LIGNOPHYTA

True roots +; lateral meristems: cork cambium producing cork abaxially, vascular cambium producing phloem abaxially and xylem adaxially.

EXTANT SEED PLANTS/SPERMATOPHYTA

Plant woody, evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins derived from (some) sinapyl and particularly coniferyl alcohols, thus containing p-hydroxyphenyl and guaiacyl lignin units, (lignins derived from p-coumaryl alcohol, i.e. S [syringyl] lignin units); true roots present, apex multicellular, xylem exarch, and branching endogenous; arbuscular mycorrhizae +; shoot apical meristem multicellular, interface specific plasmodesmatal network; stem with ectophloic eustele, endodermis 0, xylem endarch, branching exogenous; vascular tissue in t.s. discontinuous by interfascicular regions; vascular cambium + [xylem ("wood") differentiating internally, phloem externally]; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, plastids with starch grains; phloem fibres +; stem cork cambium superficial, root cork cambium deep seated; leaves with single trace from sympodium ["nodes 1:1"]; stomata ?; leaf vascular bundles collateral; leaves megaphyllous [determinancy evolved first, then ad/abaxial symmetry], spiral, simple, lamina with vein density up to 5 mm/mm² [mean for all non-angiosperms 1.8]; axillary buds associated with at most some leaves; prophylls [including bracteoles] two, lateral; plant heterosporous, sporangia eusporangiate, on sporophylls, sporophylls aggregated in indeterminate cones/strobili; true pollen [microspores, i.e. no distal pore for release of gametes] +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, crassinucellate, megaspore tetrad tetrahedral, only one megaspore develops, megasporangium indehiscent; male gametophyte development first endo- then exosporic, tube developing from distal end of grain, to ca 2 mm from receptive surface to egg, gametes two, developing after pollination, with cell walls, with many flagellae; female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large", first cell wall of zygote transverse, embryo straight, endoscopic [suspensor +], short-minute, with morphological dormancy, white, cotyledons 2; plastid transmission maternal; two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], nrDNA with 5.8S and 5S rDNA in separate clusters; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.

MAGNOLIOPHYTA

Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, non-hydrolysable tannins, quercetin and/or kaempferol +, apigenin and/or luteolin scattered, [cyanogenesis in ANITA grade?], S [syringyl] lignin units common, positive Maüle reaction [syringyl:guaiacyl ratio more than 2-2.5:1], and hemicelluloses as xyloglucans; root apical meristem intermediate-open; root vascular tissue oligarch [di- to pentarch], lateral roots arise opposite or immediately to the side of [when diarch] xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, with gelatinous fibres; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, cytoplasm not occluding pores of sieve plate, companion cells from same mother cell that gave rise to the sieve tube; sugar transport in phloem passive; nodes unilacunar [1:?]; stomata with ends of guard cells level with pore, paracytic, outer stomatal ledges producing vestibule; leaves petiolate, lamina [formed from the primordial leaf apex], development of venation acropetal, 2ndary veins pinnate, fine venation reticulate, veins (1.7-)4.1(-5.7) mm/mm², endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, polysymmetric, parts spiral [esp. the A], free, numbers unstable, development in general centripetal; P not sharply differentiated, with a single trace, outer members not enclosing the rest of the bud, often smaller than inner members; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], ± embedded in the filament, with at least outer secondary parietal cells dividing, each theca dehiscing longitudinally by action of hypodermal endothecium, endothecial cells elongated at right angles to long axis of anther; tapetum glandular, binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellar, endexine thin, compact, lamellate only in the apertural regions; nectary 0; G free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, dry [not secretory]; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across [crassinucellate], nucellar cap?; megasporocyte single, hypodermal, megaspore tetrad linear, functional megaspore chalazal, lacking sporopollenin and cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; P deciduous in fruit; seed exotestal; pollen binucleate at dispersal, trinucleate eventually, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing at 80-600 µm/hour, with pectic outer wall, callose inner wall and callose plugs, growing between cells, penetration of ovules via micropyle [porogamous] within ca 18 hours, distance to first ovule 1.1.-2.1 mm, tube moves between nucellar cells; double fertilisation +, endosperm diploid, cellular [micropylar and chalazal domains develop diffently, first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous, embryo cellular ab initio, minute; germination hypogeal, seedlings/young plants sympodial; Arabidopsis-type telomeres [(TTTAGGG)_n]; whole genome duplication, ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, paleo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]].

