EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, initially ±globular; showing gravitropism; acquisition of phenylalanine lysase [PAL], phenylpropanoid metabolism [lignans +, flavonoids + (absorbtion of UV radiation)], xyloglucans in primary cell wall with distinctive side chains; plant poikilohydrous [protoplasm dessication tolerant], ectohydrous [free water outside plant physiologically important]; thalloid, leafy, with single-celled apical meristem, tissues little differentiated, rhizoids +, unicellular; chloroplasts several per cell, pyrenoids 0; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles/centrosomes in vegetative cells 0, microtubules with γ-tubulin along its length [?here], interphase microtubules form hoop-like system; metaphase spindle anastral, predictive preprophase band of microtubules [where cell plate will join parental cell wall], phragmoplast + [cell wall deposition spreading from around the spindle fibres], plasmodesmata +; antheridia and archegonia jacketed, surficial; blepharoplast +, centrioles develop de novo, bicentriole pair coaxial, separate at midpoint, centrioles rotate, associated with basal bodies of cilia, multilayered structure + [4 layers: L1, L4, tubules; L2, L3, short vertical lamellae] (0), spline + [tubules from L1 encircling spermatid], basal body 200-250 nm long, associated with amorphous electron-dense material, microtubules in basal end lacking symmetry, stellate array of filaments in transition zone extended, axonemal cap 0 [microtubules disorganized at apex of cilium]; male gametes [spermatozoids] with a left-handed coil, cilia 2, lateral; oogamy; sporophyte multicellular, cuticle +, plane of first cell division transverse [with respect to long axis of archegonium/embryo sac], sporangium and upper part of seta developing from epibasal cell [towards the archegonial neck, exoscopic], with at least transient apical cell [?level], initially surrounded by and dependent on gametophyte, placental transfer cells +, in both sporophyte and gametophyte, wall ingrowths develop early; suspensor/foot +, cells at foot tip somewhat haustorial; sporangium +, single, terminal, dehiscence longitudinal; meiosis sporic, monoplastidic, MTOC [MTOC = microtubule organizing centre] associated with plastid, sporocytes 4-lobed, cytokinesis simultaneous, preceding nuclear division, quadripolar microtubule system +; wall development both centripetal and centrifugal, sporopollenin + laid down in association with trilamellar layers [white-line centred lamellae; tripartite lamellae], >1000 spores/sporangium; nuclear genome size <1.4 pg, main telomere sequence motif TTTAGGG, LEAFY and KNOX1 and KNOX2 genes present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes, precursor for starch synthesis in plastid.
Many of the bolded characters in the characterization above are apomorphies of subsets of streptophytes along the lineage leading to the embryophytes, not apomorphies of crown-group embryophytes per se.
All groups below are crown groups, nearly all are extant. Characters mentioned are those of the immediate common ancestor of the group,  contains explanatory material, () features common in clade, exact status unclear.
Abscisic acid, L- and D-methionine distinguished metabolically; sporophyte with polar transport of auxins, class 1 KNOX genes expressed in sporangium alone; sporangium wall 4≤ cells across [≡ eusporangium], tapetum +, secreting sporopollenin, which obscures outer white-line centred lamellae, columella +, developing from endothecial cells; stomata +, on sporangium, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and of rhizoids/root hairs; spores trilete; shoot meristem patterning gene families expressed; MIKC, MI*K*C* genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns, mitochondrial trnS(gcu) and trnN(guu) genes 0.
[Anthocerophyta + Polysporangiophyta]: xyloglucans in the primary cell wall with fucosylated subunits; gametophyte leafless; archegonia embedded/sunken [on;y neck protruding]; sporophyte long-lived, chlorophyllous; cell walls with xylans.
Sporophyte dominant, branched, branching apical, dichotomous, potentially indeterminate; vascular tissue +; stomata on stem; sporangia several, each opening independently; spore walls not multilamellate [?here].
EXTANT TRACHEOPHYTA / VASCULAR PLANTS
Sporophyte with photosynthetic red light response; (condensed or nonhydrolyzable tannins/proanthocyanidins +); plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; plant endohydrous [physiologically important free water inside plant]; (condensed or nonhydrolyzable tannins/proanthocyanidins +); xylans in secondary walls of vascular and mechanical tissue; lignins +; stem apex multicellular, with cytohistochemical zonation, plasmodesmata formation based on cell lineage; tracheids +, in both protoxylem and metaxylem, G- and S-types; sieve cells + [nucleus degenerating]; endodermis +; leaves/sporophylls spirally arranged, blades with mean venation density ca 1.8 mm/mm2 [to 5 mm/mm2], all epidermal cells with chloroplasts; sporangia adaxial, columella 0; tapetum glandular; ?position of transfer cells; MTOCs not associated with plastids, basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; suspensor +, shoot apex developing away from micropyle/archegonial neck [from hypobasal cell, endoscopic], root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Sporophyte endomycorrhizal [with Glomeromycota]; growth ± monopodial, branching spiral; root cap +, protoxylem exarch, lateral roots +, endogenous; G-type tracheids +, with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangium dehiscence by a single longitudinal slit; cells polyplastidic, MTOCs diffuse, perinuclear, migratory; blepharoplasts +, paired, with electron-dense material, centrioles on periphery, male gametes multiciliate; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; LITTLE ZIPPER proteins.
