EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, not motile, initially ±globular; showing gravitropism; acquisition of phenylalanine lysase [PAL], microbial terpene synthase-like genes +, triterpenoids produced by CYP716 enzymes, phenylpropanoid metabolism [lignans +, flavonoids + (absorbtion of UV radiation)], xyloglucans in primary cell wall, side chains charged; 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 their lengths [?here], interphase microtubules form hoop-like system; metaphase spindle anastral, predictive preprophase band + [with microtubules and F-actin; where new cell wall will form], phragmoplast + [cell wall deposition centrifugal, from around the anaphase spindle], 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, 1000 spores/sporangium, sporopollenin in the spore wall laid down in association with trilamellar layers [white-line centred lamellae; tripartite lamellae]; nuclear genome size [1C] <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 [precursors for starch synthesis], tufA gene moved to nucleus; mitochondrial trnS(gcu) and trnN(guu) genes +.
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; pro- and metaphase spindles acentric; 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]: gametophyte leafless; archegonia embedded/sunken [only neck protruding]; sporophyte long-lived, chlorophyllous; cell walls with xylans.
Sporophyte well developed, branched, branching apical, dichotomous, potentially indeterminate; hydroids +; stomata on stem; sporangia several, terminal; spore walls not multilamellate [?here].
Vascular tissue + [tracheids, walls with bars of secondary thickening]; stomata involved in gas exchange.
EXTANT TRACHEOPHYTA / VASCULAR PLANTS
Sporophyte with photosynthetic red light response, stomata open in response to blue light; plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; plant endohydrous [physiologically important free water inside plant]; sporophyte with polar auxin transport, PIN [auxin efflux facilitator] involved; (condensed or nonhydrolyzable tannins/proanthocyanidins +); xyloglucans with side chains uncharged [?level], in secondary walls of vascular and mechanical tissue; lignins +; stem apex multicellular, with cytohistochemical zonation, plasmodesmata formation based on cell lineage; vascular development acropetal, 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; roots +, endogenous, positively geotropic, root hairs and 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]; mitochondrion with loss of 4 genes, absence of numerous group II introns; 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); microbial terpene synthase-like genes 0; primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignin chains started by monolignol dimerization [resinols common], particularly with guaiacyl and p-hydroxyphenyl [G + H] units [sinapyl units uncommon, no Maüle reaction]; root stele diarch to pentarch, xylem and phloem originating on alternating 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; chloroplast ycf2 gene in inverted repeat, trans splicing of five mitochondrial group II introns, rpl6 gene absent; 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 cap meristem closed (open); pith relatively inconspicuous, lateral roots initiated immediately to the side of [when diarch] or opposite 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; ?phloem loading/sugar transport; 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; suprastylar 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 towards the ovule, 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 [<5 mm long], 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 size [1C] <1.4 pg [mean 1C = 18.1 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]]]]: phloem loading passive, via symplast, plasmodesmata numerous; 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]: mitochondrial rps11 gene lost.
CORE EUDICOTS / GUNNERIDAE Back to Main Tree
(Ellagic and gallic acids +); leaf margins serrate; compitum + [one position]; micropyle?; γ whole nuclear genome duplication [palaeohexaploidy, gamma triplication], x = 21, PI-dB motif +; small deletion in the 18S ribosomal DNA common.
Age. The crown group age of core eudicots is around 115.5 m.y. (Anderson et al. 2005). Other crown group ages are 132-119(-89) m.y. in Soltis et al. (2008: a variety of estimates), 114.4 or 115.1 m.y. in Magallón and Castillo (2009), (113-)110(-105) m.y. (Moore et al. 2010: 95% HPD), (139-)127, 119(-109) or (127-)121, 117(-107) m.y. (Bell et al. 2010), (116-)112(-107) m.y. (N. Zhang et al. 2012) and (118.3-)112.9-111.7(-105.3) m.y. (Magallón et al. 2013: with temporal constraints); Schneider et al. (2004) offer a range of dates up to over 180 m.y., and another high estimate is ca 171 m.y. by Z. Wu et al. (2014). Wikström et al. (2003) suggested a crown group age of (131-)127, 116(-111) m.y., Magallón et al. (2015) an age of around 125.1 m.y.a., ca 118.1 m.y. is the age in Naumann et al. (2013), about 117.5 m.y. in Tank et al. (2015: Table S1), but only (108-)98(-87) m.y. in Murat et al. (2017) and around 130.2-124.4 m.y. in Zeng et al. (2017).
