EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, not motile, 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; 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]; 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; fruit dry [very labile].
Age. Bell et al. (2010: BEAST exponential and lognormal respectively) suggested ages of (168-)156(-146) or (142-)136(-130) m.y. for this node. Wikström et al. (2001) suggested ages of (162-)155, 140(-133) m.y., Soltis et al. (2008: a variety of estimates), 160-123 m.y., Magallón and Castillo (2009) ages of ca 201.4 and 128 m.y. for relaxed and constrained penalized likelihood datings respectively, Moore et al. (2010: 95% HPD), (140-)132(-125) m.y., Xue et al. (2012) an age of around 137.3 m.y.a, Naumann et al. (2013) an age of ca 138.1 m.y.a., Tank et al. (2015: Table S1, S2, but stem eudicots 136.9 m.y.) ages of around 191.7-185.6 m.y., while at the other extreme Magallón et al. (2013, 2015) suggested ages of about 132.5 m.y.a. and 134.4 m.y.a. respectively.
Bell et al. (2010: monocots sister to Chloranthaceae, magnoliids, etc.) suggested ages for stem monocots[??] of (156-)146(-139) or (138-)130(-123) m.y. depending on the method used, Chaw et al. (2004: 61 chloroplast genes, sampling poor) an age of 150-140 m.y., and Davies et al. (2011: 95% credibility intervals) ages of (161-)137(-124) m. years.
A fossil-based estimate for the age of this clade is ca 100 m.y. (Crepet et al. 2004). For several fossils assigned around here, see Doyle and Upchurch (2014). Kvacek et al. (2012) linked Pseudoasterophyllites, vegetatively quite like Ceratophyllum and perhaps growing in somewhat saline conditions, with Tucanopollis, an abundant palynomorph from Africa-South America over 125 m.y. ago, while Montsechia, a fossil from Portugal in deposits 130-125 m.y.o. may be in this area (Gomez et al. 2015). See also Doyle et al. (2015), while there is more discussion at the mesangiosperm node.
Divergence & Distribution. The question is, how to optimise characters that are placed at or near the eudicot node. Are some of these to be placed below the node [Ceratophyllales + eudicots]? Did the common ancestor of this clade have tricolpate pollen? Had it already lost ethereal oils? These are going to be very difficult questions to answer unless, e.g., detailed studies of the development of the distinctive inaperturate Ceratophyllum pollen gives clues as to its derivation. Being a very old and aquatic lineage, Ceratophyllaceae have a very derived morphology, and relationships suggested by morphology are likely to be ambiguous. However, somewhat less radically modified fossils like Montsechia, if correctly assigned to this area, may help - thus Montsechia has anomocytic stomata (Gomez et al. 2015), otherwise pegged to the eudicot node.
If Ceratophyllaceae are sister to Chloranthaceae, features common to the combined clade include: Leaves opposite, margin toothed; flowers small, [<4 mm across], sessile; anthers embedded in broad filament, G 1, ovule 1, pendent, straight, nucellar cap +; fruit indehiscent (see in part also Duvall et al. 2006; Endress & Doyle 2009, 2015 - similarities greater if the male flower is treated as an inflorescence). The well-preserved and distinctive Canrightia resinifera from around m.y.a. in Portugal with its syncarpous unilocular gynoecium that has apical placentation and ovules that have an endothelium, etc., may be associated with this clade (Friis & Pedersen 2011; Friis et al. 2011). Montsechia may also belong in this area, if not assignable to Ceratophyllales in particular (Gomez et al. 2015)
If Ceratophyllaceae are sister to monocots, features for that combined clade would include: Plant herbaceous; primary root at best weak; vascular bundles in stem closed [no interfascicular cambium developing]; vessels in stem and leaves 0; (lamina margin spiny toothed); microsporogenesis successive.
If Ceratophyllaceae are sister to eudicots, as now seems perhaps more likely (Jansen et al. 2007; Saarela et al. 2007; Moore et al. 2007), any similarity between Ceratophyllaceae and monocots that could be linked with a more or less aquatic habitat are likely to be parallelisms. There are no morphological characters in particular linking Ceratophyllaceae with eudicots, since one might almost expect a submerged aquatic plant to lack ethereal oils.
Chemistry, Morphology, etc. Martín and Sabater (2010) note a change from cytosine to thymidine at certain editing sites of some chloroplast ndh genes (it is also possible that there are interesting changes within the ANITA grade).