Sporophyte woody; stem branching lateral, meristems axillary; lateral root origin from the pericycle; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].
Plants heterosporous; megasporangium surrounded by cupule [i.e. = unitegmic ovule, cupule = integument]; pollen lands on ovule; megaspore germination endosporic [female gametophyte initially retained on the plant].
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 particularly with guaiacyl and p-hydroxyphenyl [G + H] units [sinapyl units uncommon, no Maüle reaction]; root stele with xylem and phloem originating on alternate radii, cork cambium deep seated; stem apical meristem complex [with quiescent centre, etc.], plasmodesma density in SAM 1.6-6.2[mean]/μm2 [interface-specific plasmodesmatal network]; eustele +, protoxylem endarch, endodermis 0; 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 +; cork cambium superficial; leaf nodes 1:1, a single trace leaving the vascular sympodium; leaf vascular bundles amphicribral; guard cells the only epidermal cells with chloroplasts, stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; axillary buds +, exogenous; prophylls two, lateral; leaves with petiole and lamina, development basipetal, lamina simple; sporangia borne on sporophylls; spores not dormant; microsporophylls aggregated in indeterminate cones/strobili; grains monosulcate, aperture in ana- position [distal], primexine + [involved in exine pattern formation with deposition of sporopollenin from tapetum there], exine and intine homogeneous, exine alveolar/honeycomb; ovules with parietal tissue [= crassinucellate], megaspore tetrad linear, functional megaspore single, chalazal, sporopollenin 0; gametophyte ± wholly dependent on sporophyte, development initially endosporic [apical cell 0, rhizoids 0, etc.]; male gametophyte with tube developing from distal end of grain, male gametes two, developing after pollination, with cell walls; female gametophyte initially syncytial, walls then surrounding individual nuclei; embryo cellular ab initio, suspensor short-minute, embryonic axis straight [shoot and root at opposite ends; plant allorhizic], cotyledons 2; embryo ± dormant; ycf2 gene in inverted repeat, mitochondrial trans- nad2i542g2 and coxIIi3 introns present; whole nuclear genome duplication [ζ - zeta - duplication], two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], 5.8S and 5S rDNA in separate clusters.
ANGIOSPERMAE / MAGNOLIOPHYTA
Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANA grade?], lignin also with syringyl units common [G + S lignin, positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], hemicelluloses as xyloglucans; root apical meristem intermediate-open; stele di- to pentarch [oligarch], pith relatively inconspicuous, 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, hypodermis suberised and with Casparian strip [= exodermis]; shoot apex with tunica-corpus construction, tunica 2-layered; 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, not occluding pores of plate, companion cell and sieve tube from same mother cell; sugar transport in phloem passive; nodes 1:?; dark reversal Pfr → Pr; protoplasm dessication tolerant [plant poikilohydric]; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance with increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, secondary veins pinnate, fine venation hierarchical-reticulate, (1.7-)4.1(-5.7) mm/mm2, vein endings free; flowers perfect, pedicellate, ± haplomorphic, protogynous; parts free, numbers variable, development centripetal; P +, ?insertion, 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], each theca dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, endothecium +, cells elongated at right angles to long axis of anther; tapetal cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine lamellate only in the apertural regions, thin, compact, intine in apertural areas thick, pollenkitt +; nectary 0; carpels present, superior, free, several, ascidiate [postgenital occlusion by secretion], stylulus at most short [shorter than ovary], hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry, extragynoecial compitum +; 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, nucellar cap?; megasporocyte single, hypodermal, functional megaspore lacking cuticle; female gametophyte lacking chlorophyll, not photosynthesising, 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 grains land on stigma, bicellular at dispersal, mature male gametophyte tricellular, germinating in less than 3 hours, pollen tube elongated, unbranched, 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, ciliae 0, siphonogamy; double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; mature seed much larger than fertilized ovule, small , dry [no sarcotesta], exotestal; endosperm +, cellular, development heteropolar [first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous, embryo short [<¼ length of seed]; plastid and mitochondrial transmission maternal; Arabidopsis-type telomeres [(TTTAGGG)n]; nuclear genome very small [1C = <1.4 pg, 1 pg = 109 base pairs], whole nuclear genome duplication [ε/epsilon event]; 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, palaeo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]]; chloroplast chlB, -L, -N, trnP-GGG genes 0.
[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 + [reaction wood: with gelatinous fibres, g-fibres, on adaxial side of branch/stem junction]; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; 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 [?here]; pollen tube growth intra-gynoecial [extragynoecial compitum 0]; carpels plicate [?here]; 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.]; (vessel elements with simple perforation plates in primary xylem); nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; protandry common; K/outer P members with three traces, ("C" +, with a single trace); A ?, 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 position]; micropyle?; γ 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; (monosymmetric flowers with adaxial/dorsal CYC expression).
