Plant a shrub or tree; true roots +, origin endogeneous, root cap +, apex multicellular; endodermis +; shoot apical meristem multicellular; lateral meristems +, cork cambium producing cork abaxially, vascular cambium producing phloem abaxially and xylem adaxially; lamina with mean venation density 1.8 mm/mm2 (to 5 mm/mm2).
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 [so no Maüle reaction]; root xylem exarch, cork cambium deep seated; arbuscular mycorrhizae +; shoot apical meristem interface specific plasmodesmatal network; stem with vascular tissue around central pith [eustele], vascular bundles with interfascicular tissue, ectophloic, endodermis 0, xylem endarch; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; stem cork cambium superficial; branches exogenous; leaves with single trace from vascular sympodium ["nodes 1:1"]; vascular bundles collateral [stem: phloem external; leaf: phloem abaxial]; stomata morphology?, pore opening in response to leaf hydration active, control by abscisic acid, metabolic regulation of water use efficiency, etc.; leaves with petiole and lamina, spiral, development basipetal, blade simple; axillary buds +, not associated with all leaves; prophylls two, lateral; plant heterosporous, sporangia borne on sporophylls; microsporophylls aggregated in indeterminate cones/strobili; true pollen +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, parietal tissue 2+ cells across, 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, flagellae numerous; ovules increasing considerably in size between pollination and fertilization, female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large" [ca 8 mm3], but not much bigger than ovule, with morphological dormancy; embryo cellular ab initio, endoscopic, plane of first cleavage of zygote transverse, suspensor +, short-minute, embryo straight, shoot and root at opposite ends [allorrhizic], white, cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, 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.
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, exodermis +; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, associated gelatinous fibres [g-fibres] with innermost layer of secondary cell wall rich in cellulose and poor in lignin; 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 cell and sieve tube from same mother cell; sugar transport in phloem passive; nodes unilacunar [1:?]; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance to increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, secondary veins pinnate, overall growth ± diffuse, venation hierarchical, fine venation reticulate, veins (1.7-)4.1(-5.7) mm/mm2, endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, ± haplomorphic, 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, endothecium +, endothecial cells elongated at right angles to long axis of anther; tapetum glandular, cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine thin, compact, lamellate only in the apertural regions; nectary 0; G superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, 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]; ovule not increasing in size between pollination and fertilization; pollen binucleate at dispersal, male gametophyte trinucleate, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing between cells, growth rate 20-20,000 µm/hour, outer wall pectic, inner wall callose, with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametes lacking cell walls, flagellae 0, double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; seed exotestal, becoming much larger than ovule at time of fertilization; endosperm diploid, cellular [micropylar and chalazal domains develop differently, 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; embryogenesis cellular; germination hypogeal, seedlings/young plants sympodial; dark reversal Pfr -> Pr; Arabidopsis-type telomeres [(TTTAGGG)n]; 2C genome size 1-8.2 pg [1 pg = 109 base pairs], 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]].
[NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]]: wood fibres +; axial parenchyma diffuse or diffuse-in-aggregates; pollen monosulcate [anasulcate], tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.
[AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood +; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; carpels plicate; nucellar cap + [character lost where in eudicots?]; 12BP [4 amino acids] deletion in P1 gene.
[[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]] / MESANGIOSPERMAE: benzylisoquinoline alkaloids +; polyacetate derived anthraquinones + [?level]; outer epidermal walls of root elongation zone with cellulose fibrils oriented transverse to root axis; P more or less whorled, 3-merous [possible positiion]; embryo sac bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid; ?germination.
[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (extra-floral nectaries +); (veins in lamina often 7-17 mm/mm2 or more [mean for eudicots 8.0]); (stamens opposite [two whorls of] P); (pollen tube growth fast).
[CERATOPHYLLALES + EUDICOTS]: ethereal oils 0.
