that commonly have such branching (e.g. Lauraceae). Although this character is mentioned quite frequently in the characterisations, comparative knowledge of it is poor. The relative development of the branches along a season's growth has been modelled (e.g. Lück et al. 1990), and for modelling branching, bud break and the like, see Evers et al. (2011).

Stems, including inflorescences, roots and leaves, may be variously modified as spines (leaves, or parts of leaves: vascularized), thorns (stems or toots: vascularized) and prickles (unvascularized enations, epidermis + cortex) for protection, and as tendrils for climbing. For the mode of action of tendrils which involves gelatinous fibers, as in twining stems and reaction wood, but not in the roots of root-climbers, see Bowling and Vaughn (2009). Stems may also become flattened and leaf like, i.e. they are cladodes (e.g. Kaplan 1970b, 1980, 1997, vol. 1: chap. 11), while compopund leaves in particular can become phyllodinous, i.e., they appear to have a simple blade. Thus there has been much discussion whether "leaves" of Asparagus really are foliar or not; Nakayama et al. (2010, 2012) discuss gene expression in such structures.

Leaf insertion or phyllotaxis. Mention of this character refers to the insertion of leaves on flowering branches, not on non-flowering axes (when these are distinct) unless specified otherwise. The main variations mentioned are spiral, 2-ranked (distichous), 3-ranked (tristichous) and opposite (usually decussate). Mabberley (2007), too, makes the important distinction between spiral and distichous (see also Corner 1946a), which are too often lumped together and ambiguously referred to as 'alternate'. For a good brief discussion on phyllotaxy and its measurement, see Rutishauser and Peisl (2001). For systematically informative variation in leaf insertion on the main stem/trunk when leaves on branches are invariant in their insertion, see Johnson (1993). I make no distinction between opposite and whorled leaf insertion in the family characterizations since this commonly varies within a family or genus; most families of any size in which opposite leaf insertion is common also have taxa with whorled leaves. I include bijugate leaves with opposite leaves, although there are distinct consequences in having bijugate leaves - shading of the lower leaves is reduced, compared to strictly decussating opposite leaves. Variation of internode length is usually not of interest at higher levels, but taxa with short shoots (brachyblasts) in which internodes do not develop are conspicuous - Pinus and some other conifers, Cercidiphyllum, Ginkgo and Euptelea are well-known examples (see Dörken et al. 2012 for a summary).

For details on the control and modelling - becoming ever more realistic - of phyllotaxis, see Reinhardt et al. (2003), Hotton et al. (2006), Kuhlemeier (2007) and especially Smith et al. (2006). Earlier work (see e.g. Hofmeister; Snow & Snow e.g. 1932, 1952) had suggested that the development of a leaf primordium somehow inhibited the development of new primordia immediately adjacent to it.

Many aspects of foliar variation are covered by the umbrella concept of leaf architecture, and this is of particular interest to palaeobotanists. Standardized terms allow that community to describe accurately details of fossil leaves. For a convenient summary of terms used, most of which should have the same definitions as are used here, see Ellis et al. (2009).

Leaves are generally organs of determinate growth, but secondary growth has been noted in the leaves of a few angiosperms and conifers (Mathuse 1906; Ewers 1982). In Meliaceae like Chisocheton the apex of the compound leaf adds new leaflets over a period of several years, although the leaf always remains a leaf (Fisher & Rutishauser 1990; Tsukaya 2005).

Leaves in broad-leaved angiosperms are typically made up of petiole, lamina, and leaf base; stipules (see also below) are associated with the latter. The terms petiole and lamina in monocots and other angiosperms are equivalent only by designation (Tillich 1998); they may represent developmentally quite different parts of the leaf. For details of general leaf morphology and development, e.g. whether the lamina develops from the leaf base (most monocots) or leaf apex (broad-leaved angiosperms), see Hagemann (1970), Kaplan (1973, 1997), Bharathan (1996), Tillich (1998), Rudall and Buzgo (2002), and Nardmann et al. (2004); Sinha (1999), Piazza et al. (2005) and especially Townsley and Sinha (2012) review leaf development in angiosperms. The terete, unifacial blades with stomata all over the surface that are found in monocots may represent a development of the unifacial "tip" or "Vorläuferspitze" of the leaf (e.g. Arber 1925; Troll 1955; Troll & Meyer 1955; Kaplan 1975 - Oxypolis [Apiaceae] and monocots that are compared here would seem rather distant), or from the middle portion of a bifacial leaf (see illustrations in Linder & Caddick 2001, q.v. for a summary of the literature). The leaves of some broad-leaved angiosperms have stomata on both sides of the blade (amphistomatic), but the blade is still dorsi-ventrally flattened, i.e., they are isobifacial. In some monocots, apparently similar leaves are also isobifacial, but they are laterally flattened and they are often equitant at the base. There they appear to represent a normal bifacial dorsiventral blade that has folded and become connate adaxially, but they could be developed from a "midrib", or, developmentally both they and terete unifacial leaves may represent the genetic abaxialization of the leaf, the genes normally expressed abaxially being the only genes expressed at the leaf surface (Yamaguchi & Tsukaya 2010; Yamaguchi et al. 2010). Much more work is needed on this suite of characters: the development of an isobifacial monocot leaf such as are found in Acorus can be explained classically in quite different ways - is it a hyperphyll, and so equivalent to a broad-leaved angiosperm leaf, or does it originate from an intermediate zone between hyperphyll and hypophyll (Rudall & Buzgo 2002)? - but of course such descriptions are separate from those that result from developmental genetic studies. Similarly, the "blade" of Hosta and Orontium may not be equivalent structures in other than a functional sense (Troll 1955). Ichihashi et al. (2011) recently noted the occurence of what was effectively an intercalary meristem at the base of the leaf blade in Arabidopsis. Cells were cut off both proximally and distally from this zone, rather like the pattern of development in many monocot leaves. A general survey of leaf development in angiosperms, with particular emphasis on monocots, will be very valuable; patterns of leaf development evidently vary at high levels. See below for connections between ligules, sheathing leaf bases, and stipules.

It is interesting that the anodic (better, ascending) side of a leaf, i.e. that side of the leaf that faces up the genetic spiral, is often slightly less developed than the cathodic (descending) side, or a bud on the ascending side of the axil is less developed than that on the descending, etc. (see Korn 2006 for a summary; Chitwood et al. 2012 for an explanation).

Leaf type. The main distinction is between simple and compound leaves (see Doyle 2007 for this variation in the context of a phylogeny). In truly compound leaves the leaflets arise from separate primordia along the leaf, the activity of the blastozone having become restricted to those areas that later develop into leaflets (see Gunawardena & Dengler 2006, Rosin & Kraemer 2009, and Blein et al. 2010 for useful reviews). Most families of any size that commonly have compound leaves also have some members with apparently simple leaves (derived); there, however, the blade is sometimes joined to the petiole by an articulation, as in Citrus, and such leaves are really unifoliolate, not simple. This variation is common and is rarely mentioned.

However, the distinction simple/compound may not be so clear-cut as it seems when the phenomenon is observed at the level of gene expression. Thus Bharanthan et al. (2002) showed that in many leaves dissection in general - both that resulting in simple lobing, and in fully compound leaves - was associated with expression of the KNOXI (Class 1 KNOTTED1-like) gene. Normally it was expressed in the stem apex, but not in leaves as they were initiated, however, KNOXI was normally expressed during the development of compound leaves, even in secondarily unifoliolate ones (Bharathan et al. 2002; Champagne et al. 2007; Uchida et al. 2010); exceptions to this may be of phylogenetic interest (see Fabaceae). Some simple leaves may show KNOXI expression early, but any lobing that develops is subsequently obliterated by inner blade growth. The result is that all simple leaves are not developmentally identical. Other aspects of leaflet development are also similar across a broad array of angiosperms. An example is the genes that promote first the formation of boundaries between leaflets in the developing leaf, i.e., the leaflets separate, and later the formation of leaflets (Blein et al. 2008). The same genes are also implicated in the development of serrations on the leaf or leaflet margin and also the demarcation of the whole leaf at the stem apex (Blein et al. 2008). Efroni et al. (2010) analyze leaf development in terms of several distinct ontogenetic programs.

A number of taxa with pinnate leaves also have palmate leaves, however, Kim et al. (2003) have made a distinction between peltately palmate and non-peltately palmate leaves. In peltately palmate leaves the petiole vasculature is strictly annular (or the vascular bundles form a circle), there being no adaxial surface, whereas in non-peltately palmate and pinnate leaves the petiole bundle is more or less obviously dorsiventral, the adaxial surface being evident. A number of taxa have more or less peltate simple leaves; see Troll (1932) for a still useful review. Such leaves are notably common in Menispermaceae and are scattered elsewhere.

Monocots, with the exception of a few Araceae and Dioscoreaceae, lack truly compound leaves (Gunawardena & Dengler 2006). In monocots, most apparently compound leaves in Araceae, as well as the fenestrate leaves found in some Araceae and Aponogetonaceae, are basically simple leaves. These subsequently become more or less modified by localized cell death (e.g. Gunawardena et al. 2004), or, in the case of palms, the deep lobes in simple leaves, and the leaflets in apparently compound leaves, are probably the result of a process rather like abscission (Nowak et al. 2007, 2008), although nothing - apart, sometimes, from the leaf margin - falls off.

Lamina vernation (ptyxis) - terms and some data are taken from Cullen (1978) and Keller (1996: note that his convolute is Cullen's supervolute). In descriptions of the vernation of compound leaves, the reference is to the folding of the leaflets. The sampling of this character is poor, the delimitation of the states needs attention, and variation may turn out to be rather too much for comfort when used at the level of this site. Indeed, Charlton (1993) shows how the plane of flattening of conduplicate leaves changes during development, and there is quite commonly variation in the plane of flattening within the individual, while in Begonia the vernation of the prophyll is different from that of the other leaves. When leaves remain rolled up as they elongate, the lower surface in particular of the fully expanded blades may have faint but distinct longitudinal lines; these often help in familial or generic identification of sterile material. The significance of the colours of the young leaves has occasioned some discussion; see Queenborough et al. (2013) for references.

Three generalizations can be made about vernation types: first, in water plants with floating, peltate or cordate leaf blades, involute vernation is very common, second, the leaflets of compound leaves tend to be conduplicate, and third, vernation in monocots is usually supervolute or supervolute-curved. See also Couturier et al. (2009) for how palmately-lobed leaves may be folded in bud.

Blade size. Ecologists in particular can find it useful to divide the size of the leaf or leaflet blade into a number of classes (Raunkiaer 1934; Webb 1959). Rather small, narrow leaves with very strongly revolute margins, ericoid leaves, are quite common in taxa that grow in warm and dry climates.

Blade margin. In the category "toothed" are all margins that are serrate or dentate, even minutely so; the margin may even appear to be smooth, but close inspection may show small, more or less regularly spaced dots or glands. A number of tooth morphologies have been described for the leaves of broad-leaved angiosperms (Hickey & Wolf 1975). However, these are difficult to recognize on simple inspection of a leaf, and intermediates are also known, as in Fagales (Hickey & Taylor 1991), where two "types" and their intermediates may occur on the one leaf, and elsewhere (Doyle 2007). However, tooth morphology may yield information of systematic significance if analysed more carefully than it has been treated here (see also Doyle 2007). Note that nearly all families described as having leaves with teeth have some members with entire margins. Interestingly, the tips of some leaf teeth are colleter-like in structure and secretion, i.e., producing more or less mucilaginous exudate (Chin et al. 2013) that is perhaps involved in the lubrication of the leaf as it enlarges in bud; see also González and Tarragó (2009) and Paiva (2012) for a connection between leaf teeth and colleters (families: Aquifoliaceae, Lecythidaceae, Rosaceae; salicoid leaf teeth?). Interestingly, the genes involved in the demarcation of leaflets are also implicated in the development of serrations on the leaf or leaflet margin (Blein et al. 2008). Although many woody plants with 1:1 nodes have leaves with entire margins; Celastraceae (1:1 nodes; serrate lamina) are an important exception (Sinnott & Bailey 1914); see also correlation of nodal anatomy with stipule presence. In monocots, leaf teeth are rather uncommon. There they are never glandular, rather, they are more or less spiny.

Taxa with serrate leaves tend to be more common in temperate climates, but serration of leaves or leaflets also shows a correlation with phylogeny - e.g. the predominantly serrate lamina margins in the predominnantly tropical Malvaceae (Burnham & Tonkovich 2011). Burnham and Tonkovich (2011 and references) discuss the complexity introduced into the use of features like lamina teeth as palaeoclimatic indicators because of such correlations (see also Little et al. 2010; Walls 2011; Schmerler et al. 2012).

Prusinkiewicz and Barbier de Reuille (2010) discuss the generation of various kinds of leaf margins in the context of space constraints. Tsukaya (2006) and Kuchen et al. (2012) surveyed how leaf shape developed, while in a study of the relative importance of cell division frequency and cell size for the determination of leaf shape, Kuwabara et al. (2011) found that the latter could be more important than you might think.

Lamina venation. A distinction is drawn between leaves in which two or more major veins leave the midrib at or almost at the base of the lamina (palmate), those in which these veins leave the midrib along its length (pinnate), and those in which there is no distinction between a midrib and secondary veins, all veins being similar, parallel, and proceeding to the apex (parallel, especially common in monocots); further details of venation are rarely given.

Klucking (1986 onwards) provides a comprehensive survey of leaf venation and Christophel and Hyland (1993) is another useful source of information, however, the detail shown by Ettingshausen (e.g. 1858) has hardly been improved upon. Variation in the patterns made by the secondary and tertiary veins are important elements in the various venation types, but these are referred to only sporadically in the characterisations. Similarly, there are a number of different tooth "types" that are based on the nature of the tooth and of is innervation, although given the variation in these types, the use of venation characters in phylogenetic studies may not be very comforting (e.g. Hickey & Taylor 1991; see also Doyle 2007 for leaf venation placed in a phylogenetic context). For definitions of the terms used, see e.g. Hickey and Wolfe (1975), Hickey (1979), the Leaf Architecture Working Group (1999) and Ellis et al. (2009); Roth-Nebelsick et al. (2001) discuss venation patterna and its development from a functional (support, transport) point of view.

Conover (1983) and Inamdar et al. (1983) discuss leaf morphology and architecture in broad-leaved monocots with reticulate venation; such leaves have evolved several times and are associated with particular ecological conditions (e.g. Givnish et al. 2004c). In many broad-leaved monocot taxa the parallel main veins are linked by well developed ladder-like cross veins.

Venation density varies considerably, and this has been placed in an evolutionary/phylogenetic context, for example by Boyce et al. (2008, 2009), Feild et al. (2011), etc. Venation density tends to be notably higher in angiosperms, especially eudicots, than in other vascular plants, although it is lower in succulents, epiphytes, etc. Venation density affects the flow of water from vascular bundle to stomatal aperture and hence greatly affects photosynthetic rates. (Another important feature of the lamina, more anatomical and rarely mentioned below, is the presence of bundle sheath extensions. If present, they greatly facilitate flow of water from the vascular bundle to the epidermis, so affecting stomatal opening and closing - and hence photosynthetic rate again - Buckley et al. 2011.)

Nelson and Dengler (1997) surveyed the development of leaf venation. Unfortunately, sampling within broad-leaved angiosperms was largely restricted to rosids, and within these, Arabidopsis (Brassicaceae) differed in having basipetal development of tertiary venation (it is normally acropetal in Rosids). Taxa such as Liriodendron (Magnoliaceae) have an intermediate pattern of initiation. Runions et al. (2005), Prusinkiewicz and Barbier de Reuille (2010), and others analyze leaf venation patterns from a more "process" point of view.

For a useful general discussion of variation in the surface of the leaf blade, see Wilkinson (1979). Hydathodes, domatia, and even lenticels may be found on the leaf surface, although they rarely mentioned in these pages because their variation is mostly at a level lower than is the focus here. Hydathodes are particularly well supplied with tracheids, not with phloem; extra-floral nectaries show the reverse relationship. A few taxa have nodules on the leaf blade that are inhabited by bacteria, although details of their functional significance are unclear (Miller 1990 for a review).

Extra-floral nectaries (see e.g. Elias 1983; Schmid 1988; Blüthgen & Reifenrath 2001; Marazzi et al. 2013a; Weber & Keeler 2013: Zimmermann 1932 for an early summary; Lüttge 2013 for some information on nectar secretion) are also often found on the leaf, but also on other parts of the plant - stem, the outside surface of the calyx, the developing fruit, etc. (e.g. Koptur 1992). The morphological and developmental relationship between nectaries found at various places on the plant, and between nectaries and leaf teeth, is complex. Thus for the expression of the CRABS CLAW gene in floral but not extra-floral nectaries in core eudicots, see Lee et al. (2005a, b; but c.f. Krosnick et al. 2008a; Nakayama et al. 2010 - not in septal nectaries); extra-floral nectaries in Passiflora are rather different both from those in other broad-leaved angiosperms and from floral nectaries (see e.g. Krosnick et al. 2008a, b, 2011). Escalante-Pérez et al. (2012) recently found that foliar nectaries on two species of Populus differed considerably in structure and mode of action; in one species they were persistent, with continuous nectar flow, while in another, large amounts of nectar were produced over a short time and cell death occured, but new nectaries could be produced; Thadeo et al. (2008) discuss the similarities between leaf teeth and foliar nectaries in Salicaceae (see also Leitão et al. 2005). One kind of nectary on the leaf margin in Prunus was functionally and anatomically similar to flat glands on the abaxial surface of the lamins (Chin et al. 2013). There is a close connection between nectary-like leaf teeth and colleters (see above). Various other kinds of surface "glands" and nectariferous structures are found on the lamina. Thus black-drying flat glands on the leaf surface are useful in identification as well as being common in and perhaps synapomorphies for sizable clades such as Ebenaceae, Chrysobalanaceae and relatives, etc. (these, too, are really a kind of extra-floral nectary), while other "glands" may in fact be cork tissue associated with stomata, as in a few species of Prunus (Chin et al. 2013).

A distinction can be made between extrafloral nectaries that are intimately involved in pollination, such as the nectaries on the cyathia of Euphorbia (nuptial nectaries), and those that have nothing immediately to do with pollination, but may attract ants that help protect the plant against herbivores or destroy the young stems of vines that would otherwise use the plant as support and in the process smother it (extra-nuptial nectaries).

Punctations, often "glands" of various kinds, are evident when the leaf is viewed in transmitted light. Note that magnoliids with ethereal oils tend to have ± punctate laminas (e.g. van Balgooy 1997), as well as the text-book examples of Rutaceae and Myrtaceae where the glands are often much larger and more organized. Other taxa secreting oils, tanniniferous substances, etc., or with cystoliths or sclereids (see above) may also be punctate, and punctations may also be evident in the calyx, corolla, etc. Other oil bodies, especially in leaf mesophyll cells, may contain neutral oils, triglycerides (triacylglycols). This kind of oil body is widely distributed in angiosperms, although they have not been reported from the ANITA grade or the magnoliids (Lersten et al. 2006). Punctations are mentioned only when they are conspicuous, however, they can suggest the presence of these anatomical features and are, along with the presence of nectaries, etc., often very useful in identification.

The leaf base is commonly sheathing in monocots; the sheath may be open, with free edges, or closed and continuous around the stem. Cells that are recruited to become stipules (as in Arabidopsis) or sheathing leaf bases (as in grasses) come from the lateral part of the primordium, and mutations that abaxialize the leaf interfere with this process (Townsley & Sinha 2012). Monocot leaves may bear distinctive, adaxial flanges or ligules at the very base or some way up the sheath; auricles, lateral projections of the "petiole" or sheath/blade junction, also occur. The ligule in at least some cases in monocots demarcates the Vorläuferspitze from the rest of the leaf; in Zamioculcas the ligule is very near the base of the petiole, which would suggest that the leaf there is developmentally similar to that in broad-leaved angiosperms. In broad-leaved angiosperms the leaf base is commonly narrow, but it is distinctly wider in Dilleniaceae, Caryophyllaceae, Nepenthaceae, etc., while the leaf base in many Liliales is notably narrower than that of most other monocots.

Stipules in broad-leaved angiosperms are more or less foliaceous, vascularised, often paired outgrowths laterally or adaxially on the base of the petiole or on the stem lateral to the petioles; they are a part of the leaf. They can bear nectaries or colleters, be modified as spines, etc. They may be petiolar, clearly inserted on the petiole, or cauline, largely inserted on the stem. Of cauline stipules, intrapetiolar stipules are inserted between the petiole and stem, interpetiolar stipules are single, often lobed stipules borne between opposing leaves, while sheathing stipules (= ochreae) completely surround the stem and form a tubular structure, whether or not they are more or less scarious, as in Polygonum, thick and robust, as in Coccoloba and some species of Fagraea, or bear foliar outgrowths, as in Platanus. Useful studies of stipules and stipuliform structures may be found in Weberling (e.g. 1968, 1970, and especially 2006 [largely a summary]) and Weberling and Leenhouts (1965); see above for correlations between nodal anatomy and stipule presence/absence. See Colomb (1887), Lubbock (1891, 1899) and Tyler (1897) for some of the older literature.

Little attempt has been made to distinguish between "true" stipules and other structures that are in the stipular position. However, some things called stipules appearance to be more or less modified colleters (see below: e.g. some Myrtales, Apocynaceae-Asclepiadoideae) or leaflets (e.g. Burseraceae and Sapindaceae), and when this is obvious the characterisations are qualified. However, from a gross morpho-anatomical point of view, what a stipule "is" and how it can be distinguished from a monocot ligule, etc., is problematic. Recently de Aguiar-Dias et al. (2011) suggested that the paired nectary glands at the base of the leaf in Polygala are stipules because they are also vascularized from the nodal trace; nodes here are unilacunar. On the other hand pallisade glandular tissues with protein rich secretions are found on the leaf teeth and stipules of some species of Ilex; the latter have been called colleters as a result (González & Tarragó 2009); Ilex often has trilacunar nodes. But there is more. Some suggest that stipules ex definitio do not occur in monocots. However, as has been pointed out by authors like Roth (1949) and Rudall and Buzgo (2002), the developmental origins of monocot ligules and at least some stipules of broad-leaved angiosperms seem not to be fundamentally different; both arise from adaxial cross meristems in the transition zone between hyperphyll and hypophyll; Kaplan (1997: 1 ch. 5) called such structures - which would include seedling coleoptiles - stipules. Although I have not used the term "stipule" in the monocot characterisations, it is probable that there are structures there that have at least as good a title to the name as some of the things called stipules in broad-leaved angiosperms; there are certainly developmental connections between stipules, sheathing leaf bases, and ligules.

Colleters are multicellular, more or less glandular but usually unvascularised structures secreting resin, mucilage, or similar material and usually found in the axils of petioles or stipules - and quite often the calyx, too, indeed, colleters are in other than the axillary position, as in several Apocynaceae, Rubiaceae, and Caricaceae. The secretion they produce may be involved in the lubrication of the tightly-pressed young parts of the plant as they slide over one another as the bud expands, or they may have a bacteriostatic function (Klein et al. 2004). The "intravaginal squamules" of monocots are included here, their only difference from colleters seems to be that they are flattened (Doyle & Endress 2000). A useful survey is provided by Thomas (1991), but the distribution of colleters is definitely under-recorded. Lersten (1974) described the distinctive colleters found in some species of Psychotria that are perhaps involved in the bacterial leaf nodules there. Indeed, it is becoming unclear what a colleter might be. Thus Cardoso-Gustavson et al. (2014) describe the mucilage-secreting bicellular hairs found on floral parts - often the outer floral parts - in some Epidendroideae as colleters, and also suggest connections with the extra-floral nectaries on the inflorescence that are also found in some genera of that subfamily. Pallisade glandular tissues with protein rich secretions are found on the stipules of Brazilian species of Ilex (Aquifoliaceae), and the latter have been called colleters ipso facto (González & Tarragó 2009). There is also a connection between colleters and some kinds of deciduous leaf teeth (see above).