Evolution. Possible apomorphies for flowering plants are in bold. Note that the actual level to which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is because some taxa basal to the [magnoliid + monocot + eudicot] group have been surprisingly little studied, there is considerable homoplasy as well as variation within and between families of the ANITA grade in particular for several of these characters, and also because details of relationships among gymnosperms will affect the level at which some of these characters are pegged. For example, if reticulate-perforate pollen is optimized to the next node on the tree (see Friis et al. 2009 for a discussion), it effectively makes the pollen morphology of the common ancestor of all angiosperms ambiguous... For other features such as details of sugar transport in the phloem, their placement on the tree is frankly speculative. Finally, for features such as parietal tissue/a nucellus only one (Nymphaeales) to three cells thick above the embryo sac and a stylar canal lacking an epidermal layer, although plesiomorphous for basal grade angiosperms (Williams 2009), I am unsure where on the tree a thicker nucellus and a stylar epidermal layer are acquired.

NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: vessels +, elements with elongated scalariform perforation plates; wood fibres +; axial parenchyma diffuse or diffuse-in-aggregates; tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.

ASTERIDS / Sympetalae redux? / ASTERIDAE / ASTERANAE Takhtajan: nicotinic acid metabolised to its arabinosides; (iridoids +); tension wood decidedly uncommon; C enclosing A and G in bud, connate, if evident only early in development and then petals often appearing to be free; anthers dorsifixed?; (nectary gynoecial); style +, long; ovules unitegmic, integument thick, endothelium +, nucellar epidermis does not persist; exotestal cells lignified, esp. on anticlinal and/or inner periclinal walls; endosperm cellular, embryo long.

[ERICALES [ASTERID I + II]]: ovules tenuinucellate.

ASTERID I + II / CORE ASTERIDS   Back to Main Tree

Ellagic acid 0, non-hydrolysable tannins not common; sugar transport in phloem active; inflorescence basically cymose; C forming a distinct tube; A epipetalous, = and opposite sepals or P, polyandry associated with increased numbers of C or G, very uncommon; (pollen with orbicules); duplication of the PI gene.

Evolution. Divergence & Distribution. Soltis et al. (2008: molecular data, a variety of estimates) suggest an age of divergence of the asterid I and II clades of 124-106(-85) million years ago, while Martínez-Millán (2010: fossils) targeted a much later date of around the Eocene 55-33.9 million years ago for the diversification of most of the euasterid orders.

This whole clade is notably speciose (Magallón & Sanderson 2001; Magallón & Castillo 2009), although it is more accurate to say that the six major clades, Boraginaceae s.l., Lamiales, Solanales, Asterales, Apiales and Dipsacales have high diversification rates, Of these clades, Magallón and Sanderson (2001) suggest that Asterales have the highest diversification rate (0.2717, 0.3295) while the honour goes to Lamiales in Magallón and Castillo (2009: 0.0928-0.1257). Note that within Asterales, Asteraceae are very speciose, and within Asteraceae, Asteroideae... Garryales and Aquifoliales in particular are noticeably less diverse. Indeed, both the asterid I and II clades have small clades sister to the rest, and members of these small clades have rather small flowers, a woody habit, and usually fleshy fruits (drupes, for the most part) with relatively large seeds - rather different from the mega-clades. Within the main clades are other species-poor pectinations, some also for the most part including woody plants. So if any one(!) thing is driving diversification, it may have evolved independently in the asterid I and II clades, although more likely it is a combination of factors. Endress (2011a) suggested that stamens adnate to petals, haplostemony (see also below), and unitegmic ovules are key innovations somewhere around here.

There may also be a change in chemistry in this part of the tree, ellagic acid being notably uncommon in the [asterid I + II] clade. This is perhaps to be expected, there being a correlation between woodiness and tannin frequency and a negative correlation between tannin (generalized defence) frequency and alkaloid and other secondary metabolites (specific defence) frequencies (e.g. Feeny 1976; Silvertown & Dodd 1996: given the information in Levin 1976 the correlation of alkaloid presence with other features should be re-examined). Indeed, no family in the [asterid I + II] clade had 50% or more species tanniniferous, and only Rubiaceae and Caprifoliaceae, both with many woody members, had an appreciable proportion of tanniniferous species (Mole 1993); the tannins involved are non-hydroysable tannins.

Ecology & Physiology. Cornwell et al. (2008) found that litter decomposition of forbs was faster than that of graminoids, and although he did not compare deciduous trees and forbs, breakdown of litter was faster in deciduous trees than in evergreen trees; such differences are related to changes in the rate of nutrient cycling.

In both clades there are many annuals and herbaceous to shrubby perennials, and many of these have very small seeds of 10^-2 grams or less ((Linkies et al. 2010; Haig & Westoby 1991 for situations in which small seeds may be at an advantage).