EUDICOTS: (Myricetin, delphinidin +), asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; (vessels with simple perforation plates in primary xylem); nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; K/outer P members with three traces, ("C" +, with a single trace); A few, (polyandry widespread, initial primordia 5, 10, or ring, ± centrifugal), filaments fairly slender, anthers basifixed; microsporogenesis simultaneous, pollen tricolpate, apertures in pairs at six points of the young tetrad [Fischer's rule], cleavage centripetal, wall with endexine; G with complete postgenital fusion, stylulus/style solid [?here]; seed coat?
[PROTEALES [TROCHODENDRALES [BUXALES + CORE EUDICOTS]]]: plant woody; (axial/receptacular nectary +).
[TROCHODENDRALES [BUXALES + CORE EUDICOTS]]: benzylisoquinoline alkaloids 0; euAP3 + TM6 genes [duplication of paleoAP3 gene: B class], mitochondrial rps2 gene lost.
[BUXALES + CORE EUDICOTS]: ?
CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one place]; micropyle?; palaeohexaploidy [gamma triplication], PI-dB motif +, small deletion in the 18S ribosomal DNA common.
[ROSIDS ET AL. + ASTERIDS ET AL.] / PENTAPETALAE: root apical meristem closed; (cyanogenesis also via [iso]leucine, valine and phenylalanine pathways); flowers rather stereotyped: 5-merous, parts whorled; P = calyx + corolla, the calyx enclosing the flower in bud, sepals with three or more traces, petals with a single trace; stamens = 2x K/C, in two whorls developing internally/adaxially to the corolla whorl and successively alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G , G  also common, when [G 2], carpels superposed, compitum +, placentation axile, style +, stigma not decurrent; endosperm nuclear; fruit dry, dehiscent, loculicidal [when a capsule]; RNase-based gametophytic incompatibility system present; floral nectaries with CRABSCLAW expression.
[SANTALALES [BERBERIDOPSIDALES [CARYOPHYLLALES + ASTERIDS]]] / ASTERIDS ET AL. / SUPERASTERIDS : ?
[BERBERIDOPSIDALES [CARYOPHYLLALES + ASTERIDS]]: ?
[CARYOPHYLLALES + ASTERIDS]: seed exotestal; embryo long.
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.
[ERICALES [ASTERID I + ASTERID II]]: (ovules lacking parietal tissue) [tenuinucellate].
[ASTERID I + ASTERID II] / CORE ASTERIDS / EUASTERIDS Back to Main Tree
Ellagic acid 0, non-hydrolysable tannins not common; sugar transport in phloem active; inflorescence basically cymose; (numerous, usu. associated with increased numbers of C or G); (pollen with orbicules); style short[?]; duplication of the PI gene.
Age. Bremer et al. (2004) suggested an age of around 123 m.y. for the euasterid node, Soltis et al. (2008: a variety of estimates) ages of 124-106(-85) m.y.a., Bell et al. (2010) suggested ages of (109-)100, 93(-85) m.y. - (116-)108, 99(-93) m.y. in the supplement - Lemaire et al. (2011b) offered estimates of (125-)114(-101) m.y. and N. Zhang et al. (2012), (96-)83(-68) m.y.. The age in Wikström et al. (2001) is (117-)112, 102(-97) m.y. for this node.
Evolution. Divergence & Distribution. From fossil evidence Martínez-Millán (2010) suggested a late date of around the Eocene, only 55-33.9 m.y.a., for the diversification of most of the asterid I and II orders, but this estimate is about half the ages suggested by others, e.g. see Beaulieu et al. (2013) for asterid II orders.
Endress (2011a) suggested that stamens adnate to petals, haplostemony, and unitegmic ovules are key innovations somewhere around here. 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, partly because of topological uncertainties, but partly because in Lamiales (for example), the four clades that are successively sister to other Lamiales either lack iridoids or have iridoids distinctively different (Oleaceae) from those in the other members of the clade; whether or not Carlemanniaceae have iridoids is unknown.
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. Furthermore, within Asterales, it is Asteraceae in particular that are very speciose, and within Asteraceae, Asteroideae, while within some orders there are series of species-poor pectinations at the bases of the trees, and these are often made up of woody plants that may have fleshy and few-seeded fruits (e.g. Lamiales, Apiales). Magallón and Sanderson (2001) suggested 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). Whatever may be driving diversification, it is likely to be combination of factors and acting at several places on the tree.