Prophyll number, position, and orientation. Prophylls, the first leaves on axillary shoots, are usually either paired and lateral (probably the basic condition for seed plants) or single and adaxial, as in monocots. Piperaceae in particular seem to show variation in prophyll position, and monocots are also quite variable in this, especially in the inflorescence (see below: e.g. Eichler 1875; Engler 1888; Remizova et al. 2006b; Stuetzel & Marx 2005). Especially in monocots, there is extensive discussion as to what prophylls "are" - one leaf, two connate leaves?; Blaser (1944) summarized the often exasperating early literature on the topic. The bracteoles of flowers are simply the prophylls of the short shoot that makes up the flower.

Whether or not prophylls are basal on the branch is often, but not always, associated with whether branches are proleptic or sylleptic; in proleptic branches the prophylls are usually basal, while in sylleptic branches they have a well-developed internode, the hypopodium, below them. Exceptions have both biological and systematic significance. A major group in Rosales, including Ulmaceae, Cannabaceae, etc., have basal prophylls whatever the dynamics of shoot growth, and buds in the axils of these prophylls may be very conspicuous. Inflorescences here are often axillary in pairs, or paired and borne at the bottom of branches; in either case they come from buds is the axils of the prophylls. Taxa with axillary thorns or branch tendrils - these are usually sylleptic - may also show distinctive patterns of variation. Prophylls that are not basal on the thorn (e.g. Gleditsia, Fabaceae) are often associated with the development of conspicuous serial buds in the axils of leaves that subtend the thorns, and these buds provide replacement meristems for the main axillary shoot that has been converted into an heavily lignified and dead thorn. On the other hand, thorns with basal prophylls (e.g. Crataegus, Rosaceae) have functional buds in the axils of these prophylls and often lack obvious serial buds in the axils of the leaves of the main stem.

Breeding systems, Inflorescences, and Pollination.

The breeding system predominating in the family is often mentioned. There is much variation in breeding systems, and this may be in floral type, i.e., whether the flowers have stamens and/or carpels, or in the relative timing of the maturity of the stamens and carpels - specifically, the receptivity of the stigma - of a single flowers or plant. As regards the former, any sizeable family recorded as being monoecious or dioecious is rarely consistently so, conversely, families predominantly with "perfect" flowers (the common condition, and not mentioned when it occurs) nearly always have some taxa with other flower types/breeding systems (the literature on this general topic is huge, see e.g. Ehlers & Bataillon 2007; Schaefer & Renner 2010; Barrett 2013). Wind-pollinated plants are predominantly monoecious, sometimes dioecious (the latter especially in gymnosperms). In angiosperms the fruits of wind-pollinated plants are often dry and single-seeded, while in gymnosperms there is a correlation between dioecy and fleshy, animal-dispersed disseminules and monoecy and wind-dispersed disseminules (e.g. Bateman et al. 2011). For mechanisms of sex determination, see e.g. Charlesworth (2008) and Chuck (2010), for the literature on dioecy, see Schlessman et al. (2014).

When staminate and carpellate flowers occur on the same inflorescence, the carpellate flowers are usually topologically basal; this is true of both monocots (e.g. Tomlinson 1982; Rudall 2003; Ambrose et al. 2005) and broad-leaved angiosperms (e.g. Krosnick et al. 2006), e.g. see many Euphorbiaceae, Kirkiaceae, etc. Exceptions in the latter group include Begonia (Begoniaceae) in which the carpellate flowers are produced in the cymose inflorescence after the staminate flowers, Ricinus (Euphorbiaceae) in which the carpellate flowers are in the top part of the inflorescence, Pteleopsis (Combretaceae), and even the fossil Archaefructus, at least under some interpretations of its morphology (Friis et al. 2003b).

Very often the stigma of a flower is not receptive at the same time that pollen is picked up by the pollinator. Dichogamy is the condition in which stamens and carpels of the one flower mature (anthers dehisce, stigmas are receptive) at different times, and it at least reduces the possibility of a flower selfing itself. Heterodichogamy, in which the reproductive phase of a flower varies between separate plants within a population, is scattered, but is likely to be under-recorded (Renner 2001; Zhao et al. 2012); Rohwer (2009) suggested interesting possible variation based on a heterodichogamous theme in the [Lauraceae + Hernandiaceae] clade. Protandry is supposed to be the default option in dichogamous plants since stamens would seem likely to mature before the carpels in flowers in which floral development was centripetal (Kalisz et al. 2006), however, protogyny is probably the plesiomorphic condition in angiosperms.

Inflorescence position and morphology affects the access of pollinators to the flowers. Inflorescences may be axillary and/or terminal, or they may be borne along the branches, at the base of the trunk, or sometimes on long, slender branches that extend metres from the trunk. A few taxa are geocarpous, the inflorescences being underground (Kaul et al. 2000); the terms used to describe this and other similar behaviours are complex (Barker 2005). Epiphyllous inflorescences that arise from along the petiole or lamina tend to be sporadic in occurrence (see Stork 1956; Dickinson 1978), but in Dichapetalaceae, Arecaceae-Calamoideae, etc., such inflorescences are common in quite substantial clades.

Inflorescence morphology. For a generally accessible introduction to classical inflorescence morphology, which can be very typological and complex and with a correspondingly complex and daunting terminology, see Weberling (1989, also Parkin 1914; Rickett 1944; Troll & Weberling 1989; Troll 1964, 1969; Weberling 1998; the papers in Ann. Bot. 112(8). 2013). Leins (2000) distinguished between indeterminate (open) and determinate (closed) inflorescences. The former included racemes, etc., as well as thyrses, rather confusingly defined as inflorescences in which the main and sometimes the lateral axes might not be terminated by flowers, while the latter included "Vorblatt-Inflorescenzen" (cymes), panicles, etc. Briggs and Johnson (1979) suggest a "more logical (but not theory-limited)" approach to inflorescence description and comparison, but it is difficult to apply to a study at this level, while Claßen-Bockhoff (2000) discusses previous attempts to describe and classify inflorescences (and suggests a general evolutionary schema for inflorescences in flowering plants herself). Prenner et al. (2009) and Endress (2010a) also discuss the need to revise inflorescence terminology; see also Stebbins (1973), Tucker (1999a), Tucker and Grimes (1999) and other articles in Bot. Review 65(4). 1999.

As Castel et al. (2010: p. 2236) note when discussing the complex set of terms used to describe inflorescences, "no science can afford to have its descriptive terms, which are supposed to clarify, be such major sources of confusion". Indeed, if one decomposes the basic growth processes that are likely to be going on in inflorescences, the variables are encompassed by thinking of an axis that is terminated by a flower, or not; that keeps on growing, or dies; that produces branches or flowers; and has inflorescence bracts/prophylls subtending branches, or just flowers (branching is more important than any apparent absence of prophylls - for the latter, see below). An additional variable is, do internodes elongate, or not? - and that is basically that (Kellogg 2000b; see also Singer 2006). Castel et al. (2010) develop the approach adopted by Prusinkiewicz et al. (2007) in their discussion of the inflorescences of Solanaceae as they attempt to think of inflorescence morphology from a more dynamic and less typological point of view. Important questions are now what determines whether a terminal flower is produced or not? what causes internode elongation? Here Prusinkiewicz et al. (2007) have suggestions; see also Singer (2006) and Prusinkiewicz and Barbier de Reuille (2010) for more ideas, and Teo et al. (2013) for archicture regulation at the molecular level. Benlloch et al. (2007), Thompson and Hake (2009) and Preston (2010) examine inflorescence architecture from the point of view of floral gene expression, Benlloch et al. (2007) emphasizing that the diversity of inflorescence architecture seems to be the result of the interactions of only a few genes in a rather simple regulatory network, while Bull-Hereñu and Claßen-Bockhoff (2011) note that gain and loss of a terminal flower in an inflorescence can happen by more than one ontogenetic pathway - and quite easily.

Given all this, how should one describe inflorescences? Since most inflorescence types represent morphologies produced by several largely independent variables (see above), I shall (as of viii.2011!) try to be more simply descriptive when mentioning inflorescences. In the characterizations I will refer mainly to racemes or racemose (polytelic/indeterminate) inflorescences where the main axis does not terminate in a flower, the flowers being borne singly in axils along the axis (and the same for any branches of the inflorescence that are present), and cymes of various kinds, when there is no extended main axis and all lateral axes are immediately terminated by flowers; for a discussion of the various kinds of monochasial cymes, see Buys and Hilger (2003).

More complex inflorescences include a thyrse, in which the main axis may or may not be terminated by a flower, but the branches are cymes, and panicle ("Rispe"), in which the inflorescence is branched, there are no simple, bracteate cymes, but all axes are terminated by flowers (extreme polytely); both terms are often used in the literature, but with more than one definition. Capitulae, corymbs, umbels and fascicles are also mentioned in the characterisations below. These are useful terms that describe what an inflorescence looks like, but, with the exception of a corymb carry no implications as to whether the inflorescence is racemose or cymose.

Bracts and bracteoles are usually mentioned only when they are absent. However, as Castel et al. (2010 and references) note, bracts that appear to be absent when looking at the adult plant, as in Brassicaceae and Solanaceae, may indeed be present if one looks carefully at the young plant; bracts and bracteoles that are entirely absent may be quite uncommon (see for old arguments about this issue). The position of bracteoles is normally the same as that of prophylls on vegetative shoots (see above), since they are simply the prophylls of shoots that bear flowers. Nevertheless, in many monocots that have single adaxial prophylls on vegetative shoots the bracteoles are depicted as being lateral, or paired, or even abaxial. These positions are often associated with monosymmetric flowers that have inverted or oblique symmetry (see below: Eichler 1875, 1880; see also Bruhl 1995; Choob & Mavrodiev 2001; Buys & Hilger 2003); prophyll number and position in monocots will clearly repay further study. For genes controlling floral prophyll development, see Masiero et al. (2004). Bracts and bracteoles cannot be recognized when the flower is single and terminal.

Pedicel articulation may be a useful character, especially in monocots (for information there, see Schlittler 1953a; Kubitzki 1998a); there is a line across the pedicel where non-fertilized flowers abscise. The part of the pedicel above the point of articulation has been considered to be different from the part below, being more strictly part of the flower proper; the term "pericladium" has been used.

Floral Morphology.

For definitions, etc., see the Glossary.

Particularly valuable sources of information for basic floral morphology are Eichler (1875-1878), Engler's Die natürliche Pflanzenfamilien, and the great Flora brasiliensis (Martius & others 1840-1906). Batygina (2002, 2006, 2009) has edited three volumes on terms used to describe flowers, embryology, and seed, etc., while Leins and Erbar, Ronse de Craene and coolaborators, and Endress and collaborators have revitalized the field over the last twenty years or so. There are a number of useful summaries of aspects of floral morphology and development, including those of Leins (2000), Endress (1994b; 2005a [especially development], 2005c, 2011), and Leins and Erbar (2010).

Pollination and pollination syndromes are mentioned relatively infrequently (for summaries, see Faegri & van der Pijl 1979; Endress 1994b; Leins & Erbar 2010). This is because floral variation associated with such syndromes is often at a finer scale than is the focus of these pages. In general, similar floral morphologies have evolved independently many times, indeed, past over-reliance on similarity in pollination syndromes as an indicator of relationships is now causing serious taxonomic problems from the ordinal level down (e.g. see the demise of the old "Amentiferae"), and now perhaps particularly at the generic level, e.g. in Bignoniaceae, Ericaceae, Gesneriaceae, Orchidaceae, and Melastomataceae.

Nevertheless, variation in pollination mechanisms is extensive and biologically and taxonomically interesting, even if the morphological characterization of these syndromes, e.g. as ornithophily (see Cronk & Ojeda 2008), may be overly simplistic (Waser et al. 1996; Johnson & Steiner 2000; Waser & Ollerton 2006; Olesen et al. 2007; Raguso 2008; Smith et al. 2009; Ollerton et al. 2009a for references; c.f. in part Fenster et al. 2004; Willmer 2011); see also the papers in Ann. Bot. 113(2). 2014. Even within individual species, pollinator variation may be extensive, thus the large flowers of Catalpa speciosa are pollinated by several species of both day- and night-flying insects (Stephenson & Thomas 1977). Photographing the flower under u.v. light (see above) may help clarify exactly what the pollinator sees, and what the pollinator sees (and smells) is critical (e.g. Schaefer & Ruxton 2009, 2010; Schiestl et al. 2010). In general, flowers effectively exploit the sensory biases of insects and other pollinators, and strict coevolution = co-speciation between plant and pollinator seems to be rather uncommon (Schiestl 2010; see also Amborellales page). Barth (1985) provides a very readable if somewhat out-dated summary of the interrelationships between insects and flowers; surveys such as that by Vogel (1954) remain interesting.

Comments on particularly distinctive pollination mechanisms, or pollination mechanisms that are common in a group, are sometimes made after the family characterizations, for example, when there are oil flowers (Renner & Schaefer 2010), bat pollination (Fleming et al. 2009), or wind pollination (for which, see Friedman & Barrett 2008); for reversals from wind- to insect pollination, see Wragg and Johnson (2011). Wind pollination in angiosperms is often associated with monoecy or dioecy, catkinate male inflorescences, single-seeded fruits, etc. (Linder 1998). Seymour (2001) lists taxa in which thermogenic flowers (i.e., with respiratory heat production) have been found (see Onda et al. 2008 for the different systems involved, which may co-exist in a single plant); Gottsberger (1977) summarizes what was known about beetle pollination, which he thought was common in basal angiosperms. Deceit pollination - no particular morphological syndrome, of course - is perhaps surprisingly common, especially in Orchidaceae (e.g. Renner 2006a; Lunau 2006; Ledford 2007; Cozzolino & Widmer 2005; Schiestl 2005; Peakall 2009: Schaefer & Ruxton 2010) and floral mimicry, neither well understood nor easy to categorize in terms of the classic Batesian/Müllerian dichotomy, has been reported quite often (Roy & Widmer 1999 for a review; Benitez-Vieyra et al. 2007; Papadopulos et al. 2013). Flowers of many submerged aquatic (Cox & Humphries 1993; Philbrick & Les 1996; Les et al. 1997), parasitic, and myco-heterotrophic angiosperms may have very distinctive pollination devices and consequently their morphology can be difficult to understand. Parasitic and mycoheterotrophic plants in particular may have similar pollinators, being variously visited by flies and fungus gnats, which of course pollinate other angiosperms as well (see Vogel 1978a, 1978b).

Flowers in which buzz pollination occurs are easily recognizable - they are usually radially symmetrical, often with spreading or recurved petals, porose anthers, dry pollen, and a punctate stigma; nectar is often absent, there is often no endothecium (see below, Anther Wall) and heteranthy and enantiostyly are common (Buchmann 1983; Buchmann & Hurley 1978 [biophysical model for the mechanism]; Roubik 1988; Endress 1994; Vallejo-Marín et al. 2010; de Luca & Vallejo-Marín 2013). This syndrome is quite distinctive and has often been used to characterize genera. However, these may turn out to be derived from within another zoophilous clade since they can look very different from those of their close relatives with different pollination syndromes. Examples are Dodecatheon [= Primula], Oxycoccus [= Vaccinium], etc.; recognition of the first genus in each pair makes the second paraphyletic. Buzz pollination is often associated with great variation in the androecium and sometimes also gynoecium, as in Commelinaceae, Melastomataceae, and the Cassia group (Fabaceae), although rather less so in Solanum. Goldenberg et al. (2008) note the diversity of anther morphologies associated with buzz pollination within Miconia and its immediate relatives; anther characters are not always a good guide to taxon relationships, and buzz pollination itself occurs in anthers with a variety or morphologies.

There is often tactile/colour patterning of the corolla/perianth. In taxa with monosymmetric flowers this is commonly centred on the median petal, as in the median abaxial petal of many asterid I taxa (e.g. Lamiaceae, Plantaginaceae), and it is scattered in monocots. This disposition of this patterning is perhaps connected with the orientation of the incoming pollinator, since the lower part of the visual field is important in shape recognition when the colours have long wavelengths (see Neal et al. 1998). However, patterning is centered on the two adaxial petals of the normally-oriented flower of Collinsia (Plantaginaceae, asterid I), which has a very distinctive pollination mechanism for asterids; it has a papilionoid flower. Similar adaxial patterning is found in Rhododendron (Ericaceae: floral orientation inverted, see below) and Schizanthus (Solanaceae: also inverted and more or less papilionoid) and of course it is widespread in Fabaceae other than Mimosoideae. Patterning also occurs on the adaxial petals alone of some Pelargonium (Geraniaceae), the adaxial petal in several Pontederiaceae (flowers more or less obliquely symmetrical), and the two adaxial inner tepals in Alstroemeria (Alstromeriaceae: flowers presented inverted). This adaxial patterning may be connected to the fact that in ultraviolet light the upper part of the insect's visual field is most important in the recognition of shape (Neal et al. 1998); do such flowers show u.v. patterning on these upper petals (Faboideae do!)? Simple petal spots are common and are also involved in pollinator attraction; how they develop in Clarkia gracilis has recently been worked out in some detail (Martins et al. 2012).

In a number of taxa the pollinator does not pick up pollen from individual anthers, but from some other part of the flower. This phenomenon is known as secondary pollen presentation. Here, pollen may be deposited on petals or styles and so presented to the pollinator, or forced out of a tube formed by connate anthers or the corolla either by the elongation of the style or mechanically by the activity of the pollinator (Yeo 1993; Howell et al. 1993; Ladd 1994; Leins 2000). Although such secondary pollen presentation tends to characterize groups of related genera, it has evolved many times and in a number of ways even in fairly closely related taxa (perhaps most notably in Asterales: see Leins & Erbar 2003b). One of the most spectacular examples of secondary pollen presentation I have seen was in a species of Dombeya (Malvaceae), a genus in which I never expected to see such a pollination mechanism; the pollen was attached to the staminodes. Pollination by such devices often occurs as the pollinator is trying to get rewards like nectar from the flower - for nectar composition and its link with particular classes of floral visitor, see Baker et al. (1999).

A final aspect of pollinator attraction is floral scent, which is produced from various parts of the flower, as in Oleaceae (see Nilsson 2000). Raguso (2008) and Schiestl (2010: note that linalool is not plesiomorphic in flowering plants given the phylogeny shown) surveyed the ecology and evolution of floral scent, which is clearly an integral part of a pollinator's reaction to the flower, just as much as is flower colour, shape, etc., however, scent composition is not known to be associated with major taxonomic groups of flowering plants, although there may be a phylogenetic correlation at lower levels (Steiner et al. 2011).

Of course pollinators do not care about the morphological nature of the parts of the flower that attract them or provide them with nectar. In many cases the inflorescence functions as a single flower (Asteraceae are a good example), or a single flower may appear to be several (e.g. Iridaceae). A few structures that look to all intents and purposes like single flowers, even on close inspection, in fact represent the aggregation of several highly reduced flowers - a good example is Cercidiphyllum. Such extremely reduced floral structures are called pseudanthia (e.g. Claßen-Bockhoff 1990, 1991a: Endress 1994b). There are all intermediates between this condition and the inflorescences in species of Viburnum, which have enlarged flowers on the margin of a flat-topped inflorescence all flowers which open more or less simultaneously, and the capitulum common in Asteraceae that is made up of numerous small flowers which open over a period of time but which similarly may be functionally a single unit when it comes to attracting the pollinator (see above); such inflorescences may also be called pseudanthia (Davis et al. 2008). However, in both these latter cases individual flowers are perfectly easily recognizable (see especially Claßen-Bockhoff 1990 for images).

Recently there has been a resurgence of interest in pseudanthia, focusing particularly on taxa like Lacandonia (Triuridaceae), Hydatellaceae (Rudall et al. 2009a) and on members of Alismatales (e.g., Rudall 2003b; Buzgo et al. 2006 for literature). The definition of pseudanthia has sometimes been broadened to include structures that are part flower, part inflorescence (Rudall & Bateman 2003; Sokoloff et al. 2006). These latter, which may be terminal (Sokoloff et al. 2006), can perhaps be confused with peloric flowers (Buzgo et al. 2006: see below); radially symmetrical terminal flowers in at least some Lamiales seem to represent complex primordia that have not separated (Mayr & Weber 2006). Indeed, the definition and recognition of pseudanthia can get very tricky. Recent work has found that in capitulae of Asteraceae and cyathia of Euphorbia genes that are normally active in flowers are active in the inflorescence, suggesting that these structures are at one level developmental hybrids or intermediates between flowers and inflorescences, whatever that might mean (Ma et al. 2008; Prenner et al. 2011). However, at another level simple heterotopy of the genes has occurred.

Much of the subsequent discussion of the flower here focuses on the flower at anthesis. The description proceeds from the outside of the flower in, from the sepals or perianth to the carpels, ending up with mention of the stigmatic surface. Numbers of stamens, tepals, sepals or petals are mentioned only when they are other than what might be expected from the basic meristicity of the flower. The number of stamens given refers to the number of fertile stamens irrespective of how they developed. For all floral parts, "many" is over fifteen. Numbers of parts for each organ type for a number of families are often summarized as floral formulae, which can become very complex (Prenner et al. 2010; Simpson 2010) - and are mentioned in many textbooks. Endress (1990) noted that variation in the number of parts of the androecium in particular was likely when the perianth is absent or the primordia are small. Here floral formulae summarize only common conditions for a family.

Ronse Decraene (2010) has recently re-emphasized the value of floral diagrams as a way of depicting the arrangement of the parts of the flower and the spatial relationships between them. They are usually best made as one dissects a mature flower bud. The floral diagrams of Eichler (1875-1878) still provide the most comprehensive survey of basic floral organization.

I have not grappled with the complexities of floral, particularly carpel, vascularization, although the vascular supply to individual organs is sometimes mentioned in the characterizations and some details of perianth/sepal/petal/tepal vascularization, are mentioned below. Cortical vascular bundles in the flower are mentioned only when they occur (for information, see Ronse Decraene 1992).

Floral development. The remarkable analyses of floral development made by Payer (1857) and his co-illustrator, a M. Faguet, about whom very little is known (A. Faguet was the illustrator for Baillon in a book on medical botany in 1889), can still be consulted with profit. Interestingly, Payer, a student of Brisseau de Mirbel, claimed to have carried out this work without any preconceived ideas (ibid., p. vii), yet (a historical "yet") as far as I know, it was largely ignored by the anglophone world, perhaps suspicious of what the microscope might disclose. Aspects of floral development, from the genetic to the gross morphological levels, are integrated into individual characterisations and throughout the hierarchy and are also discussed separately below. In general, initiation of the parts follows the outside-in sequence in which they are borne in the mature flower: sepals - petals - androecium - gynoecium, with the primordia, at least those of different whorls, all being separate. In a few cases the androecium is initiated before the corolla (Bello et al. 2004 for references) or the two are initiated as common primordia, or the gynoecium is initiated before the corolla, as in many Fabaceae (Prenner & Klitgaard 2008b); see also Sattler (1972), Rudall (2011) and Wanntorp et al. (2011b and references) for other exceptions. Lacandonia (Triuridaceae) is practically the only angiosperm in which the carpels completely surround and develop before the stamens (see Rudall 2003 and Ambrose et al. 2005 for literature). If the flower is really a pseudanthium this exception may go away, but something like heterotopy is a more likely explanation.