The annual habit may be connected with differences in the details of the distribution of different mechanisms of phloem transport. Taxa with active phloem loading are particularly common here. Sugars or sugar alcohols, not in particularly high concentration in leaf tissues, are pumped into the phloem by the metabolic activities of the plant (Rennie & Turgeon 2009; Turgeon 2010b; Fu et al. 2011). This may be associated with herbivore deterrence, the sugars causing dessication of the tissues of the herbivore, and/or cellular debris quickly clogs the sieve pores, sealing the phloem, and/or the plant economizes on sugar production (Turgeon 2010b; Fu et al. 2011). Note that woody taxa of the asterid I + II clade have "herbaceous" mechanisms of sugar transport, so the correlation may be phylogenetic and less immediately associated with plant habit. However, a somewhat different focus on/classification of transport types suggests that one active transport mechanism, the synthesis and transport of raffinose family oligosaccharides, seems to show little correlation with plant habit but some correlation with plant climate, being relatively more common in plants from warmer parts of the world (Davison et al. 2011).

Albach et al. (2001a, see also Soltis et al. 2005b) assign possession of iridoids to the base of the asterid clade. However, this feature is placed higher up the tree here, partly because of topological uncertainties, but partly because in Lamiales (for example), the four clades that are successively sister to the remaining Lamiales either lack iridoids or have iridoids different from those found in the other members of the clade (whether or not Carlemanniaceae have iridoids is unknown).

Floral Biology & Seed Dispersal. The asterid I clade in particular includes many large- and monosymmetric-flowered taxa that have dry fruits with many seeds (but cf. Convolvulaceae, Lamiaceae, Verbenaceae - four seeds/fruit at a maximum); the apices of the petals tend to be rounded (but cf. Acanthaceae). The asterid II clade has many taxa with small flowers that are aggregated into conspicuous inflorescences and the dry fruits have few seeds (but cf. Campanulaceae, Goodeniaceae, etc.); the apices of the petals tend to be pointed. In general, members of the asterid I + II clade have rather small seeds (Linkies et al. 2010).

There are relatively few cases of polyandry in the asterid I and II clades, and these seem to be associated with anisomery. There can be considerable increases in the numbers of perianth parts, and sometimes also carpels, which then occur in a single whorl. Examples are some species of Schefflera (e.g. Plerandra s. str.) (Araliales-Araliaceae), Anthocleista and Potalia (Gentianales-Gentianaceae-Potalieae) and some Gentianaceae-Chironieae (flowers to 16-merous), Lamiaceae-Symphorematoideae (Lamiales), as well as Codon, Hoplestigma, and Lennoa and relatives (all Boraginaceae s.l., but not immediately related to each other). In Plerandra, at least, a kind of fasciation of the flower seems to have occurred, and there are about as many stamens as carpels (Sokoloff et al. 2007b). Dialypetalanthus and Theligonum (both Rubiaceae) also have more numerous stamens that would be expected, but how the flowers are constructed is unclear. Paracryphiaceae (Paracryphiales) also show interesting variation in floral merism. Polyandry is much more commomn in other eudicots and it usually occurs independently of any changes in sepal, petal or carpel number - there are excaptions, such as Crassulaceae, where the stamens are equal in number to the carpels, Actinidia, where there are many carpels in a single whorl and many stamens, and Conostegia (Melastomataceae), where stamen and carpel number may be similar (see Wanntorp et al. 2011 for this and some other examples). The near absence of other kinds of increase in stamen number may reflect a change in underlying floral organisation/development in the stem [asterid I + II] clade, perhaps in turn connected with the rather stereotyped flowers so common here. As mentioned above, the corolla is more or less fused and the stamens are equal in number to the petals (or fewer) and are adnate to them (e.g. Endress 2011a).

Chemistry, Morphology, etc. For a possible duplication of the PI gene here - or in the asterid I clade - see Viaene et al. (2009), but more detailed sampling is required to fully understand the pattern of duplication and loss of this gene in asterids.

Phylogeny. Qiu et al. (2011) found weak support for a set of relationships [[paraphyletic Icacinaceae plus Garryales [Aquifoliaceae + rest of asterid 1 clade]] [rest of asterid 11 clade]] - for more on relationships of Icacinaceae, see below. Similarly, the I copy of the duplicated RPB2 gene is retained in most of the asterid I clade as well as Aquifoliaceae (and all? Aquifoliales), and there is a comparable pattern in the loss of introns 18-23 in the d copy; both point to the possibility that Aquifoliales might belong in the asterid I clade (Oxelman et al. 2004b). Since both Garrya and Eucommia have only the d copy, perhaps this is a feature of Garryales in particular, or part of them - sampling needs to be improved, and optimisation of the persistence/loss of the I copy on the asterid tree will probably be difficult (Oxelman et al. 2004b).