When looking at morphology in the context of clade diversity in this part of the tree, the situation becomes still more complicated. Garryales and Aquifoliales in particular are not very diverse and are sister to the rest of the asterid I and asterid II clades respectively. Members of these two small clades are woody, often trees of the rainforest, with rather small flowers, the fruits are usually fleshy - they are drupes for the most part - and a number have relatively large seeds, nearly always one per loculus. All in all, they are rather different from the mega-clades just mentioned, and in many respects they are more similar to Ericales, rosids, etc. They may be somewhat different in details of floral morphology, since the stamens are by no means always adnate to the petals and some taxa have ovules with parietal tissue and/or are bitegmic, although little is known about their ovules, embryology, etc.
There may be a change in chemistry around here, ellagic acid being notably uncommon throughout the asterid I + II clade, although it is scattered through the rosid-Ericales parts of the tree. 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. Feeney 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 + asterid II] clade has more than 50% tanniniferous species, only Rubiaceae and Caprifoliaceae, both with many woody members, being well represented (Mole 1993); the tannins involved are non-hydroysable tannins. Although sampling is sketchy, emission of isoprene gas shows a somewhat similar pattern, being known from Ericales, rosids (and also a few monocots and Magnoliales (see Kesselmeier & Staudt 1999; Sharkey et al. 2013). However, comparative phytochemical studies on Aquifoliales and the Garryales area are much needed.
Given our current understanding of phylogeny and character distribution, it is likely that the asterid I and II clades have separate origins from a morphology very different to that of the florally flashy megadiverse clades they contain. If the unplaced families around Garryales (see below) turn out to form pectinations at the base of the asterid I clade - most likely, from the results of Lens et al. (2008), the most comprehensive study so far - this evolutionary scenario would be clarified. Simple parsimony might then suggest that "corolla valvate, apex incurved; ovules 1-2/carpel, apical; fruit drupaceous" could be features of the common ancestor of the whole [asterid I + asterid II] clade. Lens et al. (2008a) note that the families involved have a primitive "Baileyan" syndrome of wood anatomical features such as long vessel elements with scalariform perforation plates, etc.. Comprehensive phylogenetic and morphological s.l. studies in this area of the tree are badly needed.
Ecology & Physiology. Cornwell et al. (2008) found that litter decomposition of forbs that predominate in the asterid I and II clades 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 and Westoby (1991) discuss 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). Since woody taxa of the [asterid I + asterid II] clade have "herbaceous" mechanisms of sugar transport, the correlation may be phylogenetic and less immediately associated with plant habit. A somewhat different focus on/classification of transport types suggests that one active transport mechanism, the synthesis and transport of raffinose family oligosaccharides shows little correlation with plant habit but some correlation with climate, being relatively more common in plants from warmer parts of the world (Davison et al. 2011).
Pollination Biology & Seed Dispersal. The asterid I clade in particular includes many large- and monosymmetric-flowered taxa that have dry fruits with many seeds (but c.f. Convolvulaceae, Lamiaceae, Verbenaceae - four seeds/fruit at a maximum); the apices of the petals tend to be rounded (but c.f. Acanthaceae). The asterid II clade has proportionally more taxa with small flowers that are aggregated into conspicuous inflorescences that appear polysymmetric to the pollinator; the dry fruits have few seeds (but c.f. Campanulaceae, Goodeniaceae, etc.; see also Beaulieu & Donoghue 2013); the apices of the petals tend to be pointed. In general, members of the [asterid I + asterid II] clade have rather small seeds (Linkies et al. 2010).
Genes & Genomes. 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. 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 [Dilleniales]), as well as in Ericales.