The relative rate of development of parts in these whorls can be important, thus in many rosids the petals often develop relatively slowly when compared with sepals and stamens, the sepals completely surrounding the flower. However, in asterids the petals/corolla usually develop notably more quickly than the calyx and surround and protect the androecium and gynoecium of the developing flower(e.g. Ronse Decraene & Smets 1995c; Roels et al. 1997). However, in Celastraceae, Santalales, and some Malpighiales, and some other groups the sepals the corolla completely encloses the developing flower, the sepals being relatively smaller (Matthews & Endress 2002; Endress 2011). Obvious variation such as diplostemony versus obdiplostemony (but see below) and centrifugal versus centripetal development of the androecium (see Rudall 2011 for literature) has been incorporated into the characterizations, but other variation, such as the sequence of initiation of parts in a single whorl, usually has not.

As Endress (2005c) emphasized when discussing petals, there are a number of criteria - position, function, development, shape, anatomy, histology, and gene activity, and also relationships to other taxa that clearly have petals - that "make" a petal a petal, so if a structure does not have one of these criteria, is it thereby excluded from petalhood? Or if it does have just one of these features, is it to be included? Related to this problem, Maturen et al. (2005) found that floral organ diversity genes (B and C) were expressed in the large, white dogwood (Cornaceae, Cornales) bracts, and Geuten et al. (2006) suggest that heterotopic SEP3-like gene expression - in bracteoles and calyx in extant members - was present in the common ancestor of Balsaminaceae et al. (Ericales) clade. It is very probable that sharply differentiated petals have evolved several times, even if they show similar patterns of gene activity (as in Aristolochia and Arabidopsis - Jaramillo & Kramer 2004; see also Kramer & Irish 1999; Zanis et al. 2003; etc.). Complications also arise in cases where the petals are believed to be modified stamens (e.g. Lauraceae, Caryophyllaceae), whether or not these modified stamens are also functional nectaries, as in Ranunculaceae. Such apparent complications are discussed where they occur.

It may be noted here that in some classical theories of floral evolution the petals of eudicots at least, if not broad-leaved angiosperms as a whole, are supposed to represent sterilized and modified stamens (see also Yoo et al. 2009 for Nymphaeaceae), but Ronse de Craene (e.g. 2006) suggests that in core eudicots they may more often be modified perianth/bract members. Ideas that some flowers may really be pseudanthia (see above), or that evolution of floral parts has been mediated by homeotic changes (e.g. Ronse De Craene 2003; Rudall 2003), confound our attempts to peg specific terms to the parts of the flower. Furthermore, the general plasticity of perianth parts especially in members of the ANITA grade compounds the difficulty of mapping of perianth evolution (for example) on the tree (e.g., Endress 2004; D. Soltis et al. 2005b). Finally, there is a kind of "pull of the present" in operation. We commonly talk about the evolution of petals because most core eudicots, which are so diverse and on which so much work is being carried out, have them, but what has evolved may be more a sharp distinction between organs that function as sepals alone and those that function as petals alone from organs in which these functions and associated morphologies were not so sharply distinct (see also Chanderbali et al. 2009 from a developmental perspective; Ronse de Craene & Brockington 2013).

Buzgo et al. (2004) in their study of Amborella noted that distinctions between different kinds of floral parts can be hard to make, even the distinction between perianth and prophylls; the numbers of parts and their arrangement also vary here and in other members of the ANITA grade and magnoliids in particular (see also Taylor et al. 2008; Endress 2008a, etc.). Molecular work (Chanderbali et al. 2009, esp. 2010) suggests that genes whose expression is quite tightly linked to particular whorls in eudicots show much less specificity in the Lauraceae and Nymphaeaceae studied (see also the summary in Ronse de Craene & Brockington 2013).

Of course, variation in floral developmental genes (also linked to gene/genome duplication, see below) is of great evolutionary and phylogenetic importance. The ABC model, developed in the context of studies on the core eudicots Arabidopsis and Antirrhinum in particular, suggests a fairly close linkage between particular classes of genes and their expressions in particular organs of the flower, but it is clear the in the ANITA grade, magnoliids, etc., expression is not so localized (e.g. Li et al. 2005; Kim et al. 2005). A genes are found only in flowering plants. In more "basal" groups of flowering plants, the pattern of AP3 expression is not always consistent and its level changes during development, but in core eudicots the expression becomes spatially restricted within the perianth. The euAP3 gene in angiosperms consists of a duplicated copy of the paleoAP3 gene with an eight BP insertion causing a frameshift mutation (Vandenbussche et al. 2003). In Asarum and monocots AP3 expression is localized on the edges of the tepals. A-class APETALA 1 genes also are of considerable interest (Litt & Irish 2003). For the distribution of SEPALLATA genes in angiosperms, see Zahn et al. (2005) and Malcomber and Kellogg (2005). APETALA 3 and similar genes and PISTILLATA are paralogous B-class genes (e.g. Stellari et al. 2004). For the duplication of B-function MADS-box genes, see Kim et al. (2004: see also Kramer & Irish 1999, 2000; Kramer et al. 1998; Theißen et al. 2000, 2002). C/D genes in gymnosperms are represented by AG-like genes that are expressed in micro- and megasporophylls, as well as ovules. There was a duplication event in the ancestor of angiosperms that gave rise to a D orthologue, expressed largely in the ovules alone, and a C orthologue, only sometimes expressed in ovules, but also in carpels and stamens. Both patterns of gene duplications within the C lineage and patterns of relationships within individual gene lineages (for which, see Kramer et al. 2004) seem to correlate with particular phylogenetic hypotheses. Patterns of duplication in such developmental genes can be taxonomically quite fine-grained (Kramer et al. 2003, 2004), thus Howarth and Donoghue (2005) have begun to untangle the patterns of gene duplication of CYC genes in Dipsacales and link it with morphological change there. [This paragraph is barely worth keeping.]

Flower part insertion. Flower parts are most commonly whorled, but they may be spiral or even chaotically arranged (Ronse Decraene & Smets 1998a). The distinction between a whorled and a spirally initiated androecium is not always sharp (see Ronse De Craene et al. 2003 for a survey of variation in this character in "basal" angiosperms; Buzgo et al. 2004); Endress (2008b) noted that in ANITA-type angiosperms transitions between spiral and whorled arrangements are common, but intermediate types are not, and he emphasized that there can be a spiral sequence in initiation even when floral phyllotaxis is in fact whorled (Endress e.g. 1987a, 2011a; Friis & Endress 1990). Even in a multistaminate, spiral androecium, the outermost stamens may be initiated in pairs, at least when it comes to timing of initiation (e.g. Ronse Decraene & Smets 1993b), although often multistaminate androecia do not show spiral initiation (Endress 2011a; see also below).

In many monocots, although much less frequently in the commelinids than elsewhere in the clade, each of the six stamens is borne opposite a tepal, and the bases of the two tepal whorls do not each separately completely surround the flower (see also below). Here, unlike the situation in broad-leaved angiosperms, a stamen may be strongly adnate to each petal-like tepal of both whorls, both when each tepal is more or less free (Androcymbium [Colchicaceae] is a particularly striking example - see also Endress 1995b) and even when the tepals form a tube. The result is often a flower that is functionally (from the point of view of the pollinator) six-merous, although of course monocots are generally thought of as having three-merous flowers (see below). Posluszny et al. (2000) discuss a perianth-androecium module in the context of the floral evolution of Alismatales (see also Endress 1995b in particular; Buzgo 2001; c.f. Rudall 2003), and I have (perhaps rather uncritically) applied a similar idea to non-commelinid monocots in their entirety and to some "basal" broad leaved angiosperms. In some of these Alismatales the stamens have a small, abaxial, basal scale; this is interpreted here as a reduced tepal.

Endress (1995b, Fig. 6) described petals and stamens arising from a common primordium in Zingiberaceae (as also in some groups of core eudicots, e.g. Primulaceae-Myrsinoideae and their relatives: see Ronse Decraene et al. 1993 for a summary; de Laet et al. 1995 for discussion), but this is a different situation. Here the perianth is completely biseriate, the outer (calycine) and inner (corolline) whorls successively completely surrounding the apex, unlike the condition that is suggested here to be plesiomorphic condition in monocots. Further complications occur in Acorales, some Alismatales and perhaps Piperales. There the slightly enlarged median (abaxial) tepal of the outer whorl encloses the young flower; it looks as if there is a composite structure made up of bract + tepal (Buzgo 2001), so being an organ of "hybrid" nature (Bateman et al. 2006b); Ronse deCraene (2010) interprets it as a bract, one tepal being missing. Such very small flowers can be described as monosymmetric (see below).

Meristicity. Especially when the parts of the flower are whorled, members of the different whorls, particularly the calyx and corolla, commonly also the androecium, and rather less frequently the gynoecium, have the same basic number. However, 2- or 3-carpellate gynoecia in otherwise 4- or 5-merous flowers are common in core eudicots. Meristicity of basal angiosperm clades and the eudicots (but less in core eudicots) is notably labile, and a trimerous perianth - and less frequently androecium - is quite common there (e.g. Kubitzki 1987; Endress 1987; Drinnan et al. 1994; Albert et al. 1998; Soltis et al. 2003; Zanis et al. 2003; P. Soltis et al. 2004; D. Soltis et al. 2005; Doyle & Endress 2011). Monocots are overwhelmingly trimerous in all five floral whorls, unlike the situation in other angiosperms (some Aristolochiaceae and Haloragaceae are close), even if the simplistic distinction (which I used to teach) of monocots - overwhelmingly 3-merous flowers; dicots - often 5-merous flowers, needs qualification. In many core eudicots there is inter- and even infraspecific variation in meristicity although a particular family may be predominantly either 4- or 5-merous.

Symmetry. Particularly valuable sources of information for the whole suite of characters associated with floral symmetry are Eichler (1875-1878) and the Flora brasiliensis (Martius & others 1840-1906); for general discussion, see e.g. Friis and Endress (1990), Tucker (1997, 1999b), Endress (e.g. 1999, 2008a, 2012), Ronse de Craene (2010) and Preston and Hileman (2009). Rudall and Bateman (2004) survey the evolution of monosymmetry in monocots, and Citerne et al. (2010) the evolution of symmetry in angiosperms in general.

Flowers may be monosymmetric (= bilateral, zygomorphic), disymmetric (two main planes of symmetry at right angles), asymmetric (clearly no plane of symmetry, see esp. Endress 2012), haplomorphic or polysymmetric (= radially symmetrical, actinomorphic - see Neal et al. 1998; Endress 1999). The last two conditions are often lumped together; however, haplomorphy refers to situations where the flowers appear to be polysymmetric, but there is no plane dividing the flower into mirror-image pairs because the parts of the flowers are numerous and spirally inserted (e.g. some Magnolia, while polysymmetry refers to situations where there are three or more mirror-image planes of symmetry (many monocots). Highly reduced flowers with only one or two stamens (e.g. Peperomia) are necessarily monosymmetric, as is Acorus with its enlarged median abaxial tepal, indeed, many highly-reduced flowers are technically monosymmetric. Monosymmetry may also be evident solely in the curvature of the style and anthers in a more or less horizontally-held flower, as in Agapanthus (Citerne et al. 2010).

The plane of symmetry in monosymmetric flowers is usually vertical, passing through the middle of the adaxial sepal and of the abaxial petal (or vice versa, as in some monocots), oblique, passing between the adaxial and adaxial-lateral sepals and the abaxial and abaxial-lateral petals, strongly oblique, passing through the middle of an adaxial-lateral sepal and of an abaxial-lateral petal, or, rarely, transverse, with the plane being at right angles to the median plane of the flower. This last is found in e.g. some Papaveraceae-Fumarioideae, although there at least the flower becomes vertically monosymmetric by resupination (Damerval et al. 2013), Vochysiaceae, and Haemodoraceae; similarly, obliquely symmetrical flowers may well appear inverted from the pollinator's perspective. The direction of the plane of monosymmetry in obliquely monosymmetric flowers may vary, even in quite closely related taxa, for instance, whether monosymmetry runs from the odd petal to the odd sepal or vice versa (Ronse Decraene et al. 2002). Flowers with oblique or transverse symmetry occur rather sporadically, although the former condition is far commoner (c.f. Neal et al. 1998).

For discussion on the evolution of lobing of monosymmetric flowers, see e.g. Endress (2001). The lobing of the corolla in the monosymmetric and more or less sympetalous flowers of the asterid 1 and 2 groups is interesting. 2:3 lobing (two corolla lobes make up the adaxial part of the corolla, three make up the abaxial lip) is common in Lamiales in particular (e.g. Weberling 1989). 0:5 corolla lobing occurs in Cichorium, for example, which has a particularly distinctive monosymmetric flower since the corolla appears to be split down one side - it can be called split-monosymmetric. Such flowers occurs in a number of Asterales, but also sporadically elsewhere, as in some Lamiaceae, Haemodoraceae (0:6), Loranthaceae, etc. The split-monosymmetric flower of Anigozanthus (Haemodoraceae) and other plants where the whole perianth is involved, as in Proteaceae, must necessarily be slightly oblique, this is not so when the corolla alone is involved, as in Asteraceae, Loranthaceae and Lamiaceae. Monosymmetry in flowers of Dilleniaceae, Melastomataceae, Commelinaceae and Lecythidaceae may barely involve the corolla at all, just the androecium. There may also be movement of some of the parts of the flower after it opens making it more or less monosymmetric, an extreme example is Passiflora mucronata (Sazima & Sazima 1978). Furthermore, the stigma quite commonly moves relative to the stamens as the flowers mature, and such slight monosymmetry these movements may cause is widespread.

There is substantial infraspecific variation in the lobing pattern of the flowers in Eriastrum eremicum (Polemoniaceae) has been noted (de Groot 2011), and there is infraspecific variation in the occurrence of monosymmetric flowers in Erysimum (Brassicaceae) that is correlated with the identity of the insect that is the predominant pollinator (Gómez & Perfectti 2010). Finally, the marginal flowers of many more or less umbellate or corymbose inflorescences in Apiaceae, Adoxaceae, and Brassicaceae may be more or less monosymmetric, the central flowers polysymmetric (Citerne et al. 2010; see also below).

Reeves and Olmstead (2003) suggested that monosymmetric flowers in different clades of the asterid I group arose in different ways. However, in clearly monosymmetric flowers of independent origin, the same genes may be co-opted in the development of asymmetry. Thus CYC gene seems to have been independently co-opted into the development of monosymmetric flowers in core eudicots (Preston & Hileman 2009; Citerne et al. 2010; Zhang et al. 2010; X. Yang et al. 2012 and references), and also at least in Commelinaceae (Preston & Hileman 2012) in monocots.

There may be a connection between monosymmetric flowers and racemose inflorescences (Stebbins 1951; see also Prusinkiewicz et al. 2007). Thus in the raceme of a foxglove, for example, polysymmetric peloric flowers are terminal. However, in Lamiaceae all flowers in the cymes that predominate there can be considered terminal, and all are monosymmetric, and this also occurs in monocots like Zingiberales, Commelinaceae, etc. - but perhaps these are not exception, since the main axis bearing the axillary cymose partial inflorescences is indeterminate (see also Citerne et al. 2010).

Recent work in monocots has emphasized that taxa like Acorus (Acoraceae), Triglochin (Juncaginaceae), Kupea (Triuridaceae) etc., all with small and apparently undistinguished flowers, may be monosymmetric (Buzgo 2001; Buzgo et al. 2006; Rudall et al. 2007b). Furthermore, detailed studies of development often suggest symmetries other than those evident in the adult flower, in particular, slight mono- or disymmetry may be evident early in development, even if not in the flower at anthesis (e.g. Sattler 1962: Primulaceae-Theophrastoideae; Olson 2002b: Moringaceae; Ronse de Craene 2005: Batis; Damerval et al. 2013: Papaveraceae-Papaveroideae). It has also been suggested that the flowers of plants like Passiflora and Nigella are monosymmetric, largely because the approach of the pollinator to the nectar is restricted (Westerkamp & Claßen-Bockhoff 2007). They note that they have circumscribed the term widely, and so would consider most nototribe flowers to be monosymmetric, but in Nigella in particular it is hard to see that the behaviour of the pollinator is particularly constrained by floral construction. However, the pollinator approaching the polysymmetric flowers of Iris will see a monosymmetric structure, and here three part-flowers or meranthia make up the whole flower.

Finally, groups of flowers or pseudanthia can form monosymmetric pollination units, examples including the Pedilanthus group of Euphorbia, some Proteaceae, etc. (Westerkamp & Claßen-Bockhoff 2007). Conversely, in Iberis amara (Brassicaceae) monosymmetric flowers contribute to giving a pollinator the impression that the whole inflorescence is functionally a single, polysymmetric flower (Busch & Zachgo 2007) and in poinsettia-type Euphorbia species groups of cyathia and associated inflorescence bracts form a single polysymmetric/haplomorphic floral unit - and in Pedilanthus-type species they form a monosymmetric floral unit.

The significance of all these observations from the point of view of the involvement of monosymmetry in specific pollination mechanisms and in its very conceptualization and evolution is considerable (Westerkamp & Claßen-Bockhoff 2007). Endress (2008a) emphasized the diversity of monosymmetric flowers and categorized monosymmetry in various ways: Active versus passive, developmentally transient, and monosymmetry by reduction; he had already distinguished between constitutional, reduced and positional monosymmetry (Endress 1999). Monosymmetry is thus another character that has to be discussed with extreme care. For some comparative purposes it may be best to refer separately to each of the floral whorls that is monosymmetric, while for other purposes a gross categorization such as "flowers obviously monosymmetrical" may suffice, but highly reduced but ex ipso facto monosymmetric flowers may need to be excluded from this category. From some ecological points of view it may be appropriate to focus on how the inflorescence appears, indeed, it is how the pollinator sees the flower that matters (Rodríguez et al. 2004). Certainly, monosymmetry is not a simple term to use.

For the distribution and morphological correlates of enantiostyly, the deflection of the style to one side of the floral axis, see Jesson and Barrett (2003); heteranthy and the loss of nectaries also commonly occur when the flower is enantiostylous. Pollen is the main pollinator reward, buzz pollination (see above) occuring in many enantiostylous taxa (Buchmann 1983; Marazzi & Endress 2008). Since the style, at least, is deflected to one side, enantiostylous flowers such as those of Chamaechrista are more or less asymmetric. Such asymmetric flowers characterize all Cannaceae and Marantaceae; in the latter family the asymmetric flowers are borne in mirror image pairs immediately next to one another.

Floral Orientation. The main variation in the orientation of the flower is whether the median ("odd") sepal, or the median member of the perianth or of the outer tepal whorl, is adaxial or abaxial. The plesiomorphic condition for the angiosperms seems to be to have the median member adaxial, although ascertaining this is complicated by the haplomorphy of the flowers of some of the basal pectinations, while in the monocots the median member is abaxial; this difference is associated with variation in prophyll/bracteole position, i.e. if this/these are absent, the median tepal may switch positions 180 degrees (see also Hofmeister's Rule; Kirchoff 2003 for discussion in the context of Zingiberales).

Spichiger et al. (2005; see also Eichler 1875-1978) suggest that Agave, Tillandsia (but this is a mistake), Allium, Galanthus, Dioscorea, and Lilium all have the median member adaxial, that is, in the reversed position for monocots. Indeed, exceptions to the rule in monocots are very common and are often systematically and biologically interesting, often - but by no means always - being associated with various forms of monosymmetry (see below). Stuetzel and Marx (2005) note the variability of the position of monocot bracteoles/prophylls, perhaps because axillary flowers may in fact represent reduced racemes. For additional discussion of tepal orientation in monocots, see also Eichler (1875), Engler (1888) and Remizova et al. (2006b); the orientation of the flower may depend on the presence of a prophyll, also on the existence of other foliar structures on the pedicel. De Groot (2011) has found infraspecific variation in floral orientation in Eriastrum eremicum (Polemoniaceae); its developmental basis is unclear.

Inverted monosymmetric flowers may arise in three ways. 1. The distinctive orientation of the flower may be evident from the beginning of development; Bremer et al. (2001) describe such variation in the corolla orientation in monosymmetric flowers of euasterids. 2. Inversion may be secondary, by resupination. Here the pedicel and/or ovary (when inferior) may twist and the flower becomes resupinate, as in many Orchidaceae, although in some species of Angraecum the pedicel twists 3600 so the flower ends up "normally" oriented. The corolla itself may twist (Daniel & McDade 2005), as in some Acanthaceae. Finally, the flower may basically just flop over, as appears to happen in Balsaminaceae, for example. There the flowers have rather slender pedicels and most of the mass of the strongly monosymmetric flowers is in the form of a large, spurred, median sepal that is initially on the adaxial side, but in the open flower the sepal + spur is in the abaxial position. The group of monosymmetric flowers is very heterogeneous. 3. The individual flowers may be normally oriented with respect to the axis that bears them, but because of how the inflorescence itself is held, they are presented inverted (or vice versa). Monosymmetric flowers that have become inverted by one of these mechanisms seem to be notably common in monocots. Fischer et al. (2007) discuss the variety of ways - of which twisting of the pedicel is but one mechanism involved - that flowers in the speciose Bulbophyllum present themselves in the Malagasy region.

An epicalyx is of sporadic occurrence, and is mentioned only when it occurs. It origin is various; it may represent modified stipules of the calyx lobes (as perhaps in Rosaceae - Rosoideae), inflorescence bracts (Malvaceae), spines surrounding the flower (Neuradaceae), etc.

The hypanthium is defined here as a disc- or cup-like structure more or less surrounding or borne on top of the gynoecium, but separate from it, and bearing perianth and stamens on its margin. One can think of it as representing receptacular/axial tissue. If the hypanthium has become adnate to the gynoecium over evolutionary time, the latter is simply described as being inferior. Thus I never describe the hypanthium as being adnate to the ovary (see also below, also Gustafsson & Albert 1999), in fact, there is rarely evidence that an ovary has become inferior by the adnation of a hypanthial tube. Many monocots have stamens adnate to a tube formed by adnation of the two whorls of the biseriate perianth, the perianth tube (see below); I have not used the term "hypanthium" for this condition because the tube is strictly appendicular in origin. The flowers of Velloziaceae and Hydrocharitaceae may have structures that are more like a "true" hypanthium. Similarly, the tube formed by the calyx and corolla in Passifloraceae, and the rather different-looking tube bearing sepals and petals in Cuphea, neither bearing stamens, are referred to as K-C tubes.

A perianth. The term perianth is often used to refer to all the more or less foliaceous structures enveloping the flower. A perianth in the strict sense (P in the characterisations) refers to situations when there is only a single whorl of foliaceous structures surrounding the flower and there is no evidence from comparative morphology what they "are". Thus the single whorl in Loranthaceae, Santalaceae, etc., is called a corolla in the characterisations because members of that whorl are interpreted as being equivalent to members of the inner whorl that is made up of petals in other members of Santalales - see the discussion on the Santalales page. In a bi- or multi-whorled perianth, all parts may be similar and then they are called tepals (T), or very frequently differentiation of the perianth occurs, and a calyx (K), made up of sepals, and corolla (C), made up of petals, are distinguishable. The four petal-like members of the flowers of Proteaceae, each opposite a stamen, are here called perianth, or the flowers could be described as having two whorls of tepals, each of two members. A rather different situation occurs when the parts are all similar, in spirals, and often quite numerous; often the outer members are more or less calyx-like/protective and the inner members are more or less corolla-like/attractive. I describe flowers with this condition as having a perianth, but I mention the fact that a spiral is involved and that some members are sepal-like and some petal-like.