ASTERID I /LAMIIDAE   Back to Main Tree

G [2], superposed; loss of introns 18-23 in d copy of RPB2 gene.

Evolution. Divergence & Distribution. Magallón and Castillo (2009) offer estimates of ca 96.7 and 97 million years for relaxed and constrained penalized likelihood datings of crown group Asterid I, while Moore et al. (2010: 95% highest posterior density) suggest ages of (80-)76(-71) million years for diversification in this clade. See Martinez-Millán (2010) for fossil-based estimates for the age of this clade.

Phylogeny. Although Garryales seem to be sister to the rest of the asterid I group, the composition of the order is unclear. Oncothecaceae have been considered close, but neither they nor the other families, genus groups or genera mentioned immediately below link strongly to Garryales (e.g. Kårehed 2001; for the position of Oncothecaceae, see also Cameron 2001, 2003; Olmstead et al. 2000; B. Bremer et al. 2002). Pyrenacantha, Chlamydocarya, Sarcostigma, Iodes, and Icacina (Icacinaceae s. str.) form a clade in the rbcL tree of Savolainen et al. (2000b), although there placed (but with very little support) at the base of the rosids; these genera belong to Icacinaceae group III of Bailey and Howard (1941) and are included below in Icacinaceae s. str. There was initially only weak support for Icacinaceae in this position (D. Soltis et al. 2000), but Kårehed (2001) has identified four ex-Icacinaceous groups associated with Garryales: Icacinaceae s. s.tr, and the Cassinopsis, Emmotum and Apodytes groups. However, groupings within a more widely circumscribed Garryales could still not be identified, nor did the larger Garryales have any strong support. Relationships in the four genera of this part of Icacinaceae included in the analysis of B. Bremer et al. (2002) are also consistent with the classification adopted here, while the Bayesian analysis of Soltis et al. (2007) recovered Icacina as sister to all other asterid I taxa included (0.99 pp). Finally, Soltis et al. (2011) found very weak support for an association of Icacina with Garryales, but Oncotheca was not a member of this clade, although support for its position (the whole lot formed a paraphyletic assemblage at the base of the asterid I clade) was also very weak. Comprehensive phylogenetic studies in this area of the tree are badly needed.

Studies on the duplication of the RPB2 gene show that the I copy persists in most of the asterid I clade almost alone in the whole rosid/asterid group (see also discussion under Trochodendrales and at the beginning of the rosid group [Dilleniales]), as well as in Ericales. In a parsimony analysis of combined molecular and morphological data Lens et al. (2008a) found [Oncothecaceae + unassigned ex-Icacinaceae] (72% bootstrap) to be sister to the asterid I clade, but with little support, while in a Bayesian analysis the first clade was joined by Garryales (but little support for the enlarged clade) as sister to other asterid I groups (1.0 p.p.).

For literature on Icacinaceae in the old sense, which may refer to any and all of these groups, see Bailey and Howard (1941: anatomy), Mauritzon (1936c) and Fagerlind (1945a), both embryology, Heintzelmann and Howard (1948: crystals and indumentum), Padmanabhan (1961: embryology), Sleumer (1971a: general), van Staveren and Baas (1973: epidermis), Baas (1973: epidermis, 1974: stomata), Lobreau-Callen (1977, 1980: pollen), Kaplan et al. (1991: chemistry), and Teo and Haron (1999: anatomy). Kårehed (2001, 2002b) discusses the taxa in their current circumscriptions, while Lens et al. (2008a) provide a detailed anatomical survey in a phylogenetic context.

Classification. This clade is called the lamiids by B. Bremer et al. (2002).

Unplaced: >note, all have valvate corollas, 1-2 apical ovules/carpel and drupaceous fruits; morphologically, it would be easy to include them in an expanded Garryales if the phylogeny suggests this, if paraphyletic at the base of the asterid I clade, characters potenitally synapomorphic for the asterid I and possibly also for the asterid I + II clades will have to be reworked.

Included: Icacinaceae, Metteniusaceae, Oncothecaceae, and assorted unassigned genera.   Back to Main Tree

Oncothecaceae + Metteniusaceae: vessel elements with scalariform perforation plates; nodes 5:5; petiole bundles arcuate, complex; bracts thick, triangular; A = and alternating with C, basifixed; G [5]; ovules 2/carpel, funicle long; fruit a drupe, K persistent; endosperm copious.

Phylogeny. Other. For characters linking these two families, see also González and Rudall (2010).