Phylogeny. Relationships between the lineages immediately above the basal pectinations in the main tree, the ANITA grade (Amborellales, Nymphaeales and Austrobaileyales here), have only recently been clarified. The topology of the main tree in this area is somewhat more conservative than that in A.P.G. IV (2016). For further information, see especially the discussion at the mesangiosperm node. Chloranthales, magnoliids, and monocots are the other clades immediately basal to the eudicots whose positions are still rather uncertain.
CERATOPHYLLALES Link Main Tree.
Herbaceous, aquatic; mycorrhizae absent; delphinidin +, alkaloids 0; roots 0; vascular cambium 0; vessels 0; nodes?; stomata 0; leaves opposite, lamina margins spiny-toothed; plant monoecious; inflorescences extra-axillary, alternating with leaves; staminate inflorescence capitate; bracts 0; perianth 0; A 1, anthers extrorse; tapetum amoeboid; microsporogenesis ?successive; pollen inaperturate, exine 0, pollen tubes branched; carpellate inflorescence: flower single; G 1, ascidiate; ovule 1/carpel, straight, apical, pendulous, unitegmic, integument ca cells across; seed coat ± obliterated; endosperm 0, embryo long, suspensor 0. - 1 family, 1 genus, 1-2+ species.
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. The distinctive fruits (with associated leaves) of Ceratophyllum are known from the Aptian and Albian onwards and are widely distributed in the Caenozoic (see Dilcher & Wang 2009; Friis et al. 2011 for references). Dilcher and Wang (2009) describe Donlesia, from deposits in Kansas of the end-Albian age some 100 m.y.a., a plant that they think may be sister to Ceratophyllum; note that it has a basal ovule, not an apical ovule as in extant Ceratophyllum. The Portugese fossil Montsechia vidalii, placed in Montsechiaceae, has been associated with Ceratophyllum. Its carpels are borne two together and the ovule is pendent on a funicle that is the length of the carpellary loculus, the placenta being basal (Gomez et al. 2015).
Ecology & Physiology. The evidence suggests that Ceratophyllales are a very ancient clade of aquatics (Gomez et al. 2015) which once may have been quite diverse.
Synonymy: Ceratophyllanae Reveal & Doweld
CERATOPHYLLACEAE Gray, nom. cons. Back to Ceratophyllales
Vascular bundles lacking associated sclerenchyma; cuticle wax crystalloids 0; colleters +; leaves dichotomously divided, venation then dichotomous, or not; vegetative bud one (two) per node; staminate flower: inflorescence bracts whorled, glandular at the apex, basally ± connate; A ± sessile, connective with ephemeral gland at apex, also two pointed productions, staminodes +; tapetal cells uninucleate; carpellate flower: style quite long, stigma small, at base of lateral groove; funicle lacking vascular tissue, nucellar cap +; fruit achenial, spiny; endosperm 0, embryo chlorophyllous, plumule well developed; n = 12.
1[list]/ca 6 (map: see Vester 1940; Hegi 1965; Hultén 1971; Les 1989; Wilson 2007). World-wide. [Photo - Habit © from D. Les website, Fruit © H. Wilson]
Evolution. Divergence & Distribution. For the ages of some intercontinental disjunctions within Ceratophyllaceae, see Les et al. (2003).
Chemistry, Morphology, etc. There is a ring of air canals in the stem outside the pericycle, and also a central air canal, although the vascular cylinder is otherwise sold, lacking pith (Rutishauser 1999). Although the leaves are whorled, there is usually a single vegetative bud (sometimes two) and a single floral bud (up to four) per node. The flowers are borne on the same orthostichy as the vegetative buds; the latter alternate their positions at each node, hence the floral buds will be lateral to the leaves (Rutishauser 1999). Iwamoto et al. (2015) suggest that the leaves are opposite (hence the up to two buds per node) and the flowers come from accessory (prophyllar) buds (hence they are up to four in number).
For floral morphology, see Endress (1994d) and Endress and Doyle (2015) in particular. The "flower" with 3 to many stamens is perhaps best treated as an inflorescence made up of flowers that consist of a single stamen and nothing more - hence with major effects on several characters. Shamrov (2009) described the gynoecium as being two-carpellate and syncarpous (c.f. Iwamoto et al. 2015 and references; Endress & Doyle 2015).
Some information is taken from Les (1993); see Batygina et al. (1982) for embryology, Floyd and Friedman (2000) for endosperm development, and Iwamoto et al. (2003) for floral morphology.
Phylogeny. See Les (1989 and references) for species limits (unclear) and sectional groupings.