EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, thalloid, with single-celled apical meristem, showing gravitropism; rhizoids +, unicellular; acquisition of phenylalanine lysase [PAL], flavonoids [absorbtion of UV radiation], phenylpropanoid metabolism [lignans, also lignins], xyloglucans +; plant poikilohydrous [protoplasm dessication tolerant], ectohydrous; cuticle +; cell wall also with (1->3),(1->4)-ß-D-MLGs [Mixed-Linkage Glucans]; chloroplasts per cell, lacking pyrenoids; 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; blepharoplast, bicentriole pair develops de novo in spermatogenous cell, associated with basal bodies of cilia [= flagellum], multilayered structure [4 layers: L1, L4, tubules; L2, L3, short vertical lamellae] + 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 dependent on gametophyte, 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, with at least transient apical cell [?level], sporangium +, single, 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]; nuclear genome size <1.4 pg, LEAFY gene present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA 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, ?D-methionine +; sporangium with 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; spores trilete; polar transport of auxins and class 1 KNOX genes expressed in the sporangium alone; shoot meristem patterning gene families expressed; MIKC, MI*K*C* and class 1 and 2 KNOX genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns.
[Anthocerophyta + Polysporangiophyta]: archegonia embedded/sunken in the gametophyte; sporophyte long-lived, chlorophyllous; sporophyte-gametophyte junction interdigitate, sporophyte cells showing rhizoid-like behaviour.
Sporophyte branched, branching apical, dichotomous; sporangia several, each opening independently; spore walls not multilamellate [?here].
EXTANT TRACHEOPHYTA / VASCULAR PLANTS
Photosynthetic red light response; plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; (condensed or nonhydrolyzable tannins/proanthocyanidins +); sporophyte soon independent, dominant, with basipetal polar auxin transport; vascular tissue +, sieve cells + [nucleus degenerating], tracheids +, in both protoxylem and metaxylem, plant endohydrous; endodermis +; 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; basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; placenta with single layer of transfer cells in both sporophytic and gametophytic generations, root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Sporophyte branching ± indeterminate; root apex multicellular, root cap +, lateral roots +, endogenous; endomycorrhizal associations + [with Glomeromycota]; 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; 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; 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 stele with xylem and phloem originating on alternate radii, cork cambium deep seated; 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 +; cork cambium superficial; 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.; buds axillary (not associated with all leaves), exogenous; prophylls two, lateral; leaves with petiole and lamina, development basipetal, blade simple; plant heterosporous, sporangia borne on sporophylls, sporophylls spiral; microsporophylls aggregated in indeterminate cones/strobili; grains monosulcate, aperture in ana- position [distal], exine and intine homogeneous; ovules unitegmic, parietal tissue 2+ cells across, megaspore tetrad linear, functional megaspore single, chalazal, lacking sporopollenin, megasporangium indehiscent; pollen grains land on ovule; gametophytes dependent on sporophyte; apical cell 0, rhizoids 0; male gametophyte development initially endosporic, 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; 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], 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, hypodermis suberised and with Casparian strip [= 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; protogynous; 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], sporangium pairs dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, 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 lamellate only in the apertural regions, thin, compact; nectary 0; carpels present, superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus at most short [shorter than ovary], 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 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, cilia 0, siphonogamy; double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; mature seed much larger than ovule when fertilized, small , dry [no sarcotesta], exotestal; 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; dark reversal Pfr → Pr; Arabidopsis-type telomeres [(TTTAGGG)n]; nuclear genome size <1.4 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.]; (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 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.
Age. Magallón and Castillo (2009) tentatively suggest an age of about 122.7 m.y., Magallón et al. (2015) an age of about 129 m.y., and Z. Wu et al. (2014) an age of around 188 m.y. for this node, Vekemans et al. (2012: MRCA Buxales and Trochodendrales) an age of around (124.1-)122.6(-121.1) m.y. or a little less. The age for stem Trochodendrales in Wikström et al. (2003) is about (140-)135, 123(-118) m.y. - but c.f. sister group [B [T + CE]].