Chemistry, Morphology, etc. Patterns of polyandry in the [asterid I + asterid II] clade differ from that in more basal clades; here polyandry is often associated with anisomery. Along with the increase in stamen number, there are also increases in the numbers of perianth parts and/or carpels, the latter occurring 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) have more numerous stamens that would be expected, but how the flowers are constructed here is unclear. Paracryphiaceae (Paracryphiales) also show interesting variation in floral merism. Polyandry is much more common in other eudicots, but there it often occurs independently of any changes in sepal, petal or carpel number - there are of course exceptions, 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, Conostegia (Melastomataceae), where stamen and carpel number may be similar (see Wanntorp et al. 2011 for this and some other examples) and in some core Caryophyllales (Ronse de Craene 2013). The near absence of other kinds of increase in stamen number in the [asterid I + asterid II] may reflect a change in underlying floral organisation/development in the stem clade, perhaps in turn connected with the rather stereotyped (in terms of basic floral construction) flowers so common here.
Phylogeny. Aquifoliaceae were included in the asterid II clade by Gustafsson et al. (1996) and B. Bremer (1996). However, Qiu et al. (2011) found weak support for a set of relationships [[paraphyletic Icacinaceae plus Garryales [Aquifoliaceae + rest of asterid I clade]] [rest of asterid II 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; one possibility is that Aquifoliales may belong in the asterid I clade (Oxelman et al. 2004b). Both Garrya and Eucommia have only the d copy, perhaps a feature of Garryales in particular, or part of them. Sampling needs to be improved, but optimisation of the persistence/loss of the I copy on the asterid tree will probably be difficult (Oxelman et al. 2004b). Aquifoliaceae also seem to lack the PI duplication of other members of the [asterid I + asterid II] clade (Viaene et al. 2009: no other Aquifoliales examined). N. Zhang et al. (2012) found weak support in an analysis of nuclear genes for an [Aquifoliales + Garryales] clade. There are several loose ends that need to be tidied up although most recent analyses place Aquifoliales (q. v.) as sister to the rest of the asterid II clade.
ASTERID I / LAMIIDAE Back to Main Tree
G , superposed; loss of introns 18-23 in d copy of RPB2 gene.
Age. Wikström et al. (2001) estimated an age of (112-)107, 100(-95) m.y. for the crown group, Magallón and Castillo (2009: major basal polytomy) an age of ca 96.85 m.y., Bremer et al. (2004: c.f. topology) an age of ca 119 m.y., Janssens et al. (2009) an age of 112±9.3 m.y.a., Moore et al. (2010: 95% HPD) ages of (80-)76(-71) m.y., and Lemaire et al. (2011b) a stem group age of (118-)98(-87).
See Martinez-Millán (2010) for fossil-based estimates for the age of this clade.
Phylogeny. Although Garryales are often found to be sister to (most of) the rest of the asterid I clade (e.g. Lens et al. 2008a: maximum parsimony analyses), the composition of any clade that might immediately include them is unclear. Oncothecaceae have been considered close, but neither they nor the other families or genera mentioned immediately below link strongly here (e.g. Kårehed 2001, 2002b; for the position of Oncothecaceae, see Cameron 2001, 2003; Olmstead et al. 2000; B. Bremer et al. 2002). In a parsimony analysis of combined molecular and morphological data Lens et al. (2008a) found a clade [Oncothecaceae + all three groups of unassigned ex-Icacinaceae] (see below: 72% bootstrap) to be sister to the asterid I clade, while in a Bayesian analysis this clade was joined by Garryales (but with little support for the enlarged clade); the other asterid I groups formed a clade with 1.0 p.p.. ().
Resolving the relationships of the Icacinaceae s.l. genera in this area is critical. 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 in Icacinaceae s. str. below. There was initially only weak support for Icacinaceae in this position (D. Soltis et al. 2000), but Kårehed (2001) identified four ex-Icacinaceous groups associated with Garryales: Icacinaceae s. str., and the Cassinopsis, Emmotum and Apodytes groups. However, groupings within a more widely circumscribed Garryales could not be identified, nor did the larger Garryales have any strong support. Relationships of 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. The Bayesian analysis of Soltis et al. (2007) recovered Icacina as sister to all other asterid I taxa included (0.99 pp), while 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 very weak. Icacinaceae s. str., strongly supported as being monophyletic, were consistently sister to a [Boraginales, Gentianales, Lamiales, Solanales] clade, but with appreciable support only when morphological data were added to the molecular data (Lens et al. 2008a). Icacina does not link with Garryales in the tree provided Bell et al. (2010), but joins the backbone at a node above. Angulo et al. (2013) recovered a well supported Icacinaceae, but relationships between the seven genera of ex-Icacinaceae in the study (Metteniusa was not included) and the position of Garryaceae varied between analyses with ndhF only and those with the addition of morphological data.