ONCOTHECACEAE Airy Shaw   Back to Unplaced

Evergreen trees; chemistry?; plant glabrous; cork cambium outer cortical; phloem stratified; nodes also 3:3; astrosclereids +; plant glabrous; lamina vernation "convolute", margin with caducous glands, petiole short; inflorescences axillary, branched; flowers small; K ± free, C ?aestivation; A extrorse, anthers bisporangiate/monothecal; pollen smooth; nectary?; G opposite petals, styles separate, conduplicate, stigma punctate; ovules (1), apical, campylotropous; stone several-seeded; embryo terete, cotyledons short; n = 25.

1[list]/2. New Caledonia.

Chemistry, Morphology, etc. The stomata, perhaps modified paracytic, are distinctive. Carpenter and Dickison (1976) described the stamens as being opposite the petals, but drew them as being opposite the sepals. Oncotheca macrocarpa, fairly recently described (McPherson et al. 1981, = O. humboldtiana), has stamens quite unlike those of O. balansae; the incurved, pointed connective of stamens of the latter species is responsible for the generic name. Oncothecaceae are embryologically unknown.

Some information is taken from Baas (1975), Lobreau-Callen (1977) for pollen, and Carpenter (1975).

Previous relationships. The family was included in Theales by Cronquist (1981) and Takhtajan (1997).

Synonymy: Oncothecales Doweld

METTENIUSACEAE Schnizlein   Back to Unplaced

Evergreen trees; chemistry?; cork?; nodes 5:5; petiole bundles several, arcuate, complex; stomata anomo-cyclocytic; mesophyll fibres +; hairs ± T-shaped; lamina margins entire; inflorescence cymose/thyrsiform; K short, quincuncial, C valvate, corolla tube formation late; connective massive, anthers latrorse, long, moniliform, with 4 vertical rows of locellae, locelli dehiscing individually, endothecium 0; mectary 0; G monosymmetric, 4 carpels ± reduced, loculus 1, style long, stigma punctate; ovules 2, apical, fertile ovule with massive funicle, ?tenuinucellate, integument massive [20+ cells across], vascularized; fruit 1-seeded, asymmetrically ridged; seed coat thin, vascularized; embryo curved; n = ?

1/7. Costa Rica, Panama and N.W. South America (map: from Lozano C. & Lozano 1988). [Photo - Flower]

• Metteniusaceae are rather undistinguished vegetatively, but the combination of exstipulate, entire leaves and pentalacunar nodes is odd. The flowers are distinctive: the petals are spreading and hairy adaxially and each long, locellate (and sometimes bright orange) anther theca becomes broadly recurved in a semicircle.

Chemistry, Morphology, etc. For general information, see Lozano C. and Lozano (1988); for floral development, see González and Rudall (20100. It is unclear if the two ovules are from adjacent carpels [Fig. 10] or from the same carpel [Fig. 6k, l]), and since the gynoecium is paracarpous, technically the placentation is parietal.

Phylogeny. In morphological phylogenetic analyses Metteniusa fits quite comfortably into Cardiopteridaceae, ex Icacinaceae (Kårehed 2001, Cornaceae were not included). However, molecular analyses suggest a position in this general area (asterid I), and petiole anatomy, carpel number, etc., are similar to Oncothecaceae in particular (González & Rudall 2007; González et al. 2007 and González & Rudall 2010, the last two of which see for much information); I have summarized characters assuming this relationship.

Previous Relationships. The flowers of Metteniusa suggest Cornales s. str., but its ovary is superior. A monotypic Metteniusales were placed immediately after a highly heterogeneous Icacinales by Takhtajan (1997); Metteniusa was not mentioned by Cronquist (1981).

Synonymy: Metteniusales Takhtajan

ICACINACEAE Miers, nom. cons.   Back to Unplaced

Trees or lianes (with non-axillary branch tendrils); (plants Al-accumulators); monoterpene indole alkaloid camptothecin +, iridoids ?; secondary thickening often atypical [included phloem often +, etc.]; vessel elements with simple perforation plates; banded and/or vasicentric axial parenchyma; (crystal sand in wood rays); phloem stratified; nodes 1:1; (medullary bundles + - Iodes), petiole bundles arcuate and wing or annular (and medullary); stomata cyclocytic (anomocytic), hairs unicellular, often adpressed and ± T-shaped, also globular; leaves spiral (opposite), conduplicate(-plicate), lamina margins entire, (toothed), (palmately lobed; 2ndary veins palmate); plant dioecious[?], inflorescence branched, spicate or racemose, pedicels articulated; (flowers 4-merous); K connate (0 – Pyrenacantha; ± free - Phytocrene), (C free), valvate, (adaxially keeled), apices of corolla lobes narrow and inflexed; nectary 0 (+): staminate flowers: A dorsifixed (epipetalous); pollen also porate, echinate; pistillode +; carpellate flowers: staminodes +/0; G also 1?, style + and stigma punctate, or style 0 and stigma broad; ovules 2/carpel, (apically bitegmic - Phytocrene), tenuinucellate/thinly crassinucellate, integument vascularized (not), funicular obturator +; fruit a 1-seeded drupe, flattened and/or ribbed or not, outer cells of sclereidal layer with sinuous interdigitating walls, (endocarp papillate internally; endosperm ruminate), K persistent; seed coat?, no testa bundles; endosperm copious to 0, chalazal haustorium + [Nothapodytes], starchy [only Merrilliodendron?], embryo usu. long, cotyledons foliaceous; n = 10, 12.