[SANTALALES [BERBERIDOPSIDALES [CARYOPHYLLALES + ASTERIDS]]] / ASTERIDS ET AL. / SUPERASTERIDS : ?
[BERBERIDOPSIDALES [CARYOPHYLLALES + ASTERIDS]]: ?
[CARYOPHYLLALES + ASTERIDS]: seed exotestal; embryo long.
ASTERIDS / 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: ellagic acid 0, non-hydrolysable tannins not common; sugar transport in phloem active; inflorescence basically cymose; A = and opposite sepals or P, (numerous, usu. associated with increased numbers of C or G); style short[?]; duplication of the PI gene.
ASTERID II / CAMPANULIDAE Back to Main Tree
Myricetin 0; vessel elements with scalariform perforation plates; style shorter than the ovary; endosperm copious, embryo short/very short. 7 orders, 29 families, 34,230 species.
Age. Wikström et al. (2001) suggested a crown-group age of (112-)107, 99(-94) m.y. for this clade, Bremer et al. (2004) an age of about 121 m.y., Wikström et al. (2015) an age of (119-)112(-104) m.y., Magallón and Castillo (2009) an age of ca 99.5 m.y., Janssens et al. (2009) an age of 113±9.8 m.y., Moore et al. (2010: 95% HPD) suggested ages of (81-)75(-71) m.y., Bell et al. (2010) ages of (109-)102, 100(-85) m.y. (about the same in Magallón et al. 2015), while Beaulieu et al. (2013a: 95% HPD) estimated ages of (115-)104(-95) m.y.; around 120-101.8 m.y. are estimates in Nylinder et al. (2012: suppl.), 92.7 m.y. is an estimate in Naumann et al. (2013), ca 91.8 m.y. in Tank et al. (2015: Table S1) and around 127.6 m.y. in Nicolas and Plunkett (2014). Rather as in this last estimate, the age is around 124 m.y. in Z. Wu et al. (2014).
The oldest fossils of this clade are ca 83.5 m.y., from the Late Santonian-Early Campanian, and have been assigned to Paracryphiales (q.v., although their identity is suspect (see also Cornales). Fossils assigned to Aquifoliaceae are about the same age (Loizeau et al. 2005; Martinez-Millán 2010; Friis & Pedersen 2012, c.f. Beaulieu et al. 2013a).
Evolution. Divergence & Distribution. Diversification at this node may have occurred in the southern hemisphere (Beaulieu et al. 2013a). For the evolution of plant habit in the campanulids, see Beaulieu et al. (2013b). Aquifoliales (and the three basal lamiid clades), Bruniales, Escalloniales, and Paracryphiales are all (largely) woody and species poor, as are basal Apiales and woody clades in Asterales.
Pollination Biology & Seed Dispersal. In the campanulids the fruits often have few (often 1-2) seeds - but c.f. families like Campanulaceae and Goodeniaceae. Even when each flower has only one or two seeds, these are generally small, indeed, euasterids as a whole have rather small seeds (Linkies et al. 2010). Beaulieu and Donoghue (2013) examined fruit evolution in campanulids from an ecological point of view and concluded that the plesiomorphic fruit type for the whole group was likely to be dry, dehiscent, and with two or more seeds, although it is more likely that the plesiomorphic fruit morphology was quite large, fleshy, indehiscent and single-seeded (see the euasterids. Achenes, dry, indehiscent, and single seeded fruits (they include Apiaceae, although such fruits there are the individual mericarps that result from the separation/dehiscence of the two-seeded fruits) and were often associated with increased diversification rates. However, they were unclear as to any causal connections. These results may have to be modified somewhat when outgroups are included (e.g., what are the likely states for the euasterids as a whole?) and if fruit types are redefined.
Plant-Animal Interactions. Clades of the dipteran agromyzid leaf miner Phytomyza diversified considerably in the campanulids; they moved there from Ranunculaceae (Winkler et al. 2009: >700 species in the genus).
Phylogeny. For discussion about the position of Aquifoliaceae and the circumscription of Aquifoliales and the other woody lineages at the base of the lamiid clade, see the euasterids.
There is moderate (Olmstead et al. 2000; Soltis et al. 2000) to strong (B. Bremer et al. 2002; Janssens et al. 2009) support for Aquifoliales as sister to the rest of the campanulids. The position of Dipsacales within this large clade in early phylogenetic analyses was unclear. Downie and Palmer (1992) associated Adoxaceae with Asterales, while they were sister to Apiales in some studies (Backlund & Bremer 1997). The clade [Asterales [Apiales + Dipsacales]] (e.g. Nandi et al. 1998; Olmstead et al. 2000; Lundberg 2001c; Lens et al. 2008a; see also B. Bremer et al. 2002; Winkworth et al. 2008a; Beaulieu et al. 2013b) is generally supported. On the other hand, Janssens et al. (2009: two genes) found weak support for the clade [Dipsacales [Asterales + Apiales]], Qiu et al. (2010) for [Apiales [Dipsacales + Asterales]], Magallón et al. (2015) recovered a topology [[Escalloniales + Asterales] [Bruniales...]], while Soltis et al. (2011) in their 17-gene study found little support for any relationships other than strong support for Aquifoliales as sister to the rest of the clade. Relationships towards the base of asterids are also different from those shown here - there is a clade [Escalloniales ["Bruniales" + Asterales]] - in Wikström et al. (2015: Bruniales are not monophyletic).