Unplaced: corolla valvate, apex incurved; ovules 1-2/carpel, apical; fruit drupaceous.
Age. Various dates have been given that may end up as being for crown-group Garryales - or the asterid I clade.... Magallón and Castillo (2009) offer estimates of ca 96.85 m.y. for stem group Icacinaceae - and also Oncothecaceae, Metteniusaceae and Garryales, the four being part of a polytomy. Lemaire et al. (2011b) date the divergence of Icacina from the rest of the asterid I clade (including Garryales) at ca 102 m.y., while Bremer et al. (2004) dated divergence of Icacinaceae from all asterid I taxa apart from Garryaceae, Oncothecaceae, etc. to 119 m.y..
Evolution. Divergence & Distribution. Morphologically, it would be easy to include this group in an expanded Garryales if the phylogeny suggests this. However, if the group turns out to be paraphyletic at the base of the asterid I clade, characters of Garryales, the asterid I, and possibly also the [asterid I + asterid II] clades will all have to be reworked (see above).
Included: Icacinaceae, Metteniusaceae, Oncothecaceae, and assorted unassigned genera. Back to Main Tree
[[Oncothecaceae + Metteniusaceae] Garryales]: ?
Age. Bell et al. (2010) estimate an age for this (possible) clade of (109-)99, 91(-80) m.y., Bremer et al. (2004) an age of ca 114 m.y..
[Oncothecaceae + Metteniusaceae]: vessel elements with scalariform perforation plates; nodes 5:5; fibres/sclereids +; petiole bundles arcuate, complex; inflorescence cymose; bracts thick, triangular; A basifixed; G ; ovules 2/carpel, apical, funicle long; fruit a drupe, K persistent; endosperm copious.
Evolution. Divergence & Distribution. For characters linking these two families, see also González and Rudall (2010).
ONCOTHECACEAE Airy Shaw Back to Unplaced
Evergreen trees; chemistry?; 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, dithecal; pollen smooth; nectary?; G opposite petals, styles branched to base, conduplicate, stigma punctate; ovules (1), 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.,/p>
Tobe (2013) suggested that the flowers were monosymmetric. 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: anatomy), Lobreau-Callen (1977: pollen), and Carpenter (1975: general).
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?; stomata anomo-cyclocytic; mesophyll fibres +; hairs ± T-shaped; lamina margins entire; inflorescence cymose/thyrsiform; K short, quincuncial, C tube formation late; connective massive, anthers long, latrorse, thecae with 4 vertical rows of locellae [moniliform], locelli dehiscing individually, endothecium 0; nectary 0; G monosymmetric, 4 carpels ± reduced, placentation parietal, style long, stigma punctate; 1 ovule fertile, funicle massive, integument vascularized, 20+ cells across, parietal tissue ?0; 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.]
Chemistry, Morphology, etc. For general information, see Lozano C. and Lozano (1988); for anatomy, etc., see Reed (1955), and for floral development, see González and Rudall (2010). It is unclear if the two ovules are from adjacent carpels (their Fig. 10) or from the same carpel (Fig. 6k, l]); since the gynoecium is paracarpous, the placentation is parietal.
Phylogeny. In morphological phylogenetic analyses Metteniusa fits quite comfortably into Cardiopteridaceae, ex Icacinaceae (Kårehed 2001: Cornaceae not included). However, molecular analyses suggest a position in the asterid I area, and petiole anatomy, carpel number, etc., are similar to Oncothecaceae in particular (González & Rudall 2007, esp. 2010; González et al. 2007); 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 + Garryales]: ?
Age. Wikström et al. (2001: Oncotheca separate) estimated the age of this node - if it exists - at (105-)100, 93(-88) m.y.a..
