EMBRYOPSIDA Pirani & Prado (crown group)
Gametophyte dominant, independent, multicellular, thalloid, with single-celled apical meristem, showing gravitropism; flavonoids + [absorbtion of UV radiation]; protoplasm dessication tolerant [plant poikilohydric]; cuticle +; cell walls with (1->4)-ß-D-glucans [xyloglucans], lignin +; rhizoids unicellular; several chloroplasts per cell; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles in vegetative cells 0, metaphase spindle anastral, predictive preprophase band of microtubules, phragmoplast + [cell wall deposition spreading from around the spindle fibres], plasmodesmata +; antheridia and archegonia jacketed, stalked; spermatogenous cells monoplastidic, centrioles develop de novo, associated with basal bodies of flagellae, multilayered structure +, proximal end of basal bodies lacking symmetry, stellate pattern associated with doublet tubules of transition zone; spermatozoids with a left-handed coil; male gametes with 2 lateral flagellae; oogamy; diploid embryo initially surrounded by haploid gametophytic tissue, plane of first division horizontal [with respect to long axis of archegonium/embryo sac], suspensor/foot +, cell walls with nacreous thickenings; sporophyte multicellular, sporangium +, single, with polar transport of auxin, dehiscence longitudinal; meiosis sporic, monoplastidic, microtubule organizing centre associated with plastid, cytokinesis simultaneous, preceding nuclear division, sporocytes 4-lobed, with a quadripolar microtubule system; spores in tetrads, sporopollenin in the spore wall, wall with several trilamellar layers [white-line centred layers, i.e. walls multilamellate]; spores trilete; close association between the trnLUAA and trnFGAA genes on the chloroplast genome.
Note that many of the bolded characters in the characterization above are apomorphies in the streptophyte clade along the lineage leading to the embryophytes rather than being apomorphies of the crown embryophytes.
Abscisic acid, ?D-methionine +; sporangium with seta, seta developing from basal meristem [between epibasal and hypobasal cells], sporangial columella + [developing from endothecial cells]; stomata +, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and in rhizoids/root hairs; polar transport of auxins and class 1 KNOX genes expressed in the sporangium alone; MIKC, MI*K*C* and class 1 and 2 KNOX genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns.
[Hornworts + Polysporangiophyta]: archegonia embedded/sunken in the gametophyte; sporophyte long-lived, chlorophyllous, nutritionally largely independent of the gametophyte; sporophyte-gametophyte junction interdigitate, sporophyte cells showing rhizoid-like behaviour.
Sporophyte well developed, branched, free living, sporangia several; spore walls not multilamellate [?here]; apical meristem +.
EXTANT TRACHEOPHYTA / VASCULAR PLANTS
Photosynthetic red light response; water content of protoplasm relatively stable [plant homoiohydric]; control of leaf hydration passive; (condensed or nonhydrolyzable tannins/proanthocyanidins +); vascular tissue +, sieve cells + [nucleus degenerating], tracheids +, in both protoxylem and metaxylem; endodermis +; root xylem exarch [development centripetal]; stem with an apical cell; branching dichotomous; leaves spirally arranged, blades with mean venation density 1.8 mm/mm2 [to 5 mm/mm2]; sporangia adaxial on the sporophyll, derived from periclinal divisions of several epidermal cells, wall multilayered [eusporangium]; columella 0; tapetum glandular; gametophytes exosporic, green, photosynthetic; stellate pattern split between doublet and triplet regions of transition zone; placenta with single layer of transfer cells in both sporophytic and gametophytic generations, embryonic axis not straight [root lateral with respect to the longitudinal axis; plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Branching ± monopodial; lateral roots +, endogenous, root apex multicellular, root cap +; tracheids with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangia borne in pairs and grouped in terminal trusses, dehiscence longitudinal, a single slit; cells polyplastidic, microtubule organizing centres not associated with plastids, diffuse, perinuclear; male gametes multiflagellate, basal bodies staggered, blepharoplasts paired; chloroplast long single copy ca 30kb inversion [from psbM to ycf2].
Plant woody; lateral root origin from the pericycle; branching lateral, meristems axillary; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].