Various small families have been placed around Escalloniaceae in the campanulids, but initially with uncertain support; recent work is clarifying their relationships (Winkworth et al. 2008a; especially Tank & Donoghue 2010; Beaulieu et al. 2013b; Wikström et al. 2015). For Polyosmaceae and Escalloniaceae, see Escalloniaceae.
Paracryphiaceae form a clade sister to Dipsacales, Paracryphia was linked quite strongly with Rutaceae + Meliaceae + Simaroubaceae by Källersjö et al. (1998), but c.f. Savolainen et al. (2000a). In a 17-gene analysis by Soltis et al. (2011), Quintinia linked with Polyosma (Escalloniales here), but support for this position came from the mitochondrial component of the analysis; Soltis et al. (2011) were inclined to think that horizontal gene transfer of the mitochondrial genes might be involved. Paracryphiaceae form a clade in Lundberg's three-gene Bayesian analysis (Lundberg 2001e); Cameron (2001, 2003) also suggested an association between Paracryphia and Sphenostemon. The clade [Paracryphia + Quintinia] was sister to Dipsacales, although not in analyses that included coding chloroplast genes (Winkworth et al. 2008a); see also especially Tank and Donoghue (2010), but support for the position adopted here was only slight in the full analysis of Soltis et al. (2011).
In pre April 2008 versions of this site [Columelliaceae + Desfontainiaceae] (= Columelliaceae s.l.) were placed sister to Dipsacales; the position of Columelliaceae s.l. in that area had been suggested by Bremer et al. (2001) and especially by Lundberg (2001e; see also Backlund 1996), although support was at best moderate. Indeed, both Columelliaceae s.l. and Dipsacales have opposite leaves, and Columellia has amoeboid tapetum (c.f. Bremer et al. 2001) like Dipsacales although Desfontainia does not (Maldonado de Magnano 1986a). The similarities that the pair has with Dipsacales may indicate either substantial homoplasy or (less likely) a suite of rather basal synapomorphies in the campanulids of which there is currently no indication. Other relationships have been suggested (Gustafsson et al. 1996; Backlund & Bremer 1997; Pyck & Smets 2000; Bell et al. 2001); for the possible association of Bruniaceae with Asterales, see Lundberg (2001e). Here Columelliaceae s.l. together with Bruniaceae make up Bruniales.
The overall topology [Bruniales [Apiales [Paracryphiales + Dipsacales]]] seem to be fairly well established (Winkworth et al. 2008a; Tank & Donoghue 2010; Beaulieu et al. 2013a); however, the position of Escalloniales is sometimes rather poorly supported.
AQUIFOLIALES Senft Main Tree.
Shrubs or trees; iridoids?; petiole bundles arcuate; inflorescence axillary; nectary +. - 5 families, 21 genera, 536 species.
Age. K. Bremer et al. (2004) suggested an age of about 113 m.y.a. for this node, Wikström et al. (2015) an age of (112-)100(-84) m.y., Magallón et al. (2015) an age of about 92 m.y., Bell et al. (2010) ages of (101-)88, 87(-85) m.y.a.; ca 95.8 and 74.4 m.y. are ages in Nylinder et al. (2012: suppl.), ca 52.3 m.y. is the age in Nicolas and Plunkett (2014; ?sampling).
Note: Boldface denotes possible apomorphies, (....) denotes a feature common in the clade, exact status uncertain, [....] includes explanatory material. Note that the particular node to which many characters, particularly the more cryptic ones, should be assigned is unclear. This is partly because homoplasy is very common, 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 are the not-so-trivial issues of how character states are delimited and ancestral states are reconstructed (see above).
Evolution. Divergence & Distribution. In their study of the evolution of plant habit in the campanulids, Beaulieu et al. (2013b) noted that growth form was notably constrained in Aquifoliales; all members of which are woody; the woody habit is a feature of the whole euasterid clade.
Chemistry, Morphology, etc. For a summary of pollen variation, see Schori and Furness (2011, esp. 2014); Lobreau (1969) included a number of taxa from this order in her study of taxa possibly associated with Celastrales....