The age of stem core eudicots has been estimated as some 120-116 m.y. (Anderson et al. 2005). Other stem group ages are 121.2 or 121.9 m.y. (relaxed and constrained penalized likelihood: Magallón & Castillo 2009), while Wikström et al. (2003) suggested a stem age about (140-)135, 123(-118) m.y. - c.f. sister groups.
Severin et al. (2011) offered a spread of 240-130 m.y. for the palaeohexploidy event that probably occurred in the immediate ancestor of Pentapetalae (see below for details). Vekemans et al. (2012) narrowed the estimate for the age of this genome triplication at (121.9-)120.4(-118.9) or (122.7-)120.05(-117.4) m.y., depending on the method used, while Jiao et al. (2012) dated duplications associated with this γ event to around 117 m.y.a; 138-11 m.y. is the estimate in Murat et al. (2015b) and ca 130 m.y. that in J. Wang et al. (2017).
Evolution: Divergence & Distribution. Vekemans et al. (2012) emphasized that the γ genome duplication event (see below) occurred ca 7 m.y. before the divergence of Gunnerales and other core eudicots; there was a lag between duplication and subsequent divergence. Indeed, if one tries to understand any link between this event and diversification, the lag may be somewhat greater, since although Gunnerales may be chemically like other core eudicots, they are not particularly similar florally, and in any event they hardly represent a particularly speciose clade (Mayrose et al. 2011; Schranz et al. 2012 for lags between genome duplication/polyploidy and diversification). Tank et al. (2015) put the increase in diversification rate possibly associated with the duplication at the Pentapetalae node.
The floral morphology of Gunnerales is more like that of Buxales, etc., than that of other core eudicots. That is, it is more like taxa on more basal eudicot branches and so it is apparently plesiomorphic (e.g. D. Soltis et al. 2003a; Doust & Stevens 2005; Kubitzki 2006a). Wanntorp and Ronse De Craene (2005) and Ronse De Craene and Wanntorp (2006) also note that the morphology of Gunnerales flowers cannot be directly related to that of the pentamerous core eudicots, the floral morphology of the former being shaped by the exigencies of wind pollination (see also Ronse de Craene & Brockington 2013). Wanntorp and Ronse De Craene (2005) observed that three successive floral whorls may be opposite each other, and this is a feature of some Ranunculales-Berberidaceae, Proteales-Sabiaceae, etc., but not of core eudicots. Indeed, the flowers cannot readily be derived from those of other core eudicots given our current knowledge of floral morphology and development, even if the duplication of a number of genes important in determining the identity of floral parts (AP3, AP1, SEP, AG) may be connected with the γ duplication event (Jiao et al. 2012; see below). For discussion of the "typical" pentapetalous core eudicot flower, see the Dilleniales page.
Chemically Gunnerales are similar to Pentapetalae in that they have ellagic acid (e.g. Soltis et al. 2005b), and general molecular data link them closely with that clade. Some perhaps important gene duplications may have occurred somewhat earlier (see the Trochodendrales page), and it is not known if they have the euAP3 gene, etc.; see
For general information on core eudicot diversification, see Magallón et al. (1999); most of the estimates of percentage diversity of clades are taken from this work. The diversification rates of many of the clades are higher than those in other angiosperms (Magallón & Sanderson 2001).
Pollination Biology & Seed Dispersal. Compitum presence can perhaps be pegged as to this node (?a key innovation?) given that it is found in Gunneraceae, the rosids, and the extended asterid clade, although it is absent in Myrothamnaceae and Dilleniaceae (c.f. Endress 2011).