EXTANT SEED PLANTS / SPERMATOPHYTA
Plant 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 [hence with p-hydroxyphenyl and guaiacyl lignin units, so no Maüle reaction]; root with xylem and phloem originating on alternate radii, vascular tissue not medullated, cork cambium deep seated; arbuscular mycorrhizae +; shoot apical meristem interface specific plasmodesmatal network; stem with vascular cylinder around central pith [eustele], phloem abaxial [ectophloic], endodermis 0, xylem endarch [development centrifugal]; 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]; stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; leaves with petiole and lamina, 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 linear, functional megaspore single, chalazal, lacking sporopollenin, megasporangium indehiscent; pollen grains landing on ovule; male gametophyte development initially endosporic, lacking chlorophyll, tube developing from distal end of grain, gametes two, developing after pollination, with cell walls; 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, embryonic axis straight [shoot and root at opposite ends; plant allorhizic], white, cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, whole nuclear genome duplication [zeta duplication], 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.
ANGIOSPERMAE / MAGNOLIOPHYTA
Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, 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 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, overall growth ± diffuse, venation hierarchical-reticulate, secondary veins pinnate, 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 +, members each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; 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; carpels present, 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, functional megaspore, chalazal, lacking cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; supra-stylar extra-gynoecial compitum +; ovule not increasing in size between pollination and fertilization; pollen grains landing on stigma, bicellular at dispersal, mature male gametophyte tricellular, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing between cells, growth rate (20-)80-20,000 µm/hour, apex of pectins, wall with callose, lumen 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, much larger than ovule at time of fertilization; endosperm diploid, cellular, heteropolar [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; dark reversal Pfr -> Pr; Arabidopsis-type telomeres [(TTTAGGG)n]; 2C genome size 1-8.2 pg [1 pg = 109 base pairs], whole nuclear genome duplication [epsilon duplication]; protoplasm dessication tolerant [plant poikilohydric]; 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 +; sesquiterpene synthase subfamily a [TPS-a] [?level], 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 position]; pollen tube growth intra-gynoecial; embryo sac bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid.
[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]]]: (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?; whole nuclear genome duplication [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, internal/adaxial to the corolla whorl, 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 [sometimes evident only early in development, petals then appearing to be free]); anthers dorsifixed?; (nectary gynoecial); G , style single, long; ovules unitegmic, integument thick, endothelium +, nucellar epidermis does not persist; exotestal [!: even when a single integument] 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
Plants woody, evergreen; ellagic acid 0, non-hydrolysable tannins not common; vessel elements long, with scalariform perforation plates; nodes 3:3; sugar transport in phloem active; inflorescence usu. basically cymose; flowers rather small [<8 mm across]; C free or basally connate, valvate, petals often with median adaxial ridge and inflexed apex; A = and opposite sepals or P, (numerous [usu. associated with increased numbers of C or G]), free to basally adnate to C; G #?; ovules 2/carpel, apical, pendulous; fruit a drupe, drupe ± flattened, surface ornamented; seed single; duplication of the PI gene.
Age. Bremer et al. (2004) estimated an age of around 123 m.y. for this 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.a., N. Zhang et al. (2012), (96-)83(-68) m.y., and Xue et al. (2012) an age of approximately 78.3 m.y. ago. Other ages are (117-)112, 102(-97) m.y. (Wikström et al. 2001) and around 96.1-91.5 m.y.a. (Naumann et al. 2013).
Evolution. Divergence & Distribution. From fossil evidence Martínez-Millán (2010) suggested a late date of 55-33.9 m.y.a. for diversification of most of the euasterid (= asterid I + II/lamiid + campanulid clades) orders, i.e. around the Eocene. This estimate is about half the ages suggested by others, e.g. see Beaulieu et al. (2013) for the ages of the campanulid orders and also the dates immediately above.