Phylogeny Discussion on the placement of the genera included in the Cardiopteridaceae and Stemonuraceae below can also be found elsewhere; nearly all genera in these two families used to be in Icacinaceae. Of the other families in Aquifoliales, rbcL and other data suggested the relationships [Phyllonoma [Hellwingia + Ilex]] (Morgan & Soltis 1993; see also Soltis & Soltis 1997; Olmstead et al. 2000; Kårehed 2002b; Winkworth et al. 2008; Lens et al. 2008b; Manen et al. 2010; Bell et al. 2010). The absence of evidence that the two taxa with epiphyllous inflorescences formed a monophyletic clade - they also have several other features in common (see below) - seemed a little odd, but a comprehensive analysis of the campanulids (Tank et al. 2007) recovered a sister group relationship between them (1.0 p.p.), as did Soltis et al. (2011: 99% ML bootstrap).
Includes Aquifoliaceae, Cardiopteridaceae, Helwingiaceae, Phyllonomaceae, Stemonuraceae.
Synonymy: Aquifoliineae Shipunov - Cardiopteridales Takhtajan, Helwingiales Takhtajan, Ilicales Martius
[Cardiopteridaceae + Stemonuraceae]: iridoids +; vessel elements also with simple perforation plates; pits usually not bordered; apotracheal parenchyma and variants common; (styloids +); stomata cyclocytic to anisocytic; hairs unicellular (adpressed); leaves two-ranked or spiral, lamina margins entire; (plant dioecious); A basifixed; (pollen grains ± asymmetric); G unilocular, adaxial carpel alone fertile; ovules epitropous, with parietal tissue, integument vascularized, funicular obturator +; (seed ruminate); endosperm nuclear.
Age. Estimated ages for this clade are broadly similar - ca 86.8 m.y. is suggested by Tank et al. (2015: Table S2), (90-)83, 65(-58) m.y. by Wikström et al. (2001), (90-)73, 66(-43) m.y. by (Bell et al. 2010), and about 74.1 m.y. by Magallón et al. (2015).
Evolution. Divergence & Distribution. Kårehed (2001, 2002b) discussed the taxa in their current familial circumscriptions, while Lens et al. (2008a) provided a detailed anatomical survey in a phylogenetic context.
Chemistry, Morphology, etc. The two sides of the gynoecium/fruit are sometimes dramatically different in appearance, as in Medusanthera; this needs to be related to gynoecial development (see also the euasterid node).
For additional information, see Sleumer (1942a, b, 1971a), Howard (1942b), and Utteridge et al. (2005), all general, also Kaplan et al. (1991: chemistry), Lens et al. (2008a: measurements = range of means and upper end of variation, Cardiopteris [immature] excluded) and Bailey and Howard (1941a-d), all vascular anatomy, Heintzelmann and Howard (1948: crystals and indumentum), van Staveren and Baas (1973) and Baas (1973, 1974:), all epidermis and stomata, Teo and Haron (1999: anatomy), Lobreau-Callen (1972, 1973, 1977, 1980: pollen), and Mauritzon (1936c), Fagerlind (1945a) and Padmanabhan (1961: Gomphandra), all embryology.
Classification. These two families have quite a lot in common morphologically, however, Kårehed (2001) recognised them as separate.
Previous Relationships. For the other genera that were until recently included in Icacinaceae s.l., see Icacinaceae themselves and relatives, i.e. Metteniusaceae, in Metteniusales, Icacinaceae, in Icacinales, and Pennantiaceae, in Apiales.
CARDIOPTERIDACEAE Blume, nom. cons. Back to Aquifoliales
(Lianes); plants Al accumulators [?all], secoiridoids +; (vessel elements with scalariform perforation plates only - Citronella), 500-1,390(-1,950) µm long, fibres 2,190-2,970(-3,450) µm long; petiole bundles annular (+ medullary); (articulated laticifers + - Cardiopteris); stomata also anomocytic and paracytic; (lamina margins toothed), (secondary veins palmate); (plant dioecious, andromonoecious); (inflorescence branched, ultimate units clearly cymose or not), (bracts 0); K basally connate, quincuncial, C (imbricate - Cardiopteris); A adnate to C or not, also dorsifixed; (pollen porate), (endoapertures enlarged - not Citronella); (nectary 0); (G , odd carpel adaxial), carpels superposed, (pseudoloculus - Pseudobotrys, Citronella), style usu. slender, (3), about as long as ovary, (± laterally positioned), stigma truncate or capitate, (branched to the base, branches heteromorphic, two stout, subconnate, lobed and grooved, the other slender, with capitate stigma – Cardiopteris); ovule (1), (integument not vascularized), (ategmic - Cardiopteris), parietal tissue ca 2 cells across; fruit endocarp C-shaped in transverse section, (2-winged samara, wings horizontally striate, stout styles accrescent – Cardiopteris); testa thin, ?structure; endosperm (ruminate), (embryo long, with foliaceous cotyledons - Gonocaryum); n = 14 [Leptaulus].
5[list]/43: Citronella (21). Tropics, inc. the Pacific, to Taiwan (map: from Sleumer 1971a, c; Utteridge & Brummitt 2007; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010).
Chemistry, Morphology, etc. Leptaulus has a violet-colored flavonoid; in L. daphnoides the shoot apex aborts.