Genes & Genomes. It is suggested that n = 7 in the ancestor of core eudicots, n = 21 after the genome triplication, and this was followed by substantial rearrangements by the time Vitales diverged from other rosids (Murat et al. 2015b and references, see also 2017; J. Wang et al. 2017). n = 21 is the ancestral core eudicot karyotype, or ARK/AEK.
The importance of the palaeohexaploidy event (the γ triplication), now placed at this node, was first suggested in work on Vitales (Jaillon, Aury et al. 2007). It was thought that there had been gene duplication, possibly because of hybridization, within the Vitis lineage itself, and that this brought the Vitis genome more into line with that of other rosids (Velasco et al. 2007). Nevertheless, Freeling et al. (2008: they included the Carica papaya genome) suggested that most rosids, i.e. the node [Vitales + rosids s. str], were palaeohexaploids, the Atg (γ) event, and two of the three genomes involved had lost notably more ancestral genes than had the other. Evidence from genome colinearity suggested that a palaeohexaploidy event had also occurred in the ancestor of the asterid Coffea (Cenci et al. 2010), and Jiao et al. (2012) placed this event before the split of the asterids and rosids but after the divergence of Ranunculales - see also Tang et al. (2008a, b), Diaz-Riquelme et (al. 2009), Barker et al. (2009), Abrouk et al. (2010), Severin et al. (2011), Dohm et al. (2011) and Zumajo-Cardona et al. (2017) for this genome triplication, whether or not also involving asterids. In any event, evidence of large genome duplications may be lost, as in Fragaria vesca (Rosaceae) (Shulaev et al. 2010).
The most recent work estimates that palaeohexaploidy happened in the immediate ancestor of this node (Jiao et al. 2012; esp. Vekemans et al. 2012). However, Chanderbali et al. (2016b) suggest that only around half the gene duplications associated with this γ event are to be placed here, the other half being earlier, being placed at the [Trochodendrales, Buxales, core eudicot] node. Given earlier genome duplications (all angiosperms, all seed plants), by the time one gets to genera like Brassica, Arabidopsis, and Gossypium in which there have been several more local duplications, the genome must have duplicated many, many times... (e.g. Paterson et al. 2012). However, there seems not to have been a subsequent global diversification at least in the clade including Coffea and Cephalotus (Fukushima et al. 2017).
There are quite a number of gene duplications in the general Dilleniales-Vitales area, perhaps a whole genome duplication is involved (e.g. Litt & Irish 2003; Kramer et al. 2004; Kim et al. 2004; Zahn et al. 2005b; Howarth & Donoghue 2006; especially Kramer & Zimmer 2006; Shan et al. 2007 - see immediately above!). Duplications include: euAP1 + euFUL + AGL79 genes [duplication of AP1/FUL or FUL-like gene], PLE + euAG [duplication of AG-like gene: C class], SEP1 + FBP6 genes [duplication of AGL2/3/4 gene]. The euAP1clade includes key regulators that have been implicated in the specification of perianth identity (Litt & Irish 2003). However, not all major core eudicot groups have been sampled for this gene, the situation in Santalales, for example, being unknown; there has been another duplication of this gene (and also of the AGL1/2/3 gene) perhaps immediately below the Pentapetalae node, but above the Ranunculales node. The roles such genes may play in many eudicot groups is unknown. Duplications of the CYC2 gene clade are widespread, and they are often associated with the evolution of monosymmetric flowers (Howarth et al. 2011 and references).
Chemistry, Morphology, etc. Wanntorp and Ronse De Craene (2005) and Ronse De Craene and Wanntorp (2006) note that the morphology of Gunnerales flowers cannot be directly related to that of the pentamerous core eudicots, the floral morphology of the former being shaped by the exigencies of wind pollination. Wanntorp and Ronse De Craene (2005) also note that three successive floral whorls may be opposite each other, and this is a feature e.g. of some Ranunculales like Berberidaceae, Sabiales, etc., but not of core eudicots. Indeed, the flowers cannot be considered as being readily derived from those of other core eudicots given our current knowledge of floral morphology and development, rather, they seem fundamentally similar to those scattered in other eudicot clades basal to Gunnerales. For discussion of the "typical" core eudicot flower, see the Pentapetalae page.