In an analysis of floral morphospace in angiosperms, lamiids were found to be significantly different from all other groups, mostly having flowers with sepals and petals, the latter being united, and few stamens and united carpels; campanulids also fit here (c.f. in part Chartier et al. 2014b). Indeed, the euasterids are notably speciose, although it is more accurate to say that the florally flashy Boraginales, Lamiales, Gentianales, Solanales, Asterales and Apiales are speciose and have high diversification rates (Magallón & Sanderson 2001; Magallón & Castillo 2009): Boraginales and Dipsacales are rather smaller. Although Magallón and Sanderson (2001: c.f. dating) suggested that Asterales have the highest diversification rate (0.2717, 0.3295), the honour goes to Lamiales in Magallón and Castillo (2009: 0.0928-0.1257), but whatever may be driving diversification, it is likely to be combinations of factors that are acting at different places on the tree rather than single factors. Indeed, within Asterales, for example, it is Asteraceae in particular that are very speciose, and within Asteraceae, it is Asteroideae. Within Lamiales and Apiales in particular there are more or less species-poor basal pectinations made up of woody plants. In Apiales, these plants have fleshy and few-seeded fruits, and one of the basal clades, Pennantiaceae, is a member of the old Icacinaceae; much of the diversity is in Apiaceae (see also Nicolas & Plunkett 2014: position of Pennantiaceae still not certain).
Endress (2011a) thought that haplostemony, stamens adnate to petals, and unitegmic ovules were key innovations somewhere around here, but exactly where the last two features are to be placed is unclear, as is becoming evident from his own work (Endress & Rapini 2014).
A number of changes in this area do seem to distinguish the euasterids from other angiosperms. Patterns of polyandry in the euasterids differ from those 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 being in a single if somewhat bowed whorl. Examples are some species of Plerandra s. str. and Tupidanthus (Araliales-Araliaceae); here there is a kind of fasciation of the flower, and there are about as many stamens as carpels, with well over 100 of both (e.g. Sokoloff et al. 2007b; Nuraliev et al. 2014); perhaps there has been an increase in the size of the floral meristem. Anthocleista and Potalia (Gentianales-Gentianaceae-Potalieae) and some Gentianaceae-Chironieae, with up to 16-merous flowers, Lamiaceae-Symphorematoideae (Lamiales), and Codonaceae, Hoplestigma (Cordiaceae), and Lennoa and relatives (Ehretiaceae), all Boraginales, but not immediately related to each other, are other examples. Dialypetalanthus and Theligonum, both Rubiaceae, have more numerous stamens than would be expected, but how their flowers are constructed is unclear, and this is true of the multuistaminate flowers of Eucommia (Garryales). Paracryphiaceae (Paracryphiales) also show interesting variation in floral merism.
Polyandry is more common in other eudicots, and there it often occurs independently of any changes in sepal, petal or carpel number. Exceptions include Crassulaceae and Conostegia (Melastomataceae), where stamen and carpel number may be similar (see Wanntorp et al. 2011 for this and some other examples), Actinidia, where there are many carpels in a single whorl and many stamens, and in some core Caryophyllales (Ronse de Craene 2013). The near absence of other kinds of increase in stamen number that involve features such as fascicles, ring meristems and centrifugal androecial development in the euasterid clade may reflect a change in underlying floral organisation/development in the stem euasterids, reflected in the rather stereotyped (in terms of basic floral construction) flowers so common here.
There may be a change in chemistry in this part of the tree, ellagic acid being notably uncommon in the euasterids, although it is scattered through the rosid to 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). No large family in the euasterids 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. Flowers of Emmotum and fruits of Apodytes (Metteniusaceae, see below) are rich in tannins (Endress & Rapini 2014; Potgeiter & van Wyk 1994b). 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: again, sampling).
The final demise of the old, broad Icacinaceae should allow us to to better understand the evolution of the euasterids as a whole. The old Icacinaceae make up all or most of three of the four orders at the base of the lamiids and campanulids and are very different from the megadiverse clades the latter contain. These orders are Garryales (the only clade without genera that have not been in Icacinaceae) and Aquifoliales, whose circumscriptions, if somewhat surprising in the context of older ideas of relationships, have been stable for a few years, and they are immediately sister to the rest of the lamiid and campanulid clades respectively. Metteniusales and Icacinales (for their relationships and delimitation, see below) are successively sister to the clade [Garryales + other lamiids] (Stull et al. 2014). Given the phylogenetic positions of the fragments of the old Icacinaceae, simple parsimony should suggest if characters can be placed somewhere around the euasterid node, these would be the characters of the old Icacinaceae.