Differentiation of the sepal/petal function in the perianth has occurred many times (see below under petals), and so the sepals and petals found in some monocot flowers and those of a core eudicot flower are equivalent only by designation, as are those in e.g. Saruma (Aristolochiaceae), Papaveraceae and core eudicots. Many monocots have biseriate petal-like tepals, and in Lilium B-class floral homeotic genes are expressed in the outer whorl alone (Kanno et al. 1999); in eudicots such genes are expressed only in the inner (petal) whorl. Indeed, in general in monocots B-class genes are expressed in the inner tepal whorl, whether or not it is petal-like in morphology. A-class genes tend to be expressed more generally in the flower (Kanno et al. 2003). However, in Commelinaceae only A class genes are expressed in the outer whorl - which is a sepal (Kanno et al. 2004). Even when there are tepals in monocots, members of the two whorls are often somewhat different in morphology. [Develop.]

Ambrose et al. (2000) suggest that flowers in Poaceae can be directly compared with those of core eudicots, with the palea, at least, representing the calyx whorl and the lodicules the corolla whorl. This argument tends to emphasize gene expression, so favoring Remane's criterion of special properties (Remane 1952) over other criteria such as position, furthermore a strong K/C distinction is likely to have evolved independently in the core eudicots and the commelinids. In such situations, questions as to what the parts "are" become close to unanswerable. However, recent work confirms this general hypothesis, which is made more likely by comparative morphological studies as well (e.g. Whipple et al. 2006) and is largely consistent with the position of Poaceae in commelinids. Nevertheless, the evolutionary and developmental relationships between the arrangement and differentiation of the perianth of monocot and eudicot flowers remains unclear.

Calyx and corolla aestivation is mentioned only when it is other than imbricate in the strict sense. Thus if there is no mention of valvate or contorted aestivation, or of flowers with open development, it can be assumed that aestivation in the group is predominantly some version of imbricate. However, note that imbricate can also be used when referring to all aestivation types in which the edges of adjacent perianth members overlap one another, and also, for example, buds in which the bud scales are overlapping. In many families with predominantly imbricate aestivation other types also occur. For a survey of aestivation that focuses on the diversity of subtypes within the the aestivation classes mentioned here, see Schoute (1935). Endress (1999) observed that the direction of corolla contortion in asterid families with contorted aestivation is usually constant (an exception is Apocynaceae), whereas in other families it is usually variable, indeed, in rosids, etc., the direction may even vary in different flowers from the one plant (see also Endress 2001b, 2010c). In Lamiales and Fabaceae variation in whether the adaxial or abaxial petal(s) of a corolla overlap the others (some form of cochleate, whether descending or ascending) affords phylogenetically useful distinctions.

Connation. It can be assumed that the calyx and corolla are free unless otherwise mentioned. Erbar and Leins in particular (Erbar 1991; Erbar & Leins 1996b; Leins & Erbar 1997, 2003b; Leins 2000) have emphasized the different ways in which a corolla may become sympetalous - early and late corolla tube formation are the two extreme conditions, but intermediates ("early/late") occur in groups like Acanthaceae and Oleaceae. In late corolla tube formation the corolla tube is formed by the confluence of originally free petal primordia, while in early corolla tube formation the part of the corolla with stamens adnate to it is evident as a ring primordium from early on. In the former petals may lag behind stamen development, while in the latter they grow rapidly and soon cover the stamen primordia (Ronse Decraene et al. 2000). The correlation of early sympetaly with a convex floral axis (itself associated with an inferior ovary) and anthers that are relatively retarded developmentally, as in Rubiaceae, and of late sympetaly with a convex floral axis and relatively retarded petals, was emphasized by Ronse Decraene and Smets (2000). This correlation is not absolute, but it does raise the issue as to what extent the "late" tube initiation is a consequence of how inferior ovaries in the asterid II clade develop.

Both filaments and petals together may form a tube. Each is an integral part of the tube, which is built up of alternating corolla and stamen sectors; such a tube occurs in some Convolvulaceae and Diapensiaceae. Calyx and corolla together may form a tube, but this is rare in eudicots (e.g. Passifloraceae); however, a rather similar condition where the tube is formed from the tepals of both whorls is quite common in monocots (see above). Indeed, in monocots as a whole there is considerable variation, even between closely related taxa, both in the degree of connation of the tepals and of the adnation of the stamens to the tepals (see also Weberling 1989).

Perianth/sepal/petal/tepal venation. Sepals in core eudicots are often innervated via a three trace:three gap vascular supply, or the lateral sepal traces come from the petal traces, etc. However, if the sepals are much reduced, there may be either a single trace, or no trace at all, as in some Ericaceae-Ericoideae and Oleaceae. In the reduced flowers of Morus (Moraceae), the perianth members of staminate flowers may have a single trace, those of carpellate flowers, three traces (Bechtel 1921). The sepals of other eudicots and of members of the ANITA grade sometimes have only a single trace (e.g. Glück 1919; von Gumppenberg 1929; Kaussmann 1941; Hiepko 1964a, b; von Balthazar & Endress 2002a). Petals often have a single trace, perhaps reflecting their derivation from stamens, which also have a single trace (e.g. Ronse de Craene 2007, 2008), although the single traces of petals in e.g. Campanulaceae represent fused branches from adjacent sepal bundles, while the single traces in many Asteraceae are commissural bundles. The single petal trace often has a complex branching pattern within the blade of the petal. Members of both tepal whorls in monocots commonly have three traces, but sometimes each member has only a single trace - perhaps particularly frequently in Asparagales (Gatin 1920; Kaussmann 1941; Utech e.g. 1984, 1987, and references) and Alismatales.

Petals. Only distinctive features such as whether or not the petals are clawed, i.e. with a sharply narrowed and more or less elongated basal portion, or ligulate, with more or less petaloid productions on the adaxial surface, are mentioned. Monocots are described as having petals only when the perianth is clearly differentiated into two morphologically distinct whorls, the outer being more or less green and smaller than the inner whorl. The terms corolla or petals are not used to refer to the undifferentiated perianth members of the large flowers of taxa like Agave, Hemerocallis, or Blandfordia, brightly coloured although they may be; these and many other monocots are described as having petal-like tepals.

In a number of taxa there are petaloid outgrowths from the adaxial side of the petals or tepals - these are variously called ligules or coronas. These may be more or less closely associated with stamens, as in some Amaryllidaceae and Apocynaceae, or be independent of them, as in some Caryophyllaceae and Erythroxylaceae.

Nectaries. Bernadello (2007) provides a useful general survey of floral nectaries with an extensive bibliography (see also Kartashova 1965; Vogel 1977; Smets 1986, esp. 1988; Schmid 1988; Smets & Crescens 1988; Weberling 1989); Stadler (1886) is a good early study of some very different nectary types, Bonnier (1879) a still earlier survey that includes colleters, etc., while Brown (1938) provides a fairly comprehensive survey. Evert (2006) summarises details of nectary secretion (see also Lüttge 2013 and green nectaries) and Nepi (2007) discusses their structure and ultrastructure, although without giving details of their vascularization; Frei (1955) described the nature of the vascular tissue supplying nectaries - none, phloem only, or phloem + xylem - but there seems to be no particular systematic signal there. Indeed, nectary vasularization varies at quite low levels (Saxena 1973; de Paula et al. 2011). The presence of a nectary is noted in the appropriate place in the descriptive sequence of the flower, i.e. proceeding from the outside in; complete absence of a nectary is noted immediately before the description of the gynoecium.

In core eudicots nectar may be secreted from a more or less annular, disc-like structure with stomata through which the nectar emerges. This commonly immediately surrounds the ovary, or is on top of it if the ovary is inferior. Although "discs" and nectaries are frequently noted in the eudicot characterisations it is by no means certain that all have a similar anatomy, etc. (e.g. see Smets 1986; Vogel 1997). Smets et al. (2003) distinguish between receptacular nectaries, characteristic of rosids, and gynoecial nectaries, typical of asterids; the names refer to the different places where the nectaries are found. There may also be a difference in their vascular supply, the former being supplied from receptacular or androecial traces, the latter by branches from the gynoecial vasculature (see Smets 1988 for a distribution of the main nectary types on a Dahlgrenogram). However, note that the CRABS CLAW gene is expressed in both floral and extrafloral nectaries in the some of the few core eudicots studied, and would appear not to pay particular attention to any distinction of floral nectary type (Lee et al. 2004; see also Fourquin et al. 2007 for the general function of CRABS CLAW orthologs), although this gene is not expressed in the extrafloral nectaries of Passiflora (Krosnick et al. 2008a) or in the septal nectaries of Asparagus (Nakayama et al. 2010). Nectar may also be secreted by hairs on the calyx or corolla or more generally from folds or other tissue on the tepals or petals, from what are clearly modified stamens or parts of stamens, and even from the surface of the gynoecium. Indeed, whether or not features like nectary vascularisation (as in e.g. Capparaceae, Passifloraceae, Salicaceae, and Cucurbitaceae) and/or the presence of stomata in the epidermis covering the nectary have systematic significance is unclear, and a detailed survey of the anatomy and development of nectaries would be useful (but see Smets 2003). Smets et al. (2000) survey monocot nectaries in general, and Rudall (2002) and Remizowa et al. (2006a) discuss the diversity of septal nectaries, epithelial nectaries in the septal position that occur in many monocots (see also Daumann 1970; Schmid 1985; van Heel 1988). Septal nectaries seem not to occur when placentation is parietal (Rudall et al. 2005) and of course when the gynoecium is initially apocarpous (it is difficult to have septal nectaries when there are no septae...); there is a correlation between the presence of septal nectaries and the occurrence of postgenital fusion of the gynoecium (e.g. van Heel 1988; Remizowa et al. 2006a). Although some broad-leaved angiosperms have cavities in the ovary septae, these are not known to secrete nectar (Ronse Decraene et al. 2000b). For nectar composition, see Baker et al. (1998).

Nectaries are quite frequently lost, and not only in connection with the development of the wind pollination syndrome, but also when there is buzz pollination, the development of enantiostyly (see above), etc. For extrafloral and extranuptial nectaries, see above under leaf surface.

Nectar is of course not the only floral reward for the pollinator. Pollen itself, sometimes collected by bees as they "buzz" the flower, leading to the distinctive buzz-pollination floral syndrome, is a frequent reward; the pollen grains are often small and protein-rich (for buzz pollination [see also enantiostyly above], see Buchmann 1983; Roulston 2000; Harter et al. 2002; Teppner 2005). Pseudopollen is also sometimes produced, as in Theaceae, although its function is poorly understood. Male euglossine bees, among others, may visit flowers for their fragrances (for euglossine bees, see e.g. Ramírez et al. 2002). Flowers that produce oils as a reward are relatively uncommon and tend to be rather restricted in their taxonomic distribution (e.g. Vogel 1974, 1986, 1990; Buchmann 1987; Renner & Schaefer 2010; see Neff & Simpson 1981 for oil-collecting bees). Interestingly, oil in a flower is not infrequently contained in two separate spurs (e.g. Vogel 1984), the oil then being collected by both forelegs of the pollinator (see also Pauw 2006 for similar morphologies within Orchidaceae - Coryciinae). Plants produce oil in epithelial or trichomatous elaiophores (Vogel 1974); the former predominate in the rosids, the latter in the asterids (P. Puppo, pers. comm.).

The common condition in many core eudicot groups is for there to be twice as many stamens as petals, and these stamens are borne in two whorls. The outer (antesepalous) whorl is normally initiated before the inner (antepetalous), the condition of diplostemony. However, in obdiplostemony (see Eckert 1966) the stamens of the antepetalline whorl appear to be outside the stamens of the antesepalline whorl. Diplostemony is by far the most common condition, and only obdiplostemony is noted specifically in the descriptions. (I also note an associated feature, the arrangement of the carpels.) If the stamens are equal in number only to the sepals or outer perianth whorl, they may be opposite (haplostemony) or alternate with them, in the latter case being opposite to the inner whorl of the perianth or petals (obhaplostemonous). Ronse Decraene and Smets (1995a) suggest that other terms should be used to describe such features in monocots, while Bachelier and Endress (2009; see also Endress 2010d for a good discussion) have perhaps unfortunately redefined the term, suggesting that in obdiplostemonous flowers the important feature is that the carpels are opposite the petals (see also below under carpel arrangement); the term cannot then be used when there are ten stamens but only three carpels. Be that as it may, obdiplostemonous androecia develop in a variety of ways (Hardy & Stevenson 2000b), and are quite common in rosids in particular perhaps because of the relatively delayed development of the petals there relative to that of sepals and stamens (Ronse Decraene & Smets 1995c; Roels et al. 1997).

Stamen development and position. When there are many stamens, or microsporophylls, the sequence of initiation may be centripetal. This is especially common in the ANITA grade and magnoliids, and seems to be the plesiomorphic condition for angiosperms. However, in a number of eudicots initiation may be in the opposite direction, being centrifugal (e.g. Corner 1946b, see Rudall 2011 for an assessment of Corner's work). This is a derived condition and is common in taxa with fasciculate androecia. Details of how centrifugal androecia develop vary considerably (Rudall 2011), and in some taxa with secondarily numerous stamens the distinction between the two modes of initiation may be unclear (e.g. Hufford 1990). Androecia with numerous stamens are relatively uncommon in monocots (see Kocyan 2007 for a summary; Nadot et al. 2011 for palms, where the condition has evolved several times).

A number of taxa with secondarily numerous stamens initially have only five or ten primordia, in the former case, the primordia are often antepetalous (see stamen insertion, below); numerous individual stamen primordia then develop on these few primordia. Stamens may also develop in separate groups, or from a common ring primordium surrounding the gynoecium (e.g. Ronse Decraene 1988; Ronse De Craene & Smets 1987). The stamens themselves may all be more or less connate, free, or in obvious groups or fascicles, members of which may be be connate (and then phalangiate) or not (see esp. Corner 1946b; also e.g. Hirmer 1917; Pauzé & Sattler 1978; Stebbins 1974; Weberling 1989; Leins 1979, 2000 and references; Prenner et al. 2008a). The androecium of Ricinus (Euphorbiaceae), with its distinctive branched stamens, has sometimes been interpreted as being cauline, but it is a modification of a fasciculate androecium (Prenner et al. 2008a). There may be variation in both mode of initiation and direction of development between quite closely related taxa, as within Loasaceae and Hydrangeaceae (e.g. Hufford 1990; Ge et al. 2007).

Other patterns of stamen development have been much commented on. Thus the stamens in some Piperales and Alismatales (for example) may be initiated in pairs and in Hydrangeaceae-Hydrangeae as triplets associated with individual perianth members. Ronse Decraene and Smets (1996) distinguished between two kinds of stamen pairs, one associated with the process of reduction in number of stamens, the other with an increase in number (dédoublement, but this term is freighted with much historical baggage and is of little value; see also Ronse Decraene & Smets 1993b for early literature on dédoublement; Wanntorp et al. 2011 for stamen doubling). By the criteria used by Ronse Decraene and Smets (1996), Caryophyllales vary in this feature, as do rosids as a whole.

Stamens within a single flower may be of different lengths, and this is commonly seen when comparing members of the two stamen whorls, although the length differences are often only slight. The androecium in Brassicaceae is tetradynamous, with four long and two short stamens, Lamiales with only four stamens are commonly didynamous, with two long and two short stamens, the anthers of the stamen pairs often being connivent (see also Caprifoliaceae-Morinoideae, although the anthers there are not connivent). In some Polemoniaceae each of the five stamens of the single whorl may be of different lengths and inserted at different heights on the corolla tube (see also Loranthaceae). There is also variation in stamen length between and sometimes within an individual when the flowers are heterostylous, as in tristylous Oxalis. Here the stamens of the separate whorls are of different lengths, and different individuals have different stamens whorls; there is also complementary variation in style length and in pollen morphology (see Schill et al. 1985; Weller 2009 for literature). The term heteranthy refers to more substantial within-flower variation in stamen morphology, and this is notably common in families such as Commelinaceae, Melastomataceae, and Fabaceae (Vallejo-Marín et al. 2010).

Ren (2008) noted that some sort of connation of the stamens is widespread. Anther connation is more common in asterids and filament connation in rosids, etc., although Campanulaceae-Lobelioideae, Calyceraceae (both Asterales), etc., have more or less connate filaments. The degree of connation of filaments and/or anthers also varies considerably, as in Campanulaceae, where variation is of systematic and floral biological interest; all Asteraceae (apart from wind-pollinated members) have connate anthers and free filaments, while the reverse situation occurs in their sister taxa, Calyceraceae. Buzz-pollinated taxa often have the anthers more or less tightly appressed to connate and forming a cone. Connation may be incomplete, as in some Fabaceae-Faboideae where nine filaments are connate and one free (this allows access to the nectar). Some Hydrangeaceae have flattened but more or less free filaments that form a tube, and in Humiriaceae interdigitating hairs from adjacent filaments help to form the tube. Finally, in Acanthaceae-Ruellieae more or less connate filaments that are also adnate to the corolla form a tube within which the nectar is found (Mantkilow 2000).

Stamen adnation. Stamens are usually adnate to the corolla only when the latter is sympetalous, but not all sympetalous taxa have stamens adnate to the corolla (e.g. Ericaceae and a number of other Ericales), some monocots with free tepals have stamens adnate to those tepals, and a few asterids (e.g. some Convolvulaceae, Diapensiaceae) have stamens adnate to otherwise free petals, the resulting tube being a composite structure. For the position of insertion of the stamens relative to the gynoecium, see Ovary Position below.

Stamen morphology is very variable, and only some of this variation is mentioned below. Hufford and Endress (1989) and Endress and Stumpf (1990, 1991) provide invaluable recent surveys of stamen morphology, Endress and Stumpf (1990) focusing on stamens that are other than tetrasporangiate; Wilson (1942), Dahlgren et al. (1985), Endress (1994b), and others also summarize variation.

Walker-Larsen and Harder (2000) review staminodes and their phylogeny (see also Ronse Decraene & Smets 2001b - lots of Staminodes vary morphologically from structures that appear to be functional stamens but produce non-functional pollen to minute and strictly rudimentary structures; they may also be very unlike stamens, being complex petal-like (especially in some Zingiberales) or nectar-secreting (Ranunculaceae) structures. The degree of development of staminodes, whether in perfect flowers (e.g. Lamiales, see Bignoniaceae, Plantaginaceae, Calceolariaceae, etc.: Endress 1998; Song et al. 2009: molecular control), or in carpellate flowers of monoecious or dioecious taxa, can vary considerably within a family, although some families consistently never have staminodes.

Filaments are usually free and slender, but rather stout filaments is the plesiomorphic condition for angiosperms. There is usually a single vascular bundle in the filament, but there are three in many Magnoliales and the single bundle may be branched, as in many Melastomataceae.

The relationship between the sporogenous tissues of the anther and the supporting tissue of the filament, the connective, provides a further useful suite of characters. The stamens may be laminar, with the anthers more or less embedded in one surface (as in many magnoliids), or they may be stout, with little distinction between the anther with its well-developed connective and the filament (in most Ranunculales, see also Rousseaceae, etc.), or the filament may be quite narrow and be attached to the base of the anther, i.e., it is basifixed. The actual point of connection may be further more or less narrowed (Nothofagaceae), or hardly narrowed, although the base of the anther thecae may still be quite distinct from the filament (e.g. Pittosporaceae, Escalloniaceae, etc.), or the filament may join the anther in what appears to be a basal pit (esp. in Saxifragales). In general in core eudicots, the anther/filament junction is often more or less dorsal (dorsifixed). Finally, Rudall (2001b) summarizes the distribution of centrifixed anthers in which the slender filament tip is inserted into a hollow in the anther in monocots (c.f. Saxifragales above). It can be very difficult to distinguish clearly between these various "types" of stamens, and my treatment of this set of features leaves something to be desired. The connective may also be distinctly prolonged, often a systematically valuable feature.

Stamens have a basically diplopyllous structure, that is, they have more or less separate ad- and abaxial parts (Baum & Leinfellner 1953). Anthers are usually tetrasporangiate, with sporangia parallel and in pairs, thecae, the paired sporangia dehiscing via a single slit they have in common, i.e. they are synangia (c.f. Green 1980, for terminology). They are sometimes bisporangiate, in which case it is the two sporangia of a single theca that are usually lost, the stamens then being unithecate (see Weberling 1989; Endress & Stumpf 1990). Anthers vary in length (c.f. Achariaceae and Salicaceae), whether or not the thecae (= sporangium pairs) are laterally or apically confluent, or are superposed, or are in part sterilized, etc. (see Trapp 1956a, b, for Lamiales in particular).

Details of anther dehiscence yield an important set of characters. Anthers are usually introrse, opening internally, but in a number of taxa they are extrorse, perhaps plesiomorphic for angiosperms; there is variation in this in the different anther whorls of a single flower in Lauraceae. As mentioned, each theca normally opens separately by longitudinal slits, less frequently by slits common to the two thecae, the thecae then being apically confluent, or by slits down each sporangium. The arrangement of the paired thecae varies; they may be in parallel, head to head, or even V-shaped. Dehiscence may be by flaps (valvate) or pores (porose), or each sporangium may open separately. Porose anthers, or pollen coming out the top of a cone formed by all the anthers, are common in buzz-pollinated plants. Only the uncommon conditions are mentioned.

Anther wall. The anatomical structure of the anther wall shows much variation, some directly connected with how the anther dehisces. There is variation in endothecial development, the endothecium normally being a single hypodermal layer of cells with distinctive thickening that is involved in anther dehiscence. Both secondary parietal cell layers (products of periclinal divisions of the primary parietal cells, themselves the product of the first division of the archesporial cells) of the anther wall normally divide further ("basic type" of wall development), or the inner cell may remain undivided (the "dicot type"), the outer divides, or the reverse occurs, in which case the endothecium develops directly from undivided outer secondary parietal cells (the "monocot type" - Davis 1966). Sampling of this character is poor and there may be considerable infrafamilial variation to the extent that the value of these types has been questioned (Hermann & Palser 2000; see also Rudall & Furness 1997; Carrizo García 2003). I have not described or analysed variation in the extent of the mature endothecium and endothecium-like tissue in any detail; Chatin (1870), Hufford and Endress (1989) and Endress and Stumpf (1991) in particular provide much information on these features. Endress and Stumpf (1991) note a correlation in eudicots, especially in the rosid area, between the development of endothecial-like cells around the connective when the latter is well developed, and around the individual thecae when the connective is less well developed. Individual taxa like Haptanthus and Styloceras (Buxaceae) show massive development of the endothecium (Doust & Stevens 2005; Shipunov & Oskolski 2011). There is also much of interest in details of the elongation of the endothecial cells relative to the long axis of the anther and in the thickenings of endothecial cells (e.g. Noel 1983; Manning 1996), but these, too, are not often mentioned below; depending on the group, there may (e.g. Manning & Goldblatt 1990) or may not (e.g. French 1986) be information of systematic interest, and the patterns of thickening are difficult to describe and categorize. In porose anthers that have lost their endothecium, a condition that is quite common in eudicots but is decidedly uncommon in monocots (Gerenday & French 1988), epidermal cells are often notably thick walled and form an exothecium; an exothecium is also present in the anthers of many gymnosperms (see also Hardy & Stevenson 2000b for wall development and buzz pollination). Some monocots that do not have porose anthers may still lack an endothecium (Johri et al. 1992).