ICACINACEAE Miers, nom. cons. Back to Unplaced
Trees, or lianes climbing by non-axillary branch tendrils or twining; (plants Al-accumulators); monoterpene indole alkaloid camptothecin +, iridoids ?; secondary thickening often atypical [included phloem +, 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 with wing bundles, or annular (and with medullary bundles); stomata cyclocytic (anomocytic); hairs unicellular, often adpressed and ± T-shaped, also globular; leaves spiral (opposite), conduplicate(-plicate), lamina (palmately lobed), (secondary veins palmate), margins entire, (toothed); plant dioecious[?]; inflorescence branched, spicate or racemose, pedicels articulated; (flowers 4-merous); K connate (0 – Pyrenacantha; ± free - Phytocrene), (C free), (adaxially keeled), apices of corolla lobes inflexed; nectary 0 (+): staminate flowers: A dorsifixed, (epipetalous); pollen also porate, echinate; pistillode +; carpellate flowers: staminodes +/0; G also 1?, style +, stigma punctate, or style 0, stigma broad; ovules (apically bitegmic - Phytocrene), integument 7-10 cells across, vascularized (not), parietal tissue 0-?, funicular obturator +; fruit a 1-seeded drupe, flattened and/or ribbed or pocked or not, (locule walls papillate internally), K persistent; seed coat?, no testa bundles; endosperm copious to 0, ruminate or not, 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): Pyrenacantha (30), Iodes (28). Pantropical, inc. W. Pacific, to China and Japan (map: Sleumer 1971a; Utteridge & Brummitt 2007; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010).
Age. Bremer et al. (2004: Cass. Icac. Pyren.) suggested an age of 115 m.y. for crown-group Icacinaceae.
Evolution. Divergence & Distribution. 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); for fossils of Iodeeae, see Pigg et al. (2008a). Endocarps identifiable as the Old World Phytocreneae are known from both North and South America in Palaeocene deposits about 60-58 m.y.o. (Stull et al. 2012).
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 it is probably protected by a change in its amino acid sequence (Sirikantaramas et al. 2009).
Chemistry, Morphology, etc. The description above largely refers to the Icacina group (see Kårehed 2001). Hoseia, with its long-petiolate leaves that have palmate venation and long-dentate margins, is particularly distinctive vegetatively.
Phytocreneae (Chlamydocarya, Miquelia, Phytocrene, Polycephalium, and Pyrenacantha) have fruits with somewhat flattened and pock-marked stones, the outer cells of the sclereidal layer having sinuous, interdigitating, anticlinal walls. Invaginations of the stone often signal invaginations into the endosperm (Stull et al. 2012 and references).
For additional information, see Utteridge et al. (2005: general), also Rankin et al. (2008), Pigg et al. (2008a), and Stull et al. (2011, 2012), all fruit anatomy, especially of fossils, and Cremers (1973, 1974) for some growth patterns.
The family is very poorly known embryologically (see in Sleumer 1942 for Pyrenacantha).
For other information about Icacinaceae and members of the three groups below, see Bailey and Howard (1941, their group II: anatomy), Mauritzon (1936c) and Fagerlind (1945a), embryology, Heintzelmann and Howard (1948: crystals and indumentum), Sleumer (1942, 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 familial circumscriptions, and Lens et al. (2008a) provide a detailed anatomical survey in a phylogenetic context. The wood occasionally fluoresces.
Phylogeny. Relationships in Lens et al. (2008a) were [[Nothapodytes + Mappia] [Natsiatum [[Iodes, Pyrenacantha, etc.] [Icacina, Alsodeiopsis]]]], although the last pair of sister taxa were not recovered in Bayesian analyses, and in Angulo et al. (2013: one gene, moderate to good support) were [[Nothapodytes + Mappia] [[Iodes, Pyrenacantha, etc.] [Icacina, Leretia etc.]]].
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
1. Apodytes. 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 asymmetric, ribbed, style thin, persistent; n = 20, ?22.
3/10: Tropics, to Australia (Queensland) (map: from Sleumer 1971a). The two genera above formed a clade in the analysis of Angulo et al. (2013). Probably to include Dendrobangia - M. Schori, pers. comm. vi.2010. For fruit morphology, see Potgeiter et al. (1994b).