Tobe (2011b) clarified the gynoecial morphology of Cardiopteris and noted that there was a nectary on the bottom part of the gynoecium. Variation of carpel number in this clade is not well understood; in Cardiopteris the carpel with a functional stigma has no associated ovules, while the two abaxial carpels with non-functional stigmas each has a single ovule (Kong et al. 2014). Kong et al. (2002) described the ovules of Cardiopteris as being ategmic, straight, tenuinucellate and with the egg at the chalazal end of the embryo sac; similarly, Kong et al. (2014; see also Kong & Schori 2014) described the megaspore mother cells as being at the end of the long, straight straight ovule near the chalaza while the zygote was at the other end (their Fig. 7J). This is rather remarkable and needs confirmation; movement of the zygote is known in Santalales, for example, and elongation of the suspensor can do wonders in this regard. The ovary apex (i.e., the apices of the abaxial carpels) develops into a fleshy appendage on the fruit; this and other distinctive features of Cardiopteris (Kong & Schori 2014) are likely to be autapomorphies for the genus.
For additional literature, see above, also Damtoft et al. (1993: iridoids), Lobreau-Callen (1982: pollen, Peripterygium), Baillon (1874: fruit), and Vera-Caletti and Wendt (2001: new genus described).
Phylogeny. Citronella was sister to the three other genera examined (Kårehed 2001); Pseudobotrys is sister to Citronella (Schori, in Schori & Furness 2014); the latter genus (and Cardiopteris) has an imbrictae corolla.
Previous Relationships. The relationships of Cardiopteris, a vine with distinctive morphology, were previously paricularly obscure. It was included in Celastrales by Cronquist (1981) and near there by Takhtajan (1997).
Synonymy: Leptaulaceae van Tieghem, Peripterygiaceae G. King
STEMONURACEAE Kårehed Back to Aquifoliales
Vessel elements with simple perforation plates, in radial multiples, 600-1,510(-2,000) µm long, fibres 2,000-3,650(-4,500) µm long; (crystal sand in wood rays); petiole bundles arcuate + wing or annular + medullary; sclereids +/0; (plant glabrous); (plant dioecious); inflorescence often cymose, flowers 4-5(-7) merous; K ± connate, (C 0, minute); A radiating, (adnate to C), filaments often stout and with club-shaped hairs, and/or connective with appendages, or filaments thin; tapetum multinucleate, (staminodes +/0 - carpellate flowers); pollen (1-)3(-9)-porate, usu. ± prolate, surface microechinate (not - Lasianthera), (columellae enlarged, only around pores); (nectary unilateral), (0); G ?, (pistillode + - staminate flowers); style 0, stigma broad; ovule with integument ca. 10 cells across, parietal tissue 1-2 cells across, (nucellar cap ca 2 cells across); drupe asymmetric [the two sides very different, one with a fleshy "appendage" developing over the sulcus], (symmetric - Stemonurus), (pseudoloculus + – Cantleya), endocarp with ridges and grooves on the side of the appendage, when present; testa thick, outer cells thick-walled, elongate, inner cells not thickened, post-chalazal bundle +; n = 22; seedling with hypocotyl, phanerocotylar. ILLUSTRATION.
12[list]/95: Gomphandra (55), Stemonurus (15). Tropics, esp. Indo-Malesia to Australia (Queensland) (map: from Sleumer 1971a; Utteridge & Brummitt 2007; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010; Schori et al. 2013).
Chemistry, Morphology, etc. The carpellate flowers of Gomphandra are monosymmetric, having a single reflexed staminode (M. Schori, pers. comm.). Schori et al. (2009) discuss fruit variation in the family; for additional literature, see above.
Phylogeny. Lasianthera is sister to the other Stemonuraceae, but only five genera were sampled (Kårehed 2001).
Thanks. I am grateful to Melanie Schori for comments.
[Aquifoliaceae [Phyllonomaceae + Helwingiaceae]]: vessel elements with simple perforation plates; nodes 1:1; petiole bundle arcuate; leaves spiral, lamina margins toothed, stipules +, small, cauline; C imbricate, lacking median adaxial ridge and incurved apex; style 0; ovule 1/carpel, integument 9-15 cells across, parietal tissue 0, endothelium +; fruit with separate pyrenes; exotesta and endotesta recognizable, rest crushed.
Age. Janssens et al. (2009) dated this node to 62±11.9 m.y.a., Magallón et al. (2015) to 64.2 m.y., while ca 69 m.y. is the age in Tank et al. (2015: Table S1, S2). Bell et al. (2010: note topology) suggested that this node was (72-)56, 51(-35) m.y.o., and in Wikström et al. (2015) the age is (90-)72(-62) m. years.
The distinctive pollen of Ilex is known from Cretaceous-Turonian deposits ca 80 m.y.o. in S.E. Australia and from deposits 75-65.5 m.y.a., almost as old, in central Australia, and there are perhaps older records, although lacking photographs of the distinctive pollen (Martin 1977; Loizeau et al. 2005; Carpenter et al. 2015; see also Manchester et al. 2015). However, Manen et al. (2010) used a date of ca 69 m.y. for the oldest fossils, Beaulieu et al. (2013a) an age of ca 65 m.y. (a fossil "seed").