A number of asterid I families, especially in Lamiales and Solanales, have placentoids, a parenchymatous outgrowth of the connective into the anther loculi (Hartl 1964; Endress & Stumpf 1990: also some Caesalpinioideae, Cannaceae, Zingiberaceae, etc.). The detailed distribution of this character is unclear.

The tapetum is usually glandular/secretory/parietal, with separate cells, and less commonly amoeboid/plasmodial, forming a syncytium, this latter condition being most frequent in monocots (Furness & Rudall 1998, 2001b). For general surveys, see Pacini et al. (1985, 2009), and for fifteen keys analysing different aspects of tapetal development, see Pacini (1997). Furness (2008a) suggests that there may be a distinction between amoeboid and invasive tapeta, although it is not easy to distinguish between these in much of the literature (Galati et al. 2007 describe an invasive, non-syncytial tapetum in Modiolastrum [Malvaceae]). The number of nuclei in tapetal cells varies from 1 to 6 or more, and nuclear fusion may also occur, but I have not handled this character well. The common situation seems for the tapetal cells to be binucleate, although some cells may be uninucleate. Wunderlich (1954) summarises information on this character; there is both much variation within families and also differences between observers. Wunderlich also noted extensive variation in the ploidy level of the tapetal cells.

Microspore mother cells usually form a more or less massive block of cells in the center of the sporangia. There are other arrangements, for instance, the sporogenous cells are sometimes in separate packets and the mature anther is then locellate. Variation in how individual pollen grains in a loculus contact the tapetum - e.g. all are in contact, maybe with pores, not all are in contact (Pacini 2009) - may be of systematic significance (e.g. Kirpes et al. 1996; Kimoto & Tobe 2008), but the details of such variation across angiosperms are hard to acquire.

For microsporogenesis, itself, data are taken in part from G. Dahlgren (1991), Johri et al. (1992) and Nadot et al. (2008). In simultaneous microsporogenesis the microspores initially form tetrahedral tetrads and wall formation is centripetal, although there is a considerable amount of variation here (Nadot et al. 2008; Furness 2011). There is less variation shown in successive microsporogenesis (common, but not universal in the monocots - see esp. Furness & Rudall 2000a, 2001b; Furness 2008b). There the microspores are initially in linear tetrads, but these become tetragonal, and wall formation is centrifugal. However, Sannier et al. (2007) find such correlations not to be as strong as one might wish. Indeed, Konta and Tsuji (1982) had earlier found all possible arrangements of cells in pollen tetrads in Japanese orchids, there being variation within a single pollinium, although there linear and T-shaped tetrads were least common. The occurrence of simultaneous microsporogenesis in monocots is correlated with that of trichotomosulcate pollen (Rudall et al. 1997), however, Furness et al. (2002b) caution against being overly typological when describing microsporogenesis. Schols et al. (2005) note that aperture morphology and microsporogenesis are not necessarily linked, as was confirmed by Sannier et al. (2006), who also observed infraspecific variation in microsporogenesis. See also immediately below for aperture development.

Much attention has been paid to variation in pollen and spore morphology as indicators of relationships. For a convenient glossary of pollen and spore terminology, see Punt et al. (2006) and especially Hesse et al. (2009b). Little is known about sporopollenin and its assembly into the diverse morphologies that characterize pollen grains (see Dobritsa 2011 for information). Here I refer consistently only to the number and nature of the germination pores, or to their absence, and the number of endoapertures per ectoaperture (e.g. Verbeek-Reuvers 1976). For the development of tricolpate pollen, which follows Garside's rule in those "basal" angiosperms with such grains and usually Fischer's rule in eudicots, see Banks et al. (2010); microsporogenesis in the former is successive and in the latter, simultaneous. Although most monocot families have mono(ana)sulcate grains, details of the developmental pathways of such grains may vary (Penet et al. 2005), and monocot families often have other pollen types as well, although I rarely mention these in the characterisations unless they are common within a clade. Harley (2004) reviewed monocot pollen grains that have three apertures. Operculate pollen is scattered (Furness & Rudall 2003). Inaperturate pollen grains - in many cases, e.g. Araceae, perhaps more properly referred to as omniaperturate - are scattered, but characterize some monocot families and Zingiberales as a whole (e.g. Furness & Rudall 1999, 2000b, 2001b); for a survey of inaperturate pollen in eudicots, see Furness (2007). Pantocolporate or pantoporate grains have apertures all over the surface, while zona-aperturate grains have a single, encircling aperture (Hesse & Zetter 2005); these pollen types may characterize substantial clades. If there is a single point of germination in the pollen grain, this is usually at the distal pole, but there are perhaps a few exceptions (Hesse et al. 2009a; Albert et al. 2010; Halbritter et al. 2012). However, the situation in Annona, one of the genera suspected of having this latter mode of germination, is complicated, since rotation of the individual grains of the pollen tetrad occurs during development, so making the distal pole difficult to recognize (Lora et al. 2009b for references).

See e.g. Muller (1979) for attempts to link pollen grain morphology and function. Katifori et al. (2010) examined how the pollen grain folds during harmomegathic changes in shape (see also Hesse & Zetter 2005). Porate pollen in broad-leaved angiosperms may be associated with wind pollination (Endress & Stumpf 1991), while Dajoz et al. (1991) and Furness and Rudall (2004) discuss functional aspects of the evolution of tricolpate grains.

Pollen grains are usually resistant to acetolysis; groups that are exceptions to this, like many Zingiberales and Laurales, are noted. Details of pollen microstructure, whether visible under S.E.M. or T.E.M., are mentioned only inconsistently; see Harley and Zavada (2000) for an attempt to think of pollen variation in monocots as a whole in the context of phylogenetic analysis, Blackmore et al. (2009) for a very useful decomposition of the pollen "types" of Asteraceae into a series of independent characters, and Mander et al. (2013) for a quantitative morphometric analysis of some grass pollen grains in an approach which clearly has a lot of potential. Indeed, although many palynologists have described variation in pollen morphology in terms of types, this effectively obscures variation. Furthermore, as Walker and Doyle (1975, p. 677) note, "probably no other palynological character has been responsible for so much terminological confusion as pollen wall morphology". Thus although the term ektexine as originally defined (Erdtman 1943) was more or less synonymous with sexine, it is now invariably used in the redefined sense of Fægri (1956; see also Faegri & Iversen 1964). Unlike ektexine, sexine does not include the foot layer. Sexine and nexine are distinguished on purely morphological criteria, whereas ektexine and endexine differ in their staining properties. The two sets of terms are therefore suited for slightly different applications. Doyle (2009) summarises much of the literature on morphological variation of the infratectum - the distinction between granular and columellar, the two main "types", can be less than clear. Endexine variation needs attention. In gymnosperms and at least some angiosperms it is lamellate (e.g. some Annonaceae, Acoraceae) or compact; it is usually absent in monocots, but it is present and spongy in Araceae (M. Weber et al. 1999; Weber & Ulrich 2010).

Data on the number of cells in the pollen grains at the time of their dispersal are taken mostly from Brewbaker (1967); see also Williams et al. (2014) for the evolution of pollen cell number. The basic condition is to have only two cells, those of the vegetative and generative cells, and this is associated with a sporophytic incompatibility system, although at the level of gene expression the difference between the two may not be that great (Dickinson et al. 2000). Subsequent division of the nucleus of the generative cell occurs as the tube grows down the style and results in the production of the two gametes. However, in some angiosperms pollen at the time of anther dehiscence has all three cells; this is associated with gametophytic incompatibility systems (see Wheeler et al. 2001, also below). Interestingly, the number of nuclei can vary between grains in the same individual and even within the one pollen tetrad (Lora et al. 2009a).

Zona (2001) surveyed the distribution of pollen grains containing starch in monocots, and Baker and Baker (1979) and Franchi et al. (1996) give further details for angiosperms as a whole. There are suggestive distribution patterns of taxa that commonly have starch, although sampling needs to be improved; it is fairly common for the odd taxon in an otherwise starch-free family to contain starch, and vice versa.

Pollenkitt, made up of oily substances on the surface of the pollen grain that help it to adhere to the stigma, is common in angiosperms, although less well developed in wind-pollinated plants (Teppner 2009). Trypine is more complex, and both pollenkitt and trypine are linked to the tapetum, although how they are deposited on the grain is unclear (Dickinson et al. 2000). Orbicules or Übisch bodies are also derived from the tapetum (Huysmans et al. 1998; Vinckier et al. 2000; Verstraete et al. 2011), and are associated with plasmodial syncytial tapetum (see above), although this correlation has been questioned (Galati et al. 2007). In a number of taxa raphides or other forms of calcium oxalate are mixed in with the pollen (Pohl 1941 for a review).

Pollen grains are not always dispersed singly, they may be in tetrads (e.g. many Ericaceae) because of the failure of the individual products of meiosis to separate, and these tetrads may become functionally a single grain by abortion of three of the cells (Cyperaceae, Ericaceae-Styphelioideae), while in many Fabaceae-Mimosoideae there are 8, 18, or even more grains associated in a single polyad. In Orchidaceae and Apocynaceae in particular the contents of single anthers or two adjacent half anthers, along with adjacent tissues and/or secretions form units, pollinaria, dispersed by the pollinator; each pollinaria bears two or more pollinia, commonly including all the grains of a single anther loculus. For a survey of plants with pollen in tetrads, see Copenhaver (2005), for the evolution of pollen that is dispersed as other than single grains, see Harder and Johnson (2008). Individual pollen grains or tetrads may be connected with viscin threads, very fine threads made of sporopollenin and derived from the tapetum; other kinds of threads are known as well (Hesse 1986 for a review).

For a general discussion of the gynoecium, see Shamrov (2012, 2013).

Carpel number. This is usually quite easy to ascertain in a transverse section of the ovary. "Many" in the characterisations means that there is a variable and large (more than 15) number of carpels. The number of lobes of the stigma or style is often useful confirmatory evidence of carpel number, although such lobes may sometimes be double the number of carpels, as in Euphorbiaceae, Phyllanthaceae, Boraginaceae, and Aextoxicaceae, or individual styluli may be bilobed, as in the ANITA grade, or there may be no obvious connection between style and carpel number (Endress 2014). However, in Primulaceae with free central placentation the stigma may give little indication of the carpel number. Carpel number in Papaveraceae and Brassicaceae and their relatives and in Berberidaceae has long been a bone of contention, and Brückner (2000, p. 273) expressed "her serious hope that she may be the last to have invested time and effort in refuting the 2n and 3n theories [basically, that the gynoecium is made up of two or three times the number of carpels it appears to be], at least for Berberidaceae, Papaveraceae, and Capparales." For the development of multicarpellate gynoecia and its morphological and functional implcations, see the review by Endress (2014) and a distinction between floral axis and floral apex.

In a number of taxa apparently with but a single carpel, it can be unclear whether there is really only a single carpel or the gynoecium is reduced from a syncarpous condition, i.e. it is pseudomonomerous, an overused term rarely mentioned here (for a discussion about pseudomonomerous gynoecia, see e.g. Eckardt 1937; also González & Rudall 2010; Endress 2011a for additional references). Apparently monomerous gynoecia have evolved in a variety of ways, and González and Rudall (2010) show how the character can be broken down into a number of states. Indeed, many pseudomonomerous gynoecia consist of two or more carpels in which all but one are more or less incompletely developed. 75 genera in Arecaceae alone may have only a single carpel, but in Geonoma interrupta there are three well-developed style-stigmas, but development of two of the ovary portions of two carpels is rudimentary (Stauffer et al. 2002). Similarly, although early-developing gynoecia of Atripliceae (Amaranthaceae-Chenopodioideae s.l.) may consist of a featureless annular rim surrounding a single ovule, the style is strongly two-lobed (Flores-Olvera 2011); similar early gynoecium development occurs in some Poales.

Carpel development and closure. Carpel primordia are initially U-shaped, and if the area between the arms of the U becomes meristematic, the meristematic cross-zone, the carpel develops as if it were a tube, the ascidiate condition. If no meristematic cross-zone develops, the carpels are plicate (e.g. van Heel 1981, 1983, for a survey). There are intermediate conditions, and even fully ascidiate carpels may have elongated stigmas, which one might otherwise think were the signature of the plicate carpel condition. Furthermore, ovule position is not tightly correlated with carpel type (Endress 2005b). Particularly in angiosperms of the basal pectinations, rarely elsewhere, the carpel margins are initially open (and ascidiate). Post genital occlusion occurs directly by tissue fusion or indirectly by secretion of the cells of adjacent margins (Endress & Igersheim 1997, 2000 [the latter a particularly useful summary]; Igersheim & Endress 1997; Doyle & Endress 2000); for this character optimized on trees, see e.g. P. Soltis et al. (2004) and D. Soltis et al. (2005b). Taylor (1991) discusses this and many other aspects of carpel morphology. Although angiosperms are characterized by their closed carpels, a number of taxa have young carpels that are open and have exposed developing ovules (Tucker & Kantz 2001 for a summary), and in a few taxa the carpels open as the seed develops - the plant then appears gymnospermous. This latter condition is sporadic, carpels that "open" during development being found in Dioncophyllaceae, some Berberidaceae, Malvaceae-Sterculioideae, etc.. There are recent suggestions that carpels are better interpreted as consisting of an axial placental region supplied by amphicribral bundles (phloem completely surrounding the xylem) that is subtended by a bract, now represented by the carpel wall (e.g. X. Wang 2010a; Guo et al. 2103; Liu & Ni 2013).

Carpel vasculature. Carpels normally are supplied by three vascular bundles, but in a few families there are five (Sterling 1969; Dickison 1971 for references). I have paid little attention to carpel vasculature

Carpel connation, syncarpy, is indicated by square brackets placed around carpel number. Details of the degree of syncarpy are often systematically useful, although syncarpy is highly homoplasious (Armbruster et al. 2002). In taxa like Boraginaceae, Ochnaceae and Lamiaceae with a lobed gynoecium and gynobasic style, it can seem that the carpels are free, however, there is a single central style. Endress et al. (1983) and others discuss secondarily apocarpous gynoecia. For the compitum, see below.

Ovary position. When the ovary, i.e., that part of the gynoecium bearing ovules, is inserted on the receptacle above the points of insertion of the sepals, petals, and stamens or the hypanthium (see above), it is superior, this being indicated in the characterizations and apomorphy lists by a line under the carpel number, and it is inferior when these structures are inserted on top of the ovary. Of course, there are intermediate conditions (semi-inferior, e.g. Gustafsson & Albert 1999), and in Peliosanthes teta, perhaps the only species in Peliosanthes (Asparagaceae-Nolinoideae), the ovary varies from superior to inferior (Jessop 1976). The ovary may become inferior by early vertical growth beneath the perianth members making the whole apical meristem concave; initiation of the youngest floral primordia occurs on this concave meristem (appendicular epigyny), or, to put it in a somewhat different way, the inferior ovary forms through congenital adnation of the carpels to the bases of the perianth members and stamens. The vascular traces to the stamens and perianth members diverge in an acropetal sequence (e.g. Costello & Motley 2004). Alternatively, vertical growth of the periphery of the receptacle may occur after initiation of the primordia of at least sepals, petals and stamens on a normal convex apex, the vascular supply to these structures is displaced and there are descending traces to the carpels/ovules; this is the rather rarer case of receptacular epigyny (e.g. Kaplan 1967; Soltis et al. 2003b). Unless mentioned otherwise, ovaries become inferior by the action of the former developmental pathway. However, note that the ovary development of relatively few plants has been studied in detail and whether or not the distinction between the two is really that sharp is questionable (e.g. Dengler 1972; Smyth 2005). Ovaries that are more or less immersed in nectariferous tissue alone, as in some Celastraceae, are described here as being superior. I do not use the terms hypogyny, epigyny and perigyny; these properly refer to floral architecture as a whole. Although the change from superior to inferior used to be thought of as one of the major evolutionary "trends", we are realizing that there is a growing number of cases where the ovary may be secondarily superior: Rhoipteleaceae (Fagales), Opiliaceae (Santalales, but see the discussion there), within Haemodoraceae (Simpson 1998a, b), also some members of Apiales, Asparagales (reversion in ovary position here is much discussed), Asterales, Commelinales, Cucurbitales, Saxifragales and Poales are possible examples, although few have been studied in any detail. There may be an association of such secondarily superior ovaries with parietal placentation, as in Menyanthaceae (Asterales) and Pittosporaceae (Apiales) (see also Endress 2005a and references). Saxifragaceae and relatives in particular show great variation in ovary position (e.g. Soltis & Hufford 2004; Soltis et al. 2005b).

Carpel orientation. The basic source of data is Eichler (1875-1878: see also Baillon 1866-1892; Le Maout & Decaisne 1868; Goebel 1887; Eckert 1966). When the flower has two carpels, they are usually median, i.e., they are one above the other in the median plane of the flower, but they are sometimes side by side in the horizontal plane and so are collateral or transverse. Only the latter condition is mentioned in the descriptions of 2-carpellate flowers, which can otherwise be assumed to have median carpels. Infrageneric variation in this character, with the carpels being either transverse or median, is known, as in Ribes (Eichler 1878). The arrangement of carpels in 4-carpellate flowers is usually median + transverse, and only the diagonal arrangement is mentioned. When there are the same numbers of carpels as members of the outer perianth whorl, the position (alternate, opposite) of the carpels relative to that whorl is mentioned. Carpels borne opposite the corolla are common in obdiplostemonous taxa, indeed, obdiplostemony was redefined by Bachelier and Endress (2009) to refer specifically to the position of the carpels relative to the the corolla, but such carpels are also found in taxa that have five stamens opposite the petals, i.e. obhaplostemonous taxa. The normal condition is for carpels to be opposite the calyx or outer tepal whorl. When there are three carpels and five sepals, the position (adaxial, abaxial) of the median carpel is mentioned.

Placentation in syncarpous gynoecia is described as being axile, lamellar, parietal, or free central. Basal ovules are nearly always ascending, apical ovules are pendulous. When multiovulate carpels are free, the ovules are often described as being marginal in their insertion (see also Endress 1994b). (Simpson and Burton [2006] atomize placentation in a different way in their study of Pontederiaceae.) In a few bicarpellate ovaries there is what is called an apical septum. This is supplied by by the dorsal median bundle of the carpel, not the ventral bundle, and is a modification of a gynobasic stylar morphology (see below). See Klopfer (1969b: parietal placentation)

Transseptal bundles are vascular bundles that run up the carpels in the septal radii, with branches vascularizing the placentae (Eyde 1988 and references). The normal condition, never mentioned in the characterisations, is for the vascular bundles to be in the placentae themselves. In the placentae of many taxa with parietal placentation there is an inverted bundle immediately underneath a normally orientated (i.e. phloem to the outside) placental bundle (Puri 1946).

Intralocular hairs and secretions may be evident in the young ovary. Such hairs are usually secretory in monocots (Rudall et al. 1998c), and they are commoner there than in broad-leaved angiosperms. In core eudicots the hairs, when they occur, appear to be non-secretory and may be very conspicuous when the fruit is mature, as in Malvaceae and Chrysobalanaceae. Ovary loculi are sometimes filled with fluid secreted by tissue other than the hairs.

Style connation. I initially tried to make a distinction between styluli, terminal to basal on separate carpels, or the terminal free parts of otherwise connate carpels, and the style, single and borne on connate carpels (e.g. Baumann-Bodenheim 1954); stylodia were branches of a style, be it ever so short. Indeed, stylulus is a useful term to describe the elongated, terminal structures of free carpels, or of carpel apices that are manifestly separate, so I use it here. Hanf (1935) made a somewhat similar distinction between a style, an elongated, apical portion of a syncarpous gynoecium, i.e. a fundamentally compound structure, and a stylodium, a simple structure that includes any separated apical portion of that style, or the elongated apical portion of an individual carpel, or the free apical portion of otherwise connate carpels. However, the term stylodium is rarely used in general botanical literature and has a rather vague definition. The morphological distinction between style and stylulus is that the first is a fundamentally compound structure, the second is simple. I refer to on occasion to style branches in these pages. Normally the presence of a style is associated with that of a compitum (see below); the style may be branched, sometimes even to the base, but a compitum is still evident in the ovary. For variation is style connation (and stigma morphology) within Cuscuta, see Wright et al. (2011).

Style/stylulus position. The style is usually terminal on the ovary and more or less continuous with it. Variants are noted. Thus the stylulus may be distinctly lateral on individual carpels (some Rosaceae-Rosoideae), or the single style of a syncarpous gynoecium may be lateral (Chrysobalanaceae: only one carpel is fully developed, the gynoecium apparently having a single carpel - pseudomonomery). In some taxa the styluli of a syncarpous gynoecium are borne towards the periphery of the gynoecium, as in Hillebrandia (Begoniaceae), not in the center, as is the normal condition in such circumstances; the ovary is then described as having a well-developed roof. The style may also appear be more or less impressed in the apex of the ovary because of the "bulging" of the apical part of the carpel, the extreme condition being a gynobasic style, the individual carpels (or divisions of the carpels, as in Lamiaceae) appearing to be separate from the style, which arises between them (Endress 2011a for bulging and gynobasy). In such cases the ovary may secondarily come to surround the style which then appears terminal (Hartl 1962; Jäger-Zürn 2003 and references), however, this condition can be distinguished from a truly terminal style i.a. by the pollen tube transmitting tissue going down what appears to be the central axis of the ovary to the very base and by the distinctive vascularization of the apical septum of the ovary (e.g. Hanf 1935, Fig. 7).

In the characterizations I make a point of mentioning when the apices of the carpels of an otherwise syncarpous gynoecium are free and the gynoecium itself is without an intragynoecial compitum (see below), and also when the styluli/stigmas of such carpels are close together, or whether they are marginal (see above). (I am very grateful to K. Kubitzki for discussion about and references to the suite of characters associated with styles, stylodia, etc.)

Heterostyly is scattered in flowering plants, although particularly common in Oxalidaceae, Primulaceae, Passifloraceae-Turneroideae, etc. (see also above). Heterostyly rarely occurs in taxa with monosymmetric flowers (Barrett et al. 2000). For a summary of work on heterostyly, see Barrett (1992) and New Phytol. 171(3). 2006.

Stylar canals. Styles or style branches may be solid, filled with pollen tube transmitting tissue, or hollow, the central cavity usually being lined by epidermal-type cells of a variety of morphologies (Hanf 1935: see also Williams 2009; Sage et al. 2009), but this feature is recorded rather erratically. The common condition in eudicots at least is for the style to be solid, while that of the monocots is generally hollow (Hanf 1935; Weberling 1989; Rudall et al. 1998c, 2002). There are intermediates, Hanf's (1935) "halbgeschlossene Pollenschlauchleiter", and Guéguen (1901a, 1901b-1902) quite often talks about some kind of canals in eudicots. Indeed, hollow styles can be difficult to see, because the stylar canal can be very narrow, moreover, the presence/absence of a stylar canal may vary between closely-related taxa (Bensel & Palser 1975a). Capus (1878), Guéguen (1901a, 1901b, 1902) and Hanf (1935, and references) are useful early sources of information; data for asterids are in part taken from Anderberg (1992) and Bhatnagar and Uma (1969), and for the style in a few monocots, see also Hartl and Severin (1981) and Johri (1966a, b: "Liliaceae"). In general information on this character is very scattered. Crawford and Yanofsky (2008) discuss details of the movement of the pollen tubes through stylar and septal tissues on their ways to the ovules.