2. Cassinopsis. Vessel elements with scalariform perforation plates; nodes 3:3; stomata cyclocytic; hairs not ± T-shaped; leaves opposite.
1/4: Africa and Madagascar. For fruit morphology, see Potgeiter et al. (1994a).
3. Emmotum. Vessel elements with scalariform perforation plates; bordered pits +; diffuse apotracheal parenchyma +; nodes 3:3; (hairs T-shaped; stellate); stomata cyclocytic(-anomocytic); lamina (± conduplicate in bud - Platea); flowers 4-5-merous, (imperfect); C (0), ridged adaxially or not, with adaxial hairs (none); G , one carpel fertile, (2-3-septate: Emmotum), style very short to medium; ovules 2/fertile carpel, collateral or superposed; fruit flattened and symmetric, (stone ± ribbed); embryo short to long; n = ? Perhaps includes Calatola – scalariform perforation plates; nodes 3:3; leaves toothed, conduplicate, Cordia growth pattern.
4(?6)/21(32): Central and South America, West Indies, rarely Malesia (map: from Sleumer 1971a). Some information is taken from Howard (1941), Sleumer (1971a) and de Stefano and Fernández-Concha (2011); see Angulo et al. (2013) for this clade; [Emmotum [Oecopetalum + Ottoschulzia]].
Synonymy: Emmotaceae van Tieghem, Emmotales Doweld
[GARRYALES [GENTIANALES [SOLANALES [BORAGINALES + LAMIALES]]]]: ?
GARRYALES Martius Main Tree.
Woody; route II decarboxylated iridoids [inc. aucubin], gutta +; fibres with bordered pits; petiole bundles arcuate; sclereids +; stomata?; hairs unicellular; plants dioecious; flowers small; C valvate, free; anthers basifixed; pollen ± atectate; ovary 1-celled, styles branched to the base, spreading, stigmatic much of their length; ovules 1-2/carpel, apical, apotropous, parietal tissue 3< cells across, endothelium 0; fertilization delayed; fruit indehiscent. - 2 families, 3 genera, 18 species.
Age. Lemaire et al. (2011b) date crown-group Garryales to (91-)63(-31) m.y., Bell et al. (96-)77, 70(-51) m.y., while Wikström et al. (2001) estimated it at (89-)84, 80(-75) m.y..
Note: Possible apomorphies are in bold. However, the actual level at which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is partly because many characters show considerable homoplasy, in addition, basic information for all too many characters is very incomplete, frequently coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there is the not-so-trivial issue of how ancestral states are reconstructed...
Evolution. Pollination 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 Metteniusaceae, Oncothecaceae, and Icacinaceae and related genera 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 nucellus on the sides of the embryo sac is not very thick, even if the ovules have parietal tissue 3-8 cells across.
Phylogeny. For the circumscription of Garryales, see Olmstead et al. (1993), D. E. Soltis et al. (2000), B. Bremer et al. (2002), Lens et al. (2008a), , etc..
Classification. 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 acids +; vessel elements with scalariform perforation plates; 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, pistillode +; carpellate flowers: staminodes 0; ovary inferior, [(3)]; 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. W. North America, Central America, the Greater Antilles and East Asia.[Photo - Fruit]
Age. Magallón and Castillo (2009) suggest that crown-group Garryaceae are some 49.8 m.y.o., Wikström et al. (2001) date them to (57-)52, 42(-37) m.y., Janssens et al. (2009) to 20±8.6 m.y. and Bell et al. (2010) to (58-)38, 36(-17) m.y.a..
Fossil leaves of Aucuba are reported from the Eocene of Washington (Wehr & Hopkins 1994).