24(?25)[list of genera in Icacinaceae in the old sense]/149(150): Iodes (28). Pantropical, inc. W. Pacific, to China and Japan (map: Sleumer 1971a; Utteridge & Brummitt 2007).

• Icacinaceae s. str. are undistinguished vegetatively, having exstipulate and usually entire leaves; a number are vines and these may have opposite leaves and branch tendrils that are not strictly axillary. The flowers are small, with a connate corolla and an at most rather short and slender style. Their single-seeded, drupaceous fruits are longer than broad and often flattened and/or ribbed.

Evolution. Divergence & Distribution. Magallón and Castillo (2009) offer estimates of ca 96.7 and 97 million years for relaxed and constrained penalized likelihood datings for stem group Icacinaceae - and Oncothecaceae and Mettiusaceae. Icacinaceae were widespread and diverse in the Northern Hemisphere during the Eocene, with genera now restricted to Southeast Asia-Malesia being found in North America (Rankin et al. 2008; Stull et al. 2011 and references).

Ecology & Physiology. For the indole alkaloid camptothecin, found in a number of genera, see Lorence and Nessler (2004). Camptothecin may be derived from secologanin and ultimately it may be synthesized by an endophytic fungus related to something like Rhizopus oryzae or the glomeromcyete Entrophosphora (Puri et al. 2005; Wink 2008; Shweta et al. 2010); the enzyme that camptothecin targets occurs in Icacinaceae, too, but there is probably protected by a change in its amino acid sequence (Sirikantaramas et al. 2009).

Chemistry, Morphology, etc. Hoseia, with its long-petiolate leaves that have palmate venation and long-dentate margins, is particularly distinctive vegetatively. Note that the description above largely refers to the Icacina group (see Kårehed 2001). The family is very poorly known embryologically.

For additional information, see Utteridge et al. (2005: general), also Rankin et al. (2008), Pigg et al. (2008a), and Stull et al. (2011), all fruit anatomy, especially of fossils, and Cremers (1973, 1974) for some growth patterns.

Previous Relationships. Other genera that used to be included in Icacinaceae are placed in the asterid II group, i.e. in Aquifoliales (as Cardiopteridaceae and Stemonuraceae) and Apiales (as Pennantiaceae: Kårehed 2001, 2002b, 2003).

Synonymy: Iodaceae van Tieghem, Phytocrenaceae R. Brown, Pleurisanthaceae van Tieghem, Sarcostigmataceae van Tieghem - Icacinales van Tieghem - Icacinanae Doweld

Apodytes - 3/10: Tropics, to Australia (Queensland) (map: from Sleumer 1971a)- vessel elements with simple [Rhaphiostylis] or scalariform perforation plates; bordered pits +; xylem parenchyma various; nodes 1:1, 3:3; stomata anomocytic (cyclocytic); leaves spiral or two-ranked; fruit very asymmetrical, ribbed, style thin, persistent; n = 20, ?22. Probably to include Dendrobangia - M. Schori, pers. comm. vi.2010. For fruit morphology, see Potgeiter et al. (1994b).

Cassinopsis - 1/4: Africa and Madagascar – vessel elements with scalariform perforation plates; nodes 3:3; stomata cyclocytic; hairs not ± T-shaped; leaves opposite. For fruit morphology, see Potgeiter et al. (1994a).

Emmotum (Emmotaceae van Tieghem) - 4(?6)/21(32): Central and South America, West Indies, rarely Malesia (map: from Sleumer 1971a) – vessel elements with scalariform perforation plates; bordered pits +; diffuse apotracheal parenchyma +; nodes 3:3; (hairs T-shaped; stellate); stomata cyclocytic(-anomocytic), (Platea; leaves ± conduplicate in bud); flowers 4-5-merous, (imperfect); C (0), valvate, ridged adaxially or not, with adaxial hairs (none); G [3], one carpel fertile, (2-3-septate: Emmotum), style very short to medium; ovules 2/fertile carpel, collateral or superposed; fruit flattened and symmetrical; (stone ± ribbed); embryo short to long; n = ? Perhaps includes Calatola – scalariform perforation plates; nodes 3:3; leaves toothed, conduplicate, Cordia growth pattern. Some information is taken from Howard (1941), Sleumer (1971a) and de Stefano and Fernández-Concha (2011),