The stigma) is that portion of the style, style branch or stylulus that has the function of picking up pollen grains. Stigma shape is variable and sometimes distinctive. It may be punctate, variously expanded, canaliculate or decurrent, sometimes being the length of the style. Some taxa have notably papillate stigmas, or the receptive surface may be localized on multicellular papillae or hairs (Y. Heslop-Harrison 1981 for a summary) or on one side of the style (Baum-Leinfellner 1953). There is no convenient access to the scattered literature on stigma morphology,although some taxa like Malvaceae-Malvoideae show considerable variation in stigma morphology. Although not strictly a shape characteristic, whether or not the stigmatic lobes are commissural is of some interest; commissural stigmas are perhaps particularly common when placentation is parietal.

The presence of secretions produced by the stigmatic surface may be of interest. Wet stigmas are quite frequently found in taxa with binucleate pollen grains and sporophytic incompatibility systems, and dry stigmas in taxa with tricellular pollen gains and a gametophytic incompatibility system (CHECK: see J. Heslop-Harrison 1981; Y. Heslop-Harrison & Shivanna 1977; Schill et al. 1985). However, variation often seems to occur between families that are closely related and taxa with porose stigmas can be hard to place (Dulberger et al. 1994); in general the nature of the stigma surface needs further study (e.g. see Igersheim et al. 2001 for conflicting reports in Alismatales). The plesiomorphic condition for angiosperms may be to have a dry stigma (e.g. Sage et al. 2009).

The correlation of stigma surface with incompatibility type is not perfect (Y. Heslop-Harrison 1981; Wheeler et al. 2001). Details of incompatibility systems are described by Charlesworth et al. (2005), Barrett (2013), and others, and there may be a correlation between pollen grains that are bicellular at dispersal and sporoophytic incompatability systems and tricellular pollen and gametophytic incompatability systems. For the evolution of cell number in pollen grains, see Williams et al. (2014). Both gametophytic and sporophytic systems seem to have evolved in parallel, but it has been suggested that the gametophytic system in both rosids and asterids may be identical (e.g. Steinbachs & Holsinger 2002: the stylar response is mediated by a glycoprotein with ribonuclease activity). At exactly what level incompatability "types" might be synapomorphies is unclear, largely because so little is known about details of the whole system. However, a RNase-based gametophytic incompatibility system might be a synapomorphy at the level of (most) core eudicots. Ingrouille and Chase (2004) analyze incompatibility in the context of phylogeny, and they show that both main incompatibility types are scattered throughout the angiosperms. Many of the incompatibility systems in monocots, where they are quite common, are as yet uncharacterized (Sage et al. 2000). For incompatibility systems and their evolution, see also Dickinson et al. (1998), Hiscock and Tabah (2003), Igic and Kohn (2001, 2006), Igic et al. (2006), Franklin-Tong and Franklin (2003), Franklin-Tong (2008), articles in Ann. Bot. 108(4). 2011, Robertson et al. (2010), and Raduski et al. (2012).

Compitum presence. In many syncarpous gynoecia with at least partly plicate carpels the loculi/placentae are in connection with each other via an intragynoecial compitum, tissue that allows pollen tubes to fertilize any ovule no matter where the pollen grains landed on the stigma, or, if the style is branched, no matter on which stigma they landed (Carr & Carr 1961; Friis & Endress 1990; Endress 1994, 2011; van der Schoot et al. 1995). If the carpels are completely synascidiate there can be no intragynoecial compitum, on the other hand, a compitum can develop by post-genital connation of the styles in taxa like Apocynaceae and Malvaceae-Sterculioideae in which the carpels are otherwise free. Some Nymphaeales, Laurales, etc., with free carpels have an extragynoecial compitum, of which the hyperstigma is a variant, and here carpels are placed in contact not by pollen tube transmitting tissue but by secretions of the stigmas through which the pollen grains grow (e.g. Endress 1982).

Ovules. Useful surveys of various aspects of ovule morphology and development are those of Takhtajan (editor: 1985, 1988, 1991, 1992), Kamelina et al. (editors: 1981, 1983), Batygina et al. (editors: 1985, 1987, 1990), Johri et al. (1992), Danilova (editor: 1996); see also Shamrov (2002, 2003, 2004, 2006) and Endress (2011b). Other earlier studies can still be consulted with profit (e.g. Chatin 1874; Vesque 1876; Warming 1876; Guignard 1882; Brandza 1891; van Tieghem 1898; Dahlgren 1916, 1927; Mauritzon 1933, 1936a, 1939a, 1939b; Maheshwari & Kapil 1967, useful summary) and indeed need to be as Endress (e.g. 2011b) has redefined some terms so that the original literature now more than ever cannot be simply mapped on to the present. Rudall (1997) surveyed ovule morphology in monocots; Endress and Igersheim (1997, 1999) and Igersheim and Endress (1997, 1998) describe ovule morphology and anatomy in magnoliids and the ANITA grade and Taylor (1991) also emphasized these taxa in his survey. However, for a number of taxa, the only information available remains that in early works such as those just mentioned.

Ovules are complex structures, and ovule morphology includes a number of characters. Much ink has been spent in working out a classification of ovule "types" (e.g. Shamrov 1998 and references), nucellus types, etc., and in providing sets of names for all the variants, although these can be difficult to recognise and the terms are inconsistently applied. There are an increasing number of suggestions that ovule terminology needs to be reformed (e.g. Shamrov 1998; Endress 2005c). Although some of the new terms that are being proposed are in part confusing and, like the old terms, are arbitrarily delimited, terminological reform is badly needed.

Some parasitic or hemiparasitic taxa lack organized ovules, an embryo sac alone being readily recognizable (see Santalales in particular, Gentianaceae s.l.), and that makes understanding aspects of their embryology difficult since ovule orientation, seed/fruit anatomy, etc., become problematic; about the only feature that can be estimated easily is the number of ovules per ovary, and even this is difficult if there is more than one archesporial cell.

Ovule number is always mentioned, although it is often very variable. "Many" means that there is a variable and large (more than 15) number of ovules.

Ovule orientation. The direction of curvature of ovules relative to the axis of the flower and the carpel margins is usually consistent within taxa where there are few ovules, and ovule orientation is usually mentioned only for such taxa. Epitropous ovules are curved adaxially (= dorsal raphe), apotropous ovules are curved abaxially (= ventral raphe: Björnstad 1970); this variation is independent of whether the ovules are apical or basal. Since I initially recorded only the apotropous condition, epitropous ovules may be under-reported. Pleurotropous ovules are held sideways so the micropyle faces laterally. When there are many ovules per carpel their orientation is either variable or pleurotropous; ovules are epi- and apotropous within a single ovary of Pittosporum floribundum (Narayana & Sundari 1983). Even in families like Rutaceae, Anacardiaceae, Sapindaceae and Menispermaceae where there are only two ovules per carpel, ovule orientation can vary within the carpel, or there can be changes during development. Thus in Burseraceae the ovules start off more or less apotropous and become epitropous (e.g. Svensson 1925; Mauritzon 1936; Bachelier & Endress 2009). Endress (1994b) suggested that it might be more useful to refer to the curvature of the ovule with respect to that of the curvature of the carpel margins. These terms, syntropous, curvature in the same direction as that of the carpel margins, versus antitropous, curvature in the opposite direction, focus on curvature that is at right angles to the axis that determines epi- versus apotropy in plicate carpels. In gymnosperms, the ovule may be erect or recurved, i.e. with the micropyle pointing away from the axis or towards it; again, ovule orientation can change during ontogeny (Taylor et al. 2009).

The orientation of the ovule in relation to its stalk, the funicle, has attracted much attention. Ovules can be described as being atropous (= orthotropous, but straight is better), anatropous, amphitropous, campylotropous, circinotropous or hemitropous, depending on the curvature of the body of the ovule and its relation to the funicle; these terms simply refer to points along a continuum, and ovule "type", as with micropyle "type" (see below), can change during development (e.g. Mauritzon 1934g). Gifford and Foster (1989) and Bouman and Boesewinkel (1991) emphasize the variety of ways in which an ovule can become campylotropous. Endress (2011b) has linked the curvature of the ovule to the development of a second integument; straight ovules are often unitegmic. This is not the case in asterids, but here the nature of the single integument is questionable (see below); bitegmic Piper has straight ovules.

Integument number is a character of some systematic interest. Shamrov (2003) provides a useful survey; see also Endress (2011b). Ovules usually have one (unitegmic - ovules often straight!) or two (bitegmic) integuments. A unitegmic ovule may arise either by adnation of these two integuments, or by suppression of one of them (Bouman 1984). The outer integument may be dermal or subdermal in origin, the inner integument epidermal (?always: van Tieghem 1898), and Grootjen and Bouman (1981) and Bouman (1984) suggest that this variation may be of systematic significance, but I have not followed up on their suggestion (see Pankow 1962 for some details); in any case, observations are relatively few and there is infrafamial variation (Bor & Bouman 1975).

Endress (e.g. 2011; Endress & Matthews 2006a) has emphasized the importance of the relative integument thickness as a systematic feature. For general information on integument thickness, see the surveys (Takhtajan, ) mentioned above, also e.g. Netolitzky (1926), Huber (1969), Corner (1976), Grootjen and Bouman (1989), and Johri et al. (1992), as well as very many studies on individual species. Integuments are commonly two or three cells thick over the body of the ovule, and only when the thickness is different is this included in the characterisations; although integuments are commonly rather thicker at the micropyle than elsewhere, this is generally not mentioned. In these pages integument thickness is recorded as the number of cell layers visible when the ovule is mature; multiplicative integuments are strictly speaking those in which integument thickness increases after fertilization (but c.f. e.g. Tokuoka & Tobe 2002 who use "multiplicative" as equivalent to a "thick" integument - several cells across - and this at the ovule stage), and so this feature is mentioned when the seed is described. In straight ovules the outer integument is often thinner than the inner, and it has been suggested that a thick (outer) integument helps to ensure curvature of the ovules (Endress 2005c). The outer integument at the time it is initiated may be cup- or hood-shaped (Yamada et al. 2001); the significance of this is unclear (but see Endress & Igersheim 2000; Endress 2005c). Lobing of the integument is uncommon (but see e.g. van Heel 1970); Endress (2011b) discussed the association of integument lobing with other features of the ovule.

The micropyle in the mature ovule, i.e., at the time of fertilization, may be formed from the outer integument only (exostomal), the inner integument only (endostomal), or both integuments (bistomal), or it may be zig-zag, the integuments overlapping in such a way that the passage from the nucellus to the outside is not straight, or in taxa with a single integument, the micropyle is clearly offset with respect to the apex of the nucellus... Most ovules with zig-zag micropyles are variants of the bistomal "type". In a few taxa, e.g. some Laurales, the nucellus is not completely covered by the integuments when the flower is at anthesis, the micropyle then being absent and the ovule being described as being naked. Extensive infraspecific variation in micropyle morphology has been observed in Putranjivaceae (Tokuoka & Tobe 1999), and given the sampling of this character, more variation is to be expected. Indeed, there appears to be extensive inframilial variation, although some of this may be the result of observations being made on ovules of different ages. For example, Agrawal (1952) noted that the micropyle of Lilaea subulata (Juncaginaceae) was naked even the 8-nucleate stage of the embryo sac, endostomal when the embryo sac was mature, the polar nuclei having fused, while it was bistomal just after fertilization (see also Nair & Joseph 1960).

Nucellus condition. Shamrov (2002) discusses nucellus morphology in some detail; Endress (2003c) provided extensive information on the distribution of the various kinds of nucellus in Malpighiales and many asterids, while Endress and Matthews (2006a) focused on variation in rosids. In crassinucellate ovules the archesporial cell (see below) divides periclinally and there are two or more hypodermal layers in the ovules above the embryo sac - effectively a eusporangium. In tenuinucellate ovules there is no periclinal division of the archesporial cell, which gives rise directly to the embryo sac, and so there are no parietal cells between the embryo sac and the epidermis of the ovule - the leptosporangiate condition. In a "pseudotenuinucellate" ovule the parietal cell does not divide again (it may even disappear), and so the ovule may look as if it were tenuinucellate; weakly crassinucellar (Endress 2003c, 2011b; Endress & Matthews 2006a) is a better name for this condition. Endress (2003c) added the term incompletely tenuinucellar; here there are no hypodermal cells above the embryo sac but there are such nucellar cells laterally and/or below it. A nucellar cap quite often develops when epidermal cells at the apex of the ovule divide periclinally (giving "pseudocrassinucellate" ovules - Davis 1966; also Bouman 1984; Rudall 1997; Endress 2003c, 2011b). Note that otherwise tenuinucellate ovules that have this nucellar cap have also been called "pseudocrassinucellate", but this term would seem to have little to recommend it; here nucellar caps are specifically mentioned whenever they occur, whether the ovule is crassi- or tenuinucellate. Nucellar caps seem to be underrecorded in gymnosperms (Singh 1978). Interestingly, a limited survey suggested that tenuinucellate ovules tend to be larger than crassinucellate ovules (Greenway & Harder 2007).

Funicle length. Some taxa, most notably in Caryophyllales, have long funicles; these are defined as being about the length of the body of the ovule at anthesis or longer. In taxa with circinotropous ovules the funicles are very long and curled. In some groups, e.g. Sapotaceae and Sapindaceae, the ovule is sessile. When funicle length is not mentioned it can be assumed that it is unremarkable.

Ovule variants. The nucellus may protrude as a beak through the micropyle (Bouman 1984, for data). Obturators, whether funicular, placental, or integumentary in origin (Shamrov 2004), are closely associated with the micropyle; the ponticulus is a kind of obturator found in some Anacardiaceae. Unfortunately, I have not been systematic in recording obturator type. Vascular bundles from the funicle usually terminates in the base of the ovule, but bundles may also occur in the outer or somewhat less frequently in the inner integument; they may be branched or not. They are mentioned in the description of the ovule, and sometimes also in that of the seed coat. The endothelium (integumental tapetum is a synonym) is a distinctive layer or layers of cells (sometimes up to 32-ploid) of the inner (or only) integument immediately abutting the nucellus; it is commonest in unitegmic taxa (Kapil & Tiwari 1978) and may directly abut the embryo sac due to the breakdown of the intervening cells. In some Lamiales the endothium has much-branched processes from the cell wall and seems to function as transfer tissue (Joel et al. 2012). Swamy and Krishnamurthy (1971) suggest that monocots lack an endothelium, but other authors describe one there; most monocots lack any parietal tissue or it is one, perhaps two, layers thick. The chalaza, tissue at the base of the embryo sac/apex of the funicle, is variously developed, and there is frequently distinctive vasculature, or thickening or staining of groups of cells in the chalazal region, the hypostase (see e.g. Vesque 1903, also Lötscher 1905 for early literature), c.f. the epistase. It has been suggested that in Onagraceae, at least, hypostase presence is correlated with dry conditions and its presence is environmentally determined (Johansen 1928) and correlations betweem absence of a hypostase and the presence of chalazal endosperm haustoria (Vesque 1903), etc., have been suggested. Sometimes a group of nucellar cells protrude into the base of the embryo sac, forming the postament (Dahlgren 1940 for a survey of taxa with a postament), or nucellar cells are simply persistent at the base of the embryo sac, forming a podium, or the chalazal cells die early and form a persistent cap-like structure, the petasus, at the base of the embryo sac. This whole set of terms is not very satisfactory. For instance, the hypostase may appear at different stages of the development of the ovule, and morphologically quite different structures may be called a hypostase (e.g. Bor & Bouman 1975) in the same family (van Tieghem 1903a: Euphorbiaceae) or even in the same article (Johri & Kapil 1953); the same is true of epistase.

Embryo sac/female gametophyte. For a review, see Kapil and Bhatnagar (1981). The archesporial cell (megaspore mother cell) is usually single. Exceptions are quite widespread, and where they are common they are usually noted; the odd occurrence of two or more megaspore mother cells is frequent and is often ignored. For megapsore mother cell development and megaspore differentiation, see Demesa-Arévalo and Vielle-Caldaza (2013). In some clades, e.g. Fagales, numerous megaspore mother cells often occur, and several embryo sacs may develop in the one ovule (see also Bachelier & Friedman 2011). Normally a single megaspore mother cell produces a single embryo sac or female gametophyte from the germination of a single megaspore, i.e., it is monosporic in origin. The megaspore itself is a meiotic product of a single megasporocyte or archesporial cell(see Bouman 1984 for some information). The Polygonum-type embryo sac, monosporic and with eight nuclei, the egg cell being adjacent to the micropyle, is commonest in angiosperms and in part for that reason had long been thought to be plesiomorphic/primitive. However, this view has been shown to be incorrect, both Nymphaeales and Austrobaileyales have 4-nucleate embryo sacs and subsequently a diploid endosperm while Amborella has a 9-nucleate embryo sac and triploid endosperm (see e.g. Friedman et al. 2003a, esp. b; Friedman & Williams 2004; Friedman 2006). There is a considerable amount of older literature on embryo sac development, e.g. Vesque (1878), Fagerlind (1938c, 1939b, 1944, esp tetrasporic embryo sacs); see also S. Maheshwari (1955) for an evaluation of reports of bisporic embryo sacs and P. Maheshwari (1947) for a now somewhat dated review of tetranucleate embryo sacs. There is sometimes substantial infraspecific variation in the development of the embryo sac (e.g. Fagerlind 1939b: Limnanthes).

The two synergid cells that lie next to the egg cell are intimately involved in the fertilization process, as is also the central cell (Puwani et al. 2007; Chen et al. 2007). For a discussion on the persistence of antipodal cells and their multiplication, see Holloway and Friedman (2008). On occasion, the whole embryo sac enlarges greatly and become haustorial (Mikesell 1990 for a review). Highly reduced ovules present problems for the interpretation of embryo sac morphology because of the absence of landmarks to orient the observer (see also above). It has been suggested that the egg apparatus arises at the lower pole of the embryo sac in some myco-heterotrophic Gentianaceae (Bouman et al. 2002), but we may be dealing with a highly reduced anatropous ovule. Ross and Sumner (2004) describe ovule development in Arceuthobium americanum in detail, but embryo sac orientation there and in Viscum seem to be diametrically opposite (cf. Zaki & Kuijt 1994, 1995).

For an outline of the major variants in embryo sac morphology, see e.g. Haig (1990: cautions on the typology of the embryo sac "types") and Johri et al. (1992). As Madrid and Friedman (2008) note, detailed studies that go beyond mere pattern and that are placed in a phylogenetic context are the best way to understand the evolution of embryo sac development, rather than considering transformations of these "types" in the abstract. Friedman (2001b) outlines the main theories of the evolution of the embryo sac, which is characterized (usually) by its bipolar development, that is, the micropylar and chalazal haves of the embryo sac are in some respects very similar. Any adaptive significance of the variation in embryo sac development, some of which affects the balance of maternal and paternal genes in the parent sporophyte-endosperm-seedling system, is still not well understood (but see Friedman et al. 2008).

Fertilization. In all gymnosperms a substantial time elapses between pollination and fertilization, whereas in most angiosperms fertilization occurs within two days of pollination. However, in some angiosperms pollination is delayed, in some species of Quercus as much as a year or so, while in Corylus avellana the ovule may not have even started developing at the time of pollination; in such cases pollen tube growth is also notably intermittent. This may lead to competition between the developing ovules (Sogo & Tobe 2006d for literature). The pollen tube usually grows down the micropyle before penetrating the embryo sac (porogamy), but in a few taxa, most notably a number of Fagales, the tube penetrates the ovule in the chalazal region (chalazogamy) or sometimes through the side.

There is interesting variation in pollen tube wall composition in seed plants (Yatomi et al. 2002). As to pollen tubes of angiosperms, Prósperi and Cocucci (1979) and Cocucci (1983) suggest that the occurrence of callose in pollen tubes as they grow down the style may be of systematic interest; these plugs were absent in Lamiales and present in Solanales, for example. Normally, as angiosperm pollen tubes move towards the ovules, callose is deposited at intervals along the tube, a feature that may be of considerable interest in the evolution of angiosperms (e.g. Williams 2008); Parre and Geitmann (2005) discuss the mechanical properties of callose. Mogami et al. (2006) suggested that both details of plug morphology and periodicity of plug deposition differs between monocots and broad-leaved angiosperms (complete and regularly deposited vs. incomplete and irregularly deposited), but there are many exceptions.

Fruit, Seed and Seedling.

For definitions, etc., see the Glossary.

General information about fruits is widely scattered; Leins (2000) and especially Leins and Erbar (2010) make interesting observations. For ideas about the evolution of fruits and seeds and of the plant as a whole that are stimulating, if now somewhat suspect, see Corner (e.g. 1953-1954). For some stunning photographs of fruits, see Stuppy and Kesseler (2008). Details of fruit (and seed) structure can be related to their function in dispersal (van der Pijl 1982); fruit and seed (diaspore) dispersal is sometimes mentioned in the section on Evolution in the order pages. When thinking about the ecology of diaspore dispersal, some of the morphological distinctions that are made below can usefully be ignored (see also the discussion on seeds). Thus seeds with elaiosomes may be functionally equivalent to achenial-type fruits with a distinct fleshy zone, and plumed seeds and fruits may also be functionally equivalent. Leins and Erbar (2010 - e.g. "nautochores"; also Vittoz & Engler 2007) provide a well-illustrated summary of terms, morphologies and mechanisms involved in diaspore dispersal; for surveys of seed dispersal, see Snow (1981) and Howe and Smallwood (1982).

Embryo development. Study of the patterns of cell division in young embryos and of the roles of the cells in the production of the different tissues of the mature embryo has resulted in embryos being placed in a number of "Types" and "Variations" (Johansen 1950; see e.g. Johri et al. 1992, pp. 62-80 for a good summary). This is perhaps because, as Souèges emphasized, there was a belief that only internal factors affected development and hence there was the possibility of getting at "laws" of embryogeny - of which he recognized four (Souèges 1937); these laws allowed him to recognize groups of embryo types and to understand why they were linked ("enchaînement"!) in a classification (Souèges 1938). In this context, it seemed that developmental variants were of potentially great phylogenetic importance (see Wardlaw 1955 for a criticism). However, there is more than one way to look at these patterns and roles. Thus Yamazaki (1982, see also 1974) emphasized the position of origin of the root cortex initials when detailing his variants (see also Charbonnier & Vallade 2011). Johansen (1950, p. 94) observed of the six "Types" he recognized, "merely to state a prophecy, it is believed that they will survive the test of time". To quote Lersten (2004: p. 179) "Many 19th century investigators of embryogeny concluded that cell walls in the early proembryo form by precise patterns of cell division that can be classified into types characteristic of certain groups of plants. Other investigators who bothered to sample several proembryos of the same species usually found that these patterns were variable, as Wardlaw (1955) pointed out." Indeed, little attention was usually paid to the sometimes quite extensive infraspecific variation in such features (but see e.g. Sachar 1956a).

Variation in the plane of the first cell division of the zygote (Philipson 1990; Kaplan 1999: 1 ch. for summaries) seems to be at a rather high level and has been mentioned. However, I have not utilized other variation in early embryo development very much, and I have largely ignored the embryo "types" that still remain the focus of some embryological studies. Taxa like Phaseolus and Poaceae have apparently disorganized cell divisions that contrast sharply with the more precise patterns found in Arabidopsis and Capsella, yet without any obvious effect on embryo development (Johri et al. 1992; Chandler et al. 2007; Lau et al. 2012).