1. Garrya Lindley
Diterpenoid alkaloids +; fibres with helical thickening; lamina cartilaginous, margins ± entire; inflorescences catkinate, bracts ± connate; staminate flowers: P [?= bracteoles] valvate, connate apically; A alternating with P; (pollen colporate, partly tectate); nectary 0; pistillode +; carpellate flowers: P [?= K] 2, minute, or 0; ovule epitropous, integument 12-30 cells across, endothelium 0, parietal tissue 4-5 cells thick, (nucellar cap 2 cells across), hypostase +, funicle quite long, with "collar" below the ovule; antipodals persistent or not; testa multiplicative, exotestal cells large, palisade, fleshy, most of testa not persistent; suspensor very long, endosperm ?green, starchy; n = 11.
1/13. W. North America, Central America and the Greater Antilles (map: from Dahling 1978).
2. Aucuba Thunberg
Gutta percha ?, flavonols, kaempferol +; vascular tracheids present; pericyclic fibres 0; lamina margins serrate; K minute or 0, C with early tube formation; staminate flowers: pollen?; carpellate flowers: G 1, stylulus +, stigma capitate to shortly decurrent, bilobed; nectary on top of G; integument "thick", parietal tissue ca 8 cells across, (nucellar cap 2 cells across), endothelium?; (megaspore mother cells several); ?seed coat; n = 8.
1/4. Sikkim to N. Burma, China and Taiwan to Japan (see map above).
Synonymy: Aucubaceae Berchtold & J. Presl
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 reported to be 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 then appear to be sepals. Liston (2003) thought that the staminate flowers had a vestigial disc, rather than a superior ovary, as had been suggested. More work on floral development is needed.
There seems to be disagreement over details of the embryology of Garrya. Thus Eyde (1964) described the ovules as being tenuinucellate, while Hallock (1930) and Kapil and Mohana Rao 1967) described and illustrated them as having a very thick parietal layer. For some details of the ovule of Aucuba, see Palm and Rutgers (1917); they noted (p. 121) that the parietal tissue kept on dividing, forming a "mighty cap on the embryosac". There are sometimes two ovules - does this imply that there are two carpels (Horne 1914)?
For chemical information, see Iwashina et al. (1997), for inflorescence morphology, esp. of Garrya, see Jahnke (1986), floral development, see Reidt and Leins (1994), and for general floral 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). For additional general information, see Liston (2009).
Classification. The apparent dissimilarity of Garrya and Aucuba masks extensive similarities, and the two can be intergrafted quite readily (Horne 1914). 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. Aucuba was placed in Cornaceae by Cronquist (1981), Garryaceae were separate, but near by, while Takhtajan (1997) placed Garryaceae and Aucubaceae in separate, but adjacent, orders.
EUCOMMIACEAE Engler, nom. cons. Back to Garryales
Deciduous trees; O-methylated flavonols, little oxalate accumulation, inulin +, tanniniferous; laticifers +, articulated; vessel elements with simple perforations; true tracheids and rays alone, tracheid/tracheid pits circular, bordered; phloem fibres +; nodes 1:1; hairs micropapillate; 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, endothecium biseriate; tapetal cells 2-6-nucleate; carpellate flowers: one carpel aborts; ovules 2/carpel, integument 5-9 cells across, micropyle long [700-1000 µm long], parietal tissue 3-5 cells across, nucellar cap ca 3 cells across; archesporium multicellular; fruit a samara, seed 1; testa thin; endosperm copious, embryo long; n = 17; chloroplast ORF184 lost.
1[list]/1: Eucommia ulmoides. Central China (map: from Guo 2000; Wang et al. 2003; green crosses are fossil distribution, approximate only, mostly from Ferguson et al. 1997).
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).
Pollination Biology & Seed Dispersal. Whether chalazogamy occurs in Eucommia is unclear. Sogo and Tobe (2006c) noted that some pollen tubes grew towards the chalaza and more than one tube could proceed down the lengthy micropyle, but Eckardt (1963) did record chalazogamy; the pollen tube is also sometimes 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. The lateral nucellar tissue is thin, ca 2 cells across, and the tissue above the embryo sac is relatively much more prominent (Eckardt 1963).
For embryology, etc., see Zhang et al. (1990).
Previous Relationships. Eucommia has often been associated with Euptelea (see Ranunculales), as in Cronquist (1981), but the chemistry and ovule of the former are consistent with a position in the asterids.