These four small orders include 10 families, about 61 genera and 717 species (405 of the latter belong to Ilex), yet they vary in many anatomical and floral characters classically considered to be of phylogenetic importance (see below). All members of these clades are woody, most are trees of l.t.r.f. (not Garryales), nearly all have rather small flowers, most have fleshy fruits - drupes for the most part - with quite large seeds, one per loculus, usually only one per fruit. They may also differ from other euasterids 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 (for the latter in particular, see Endress & Rapini 2014), although little is known about their embryology. Lens et al. (2008a) noted that some of the families involved have a primitive "Baileyan" syndrome of wood anatomical features such as long vessel elements with very scalariform perforation plates. All in all, they are rather different from the big clades just mentioned, and in some respects they are more similar to Ericales, rosids, and the like.
However, there is a dearth of basic knowledge of many critical characters. Gynoecial evolution is particularly perplexing - or perhaps it only seems to be because so little is known about gynoecial development and morphology (but see Endress & Rapini 2014 for the way forward). González and Rudall (2010) speculated that the bicarpellate gynoecium of Lamiales, Gentianales and Solanales was derived from the pseudomonomerous gynoecium of something like Metteniusa. Although this character can probably be placed one node down the tree (see Garryales), both carpel number and numbers of ovules/carpel in Icacinaceae s.l. are unclear (see below), hence the characterization of this node. There are also some interesting correlations, for instance, valvate corolla aestivation and petals with pointed, incurved apices and median adaxial ridges. A corolla with similar features is found in many Apiaceae/Araliaceae, while the valvate sepals of Rhamnaceae also have a longitudinal adaxial ridge! Finally, there is simply much variation in whether or not the corolla is fused (if it is, it is often only rather shortly connate, and corolla tube development is almost entirely unknown) and the stamens are adnate to the corolla. Indeed, a strongly connate corolla with the stamens adnate some way up the tube is quite uncommon is these orders, examples being Metteniusa (Metteniusaceae) and especially Leptaulus (Cardiopteridaceae).
One set of characters, nodal and woody anatomy, is quite well known thanks to the early work of Bailey and Howard (1941a-d) and subsequently that of Lens et al. (2008a), who began to place the variation in a phylogenetic context. Some of this variation has been added to the characterisations, although measurements for immature individuals (Lens et al. 2008a) have been excluded. There are correlations here, too, unilacunar nodes with simple perforation plates, versus tri- and pentalacunar nodes with scalariform perforation plates (see also Bailey & Howard 1941b). Features like vessel and fibre length also correlate with nodal anatomy, although not quite in such a simple fashion.
Lens et al. (2008a) drew attention to similarities in woody anatomy between the Icacinaceae s.l. and other woody clades, including Garryales), noting that the "primitive" wood characters they emphasized in the Iacinaceae s.l. were also to be found in woody clades at the base of various campanulid clades. Lens et al. (2008a) mentioned Rousseaceae, sister to Campanulaceae and in turn sister to other Asterales; Carpodetus, also Rousseaceae, has a corolla similar to that of Icacinaceae. Columelliaceae (Bruniales), Adoxaceae (Dipsacales), most Cornales (and c.f. flowers in Cornus, etc.), and Pennantia (Apiales-Pennatiaceae; again, c.f. flowers in many Apiales); although Ericaceae were also mentioed, they are embedded in Ericales, but some Tetrameristaceae have flowers similar to those of Icacinaceae s.l.. This is all rather anecdotal, and ecological parallelism must play a role here, but evolutionary patterns in the asterids as a whole need reappraisal in the light of the dissolution of the Icacinaceae.
Ecology & Physiology. Leaf size shows a sharp decrease here (Cornwell et al. 2014). Cornwell et al. (2008) found that litter decomposition of the forbs that predominate in the euasterids 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 affect the rate of nutrient cycling. These findings need to be revisited in the context the interpolation of two more orders at the base of the euasterid tree (Stull et al. 201?, see below).
In both the campanulids and lamiids 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). Seed coats with a mechanical layer more than a single cell thick are scattered throughout BLAs, but again, euasterid seed coats are rather different, usually being only one or two cells across (Convolvulaceae are a notable exception). Haig and Westoby (1991) discuss situations in which small seeds may be at an advantage. However, plants in these four orders have rather larger seeds, and since the fruits of most are drupes, the seed coat is not well developed.
REWORK: 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 euasterids 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).