Chemistry, Morphology, etc. Stipular morphology would repay study. Structures called stipules in Helwingia (e.g. F.o.C. vol. 14. 2005) appear to be aggregations of colleters; they are not vascularized. In Ilex, structures that can be called colleters terminate the triangular stipules (Gonzalez & Tarragó 2009); nodes are at least sometimes 3:3 in the genus, as is common in stipulate angiosperms.
AQUIFOLIACEAE Berchtold & J. Presl, nom. cons. Back to Aquifoliales
(Plant deciduous), (lianes); tanniniferous, iridoids 0; (vessel elements in multiples); resiniferous, laticiferous idioblasts +; nodes also 3:3, etc.; petiole bundles to annular with wing and medullary bundles; branching from previous flush; (leaves opposite; two-ranked), lamina vernation supervolute (conduplicate), teeth with single vein and opaque, glandular deciduous apex, (margins entire), (stipules 0); plants often dioecious; flowers 4-9-merous; C imbricate, often connate basally; A adnate to base of C (free); pollen surface conspicuously gemmate/clavate; G [(2-)4-6(-many)], opposite petals, gynoecial nectary +, placentation axile basally, becoming free-central, stigma broad, wet; ovules (2/carpel), parietal tissue ca 1 cell across, hypostase +, funicular obturator papillate (0); stigma prominent in fruit, K deciduous (semipersistent); exotestal cells cuboid, tangentially elongated, inner walls lignified, endotesta tanniniferous; endosperm hemicellulosic; n = 9, 10; loss of introns 18-23 in RPB2 d copy, mitochondrial coxII.i3 intron 0.
1[list]/405: Ilex. ± World-wide, esp. America and South East Asia-Malesia, one species in Africa (map: see Meusel et al. 1978; Loiseau et al. 2005). [Photo - Staminate Flower, Carpellate Flower.]
Age. Crown group Ilex, or at least its plastome, may be a mere 15 m.y. old (Miocene), which suggests that there may previously have been much extinction in the clade (Manen et al. 2010); crown and stem ages of 52 and 65 m.y.a. respectively were suggested by Quirk et al. (2012). For the distinctive pollen of Ilex, well known in the fossil record, see above.
Evolution. Divergence & Distribution. There is evidence of extensive hybridization within crown-group Ilex (Manen et al. 2010).
Cuénoud et al. (2000) obtained several clades correlating with geography, and Manen et al. (2010) also found strong geographic structure in the phylogeny (see also Selbach-Schnadelbach et al. 2009 and below). Ilex is one of the genera that has become extinct in New Zealand in the Caenozoic (Lee et al. 2001).
Pollination Biology & Seed Dispersal. The great majority of visits to the 12 species of Ilex observed on Hongkong were from the one species of bee, Apis cerana (Tsang & Corlett 2012).
The fruits are low quality and are eaten by birds (Tsang & Corlett 2012).
Chemistry, Morphology, etc. Palisade glandular tissues with protein-rich secretions are found on the leaf teeth and stipules; consequently, the latter have been called colleters (Gonzalez & Tarragó 2009). Spiral strands may join the two halves of a tranversely-torn leaf blade.
For the gynoecial nectary, see Erbar and Leins (2010); the nectar may seem to come from the petals, but in any event it collects between the stamens in a little pocket formed by the gynoecium and petals. The embryo is often minute and barely developed at the time when the fruit is dispersed, only slowly maturing afterwards (Herr 1961; Tsang & Corlett 2005 for references).
See Copeland (1964) for general information, Baas (1975) for vegetative anatomy, Lobreau-Callen (1977), Martin (1977) for pollen, and van Tieghem (1898) for ovules; Galle (1997) provides an account of the cultivated members of the family.
Phylogeny. The erstwhile genus Nemopanthus is deeply embedded in Ilex (Powell et al. 2000), the two having the same distinctive pollen, etc.. Cuénoud et al. (2000) obtained several clades in their study of Ilex s. str., however, support for some was weak; Ilex canariensis was not associated with any of these clades. Selbach-Schnadelbach et al. (2009) found the relationships [South American group [the rest + I. canariensis]]. The position of I. canariensis was still unclear in Manen et al. (2010), and Hawaiian and New Caledonian species were embedded in an American clade (MCC value of 0.84).
Previous Relationships. Phelline and Sphenostemon have sometimes been included in Aquifoliaceae (e.g. Mabberley 1997), but Phelline is here recognised as Phellinaceae (in Asterales) while Sphenostemon is in Paracryphiaceae (Paracryphiales). Aquifoliaceae were included in a very heterogeneous Celastrales by Cronquist (1981).
Synonymy: Ilicaceae Dumortier
[Phyllonomaceae + Helwingiaceae]: plant glabrous; lamina with second order vains looping and joining towards margin [brochidodromous], stipules fimbriate; inflorescence epiphyllous, on adaxial side of lamina; nectary annular; ovary inferior, stigma/styles & separate, ± elongated, recurved.