Synonymy: Emmotales Doweld

For other information, see Bailey and Howard (1941, their group II: anatomy), Fagerlind (1945: embryology), Heintzelmann and Howard (1948), Padmanabhan (1961: embryology), Sleumer (1971a: general), van Staveren and Baas (1973: epidermis), Baas (1973: epidermis, 1974: stomata), Lobreau-Callen (1980: pollen), Kaplan et al. (1991: chemistry), and Teo and Haron (1999: anatomy). Kårehed (2001, 2002c) discusses the taxa in their current circumscriptions. The wood occasionally fluoresces.

GARRYALES Martius   Main Tree, Synapomorphies.

Woody; route II decarboxylated iridoids [inc. aucubin], gutta +; vessel elements with scalariform perforation plates; fibres with bordered pits; nodes?; petiole bundles arcuate; sclereids +; stomata?; hairs unicellular; plants dioecious; flowers small; C valvate, free; anthers basifixed; pollen ± atectate; ovary 1-celled, style at most short; ovules 1-2/carpel, apical, apotropous, crassinucellate, endothelium 0; fertilization delayed; fruit indehiscent. - 2 families, 3 genera, 18 species.

Evolution. Divergence & Distribution. Janssens et al. (2009) date stem group Garryales to 112±9.3 million years ago and the crown group to 20±8.6 million years; Bremer et al. (2004) suggested a stem group age of ca 114 million years. Magallón and Castillo (2009) offer estimates of ca 96.7 and 97 and 49.8 and 49.7 million years for relaxed and constrained penalized likelihood datings for stem and crown group Garryales respectively.

Floral Biology & Seed Dispersal. In all three genera there is a lengthy period (11 days to four weeks) between pollination and fertilization (Sogo & Tobe 2006); it would be interesting to examine Icacinaceae and related genera, Metteniusaceae and Oncothecaceae from this point of view.

Chemistry, Morphology, etc. Although the iridoid aucubin is found in both families, it is not unique to them; neither family can synthesize catalpol (Grayer et al. 1999). Much work is needed on basic embryology, etc. The lateral nucellus, at least, is thin, even if the ovules are crassinucellate.

Phylogeny. The order is narrowly circumscribed (see above).

Includes Eucommiaceae, Garryaceae.

Synonymy: Aucubales Takhtajan, Eucommiales Cronquist

GARRYACEAE Lindley, nom. cons.   Back to Garryales

Evergreen shrubs or trees; tannins 0, petroselenic and chlorogenic acid +; rays at least 10 cells wide, with square or upright cells; nodes 3:3; also crystal sand +; cuticle waxes as tubules (and platelets); stomata paracytic; hairs with counter-clockwise ridges; leaves opposite, ± connate basally, lamina vernation, conduplicate; inflorescence terminal; flowers 4-merous; staminate flowers: A not epipetalous; carpellate flowers: G [(3)], inferior; ovule 1/carpel, large placental obturator +; fruit a berry; testa thick, outer part sarcotestal, inner part with cells elongated tangentially; endosperm nuclear, with hemicellulose, embryo short.

2[list]/17 - two genera below. W. North America, Central America, the Greater Antilles and East Asia (map: from Dahling 1978).[Photo - Fruit]

1. Garrya

Diterpenoid alkaloids +; fibres with helical thickening; lamina margins cartilaginous; inflorescences catkinate, main axis racemose, bracts ± connate; staminate flowers: P [?= C] valvate, connate apically; A alternate with P, (pollen colporate, partly tectate); carpellate flowers: P [= K] 2, minute, or 0; styles separate, spreading, stigmatic much of their length; ovule epitropous, integument 12-30 cells across, endothelium 0, parietal tissue ca 5 cells thick, hypostase +, funicle quite long; antipodals persistent or not; testa multiplicative, exotestal cells large, palisade, fleshy, not persistent; suspensor very long, endosperm green, starchy; n = 11.

1/13. W. North America, Central America and the Greater Antilles (see map).

2. Aucuba

Gutta percha ?, flavonols, kaempferol +; vascular tracheids present; pericyclic fibres 0; lamina margins serrate; K minute or 0; staminate flowers: pollen?; carpellate flowers: staminodes 0; style +, stigma subcapitate, bilobed; nectary on top of G; integument thick, parietal tissue ca 5 cells across, (nucellar cap 2 cells across), endothelium?; (megaspore mother cells several); n = 8.

1/4. Sikkim to N. Burma, China and Taiwan to Japan (see map above).