The embryonic suspensor is not part of the embryo s. str., and it varies considerably in size and morphology. De Fulvio (1979) suggests that this feature (along with endosperm type) characterized groups of families (e.g. in the asterid I group); in some taxa, however, the suspensor does not develop at all. Yeung and Meinke (1993) discuss the the physiological significance of the suspensor; there the cells may be highly endopolyploid and the genome size can reach 8000 C. The radicle develops where the suspensor attaches to the developing embryo, but apparently not always in monocots (Yamashita 1976).

The early literature on endosperm development also focussed on the evolution of endosperm "types". The initial divisions of the endosperm may be accompanied by cell wall formation (cellular endosperm), or they may involve the nucleus alone, only later cell walls are laid down (nuclear). In helobial endosperm, the endosperm forms two compartments in one or both of which the protoplasm is not immediately divided by wall formation despite division of the nucleus (Wunderlich 1959 for a summary). Krishnamurthy and Indra (1985) summarise discussion over the occurrence of helobial endosperm; note that some authors restrict its occurrence to monocots. This classification hardly describes the subtleties of endosperm development (e.g. Floyd et al. 1999; Floyd & Friedman 2000 [comprehensive dissection of endosperm development], 2001; Friedman 2001a, b; Linkies et al. 2010). Thus the first division is frequently variously asymmetric (c.f. embryo sac development); cell divisions in one or both of the chambers that result from the first division may be nuclear; etc. Nevertheless, Olson (2004) noted that many distinctive details of cellularization in the nuclear endosperm of Arabidopsis and cereals were similar, although cellular endosperm must have evolved indepedently in the two groups. It is usually triploid, but other ploidy levels are known; thus Nymphaeales and Austrobaileyales, with 4-nucleate embryo sacs, have diploid endosperm, while in Peperomia the endosperm may be 15n. Endosperm is not developed at all in a few angiosperms, e.g. Podostemaceae. See Olsen (2007) for the development and molecular biology of endosperm.

In a few taxa endosperm-like tissue is in fact perisperm, derived from nucellar or similar tissue of the parental sporophyte. Rudall (2000) emphasized a distinction between perisperm and chalazosperm, the latter being derived from the chalaza, not from subdermal nucellar tissue. Even perisperm s. str. originates in various ways, and can develop from the nucellar epidermis alone, as in Acorales (e.g. Floyd & Friedman 2000), or from other parts of the nucells - and there is a tendency to develop a sets of terms to describe this variation.

Fruit type. I define fruit loosely as a post-fertilization structure developed from either a single carpel; or connate carpels (ovary superior); or connate (or free) carpels (ovary superior) + associated calyx and/or corolla; or connate (or free) carpels + inferior ovary or hypanthium; or ditto + carpels of adjacent flowers; or carpels of separate flowers plus inflorescence axis...

I had initially wanted to use terms for fruit "types" that reflected whether the fruit was derived from a superior or from an inferior ovary, and if from the former, whether the carpels were free or fused. However, some of the terms were cumbersome and others flouted common usage; using separate terms for fruits from apocarpous and from monocarpellary gynoecia runs in to similar problems (e.g. Leins 2000; c.f. Leins & Erbar 2010). Furthermore, a number of fruit types used in the literature refer - more or less by convention - to fruit morphologies found only in single families or parts of families ("pepo", "hesperidium", "legume", "anthocarp"), yet they would seem to have a wider application - do not blueberries have "pomes", just like apples? Other fruit types imply distinctions when either none really exist and/or variation is at a lower level than is the focus here - thus the confusing set of terms "silique", "siliqua" and "silicula" can be disposed of, which must be something of a relief to all. If more detail is required about how fruits are categorized, extremely complex and detailed sets of terms are available, for which, see Stopp (1950), Baumann-Bodenheim (1954), Hertel (1959), Barroso et al. (1999), Spjut (1994, see also 2003 onwards), Roth (1997), Bobrov et al. (2009), etc., etc.; Judd (1985; see also Judd et al. 2007) and Leins and Erbar (2010) provide a simplified set of terms. Since the number of fruit "types" may run to three figures and like all "types" serve to obscure rather than to clarify details of variation, I find little to recommend in any of these detailed sets of terms. Nevertheless, despite the problems with fruit types (see e.g. Clifford & Dettmann 2001; Costea et al. 2003; Steel & Wilson 2012), fruits are complex structures and there is much of systematic interest to be gained from their careful study.

Details of fruit anatomy are not often mentioned in the characterizations. However, general information can be found in e.g. Vaughan (1970) and especially Takhtajan (1985 and subsequent volumes - summary and new data); some more recent studies touch on the fruit anatomy of more limited groups, e.g. Wannan and Quinn (1990), Romanov et al. (2007), Pabon Mora and Litt (2007), Bobrov et al. (2012 and references), Arecaceae, while Moon et al. (2009b) and Salmaki et al. (2009) both describe the anatomy of nutlets in Lamiaceae, and Seibert (1978), Ovczinnikova (2007) and Simpson and Hasenstab (2009), ahat of nutlets in Boraginaceae-Boraginoideae. Indeed, the anatomy of the fruit wall allows one to decide whether fruits that are ostensibly of the same basic kind really are similar enough to be considered immediately comparable - i.e., by applying Remane's criteria of special properties (anatomy), development, etc. - simple gross anatomy may be insufficient (Clifford & Dettmann 2001). Thus Bobrov et al. (2005) and others discuss the need to study the developmental origins of the woody layer surrounding the seed - not all drupes are created equal. Manchester and O'Leary (2010) report on the diversity of morphologies that is encompassed by "fin-winged" fruit, and use their knowledge to assign fossils of such fruits mostly to several different extant families.

Here I restrict myself largely to the simplified terms suggested below and defined in the glossary, although additional information may be provided in the characterisations. Any fruit descriptions/"types" must be interpreted carefully, particularly taking into account the position of the ovary, but also the presence of other organs associated with the fruit proper and involved in fruit or seed dispersal. The terms used are for descriptive purposes only, and too much importance should not be attached to the fact that two groups have the same or different kinds of fruits. Thus there may be only very slight differences between a circumscissile capsule/pyxidium and an achene/utriculus, as Costea et al. (2003) emphasize in a study of the fruits of Amaranthus. Fruit morphology is evolutionarily rather labile, berries having evolved many times, for example, within monocots (e.g. Dahlgren & Clifford 1982; Givnish et al. 2005, 2006b), and capsules may even be derived from berries (Rasmussen et al. 2006). Finally, it should be noted that there may be extensive commonality at the genetic level in the control of the development of different kinds of fruits. Thus the homologous MADS box genes SHP1/2 (Arabidopsis - the "shatterproof" gene) and TAGL1 (Solanum esculentum - tomato agamous-like) are involved in fruit dehiscence and fruit expansion and ripening respectively, and similar genes are also involved in other aspects of fruit development in other eudicots (Vrebalov et al. 2009).

Of the terms commonly used here, products of superior, syncarpous ovaries include a capsule, a dry, dehiscent, syncarpous fruit; berry, which has a ± entirely fleshy pericarp; and a drupe, which is indehiscent and fleshy, but with a more or less woody endocarp enclosing the seeds individually or together ("stones" or "pits"). An achene is a dry, indehiscent, single-seeded fruit with a moderately developed pericarp, and is generally used for the product of a single carpel, but it also used for the fruits of Asteraceae, which have a syncarpous inferior ovary; "cypsela" is a term used to distinguish these fruits from achenes, etc.). A nut is usually larger and with a very strong pericarp or fruit wall; it is generally used when the gynoecium is syncarpous, but the distinction between nut and achene is often not clear in the general literature. A follicle is a single carpel dehiscing down the adaxial side; the suffix "-let" is useful on occasion when describing fruit derived from a single carpel, so other terms sometimes used here for fruits derived from separate carpels include berrylet and drupelet. Fruits that are the products of an inferior ovary are described using the same terms as for fruits developed from syncarpous superior gynoecia. Of course, the actual tissues involved e.g. in being fleshy may well differ in the two cases (but see below). A schizocarp is any syncarpous fruit that splits into separate units, each usually based on a single carpel, and consisting of pericarp plus seed or seeds; these units are dispersed independently, and/or the seeds in them may later be released. Many schizocarps are variants of septicidal/septifragal fruit dehiscence (see below). A samara is any dry, winged, indehiscent fruit, and a lomentum is a fruit with transverse constrictions across which the fruit later breaks. A few taxa have more than one fruit type on the plant, a phenomenon known as heterocarpy (Kaul et al. 2000).

Capsules usually dehisce either down the septal or placental radii or down the interseptal or interplacental radii - such fruits are described as being septicidal (or septifragal, a variant) and loculicidal respectively. In this context, no distinction is made between fruits derived from ovaries with axile placentation and those with parietal placentation. Thus Ericoideae, Cleomaceae and Brassicaceae are all described as having septicidal capsules, even though the first has an ovary with septae and largely axile placentation, the second, a unilocular ovary and parietal placentation, and the third, a false septum and parietal placentation; dehiscence in all occurs in a topographically similar position (see also Stopp 1950). Dehiscence may also be circumscissile, the fruit opening around the circumference of the ovary or carpel (a fruit with this type of dehiscence is often called a pyxidium). In dry, dehiscent fruits with an inferior ovary, the actual dehiscence is often via openings in the pericarp at the top of the fruit, as in many Myrtales, and so dehiscence can reasonably be described using the terms just mentioned. Dehiscence may also occur through the sides of an inferior ovary, as in Campanuloideae, Orchidaceae, etc.; this situation is described clearly when it occurs, but dehiscence is here not simply septicidal or loculicidal.

The above terms are usually used to describe the products of the gynoecium of a single flower. Another way of describing fruits is to distinguish between a simple fruit, the product of a syncarpous gynoecium, or of a single, free carpel, an aggregate fruit, all the products of separate carpels of a single flower, and a multiple fruit, a unitary structure that is produced from several separate flowers, although the notion of a simple fruit so defined is rather vague. An anthocarp is a fruiting structure produced from a single flower but which is more or less closely invested by an accrescent calyx or perianth; although it is quite often used to describe the fruits of Nyctaginaceae, there is no reason why is should not apply to those of Dipterocarpaceae, Elaeagnaceae, etc., and it is a term of little utility.

Whether or not the calyx is deciduous, marcescent, persistent or accrescent (as in the fruit type anthocarp!) in fruit can be a surprisingly consistent character at higher levels and is generally mentioned in the characterizations.

For a survey of mucilages and gums in fruits, see Grubert (1981).

Seed size (mass) is obviously a continuous variable. Dust seeds (see also the micro seeds of Martin 1946) have no precise definition except that they are very small, usually less than 5µg dry weight and 0.2-0.3(-4) mm long for embryo + endosperm, and the embryo is often undifferentiated (Eriksson & Kainulainen 2011).

Seeds may have a variety of appendages. These include arils, which "typically" are fleshy, post-fertilization outgrowths of the funicle, although there has in the past been a great deal of argument about what an aril really is and how it can be distinguished from an arillode (Corner 1953, 1976; van der Pijl 1955, 1966, 1982; Endress 1973, and references). Here I do not restrict the term "aril" to funicular outgrowths alone, rather using the term for any more or less fleshy post-fertlization outgrowth of the seed, and I also try to give the position of origin of the structure; if this is not mentioned, it can be assumed to be the funicle. Caruncles are also widespread, and are generally somewhat harder outgrowths of the seed in the micropylar region; a coma is a tuft of hairs on the seed. An elaiosome is an ecological, not morphological, term, and it applies to any appendage of a small seed, often arillate or carunculate, or fruit(!) that attracts ants, although it may also have other functions (Lisci et al. 1996, see also Beattie 1983). Elaiosomes are notably common in a number of clades; Lengyel et al. (2009 [see especially the electronic Supplement], 2010) provide valuable information about their taxonomic distribution while Fokuhl (2008) focused on European ant-dispersed plants.

Details of seed coat anatomy are taken especially from Brandza (1891), Netolitsky (1926), Schnarf (1937: gymnosperms only), Huber (1969), Vaughan (1970: testa and tegmen not always distinguished), Corner (1976), Krach (1976), Takhtajan (editor: 1985, 1988, 1991, 1992, 2000, 2004), Danilova (editor: 1996), Werker (1997), and Bouman and his collaborators (e.g. Bouman & Boesewinkel 1997); see also Batygina (2006). As Wunderlich (1967a), Corner (1976), G. Dahlgren (1991) and many others have emphasized, variation in seed coat anatomy is of considerable systematic interest. Fortunately, details of seed coat anatomy can often be observed in hand sections that are stained for lignin, however, which cells are testal and which tegmic in origin - an important distinction - can be difficult to see if the coat is mature.

The testa develops from the outer integument and the tegmen from the inner integument. The prefixes exo- meso- and endo- refer to tissues developing from the outer epidermis, the middle part, and inner epidermis respectively of either the testa or tegmen (Corner 1976; see also Schmid 1986). The shape, lignification and inclusions of the cells in these layers is of interest, in particular, much attention has been paid to which part of the seed coat forms the protective or mechanical layer. A malpighian layer of vertically elongated and much thickened cells is quite common, although varying in origin (Werker 1997); it is often a systematically important character. A vascularised (see ovule variants above) and multiplicative testa and/or tegmen (see integument thickness), the latter having the number of cell layers increasing after fertilization, are mentioned only when they occur. Some seeds have more or less annular operculum in the micropylar region - this has a variety of aliases and morphologies - which is pushed off during germination. Other seeds that have hard coats and physical dormancy have a water gap, a place in the coat where water enters the seed and starts the germination process (Turner et al. 2009); this water gap may be quite a cryptic feature anatomically. Distinctively thickened transfer cells may be found in various places in the seed coat (see e.g. Boraginaceae, Lamiales [endothelium] - Joel et al. 2012) or embryo.

Many asterids have only a single integument, and the seed coat of such taxa is called a testa in the characterisations; whether or not it is the same as the testa in angiosperms with two integuments is an open question. The amount and patterning of the thickening of the walls of the exotestal cells of this single integument often varies greatly within a family, as in Gentianaceae (e.g. Guérin 1904) and Ericaceae; the thickening on the outer periclinal wall is often less than that on the other walls. However, much of the variation in thickening, cell shape, etc., of this single-layered exotestal-type seed coat is of interest at levels lower than those on which I focus here. Some Lamiales have conspicuous seed pedestals of placental origin (Rebernig & Weber 2007).

In drupe-, achene- or nut-type fruits in particular the seed coat is often undistinguished at maturity and systematically uninformative. In these fruits, protection for the embryo is afforded by the fruit wall, and development of the seed coat becomes functionally superfluous. Seed coat anatomy of myco-heterotrophs (Bouman et al. 2002) and parasites also may be of little use in detecting relationships since the seeds of such plants are often very reduced, light, and dispersed by wind.

For a survey of mucilages and gums in seeds, see Grubert (1974, 1981), and for the possible functions of these mucilages, see Yang et al. (2012) and Engelbrecht et al. (2014). Some monocots have distinctive substances associated with the testa, in particular, black phytomelan and brownish phlobaphene. The former is also found in some Asteroideae; it is an inert and very resistant compound lacking nitrogen rather like green tea polyphenolics and is probably derived from catechol (see especially Graven et al. 1998 for what is known about its chemistry [not very much], etc.; Rasmussen et al. 2006).

Endosperm presence/absence refers to the situation in the ripe seed, however, it can be a difficult character to deal with. Endosperm is very nearly always found in the very young embryo (see above), but whether or not and in what quantity it persists is of interest here. There is a continuum between scanty and copious endosperm, and even the absence of endosperm is by no means as distinct a state as it might appear - it may be reduced to a single layer, or found in only a part of the seed (e.g. Guignard 1893 for an early discussion). Indeed, the function of a thin endosperm may not be as a food reserve, but when intact it may prevent germination (Linkies et al. 2010). Endosperm has been much studied in grasses, and different cell types such as aleurone, transfer, starchy endosperm and embryo surrounding cells, each with their own histories, can be recognised (Sabelli & Larkins 2009; see also Olsen 2007). Some distinctive endosperm variants, such as ploidy levels other than triploid in the endosperm cells, are mentioned as they occur. Only Viscum and its relatives (Santalaceae), Amaryllidaceae-Amaryllidoideae-Amaryllideae, and perhaps one or two other taxa have endosperm that is green and chlorophyllous.

Ruminate endosperm is sporadically distributed, from the relatively huge seeds of Myristicaceae to the small seeds of some Scrophulariaceae (it is rare in monocots). Rumination develops in various ways, and characterizes a number of taxa mostly at the lower levels of this survey (Periasamy 1962b; Bayer & Appel 1996 for a summary); Hartl (1959, q.v. also for terms) described the small, alveolate/ruminate seeds of some Lamiales.

Especially in asterids, endosperm haustoria, generally multicellular semi-invasive projections from the micropylar and/or chalazal ends of the seed, are common (e.g. Crété 1951; Mikesell 1990). They are mentioned only where they occur, as are other endosperm variants such as the highly asymmetric early endosperm development of Acanthaceae.

Endosperm food reserves are usually oily and/or proteinaceous, and when this is the case it is rarely mentioned; starch, hemicellulose/amyloid/xyloglucans and other polysaccharides (Kooiman 1960; Czaja 1978; Meier & Reid 1982; Buckeridge et al. 2000a; Buckeridge 2011) are also to be found (but amyloid is unknown from monocots), and the occurrence of such reserves alone is recorded (amyloid may occur in the embryo, too). Starchy seeds are often associated with parasitic and aquatic habits, but starchy and/or thick-walled and hemicellulosic endosperm is especially common in the commelinid monocots, but not Arecaceae (Huber 1969). ADP-glucose pyrophosphorylase, which is involved in starch synthesis, is largely located in the cytosol of the endosperm in the PACMAD/BEP clade in grasses, and in plastids in other flowering plants, but the sampling is poor (Beckles et al. 2001; Comparot-Moss & Denyer 2009). In monocots with starchy endosperm, as in several Poales and Commelinales, the outer part of the endosperm, the aleurone layer, commonly has other than starchy reserves (e.g. Xu & Messing 2008); this, too, is rarely mentioned. Lott (1981) described the inclusions found in protein bodies/aleurone grains in the embryos of a few plant families; although the sampling was poor, there were suggestions that Cucurbitaceae and some Apiaceae were distinctive in this respect. Starch grains in the young endosperm and in the vegetative plant are commonly of the "Hülle" type, that is, circular when seen from above, and homogeneous (Czaja 1978, see also Reichert 1913 for information); only variants of this type as found in the seed are mentioned in the descriptions, but this is a difficult character to deal with.

Perisperm s. l. usually contains starch as a reserve (Floyd & Friedman 2000 for "basal" angiosperms), only rarely are the reserves oil or proteinaceous, as in Acoraceae; the nature of the reserve, where known, is mentioned in all cases.

Embryo length varies considerably, but I have not treated this feature critically enough; Martin (1946) is still a very useful - and more consistent - source of much basic information (see also Baskin & Baskin 2007; Ren & Zhu 2007; Linkies et al. 2010). Speculations on the evolution of embryo size, type, and dormancy (see below), should be treated with caution; Forbis et al. (2002) have recently evaluated embryo size (measured as the embryo:seed ratio) in the context of phylogeny (see Vandelook et al. 2012a for the ecological implications of this ratio). Coccucci (2005) provided a classification of the seeds of all spermatophytes that was based on the nature of the reserve tissue and how far the embryo had developed at maturity of the seed.

The relative length of the embryo is emphasized here. It is the length of embryo relative to the length of the endosperm or perisperm ("seed" below), the latter length being the distance from the micropylar to the chalazal ends of those structures (curved seeds may thus be absolutely longer than straight seeds). Long embryos are at least half the length of the mature seed. Medium embryos are about half the length of the seed, short embryos are between one half and about one tenth the length of the seed, while minute embryos are still smaller. The states of this character are arbitrarily delimited. Mangrove taxa, and to a certain extent aquatics in general (e.g. Nymphaeaceae, Ceratophyllaceae, Nelumbonaceae, Alismatales), have notably large and well-developed embryos, perhaps to ensure rapid establishment of the seedling after it germinates. Of course, that embryos are long does not mean that endosperm is necessarily absent, also, if seeds are minute (the "Micro" type of Martin 1946, the dust seeds of Eriksson & Kainulainen 2011, see also Baskin & Baskin 1998) their contained embryos necessarily will be minute in absolute size, although by the criterion of relative length they might well be long... I have not mentioned embryo size for such seeds, indeed, the embryos are often undifferentiated, and this is mentioned (see below, Embryo morphology, Germination).

Embryo position. The embryo is more or less central in the seed, the radicle being adjacent to the micropyle, if present, and any endosperm present surrounds the embryo. However, in a few families such as Poaceae, Polygonaceae, and also Caryophyllaceae and their relatives (this latter group makes up the old Curvembryonae) the embryo is lateral, lying against the testa on one side and adjacent to endosperm (or perisperm) on the other. Sometimes the position of the embryo relative to the fruit as a whole is of interest, thus in Lamiaceae the radicle points towards the base of the fruit and in Boraginaceae towards the apex - base and apex being relative to the pedicel.

Embryo morphology, that is, the gross morphology of the embryo in ripe seeds, varies considerably. In the characterizations I mention mainly cotyledon number, whether (and how) the cotyledons are folded, and whether the embryo is straight, curved, and flattened. In embryos derived from curved ovules the cotyledons are accumbent when the plane separating them is the same as that formed by the long axis of the seed plus chalaza or simply by the curvature of the embryo, incumbent when they are at right angles to this plane; they can (of course!) also be intermediate. In monocots the shape of the embryo varies at about the family level. The relative proportions of cotyledon:hypocotyl + radicle and the thickness of the cotyledon can be of systematic interest; in some Clusiaceae and Lecythidaceae in particular the embryo - sometimes quite massive - is largely hypocotylar. In myco-heterotrophic and/or parasitic plants with minute seeds the embryo is more or less undifferentiated, even the cotyledons not being visible (Eriksson & Kainulainen 2011). Larger seeds can also have undifferentiated embryos, thus at most weakly differentiated embryos characterize the entire Cyperaceae - Ericocaulaceae - Poaceae clade. However, the embryos of Poaceae themselves represent another extreme in embryo differentiation having the first leaves of the seedling already developed before germination, and this is true of Fabaceae-Faboideae, etc.

Data on embryo color are taken largely from Yakolev and Zhukova (1980), but see also Janzen (1982) and Wright et al. (2000). The sampling is poor, but some taxa commonly have green embryos, others have white embryos; the latter is the common condition. Embryo colour may be under the control of a single gene: (Mendelian genetics! - see Armstead et al. 2006). Seubert (1993) suggests that in monocots green embryos are found only in Alismatales.

I have not thought about the possible significance of the kind of food reserve to be found in the embryo.

Cotyledon number is usually an unambiguous character, although in taxa with two cotyledons like Cyclamen, some Ranunculaceae, etc., that produce subterranean storage organs the cotyledons may be more or less connate. Burger (1998) and others have suggested that the single cotyledon of the monocots might be equivalent to the third leaf of the nymphaealean seedling, and that the young embryo of both Nelumbo and Nymphaeales is initially monocot-like. Unfortunately for this idea, Nelumbonaceae, Nymphaeaceae and monocots are not now thought to be immediately related... For the literature on monocotyly in broad-leaved angiosperms, and suggestions that Syneilesis (Asteraceae) seems to lack cotyledons entirely, see Teppner (2001). Polycotyledony is particularly noteworthy in Pinus (as in pine "nuts"), but also occurs rarely elsewhere, e.g. Idiospermum (Calycanthaceae).