Genes & Genomes. For a possible duplication of the PI gene here or in the lamiids, 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 lamiids almost alone in the pentapetalae (see also discussion under Trochodendrales and Dilleniales), as well as in Ericales (Oxelman et al. 2004b).
Chemistry, Morphology, etc. In the following discussion, I = Icacinaceae, M = Metteniusaceae, C = Cardipteridaceae, and González and Rudall (2010) thought that the gynoecium in Metteniusa (M) was five-carpellate, and an ovule developed in each of the two ?abaxial carpels - these were smaller than the adaxial carpel. Since there are no septae, this is a form of parietal placentation, and given the findings of Endress and Rapini (2014), this gynoecial morphology should be confirmed. There are two ovules in the gynoecia of most of the old Icacinaceae, but their relationship to individual carpels is largely unknown. However, Emmotum (M) has three fertile carpels, each with 1-2 ovules, and these seem to be the three abaxial carpels of a basically 5-carpellate flower (see especially Endress & Rapini 2014). Scattered throughout the old Icacinaceae are taxa with styles that are not terminal (Casimirella - I; this can have three styles), or the styles are asymmetric (Cardiopteris - C), or the single style has two bumps at the base (Raphiostylis - M; Citronella - C; Mappia - I). Poraqueiba (M) initially has three locules, but two are obliterated, Apodytes (M) appears to have two connate styles, while Sleumer (1971) described the style of Nothapodytes (I) as being dimorphic. Fagerlind (1945) and Mauritzon (1936c) describe those Icacinaceae s.l. that they examined (S, C) as having a single carpel fertile, i.e. with two ovules/carpel. Finally, Apodytes (M) and a group of genera including Medusanthera (S) have a very asymmetric ovary (see below).
Ovule morphology is practically unknown, confirmed by the recent unexpected finding that the ovules of Emmotum (M) are bitegmic; ovules of Metteniusa (M) are unitegmic (González & Rudall 2010), the common condition (see Endress & Rapini 2014), Cassinopsis and Phytocrene (both I) are apically bitegmic, while the ategmic nature of the ovules of Cardiopteris (C: Kong et al. 2002, 2014; Kong & Schori 2014) may be the least of their oddities. Ovules may have parietal tissue or lack it, i.e. be crassinucellate or tenuinucellate, and there was considerable discussion as to whether having a thin nucellus meant that the ovules could be considered effectively tenuinucellate (e.g. Mauritzon 1936c; Fagerlind 1945a).
Fruits in general are single-seeded and drupaceous, although details of their morphology, sometimes rather complex, are poorly known. The fruits of Emmotum are sometimes 3-seeded (Sleumer 1942). Although Oncotheca has five fertile carpels, each with two ovules, seed set is poor, there being usually only one, sometimes two or three, seeds per fruit (Dickison 1986). The fruits are often somewhat flattened and/or with a prominent vertical meridional ridge; they may be very asymmetric, as in Apodytes (M: a sterile carpel? - Potgeiter & van Wyk 1994), or in Medusandra and relatives (S), but other taxa also have more or less surved fruits and the loculus of the seed sometimes has a large longitudinal inpushing. The testa is ruminate, especially in Pyrenacantha (I) and relatives.
Comparative phytochemical studies on Aquifoliales, Garryales, Metteniusales and Icacinales are much needed.
Phylogeny. Aquifoliaceae were included in the campanulid clade by Gustafsson et al. (1996) and B. Bremer (1996). However, the I copy of the duplicated RPB2 gene is retained in most of the lamiid clade as well as in Aquifoliaceae (and other Aquifoliales?), and there is a comparable pattern in the loss of introns 18-23 in the d copy. This might suggest that Aquifoliales belong to the lamiids (Oxelman et al. 2004b). Both Garrya and Eucommia have only the d copy, perhaps a feature of Garryales in particular. 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 euasterids (Viaene et al. 2009: no other Aquifoliales examined). In an analysis of nuclear genes, N. Zhang et al. (2012) found an [Aquifoliales + Garryales] clade, and in one analysis using 18S/26S nuclear ribosomal data Maia et al. (2014) recovered a topology [Helwingiaceae [Cardiopteridaceae [Aquifoliaceae [Garryales + other lamiids]]]], but with little support and Icacinaceae, etc., were not included; another analysis was not that different. Qiu et al. (2011) found the relationships [[paraphyletic Icacinaceae plus Garryales [Aquifoliaceae + lamiids]] [other campanulids]]. However, support in both cases was weak.