Whether or not the rps2 and rps11 genes occur in Gunnerales is apparently unknown, but the first is absent in Buxales and Trochodendrales and the second in Buxales alone (Adams et al. 2002b); they are probably lost slightly lower down on the tree (as are benzylisoquinoline alkaloids).
Phylogeny. This clade is strongly supported, e.g. Chase et al. (1993), D. Soltis et al. (1997, 1999, 2003a), Hoot et al. (1998), Nandi et al. (1998), D. Soltis et al. (2003a: four genes), S. Kim et al. (2004), Zhu et al. (2007), Qiu et al. (2010: support weak), and Z. Wu et al. (2014), although indistinguishable from other core eudicots in (e.g.) P. Soltis et al. (1999). However, in some earlier studies the exact position of Gunnerales was unclear (e.g. Chase et al. 1993; Morgan & Soltis 1993), but quite strong support for a position sister to the rest of the core eudicots was provided by Senters et al. (2000: Gunneraceae alone sampled), rather weaker support by Hilu et al. (2001). Zhu et al. (2007) found a weakly supported [Gunnera + Dillenia] clade sister to other core eudicots; see also pentapetalae.
Classification. Gunnerales were excluded from the core eudicots in earlier versions of this site (pre Version 7; c.f. A.P.G. I and II 1999, 2003) because of their apparently largely plesiomorphic floral morphology. However, to ensure consistency between classification systems based on the same topology their limits have been adjusted to conform with those now generally used.
GUNNERALES Reveal Main Tree.
Ellagic acid +; vessel elements?; sieve tube plastids with protein crystalloids and starch; pith with sclerenchymatous diagrams; lamina margins with hydathodal teeth, secondary veins palmate; plants dioecious; inflorescences with terminal flowers; flowers small; P ?0; A latrorse; stigma at most weakly secretory; seed coat? - 2 families, 2 genera, 42-52 species.
Age. Estimates of the age of crown group Gunnerales are (123-)118, 108(-103) m.y. (Wikström et al. 2001), about 104.6 m.y. (Magallón et al. 2015), 90-55 m.y. (Anderson et al. 2005), (132-)102, 95(-64) m.y. (Bell et al. 2010), ca 99.8 m.y. (Tank et al. 2015: Table S2), or ca 77 m.y. (Magallón et al. 2013).
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).
Chemistry, Morphology, etc. This is a rather surprising group. Gunneraceae and Myrothamnaceae look very different; one is an often gigantic mesophytic herb, the other a resurrection shrub of arid habitats. In the former, hydathodes are well developed and mucilage or possibly resinous lacquer is secreted, in the latter, hydathodes are poorly developed (but see Drennan et al. 2009) and the plant secretes resin. They do both have flowers without much of a perianth, although the plesiomorphic condition for the order may be to have some kind of perianth, but details of pollen (e.g. c.f. Zavada & Dilcher 1986; Wanntorp et al. 2004), etc., differ. González and Bello (2009) suggest possible apomorphies for the pair, including the presence of stipules, but see below for a possible interpretation of the stipules of Gunnera.
Classification. There is an option of including Myrothamnaceae in Gunneraceae in A.P.G. II (2003), both being small and monogeneric families, but they are so different in appearance that it seems best to keep them separate (see Wilkinson 2000 for a table of differences).
Includes Gunneraceae, Myrothamnaceae.