Cotyledon position. The cotyledon(s) are usually lateral structures; only in monocots, with the exception of Poaceae, does the single cotyledon appear to terminate the embryonic axis.

Baskin and Baskin (1998, 2004; see also Finch-Savage & Leubner-Metzger 2006) provide much information on various kinds of dormancy of the seed, linking it with embryo size, etc. (see also Forbis et al. 2002). "Minute" embryos as defined above, e.g. in Ilex (see also Baskin & Baskin 2007), are often undifferentiated and require a period after dispersal for maturation to be completed (morphological dormancy - see Tuckett et al. 2010); even if they have cotyledons, etc., they will have to grow to fill up the inside of the seed before germination begins (see also Forbis et al. 2002). An extreme example of morphological dormancy occurs in Hydatellaceae in which differentiation of the embryo occurs only after germination has begun and the embryo has broken through the seed coat (Tuckett et al. 2010), while in many dust seeds an association between seedling and host, whether fungus or other seed plant, has to be established if the seedling is to survive (Eriksson & Kainulainen 2011). A number of tropical trees have recalcitrant seeds where the seed needs to remain hydrated if germination is to occur, while others have very hard seed coats that may show physical dormancy; in the latter, germination begins only when water starts entering the seed through a water gap (Baskin et al. 2000; Turner et al. 2009).

Seedling morphology provides a wealth of systematically interesting characters, and there are general surveys in e.g. de Vogel (1980), who both developed a complex typology of germination patterns and provided references to other such endeavours, Lubbock (1892: general), Burtt (1991b: survey of taxa with cryptocotylar germination), Duke (1969: tropical taxa), and Garwood (2009: neotropical taxa) - see also below for monocots in particular. However, much variation in germination and seedling morphology is somewhat below the level that is of interest here (see Tillich 2007 for variation within Poales, for example). The embryos of mangrove and marine taxa tend to be large, and seed germination there is frequently more or less precocious (Juncosa 1982). For herbivory and seedlings, see Ann. Bot. 112(4). 2013.

In hypogeal seedlings the epicotyl is elongated, while in epigeal seedlings it is the hypocotyl that is elongated; cryptocotylar seedlings have non-photosynthetic cotyledons that remain enclosed by the seed coat and/or pericarp during germination, while in phanerocotylar seedlings the cotyledons are exposed and photosynthetic. There is frequent infrageneric variation in broad-leaved angiosperms in particular as to whether or not the hypocotyl is developed, and also whether or not the cotyledons are photosynthetic (e.g. Burtt 1974). The shape of the exposed cotyledons can be of systematic interest, as in e.g. Bignoniaceae and Burseraceae, and also, as in monocots, whether the cotyledon is unifacial or bifacial. Cotyedonary vasculature can vary considerably within a family, and/or differ when compared with that of adult leaves (Stone 1970). Vivipary, the germination of the seed while still in the fruit and so on the maternal plant, is sporadic; it tends to be more of ecological than of systematic interest (Cota-Sánchez et al. 2007). In many monocots, and some aquatic broad-leaved angiosperms, the radicle is poorly developed or aborts; abortion of the radicle also occurs in some Cactaceae (Rodríguez-Rodríguez et al. 2003; Shishkova et al. 2013).

When it comes to monocot seedlings, much detail can be found in Arber (1925), Boyd (1932), and Huber (1969); Kaplan (1997: 1 ch. 5) and Tillich (1992, 2007) attempt to clarify monocot seedling morphology. Tillich (e.g. 2000, 2003) suggests that, with a few exceptions, there is little variation in seedling morphology within monocot families. Rather unfortunately, the terms hypogeal and epigeal as used in descriptions of monocot seedlings (e.g. in Kubitzki ed. 1998a, c; Linder & Caddick 2001) largely correspond to the terms crypto- and phanerocotylar used to describe the seedlings of broad-leaved angiosperms, a hypocotyl rarely being much developed in monocots (although this depends in part on the morphological interpretation of the monocot seedling... see Kaplan 1997: 1 ch. 5); I have used neither of these pairs of descriptors in the monocot characterisations. In a monocot seedling the cotyledon is commonly exposed and photosynthetic at least in its lower part, although morphologically different areas may be photosynthetic in different groups, while at least the apex remains enclosed by the testa/fruit wall and is absorbtive; a seedling can thus be phanerocotylar and cryptocotylar at the same time (see also Hydatella - Sokoloff et al. 2013b). As mentioned, any hypocotyl present is at most short by comparison to that of a broad-leaved angiosperm with epigeal germination (c.f. Tillich 2007 in part). In monocots in particular the plumule is frequently carried below the soil surface during the process of germination (Haines & Lye 1979; Clarkson & Gifford 1987: literature, including examples of broad-leaved angiosperms), and this is associated with the hypogeal growth habit of many monocots - rhizomatous, cormose, bulbous.

Phyllotactic patterns of very young plants are interesting. In monocots the first leaf is generally opposite the single cotyledon, whereas in broad-leaved angiosperms it is at right angles to the plane of the two cotyledons. Henslow (1893 and references) discussed some of the abrupt shifts in phyllotaxis in monocot seedlings, while in broad-leaved angiosperms the first two foliage leaves may be opposite, even when other leaves of the plant are distichous or spiral (e.g. some species of Phaseolus); when bijugate phyllotaxis becomes established varies within Rhizophoraceae (). Furthermore, the leaves of seedlings and young plants can have a morphology very different to that of the adult.


Nucleus, Chromosome Morphology and Organization.

Chromosome numbers are taken largely from secondary sources, including the various indices of chromosome numbers. All counts have been silently converted to haploid numbers (n). Although I rarely mention the literature in which base numbers (x) for families or orders are suggested, Raven (1975) is a convenient entry into the older literature here. Mayrose et al. (2010) discuss the problems associated with establishing such base numbers.

The occurrence of polyploidy within families, etc., is rarely mentioned except when it is particularly common. It has recently been estimated that 15% of angiosperm speciation events are associated with polyploidy, even if polyploid lines do not show greater net species diversification than others (Wood et al. 2009; see also Mayrose et al. 2011); Otto and Whitton (2000) and Meyers and Levin (2006) provide general overviews of the prevalence and consequences of polyploidy. There is evidence from isozyme duplication that polyploidization has occurred in clades like Magnoliaceae, Aesculus, Salix/Populus, etc. (Soltis & Soltis 1990). The notably small stomata of some fossils when compared with extant members of clades also suggests polyploidization within these clades, some extinct members perhaps having chromosome numbers half of any of those known (Lauraceae, Magnoliaceae and Platanaceae: Masterson 1994). However, most of the examples just mentioned are from woody groups that are unlikely to have had herbaceous ancestors, and given our current understanding of the problem, polyploidy is supposed to be less likely in such groups. At the same time atmospheric CO2 concentration has been decreasing, and this may have affected stomatal size and density... There has also been widespread reduction in chromosome numbers (e.g. Wolfe 2001), and in clades like Brassicaceae and Asteraceae chromosome number is especially plastic. For these and other reasons, working out the evolution of chromosome numbers can be difficult; Cusimano et al. (2012) show how using different methods of inferring ancestral numbers result in different estimates. Finally, the evolution of genome size (see below) is at least in part independent of the evolution of chromosome numbers (e.g. Schnable et al. 2009; Garcia et al. 2010). All in all, the genome is turning out to be remarkably plastic.

There is increasing evidence that genome duplications have been quite common throughout the history of land plants and are increasingly being implicated in their evolution and diversification (e.g. Vision et al. 2000; Bowers et al. 2003; Blanc & Wolfe 2004a; Schlueter et al. 2004; Adams & Wendel 2005; Maere et al. 2005; de Bodt et al. 2005; Chapman et al. 2006; Cui et al. 2006; Jaillon, Eury et al. 2007; Soltis et al. 2009; van de Peer et al. 2009b; Barker et al. 2010; Jiao et al. 2011; Mühlhausen & Kollmar 2013: myosin motor proteins; Guo et al. 2013). They have occurred at all levels from small groups of genera, as well as deep within Poaceae and Brassicaceae, the common ancestor of the asterid and core eudicots, and even of all seed plants. However, exactly where many are to be put on the tree remains unclear because of limited sampling. There is relatively little colinearity and synteny when monocots and rosids are compared, although these are extensive within each group (Tang et al. 2008). Genome duplications are distinct from the nuclear fusions that may occur in specific tissues in flowering plants, as sometimes in tapetal cells (see above), and rates of gene duplication independent of polyploidy are also appreciable (Lynch & Conery 2000).

Both gene and genome duplication are valuable sources of phylogenetic information and also clues for understanding clade diversification and the evolution of morphology. The functions of the duplicated genes may initially remain similar, but subsequently there is often subfunctionalisation, neofunctionalisation, or loss of one of the genes (for a nice example, see de Martino et al. 2006), but gene loss following gene and genome duplication is perhaps particularly common in important housekeeping genes, which thus revert to being single copy genes (de Smet et al. 2013). Other explanations for the role of genome duplication in plant evolution include reducing the probability of extinction by e.g. increasing genetic variation and environmental tolerance (Crow & Wagner 2006 and references; Fawcett et al. 2009).

Some of the gene duplications that are often mentioned in the literature are linked to these genome duplications. For instance, much work has been done on the duplication of the PHY genes (genes for phytochrome variants); Mathews et al. (2003) follow the early evolution of the PHYA and PHYC genes (see also Mathews et al. 1995; Mathews & Sharrock 1996, etc.; for general background see Karniol et al. 2005 and especially Mathews 2006b [the big picture of phytochrome evolution in an ecological context]), while Schmidt and Schneider-Poetsch (2002) discuss the complex pattern of duplication of the PHY genes in the gymnosperms. The duplication of the RPB2 gene (the gene coding for the second largest subunit of RNA polymerase II) provides important phylogenetic information (Oxelman et al. 2004). For the duplication and distribution of the LEAFY gene, see Frohlich and Parker (2000) and Frohlich (2002).

Endoreduplication of the genome is common in flowering plants, especially in the endosperm and cotyledons (Joubès & Chevalier 2000; Larkins et al. 2011), with a figure of 24,576n estimated for the cells of the endosperm haustorium in Arum maculatum (Bennett 2004). Endoreduplication may be absent in some families, but there is no obvious correlation with phylogeny (Barow & Jovtchev 2007). Interestingly, endoreduplication is not recorded from liverworts, but it is quite common in mosses (Bainard & Newmaster 2010a, b).

Karyotype. Detailed features of the karyotype have been used to characterize a number of monocot (in particular) groupings at around the family level in Asparagales and Liliales (Tamura 1995 summarises much information). Although I may have made less of such characters than I might (but some details are being added to the pages), the karyotype is not notably conservative as was once thought. Thus a bimodal karyotype characterizes an Agavaceae (= Asparagaceae-Agavoideae) that includes genera that used to be in Hostaceae and Hyacinthaceae-Chlorogaloideae, etc., but it is also found elsewhere in Asparagales; indeed, the decision that a karyotype is bimodal is not easy (e.g. Chase et al. 2000a). Most chromosomes have telomeres, and it was thought that telomere construction was rather invariant, the sequence that was repeated being very conservative. However, there is quite a bit of variation that is systematically interesting at various level from individual genera on up, e.g. within Asparagales and within Solanaceae (e.g. Adams et al. 2001; Sýkorová et al. 2003a, b, 2006); there is also variation in telomere size, which is long in Caricaceae and Solanaceae and short in Brassicaceae and Caryophyllaceae (Shakirov et al. 2009).

Nuclear genome size, whether measured as the 1C or C-value (C = unreplicated gametic genome) or Cx value (unreplicated basic genome), shows considerable variation; within angiosperms, the genome varies 2000-fold in size, Genislea margaretae (Lentibulariceae), has a 1C value of only 63 mbp (Greilhuber et al. 2006). Bennett and Leitch (1997) list DNA values for angiosperms, Leitch et al. (2005) summarise what is known about genome size for all seed plants (see Leitch et al. 2001 for gymnosperms; Leitch 2007) and Bennett and Leitch (2005) extend this to all land plants (see also Bai et al. 2012). Bennett and Leitch (2010) have set up a Plant DNA C-values Database. The variation they detail is largely consistent with broad-scale phylogeny; seed plants have small genomes (less than 1.4 pg) compared to those of most gymnosperms. Others are assembling lists of genome sizes in angiosperms (e.g. Hanson et al. 2005; Zonneveld et al. 2005; Garcia et al. 2010; Zonnefeld 2012); see also Suda et al. (2005) who suggested that members of the Macaronesian flora tended to have particularly small genomes.

However, the significance of genome size is unclear. Bennetzen and Kellogg (1997) floated the idea that increase in genome size might be irreversible - there is more likelihood of this in some gymnosperms (e.g. Nystedt et al. 2013) than in angiosperms. There is often no correlation between C measures and chromosome number and in particular ploidy level (e.g. Weiss-Schneeweiss et al. 2005; Lysack et al. 2007, 2009; Schnable et al. 2009; Peruzzi et al. 2009; Bliss & Suzuki 2012; Vaio et al. 2013; c.f. in part Jakob et al. 2005). However, C measures are correlated positively with cell size and guard cell length and negatively with stomatal density in angiosperms; trees, with rather small genomes, have the highest stomatal density (Beaulieu et al. 2008, see also Bainard et al. 2012, c.f. Rupp et al. 2010 for Polystachya [Orchidaceae]). However, by and large, strong correlations seem hard to come by (Garcia et al. 2010), and most studies are simple correlations. Furthermore, changes in the amount of repetitive DNA, rather than changes in gene number, can have major effects on C-values (Jakob et al. 2004). Indeed, root meristem growth rate seems to be negatively correlated with genome size, and since holoparasites in particular have little need for roots (Gruner et al. 2010), they may show much increased genome sizes (e.g. Piednoël et al. 2012). Franks et al. (2012) do suggest that long-term changes in CO2 concentration are linked with changes in the genome size of plants, and hence possibly with evolutionary changes, but c.f. their Fig. 4, where ancestral nodes vary haphazardly, the test organisms for correlation of guard cell, nuclear and genome size are all N. temperate herbs, etc.. Lomax et al. (2013) found that maximum genome size (= maximum guard cell length) has been steadily increasing from 360 m.y.o. (the Mississippian), but a time-binned average shows a decrease over the last 250 m.y. (Lomax et al. 2013: c.f. fig. 2A and 2B). There are a number of articles on genome size in the online Journal of Botany 2010.

For variation in the length of the mitotic cycle, see Evans and Rees (1971); the length seems to be associated with the degree of coiling of the chromosomes.

Nuclear inclusions such as protein bodies in nuclei of various shapes and sizes are occasional (e.g. Thaler 1966; Speta 1977, 1979 for information); they are mentioned only when they occur. Other nuclear inclusions in asterids are described by Bigazzi (e.g. 1995). Note that some literature describing such inclusions dates back to the late nineteenth century (see Speta 1979).

Plastid and Mitochondrion Organization.

For surveys of chloroplast inheritance, whether via the pollen grain or the egg cell, see Corriveau and Coleman (1986), Owens et al. (1995) and Mogensen (1996). For general information on mitochondrion and chloroplast evolution, see Hagemann (2004) and Volkmar and Knoop (2010), and for plastome evolution in parasitic plants, see Krause (2011).

For a summary of much literature on the evolution of the chloroplast genome in seed plants, see Jansen and Ruhlman (2012). Some major genome rearrangements are mentioned in the characterizations. The chloroplast inverted repeat characterizes most land plants and a few of their immediate relatives (e.g. Turmel et al. 1999), but it can be lost, as in a major clade of Fabaceae-Faboideae. Downie and Palmer (1992b) summarise early literature on the use of chloroplast DNA rearrangements in reconstructing phylogeny, and there is much information on later work in Raubeson and Jansen (2005); see also Cosner et al. (2004). Data on the loss of the intron in the chloroplast rpl2 gene is taken from Downie et al. (1991), that in the rpoC1 intron from Downie et al. (1996), and in the rpl16 gene from Campagna and Downie (1998); see Jansen et al. (2010 and references) for the movement of the rpl22 gene from the chloroplast to the nucleus. Millen et al. (2001) summarize information about the loss of the infA gene from the chloroplast and Joly et al. (2001). There may be substantial phylogenetic signal in such characters. For the loss of the ndh genes in the chloroplast of Pinus thunbergii, see Wakasugi et al. (1994) and Martín and Sabater (2010). Overall there is relatively little variation in the size of the chloroplast genome, bar variation in the size of the inverted repeat. Graham et al. (2000) discuss microstructural changes in noncoding DNA; the distributions of these changes support clades such as all angiosperms, the eudicots, monocots minus Acorus, and Austrobaileyales.

There has been a certain amount of horizontal (or lateral) gene transfer in seed plants (Keeling & Palmer 2008; Bock 2009; Talianova & Janousek 2011 for a summary), although the extent of this is still unclear. Mitochondrial genes in particular are transferred relatively easily, and this may wreak havoc in phylogenetic analyses (Hao et al. 2010). Adams et al. (2001, 2002a, b) follow the loss of a number of genes from the flowering plant mitochondrial genome, probably because of their transfer to the nucleus; the rps13 gene seems to have been replaced in many Rosids by a chloroplast gene that is now in the nucleus. In a number of cases, fairly high-level groupings appear to be marked by gene migration, the loss of the rps2 and rps11 genes perhaps being particularly significant systematically (see also Bergthorsson et al. 2003; Ong & Palmer 2006), although in other cases individual genera (or perhaps groups of genera) such as Phlox, Allium, etc., show more extensive migration of genes. Genes involved in these transfers are mostly ribosomal protein and succinate dehydrogenase genes, not respiratory genes (Palmer et al. 2000; Adamas et al. 2002). Y. L. Qiu has suggested that how mitochondrial introns are spliced (cis or trans) may be of systematic significance (see Cameron et al. 2003).

DeBenedetto et al. (1992) discuss the loss of the coxII.i.3 intron from the mitochondrion; there is substantial variation in this within Dipsacales and Gentianales, for example. There is extensive parallel transfer of the cox1 gene in plants (Sanchez-Puerta et al. 2011: mechanism?, c.f. Cusimano et al. 2008). Mitochondria can also incorporate substantial amounts of the chloroplast genome (Richardson & Palmer 2007 for a summary; Sanchez-Puerta et al. 2008; Chaw et al. 2008; Alverson et al. 2010; Wenqin Wang et al. 2012), and in some host-parasite associations genes move from the latter to the former (Davis & Wurdack 2004; Mower et al. 2004; Filipowicz & Renner 2010 and references); movement may be extensive, and the genes moved functional (Xi et al. 2013). Other cases involve transfer of genes between angiosperms and gymnosperms and even bryophytes and angiosperms that result in large and complex chimaeric mitochondrial genomes, and these are even less understood (Won & Renner 2003; Bergthorsson et al. 2004; Renner & Bellot 2012; Rice et al. 2013); G. Petersen et al. (2006) sound a note of caution in the interpretation of such phenomena.

Recently, evidence has been found of some movement of mitochondrial genes into the chloroplast genome (D. R. Smith 2013 for a summary). Finally, parasite-mediated exchange of nuclear genes between host and parasite is known (e.g. Yoshida et al. 2010).

Sequence Data.

Support for many of the relationships suggested here comes from analyses of the variation in molecular sequence data that continue to pour out; many of the papers involved are cited separately in the appropriate places on the order pages. Not all sequences are of equal value when it comes to understanding relationships, with mitochondrial ITS sequences (Álvarez & Wendel 2003) and mitochondrial information in general (G. Petersen et al. 2006b) perhaps being particularly difficult to use. It is going to be interesting to see how hypotheses of relationship hold up as massive amounts of data from all three genomic compartments become available for analysis in the next few years (e.g. Davis et al. 2014).

For the evolution of plastid ndh genes, see Martín and Sabater (2010).

The rate of change in molecular sequences is very unequal across the tree, and some clades show notably accelerated rates. These are often clades with distinctive life styles, whether parasitic, myco-heterotrophic, or carnivorous, although abrupt rate changes may also occur elsewhere (e.g. Duff & Nickrent 1997; Caddick et al. 2002a; Müller et al. 2004; G. Petersen et al. 2006b). The rate of change of the nrITS region was found to be faster in herbs than in woody plants (Kay et al. 2006), and the rate of molecular evolution in general is faster in herbs than in trees (e.g. Smith & Donoghue 2008; Couvreur et al. 2009). For rate changes in molecular evolution of 18S rDNA of myco-heterotrophic and parasitic taxa, see Lemaire et al. (2011a); it has had little effect on function. A number of these rate changes are indicated on the order pages. Although the rate of change of mitochondrial sequences tends to be low, there have been some cases of spectacular acceleration (up to 10,000X the normal rate of change: e.g. Mower et al. 2007) and the mitochondrial genome varies greatly in size (Alverson et al. 2010).


Host-plant preferences, particularly of butterfly larvae (e.g. Forbes 1958; Ehrlich & Raven 1964; Ackery 1988, 1991; Farrell et al. 1992; Powell et al. 1999; Ward et al. 2003) can provide information indirectly bearing on relationships, although interpretation may be difficult and there is no recent synthesis of the huge and scattered literature. Any synthesis is made more difficult because studies have tended to focus on temperate or tropical areas (see Janz & Nylin 1998; Novotny & Basset 2005; Lewinsohn et al. 2005). Fielder (1997) compared host plant utilization by temperate and tropical butterflies, while Nishida (2002) summarized sequestration of defensive compounds from plants by lepidoptera. Larvae of individual species may also show interesting host-plant preference patterns. There is a valuable database of caterpillar host plants that I have consulted - see Hosts - and associated with this are conventional books that detail food preferences of the caterpillars of parts of the area covered in the database (Robinson et al. 2001, 2002); see also papers in Scriber et al. (1995) and especially Berenbaum (1995) for swallowtails (Papilionidae) and their foodplants.

The patterns of fungal parasite/host associations (see also mycorrhizae, endophytes above) are also often of some systematic interest, and Savile (1979b) provided a comprehensive and appropriately cautious summary of these associations.

Since both fungi and insects that eat or parasitize plants are often affected by the chemistry of their hosts, parallelisms in chemistry may be reflected by finding related fungi, or butterfly or moth groups, (for example) on plants with similar chemistries. Thus members of the unrelated pairs magnoliids and Rutaceae (both have similar alkaloids), Putranjivaceae and Brassicales (glucosinolates), and Daphniphyllaceae and asterids (iridoids) have caterpillars of related butterflies eating them. Along the same lines, that similar caterpillars are found e.g. on both Onagraceae and Vitaceae (Forbes 1956) may reflect the fact that both groups have raphides.

The ability of grafts of different species, genera, and even families to take also probably reflects something of the underlying physiology of the plants concerned. However, the literature dealing with graft compatibilities is very scattered, and grafts between very distantly related plants seem to be possible (e.g. see Horne 1914; Hartmann 1951). Thus Horne (1914) noted that Ilex and Buxus could be intergrafted, but the graft did not really take - see also Garryaceae, Pinaceae and Portulacaceae. Recent work has shown that chloroplasts can move across graft junctions, at least in Nicotiana (Stegemann et al. 2012).