There are several loose ends to be tidied up. For instance, Sun et al. (2014) found that Ilex and Garrya (the only members of their respective clades examined) switched positions in analyses of mitochondrial genome data, and the two formed a clade sister to the lamiids when nuclear data were examined. Most recent analyses do place Aquifoliales sister to all other campanulids, and that is their position here. The main problem for a long time was the relationships of a group of genera that made up the old Icacinaceae.
Although Garryales were often found to be sister to (most of) the rest of the lamiid clade (e.g. Lens et al. 2008a: maximum parsimony analyses), the composition of any clade that might immediately include them was unclear. Oncothecaceae have been considered close, but neither they nor the other taxa mentioned immediately below linked strongly with them (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 + some ex-Icacinaceae] (taxa assigned to Metteniusaceae below + Cassinopsis) to be sister (72% bootstrap) to other lamiids, while in a Bayesian analysis this clade was joined by Garryales (but with little support for the enlarged clade); the other lamiids formed a clade with 1.0 p.p. support. Relationships remained unclear in a study of the lamiids that focussed on the large lamiid clades (Refulio-Rodriguez & Olmstead 2014), but sampling was skimpy. Nazaire et al. (2014: Suppl. Fig. 4A) found Oncothecaceae, Garryales and Icacinaceae to form a grade at the base of the lamiid clade, but support was weak.
Some of the Icacinaceae had already moved. Thus Irvingbaileya and Gomphandra were placed with strong support in Aquifoliales (D. Soltis et al. 2000), and the group was expanded by Kårehed (2001). There is very strong support for the basic structure [[Cardiopteridaceae + Stemonuraceae] [Ilex, Phyllonoma, Helwingia]] (Kårehed 2001; only 1 sp. of Ilex included; Lens et al. 2008b). Cardiopteridaceae and Stemonuraceae are both very largely populated by ex-icacinaceous genera. The grouping [Cardiopteridaceae + Pentaphylacaceae] had weak support in an earlier single gene analysis (Savolainen et al. 2000b); for the latter family, see Ericales.
Resolving the relationships of the remaining genera that used to be in Icacinaceae is critical. Pyrenacantha, Chlamydocarya, Sarcostigma, Iodes, and Icacina (here all Icacinaceae) form a clade in the rbcL tree of Savolainen et al. (2000b), although placed (but with very little support) at the base of the rosids; these genera belong to Icacinaceae group III of Bailey and Howard (1941). 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, and the Cassinopsis, Emmotum and Apodytes groups (here all Metteniusaceae: see also B. Bremer et al. 2002: 4 genera included). The Bayesian analysis of Soltis et al. (2007) recovered Icacina as sister to all other lamiid 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 lamiids) 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 lamiid backbone at a node above.
In morphological phylogenetic analyses Metteniusa fits quite comfortably into Cardiopteridaceae, ex Icacinaceae (Kårehed 2001), in Aquifoliales here. However, molecular analyses suggest a position in the lamiids. Petiole anatomy, carpel number, etc., are similar to Oncothecaceae (Icacinales here) in particular (González & Rudall 2007, esp. 2010; González et al. 2007), and recent molecular work suggests relationships with another clade of ex-Icacinaceae, within which it is well embedded, Metteniusaceae s.l. (Stull et al. 2014).
Angulo et al. (2013) recovered a well supported Icacinaceae s. str., but relationships between the seven genera of ex-Icacinaceae in the study (Metteniusa was not included) and the position of Garryaceae varied in the analyses of ndhF and ndhF plus morphological data. Byng et al. (2014) found four clades, Icacinaceae s. str. and the Apodytes, Emmotum and Calatola groups, Cassinopsis was by itself, and relationships between all five were unclear. There was some Bayesian support for the grouping [Cassinopsis + Icacinaceae s. str.], and there was weak support for a clade [Oncotheca + the Apodytes group].