Synonymy: Myrothamnales Reveal - Gunnerineae Shipunov - Myrothamnanae Takhtajan
GUNNERACEAE Meisner, nom. cons. Back to Gunnerales
Perennial (annual) herbs, rhizomatous or stoloniferous; close association with the N-fixing Nostoc in stem and root; cork ?; root stele polyarch; vascular cambium 0 [?all taxa]; vessel elements with simple or few-barred scalariform perforation plates [stems] or scalariform, bars to ca 150 [stolons]; axis polystelic [erect stem] or vascular cylinder [stolons]; nodes multilacunar; stem with endodermis, also low glandular areas; petiole anatomy complex; cataphylls common; stolons with opposite scales; leaves spiral, colleters +; inflorescence usu. branched-racemose, (plant polygamous), bracteoles 0; P 2 (3), valvate; staminate flowers: (P 4, 0); A 1-2; pollen semitectate-reticulate; pistillode +; carpellate flowers: staminodes +; G , inferior, transverse and alternate with P, uni(bi)locular, stigmas dry; compitum +; ovules 1(-2)/carpel, apical, pendulous, epitropous, micropyle endostomal, outer integument ca 3 cells across, inner integument ?2/ca 4 cells across; embryo sac tetrasporic, 16-celled [Peperomia-type]; fruit drupaceous (nut); seed coat?; endosperm with some starch; n = 17.
1[list]/40-50. Circum S. Pacific, Africa and Madagascar (map: see van Balgooy 1975; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Wanntorp & Wanntorp 2003; fossil records [green] from the Late Cretaceous, see Jarzen & Dettmann 1989, also Osborne & Sprent 2002). [Photo - Leaf, Inflorescence]
Evolution: Divergence & Distribution. The pollen is distinctive and is known from the Early Cretaceous onwards (Wanntorp et al. 2004b) in all four continents of the Southern Hemisphere, as well as from North America, India and deposits in the Indian (Ninetyeast Ridge) and south Atlantic Oceans (the latter three localities in the Palaeogene - see Jarzen & Dettmann 1989). Wanntorp and Wanntorp (2003) interpreted the distribution of Gunnera in the context of its phylogeny and assuming Gondwanan-age vicariance events (c.f. Beaulieu et al. 2013), so not independent evidence for vicariance.
Bacterial/Fungal Associations. All taxa have an association with the cyanobacterium, Nostoc (Osborne & Sprent 2002 for the ecology of the interrelationship; Santi et al. 2013 for literature). Glands on the stem found immediately below the leaves secrete mucilage, and Nostoc enters the plant here as motile hormogonia. Johansson and Bergman (1994, and references) and in particular Khamar et al. (2010) describe the establishment of this association; there are different sugars in the mucilage that attracts Nostoc and in the gland tissue in which Nostoc grows (Khamar et al. 2010). Nostoc infects as hormogonia, but in the plant it loses its motility and produces many heterocysts; it may not photosynthesise at all there (Bergman 2002). Söderbäck and Bergman (1993) detail the physiology of the two partners; see also Adams et al. (2006).
Chemistry, Morphology, etc. There are stipule-like structures on the stem of many species (but this is not an apomorphy for the family) that are interpreted as being cataphylls by Wanntorp et al. (2003). Since they are at least sometimes opposite they may be prophylls; they range in shape from suboblong and entire to deeply laciniate with linear lobes. The lamina varies from 7 mm to 3 m across, and the teeth have a glandular apex that broadens distally; two higher order veins are also involved. The difference in anatomy between stems and stolons is striking; the roots are triarch to polyarch (Wilkinson 2000). Although Gunnera herteri, sister to the rest of the genus, has normal stem anatomy, it is an annual and its anatomy is conceivably derived. The difference in size, etc., between the inner and outer tepals is such that they are sometimes described as sepals and petals (e.g. Wanntorp & Ronse de Craene 2005; Ronse de Craene & Wanntorp 2006; González & Bello 2009). The rather uncommon perfect flowers then have two median sepals, two lateral petals, two stamens opposite the petals, and two carpels also opposite the petals (Ronse de Craene & Wanntorp 2006; González & Bello 2009), indeed, there is considerable infraspecific variation in floral morphology (González & Bello 2009).