Age. The age of this node is estimated at around 66 m.y. (K. Bremer et al. 2004), ca 61.3 m.y. (Tank et al. 2015: Table S2), ca 56.5 m.y. (Magallón et al. 2015) or (82-)59(-32) m.y. (Wikström et al. 2015).
Chemistry, Morphology, etc. More work is needed on both Helwingiaceae and Phyllonomaceae to clarify their anatomy and floral morphology.
PHYLLONOMACEAE Small Back to Aquifoliales
Plants Al accumulators, other chemistry?; stem anatomy?; young stem with separate bundles; petiole bundle annular; plant glabrous, leaves ?two-ranked; inflorescences monochasial cyme, bracteoles 0; flowers perfect, odd sepal abaxial; K 4-5, with one trace, quincuncial, with stout marginal glandular hairs, C 3-5, adaxially weakly ridged; filaments shorter than anthers; tapetal cells binucleate; G collateral(-suboblique), placentation intrusive parietal; ovules 6-7/carpel, endothelium 0, nucellar podium +, developing late; fruit a berry, few-seeded; testa multilayered, exotestal cells large, thick-walled, mucilaginous, forming irregular (multicellular) papillae, Palisade or not, 2-3 layers of flattened cells; endosperm with lipids, embryo small; n = ?
1/4. Mexico to Peru (map: see Mori & Kallunki 1977). [Photo - Leaves, Flowers.]
Chemistry, Morphology, etc. Although the inflorescence of Phyllonoma has been described as being "truly phyllogenous", it appears to represent a displaced axillary shoot, as in Helwingia (Weber 2004c, and references; see also Dickinson and Sattler 1974); it is a monochasial cyme (Tobe 2014), although it has been described as racemose, etc., in the past (including here).
See Thouvenin (1890) and Mori and Kallunki (1977) for general information, Tobe (2013) for floral morphology, Mauritzon (1933) and especially Tobe (2015a) for some embryology, Krach (1976) and Takhtajan (2000) for seed anatomy, Mori and Kallunki (1977) for a revision.
Previous Relationships. Krach (1977) suggested that the seeds of Phyllonoma and those of Grossulariaceae were similar. Phyllonoma was included in Grossulariaceae by Cronquist (1981), and as Phyllonomaceae, in Hydrangeales, by Takhtajan (1997).
Synonymy: Dulongiaceae J. G. Agardh, nom. illeg.
HELWINGIACEAE Decaisne Back to Aquifoliales
(Plant deciduous); flavones, chlorogenic acid, unidentified iridoids +; septate fibres with minutely bordered pits; silica grains +; pericyclic fibres 0; petiole also with two small inverted adaxial bundles; cuticle wax crystalloids 0; lamina vernation supervolute-curved; plant dioecious; inflorescence fasciculate; P +, uniseriate, 3-5, valvate (± imbricate), apex ± incurved; nectary stomatiferous, on top of G; staminate flowers: stamens alternating with P; pollen with diffuse endoapertures; pistillode 0; carpellate flowers: staminodes 0; G [(2-)4], alternating with P, stigma dry; ovule apotropous, parietal tissue 0, suprachalazal tissue very long, narrow; embryo sac with rich cytoplasm; testa multiplicative, to 20 cells across, most collapsed endosperm weakly ruminate; n = 19.
1/3. Himalayas to Japan (map: from Hara 1972). [Photo - Fruit.]
Chemistry, Morphology, etc. The fasciculate inflorescence is clearly cymose (Weber 2004c; pers. obs.). Helwingiaceae have a single perianth whorl, and probably lack a calyx (e.g. Takhtajan 1997); in this interpretation, stamens and corolla alternate, as is almost universal in the euasterids. Eichler (1878) noted that there was a little rim outside the perianth members in carpellate flowers, suggesting that they were indeed petals. If the corolla is absent (Tobe 2013, tentative suggestion; esp. Ao & Tobe 2015), the stamens would be antepetalous, very odd for an euasterid, and the carpels are also antepetalous, a little odd if the stamens are antepetalous. Furthermore, Ao and Tobe (2015) draw the flower of both genera with the odd sepal abaxil, unusual for a broad-leaved angiosperm; nothing is said about either stamen position or floral orientation. The ovule is described as "epitropous dorsal at maturity" (Ao & Tobe 2015: p. 169). The ventral carpel bundles are central.
See also Decaisne (1836), Wangerin (1906) and Hara and Kurosawa (1975), all general, Iwashina et al. (1997: chemistry), Noshiro and Baas (1998: anatomy), Horne (1914: flower), Dickinson and Sattler (1975: inflorescence), and Korobova (1980: embryo and seed).
Previous Relationships. Helwingiales were included in Aralianae by Takhtajan (1997); Helwingia was included in Cornaceae by Cronquist (1981) and Mabberley (1997), in the latter only with hesitation.