Evolution. Divergence & Distribution. Doyle (2013) is inclined to think that the evolution of 2-merous, wind pollinated flowers can be pegged to this node.
Genes & Genomes. For the paleoAP3 duplication, etc., see Lamb and Irish (2003), S. Kim et al. (2004b, 2005a), Zahn et al. (2005a), and especially Kramer et al. (2006); Kramer and Zimmer (2006) note that although the paleoAP3 gene has been found in Proteales and Sabiales, whether or not it occurs in Buxales and Trochodendrales remains unclear. EuAP3/PI are involved in stamen identity very much as paleoAP3/PI, but the former may be involved in petal development in core eudicots. For the loss of the rps2 mitochondrial gene, see Adams et al. (2002b), and for the duplication of the RPB1 and RPB2 genes, which may have occurred in the immediate ancestor of Trochodendrales, see Oxelman et al. (2004) and Luo et al. (2007). This latter is a complicated problem, since Buxaceae have no duplication in either gene and there has also been widespread loss of both genes. See the Gunnerales page for a genome triplication.
Phylogeny. For discussion on the position of Trochodendrales, see the Ranunculales page.
TROCHODENDRALES Cronquist Main Tree.
Stomata laterocytic; anthers valvate, latrorse, filaments thin; G laterally connate, nectariferous abaxially, 5 vascular bundles/carpel; ovules apotropous, integuments long, micropyle bistomal; fruit an aggregate of follicles, styles becoming ± basal on the outer surface; endotestal cells with slightly thickened walls, exotegmic cells thick-walled, tracheidal, elongated; endosperm development? - 1 family, 2 genera, 2 species.
Note: (....) denotes a feature common in the clade, exact status uncertain, [....] includes explanatory material. 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).
Synonymy: Trochodendrineae Engler - Trochodendranae Reveal
TROCHODENDRACEAE Eichler, nom. cons. Back to Trochodendrales
Evergreen trees; flavonols +; petiole bundle arcuate; buds with scales; lamina toothed, secondary veins proceed to a clear, persistent cap, lateral veins also enter; cuticle waxes with nonacosan-10-ol a major component; flowers with cortical vascular system; pollen tectum reticulate-striate; G very slightly inferior; ovules with chalazal protrusion; seeds flattened, with marginal flange, chalazal hair-pin bundle +.
2/2 [list]. Southeast Asia, scattered.
Age. Estimates for the divergence times of the two genera are (113-)106, 95(-88) m.y. Wikström et al. (2001) or (65-)20, 19(-7) m.y.a. (Bell et al. 2010).
Fossils of Trochodendraceae are known from since the late Cretaceous as Nordenskioldia, more properly Nordenskioeldia, close to Trochodendron (see also Friis et al. 2011). They are widely distributed around the northern hemisphere in the Eocene, and are sometimes at very high latitudes (Crane et al. 1991; Pigg et al. 2001, 2007; Taylor et al. 2009; Harrington et al. 2011). However, the hairpin loop in the seed is not found in at least some fossil Trochodendraceae (Crane et al. 1991, but c.f. Doweld 1998c); postgenital fusion of the carpels may not occur. Both the extant genera are kown fossil from the Eocene onwards (Friis et al. 2011 and references).
1. Trochodendron Siebold & Zuccarini
Myricetin +; plant glabrous; pits bordered; vessels 0; young stem with separate vascular bundles; rays ca 12-seriate; nodes 1:1-7:7; ± branched sclereids +; leaves spiral, venation subpinnate; plant androdioecious, inflorescence terminal; P 0-5, minute, not vascularized; A many, ± spiral; G [(4-)6-11(-17)], with a secretion canal, placentation apical-axile, styluli erect, stigma decurrent in two crests; ovules many/carpel; (follicles also opening abaxially); seeds pendulous, endotesta sclerotic; endosperm cellular; n = 20.