Much information is taken Wilkinson and Wanntorp (2006: general), see also Wilkinson (1998: anatomy), and for floral morphology and development see Rutishauser et al. (2004), Wanntorp and Ronse De Craene (2005) and Ronse De Craene and Wanntorp (2006), for pollen, Wanntorp et al. (2004a), and for ovules, etc., see Schnegg (1902) and Warming (1913).
Phylogeny. For a phylogeny of Gunnera, see Wanntorp et al. (2001, also Wanntorp 2006: summary); the annual G. herteri is sister to the rest of the genus.
Previous Relationships. Gunneraceae have often been associated with Haloragaceae (e.g. cronquist 1981), also with an inferior ovary and reduced flowers, but in the latter the stamens are as many as the sepals, and opposite them, the gynoecium is multilocular, with one ovule/loculus, etc. - see Saxifragales. Gunneraceae were included in Saxifraganae: Rosidae by Takhtajan (1997). Fuller and Hickey (2005), examining details of leaf architecture, etc., suggested that Gunneraceae were best associated with the herbaceous Saxifragaceae, but this is probably because of habit/habitat-associated parallelisms.
MYROTHAMNACEAE Niedenzu, nom. cons. Back to Gunnerales
Aromatic-resinous shrubs, resurrection plants; essential oils +, gallotannins, myricetin, dihydro/chalcones +; cork?; vessel elements with reticulate perforations; pith star-shaped/tetragonal; nodes split-lateral; petiole bundle arcuate; individual epidermal cells resiniferous, midrib bundle lacking fibres, palisade tissue 0; plant glabrous; leaves amphistomatic; leaves opposite, basally forming a sheath, lamina vernation plicate, secondary veins palmate-flabellate, stipules 2, small, persisting on the petiolar sheath; spikes bracteate, with terminal flowers; staminate flowers: A 3-4, or (3-)4(-8) and connate, anthers valvate basally, connective produced; pollen in tetrads, triporate, intectate, with clavate projections themselves papillate; pistillode 0; carpellate flowers: staminodes 0; G 3-4, only basally connate, with 5 vascular bundles and surface oil cells, the odd member abaxial, styluli short, recurved, stigma decurrent, in two crests; compitum 0; ovules many/carpel, micropyle bistomal, parietal tissue ca 3 cells across; embryo sac bisporic [chalazal dyad], eight-celled [Allium-type]; fruit follicular (and septicidal); exotestal cells with somewhat thickened outer walls; endosperm development?; n = 10.
1[list]/2. Africa and Madagascar (map: from Puff 1978b; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photos - Collection]
Evolution. Ecology & Physiology. Myrothamnaceae are resurrection plants. The leaves may appear to dry out completely, but they quickly regain turgor, etc., when conditions improve. Moore et al. (2007) discussed the physiology of Myrothamnus, which shows surprising infraspecific variation; Bianchi et al. (1993) found much glucopyranosyl-ß-glycerol and some trehalose along with the more normal high concentrations of sucrose in the dry leaf (see also Farrant 2000). Mitochondria and perhaps also chloroplasts are surrounded by membranes when the leaf is dry, and the stacking of the chloroplast grana (offset) is very unusual (Wellburn & Wellburn 1976).
Chemistry, Morphology, etc. The stems are narrowly winged and there is no axial parenchyma. There are four veins in the leaf sheaths - two bundles going directly to the midrib, and two commissural veins (Grundell 1933). Since carpellate flowers lack perianth and staminodes, it is not clear if the ovary is inferior. When flowers are terminal - on the main or lateral axes - there are four "Hochblätter" as well as bracts and bracteoles, and the four carpels are opposite the "Hochblätter" (Jäger-Zürn 1966) which might even be interpreted as perianth or tepals (Wanntorp and Ronse De Craene 2005) and so the ovary would be superior; see also Puff (1978a, 1978b). The carpellate flowers have been described as being zygomorphic (Moore et al. 2007).
For more information, see Carlquist (1990a: leaf anatomy) and Dahlgren (in Dahlgren & Van Wyk 1988) and Kubitzki (1993b), both general.
Previous relationships. Myrothamnaceae were included in Hamamelididae by Takhtajan (1997).