However, in an analysis of chloroplast genomes with very good generic-level sampling, Stull et al. (2014) found two major clades. One was made up of the well supported Apodytes, Emmotum and Calatola groups (= Metteniusales); Metteniusa was well embedded in the second group and perhaps sister to Ottoschulzia. The other clade had the structure [Oncotheca [Cassinopsis + Icacinaceae s. str.]] (= Icacinales). The topology at the base of the lamiids is [Icacinales [Metteniusales [Garryales + other lamiids]]], however, support for the position of Metteniusales became strong only when.....
Classification. Of the two major clades recovered by Stull et al. (2015), the first, recognized here as Metteniusaceae, is placed in Metteniusales. In Icacinales, Oncothecaceae are rather different from the rest, Icacinaceae s. str.; they are treated below.
ASTERID I / LAMIIDAE Back to Main Tree
Loss of introns 18-23 in d copy of RPB2 gene.
Age. Bell et al. (2010) estimate a crown-group age for this clade of (109-)99, 91(-80) m.y., Bremer et al. (2004) an age of ca 114 m.y. ago, and Magallón and Castillo (2009) an age of ca 96.85 m.y. for the crown-group age of this clade while Lemaire et al. (2011b) date it to ca 102 m.y. ago.Check and integrate - Wikström et al. (2001) estimated an age of (112-)107, 100(-95) m.y. for the crown group, 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.
ICACINALES van Tieghem Main Tree.
Woody; endosperm copious, embryo long. 2 families, 24 genera, 162 species.
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 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 (see above).
Includes: Icacinaceae, Oncothecaceae
Synonymy: Oncothecales Doweld - Icacinanae Doweld
ONCOTHECACEAE Airy Shaw Back to Icacinales
Evergreen trees; chemistry?; cork cambium outer cortical; nodes 5:5; petiole bundles arcuate, complex; astrosclereids +; stomatal accessory cells divided; plant glabrous; lamina vernation "convolute", margin with caducous glands, petiole short; inflorescences axillary, cymose, branched; K ± free, quincuncial, C quincuncial, basally connate, lacking median adaxial ridge and incurved apex; A adnate to C, extrorse, anthers bisporangiate, dithecal, ± sessile; pollen 3-colporate, smooth; nectary?; G , opposite C, styles ± separate, conduplicate, stigma punctate; ovules (1), campylotropous, integument 4-7 cells across, "crassinucellate", funicle long; fruit not flattened, stone 1-3-seeded; 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; the latter is more likely. Oncotheca macrocarpa, fairly recently described (McPherson et al. 1981, = O. humboldtiana), has stamens quite unlike those of O. balansae; the incurved, pointed connectives of stamens of the latter species are responsible for the generic name. The ventral carpellary bundles of O. macrocarpa are distinct and opposite the loculi, those of O. humboldtiana and fused, separating only towards the top of the ovary and then they are in the septal radii (Dickison 1986c).
Additional information is taken from Baas (1975) and Dickison (1982), both anatomy, Lobreau-Callen (1977: pollen), and Carpenter (1975: general).
Oncothecaceae are embryologically unknown.
Previous relationships. The family was included in Theales by Cronquist (1981) and Takhtajan (1997), although relationships with Aquifoliaceae had been suggested (see Carpenter & Dickison 1976 for literature).
ICACINACEAE Miers, nom. cons. Back to Icacinales
Evergreen trees; tangential vessel element multiples ±+; (vasicentric axial parenchyma +); stomata cyclocytic (anomocytic); leaves spiral (opposite), conduplicate(-plicate), lamina (margins toothed); pedicel articulated; nectary 0/+; 1 carpel fertile; ovules 2/carpel; fruit ± compressed or not; seed coat?, no testal bundles.
23[list]/160: 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 this clade.
Verbascosides +; vessel elements 1,139-2,200(-2,900) µm long, fibres 1,700-3,120(-3,800) µm long; plant glabrous; (axillary thorns +); leaves opposite; C imbricate, lacking median adaxial ridge and incurved apex; A basally epipetalous; nectary 0; (2 carpels fertile), style excentric; ovule (1/carpel), ovule partly bitegmic; embryo short.
1/6-11: Africa and Madagascar.
The Rest: vessel elements with simple perforation plates, 175-860(-1,200) µm long, fibres 650-1,630(-2,300) µm long; nodes 1:1.
2. [Nothapodytes + Mappia]: C free to at most basally connate; A free; style +, stigma capitate to punctate.