1/1: Trochodendron aralioides. Japan to N. Taiwan (map: red, fossils blue [Japan - N.E. Honshu, not in the sea...], Pigg et al. 2001, 2007). [Photo - Collection, Inflorescences.]
2. Tetracentron Oliver
Chalcones or dihydrochalcones +; secretory cells +; leaves two-ranked, lamina vernation supervolute, secondary veins palmate, leaf base broad, thin latero-basal flange enveloping axillary bud, lamina with palmate venation; inflorescence axillary, spicate; flowers small, 4-merous; P 4, vascular bundle rudimentary; A equal and opposite P; G , alternate with P, styluli short, spreading, placentation axile; ovules 5-6/carpel; testa multiplicative, meso- and endotesta lignified, tegmen two layered; endosperm nuclear; n = 24.
1/1: Tetracentron sinense. China, Nepal (map: from Hara & Kanai 1964; fossils green, from Grímsson et al. 2008).
Synonymy: Tetracentraceae A. C. Smith, nom. cons.
Evolution. Divergence & Distribution. Both Trochodendron and Tetracentron were widely distributed in the northern hemisphere is the Caenozoic (Grímsson et al. 2008: Tetracentron; Friis et al. 2011). However, in some fossils assigned to Trochodendron there are paired auricles or foliaceous stipels at the base of the lamina (Pigg et al. 2007).
Chemistry, Morphology, etc. Vessel elements with scalariform to scalariform-reticulate perforation plates have recently been reported from Tetracentron and Trochodendron, although both genera had long been considered to lack vessels (Hacke et al. 2007; Ren et al. 2007a; Li et al. 2011; c.f. Bailey & Thomopson 1918).
In Tetracentron the petiole becomes round towards the base, and there is a marginal flange that tightly and totally envelops the axillary bud; the base of the petiole is broad and the scar encircles much of the stem. In Trochodendron, on the other hand, not only is nodal anatomy variable and the leaves on the adult plant have a narrow petiole and often lack axillary buds, in the young plant the leaves are more similar to those of Tetracentron (Bailey & Nast 1945; Nast & Bailey 1955). Although Baranova (1983) described both genera as having laterocytic stomata, Metcalfe and Chalk (1950) described and drew the stomata of Trochodendron as being laterocylic, while the stomata are of Trochodendron are cyclocytic, according to Carlquist (1982)....
The micropyle of Trochodendron is described as being endostomal in Johri et al. (1992) and Endress and Igersheim (1999), but it looks bistomal in Takhtajan (1991). In both genera the adaxial side of the carpel develops greatly as the fruits ripen and so the style becomes basal on the abaxial side of the follicle.
See Nast and Bailey (1945) for flowers, fruits and summary, Endress (1986b) for floral morphology, Endress (1993) general, Wu et al. (2007) for perianth evolution and Chen et al. (2007) for floral morphology of Tetracentron; Rix and Crane (2007) provide general information about Tetracentron.
Previous Relationships. The relationships of the two genera included in Trochodendraceae have been somewhat obscure, although their apparent lack of vessels had long typed them as being primitive angiosperms. Endress (1986b) compared the sclereids of Trochodendron and the secretory cells of Tetracentron with the cells secreting ethereal oils in magnoliids, etc., and linked the two genera with Cercidiphyllaceae (Saxifragales) and Eupteleaceae (Ranunculales) in an expanded Trochodendrales (c.f. also Takhtajan 1997 and Thorne 2007 in part). Kai-yu et al. (1993) suggested that Tetracentron should be put in its own order.
Classification. Including Tetracentraceae in Trochodendraceae was an option in A.P.G. II (2003). The two families do have quite a lot in common, as is clear from the fairly lengthy ordinal description, and since both are monotypic, combination is in order (see A.P.G. III 2009).