Synonymy: Aucubaceae Berchtold & J. Presl

• Garryaceae are evergreen, woody plants that can be recognised by their exstipulate, opposite leaves that are basally connate, flowers with an inferior ovary and only one whorl of the perianth well developed, and baccate fruits.

Evolution. Divergence & Distribution. Fossil leaves of Aucuba are reported from the Eocene of Washington (Wehr & Hopkins 1994).

Chemistry, Biology, etc. For discussion of the flowers of Garrya, in which both calyx and corolla may be absent when mature, see Baillon (1877), Hallock (1930) and Eyde (1964); Baillon provides perhaps the only report of minute sepals being visible in the very young carpellate flower. The calyx is much reduced in staminate flowers, but the corolla is more reduced than the calyx in carpellate flowers; in the latter, the bracteoles may be adnate to the ovary and appear to represent the calyx, however more work on floral development is needed. Liston (2003) suggested that staminate flowers may have a vestigial disc, rather than a superior ovary, as has been suggested). Eyde (1964) described the ovules as being tenuinucellate, while others (e. g. Hallock 1930; Kapil & Mohana Rao 1967) describe and illustrate them as being crassinucellate. For additional general information, see Liston (2009).

Aucuba shows early corolla tube formation (Reidt & Leins 1994). Van Tieghem (1898) described the three outer layers of the integument as persisting in the fruit. There seems to be quite a bit of disagreement over embryological details - e.g. cf. Hallock (1930) and Kapil and Mohana Rao (1966 and references).

For chemical information, see Iwashina et al. (1997), and for general information, see Horne (1914). For wood anatomy of Garrya, see Moseley and Beeks (1955), and for that of both genera, see Noshiro and Baas (1998).

Classification. The apparent dissimilarity of Garrya and Aucuba masks extensive similarities, and the two can be intergrafted quite readily (Horne 1914: note that Ilex and Buxus could also be intergrafted, but the graft did not really take - see also Pinaceae and Portulacaceae). The two families are combined (see A.P.G. 2009).

For a monograph of Garrya, see Dahling (1978).

Previous Relationships. The relationships of Garrya in particular have been a bit of an enigma: Moseley and Beeks (1955) compared its wood anatomy with that of taxa that are here placed in 12 separate orders, mostly rosids.

EUCOMMIACEAE Engler, nom. cons.   Back to Garryales

Deciduous trees; O-methylated flavonols, little oxalate accumulation, inulin +, tanniniferous; hairs micropapillate; plant with articulated laticifers, producing gutta; vessel elements with simple perforations; true tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, plastids with starch grains; phloem fibres +; nodes 1:1; cuticle wax crystalloids 0; stomata anomocytic; buds perulate; leaves spiral, lamina vernation, supervolute-curved, margins toothed; flowers axillary, bracteoles 0; P 0; staminate flowers: A 5-12, filaments short, connective prolonged; carpellate flowers: one carpel aborts, stigmas spreading, decurrent; ovules 2/carpel, integument 5-9 cells across, micropyle long [700-1000 µm long], parietal tissue ca 3 cells across, nucellar cap +; fruit a samara; seed 1, testa thin; endosperm copious, ?embryo; n = 17.

1[list]/1: Eucommia ulmoides. Central China (map: from Fu & Hong 2000; Wang et al. 2003; fossil distribution, approximate only, mostly from Ferguson et al. 1997, green crosses).

• The family can be recognised vegetatively by its strongly serrate, spirally arranged, exstipulate leaves; when the lamina is pulled apart, the two halves are held together by threads of gutta. The flowers, with their two, spreading, decurrent stigmas and the samara fruits, are rather like those of an elm (Ulmaceae), but there is no perianth.

Evolution. Divergence & Distribution. Eucommia fossils occur widely in the North Temperate region from the Palaeocene onwards, being found as far south as central Mexico (Call & Dilcher 1997; Y.-F. Wang et al. 2003; Manchester et al. 2009).

Floral Biology & Seed Dispersal. Although chalazogamy appears not to occur here, some pollen tubes may grow towards the chalaza; more than one tube may proceed down the lengthy micropyle (Sogo & Tobe 2006c, but cf. Eckardt 1963, in part, pollen tube also soemetimes branched).

Chemistry, Morphology, etc. The teeth have glandular apices, and associated veins approach them (Hickey & Wolfe 1975). Cullen (1978) described the leaf vernation as being involute. For embryology, etc., see Zhang et al. (1990). The lateral nucellar tissue is thin, ca ca 2 cells across, and the tissue above the embryo sac is relatively much more prominent (Eckardt 1963).

Previous Relationships. Eucommia has often been associated with Euptelea (see Ranunculales), but the chemistry and ovule of the former are consistent with a position in the asterids.