3. The Rest.
Also lianes climbing by non-axillary branch tendrils or twining, (plants with massively swollen stem bases); (plants Al-accumulators); monoterpene indole alkaloid camptothecin +, iridoids ?; secondary thickening often atypical [included phloem +, etc.]; banded and/or vasicentric axial parenchyma; (crystal sand in wood rays); (medullary bundles + - Iodes); petiole bundles arcuate and with wing bundles, or annular (and with medullary bundles); hairs unicellular, often adpressed and ± T-shaped, also globular; leaves spiral (opposite), conduplicate(-plicate), lamina (palmately lobed), (secondary veins palmate); (plant dioecious); inflorescence cymose, or spicate or racemose, branches cymose or not; (bracts 0); K ± connate (± free - Phytocrene), valvate, (0 – staminate flowers Pyrenacantha), (C connate); A (epipetalous); pollen usu. porate, echinate; style +, stigma punctate to broad (lobed, with processes), or style 0, stigma capitate, (styles 2-3 - Casimirella); ovule (1/carpel), (apically bitegmic Phytocrene), integument 7-10 cells across, vascularized/not, parietal tissue 0, funicular obturator +; (endocarp pitted - Phytocreneae), (C accrescent, surrounding fruit - Pyrenacantha); seed ruminate [esp. Phytocreneae] or not; endosperm (± 0 - Sarcostigma), (starchy ["seed starchy": Merrilliodendron]), chalazal endosperm haustorium + [Nothapodytes], (embryo short); n = 10, 12; seedling with hypocotyl, phanerocotylar.
Evolution. Divergence & Distribution. Icacinaceae were widespread and diverse in the Northern Hemisphere during the Palaeocene/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 protective indole alkaloid camptothecin, found in a number of genera, see Lorence and Nessler (2004). The enzyme that camptothecin targets occurs in Icacinaceae, too, but it is probably protected by a change in its amino acid sequence (Sirikantaramas et al. 2009).
Bacterial/Fungal Associations. 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).
Chemistry, Morphology, etc. Hoseia, with its long-petiolate leaves that have palmate venation and long-dentate margins, is particularly distinctive vegetatively.
Phytocreneae (Stachyanthus, Miquelia, Phytocrene 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 the fruit morphology of Cassinopsis, see Potgeiter et al. (1994b).
For additional information, see Sleumer (1942a, 1971a), Howard (1942a, b), Kårehed (2001, 2002b) and Utteridge et al. (2005), all general, also Cremers (1973, 1974: growth patterns), Kaplan et al. (1991: chemistry), Lens et al. (2008a: measurements = range of means and upper end of variation, immature specimens excluded) and Bailey and Howard (1941a-d) all vascular anatomy, Heintzelmann and Howard (1948: crystals and indumentum), van Staveren and Baas (1973: epidermis), Baas (1973: epidermis, 1974: stomata), Teo and Haron (1999: anatomy), Mauritzon (1936c) and Fagerlind (1945a), embryology, Lobreau-Callen (1972, 1973, 1977, 1980: pollen), and Potgeiter and van Wyk (1994a), Rankin et al. (2008) and Pigg et al. (2008a), fruit anatomy, the latter two especially of fossils.
The family is very poorly known embryologically (see Mauritzon in Sleumer 1942 for Pyrenacantha in particular).
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. There were similar relationships in Angulo et al. (2013: one gene, moderate to good support): [[Nothapodytes + Mappia] [[Iodes, Pyrenacantha, etc.] [Icacina, Leretia etc.]]]. Trees with this basic topology were also recovered by Stull et al. (2014); the position of Cassinipsis as sister to all other Icacinaceae, that of the [Nothapodytes + Mappia] clade as sister to the rest, and many other internal phylogenetic details all have strong support.
Classification. For some generic limits, see Byng et al. (2014).
Previous Relationships. Other genera that used to be included in Icacinaceae are placed in the campanulids, i.e. in Aquifoliales (as Cardiopteridaceae and Stemonuraceae) and Apiales (as Pennantiaceae, but position there still a bit suspect); see also Metteniusales.
Synonymy: Iodaceae van Tieghem, Phytocrenaceae R. Brown, Pleurisanthaceae van Tieghem, Sarcostigmataceae van Tieghem