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.

STOMATOPHYTES

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.

POLYSPORANGIOPHYTA†

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.

LIGNOPHYTA†

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.

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., and 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.y..

A fossil-based estimate for the age of this clade is ca 100 m.y. (Crepet et al. 2004). For several fossils assigned somewhere around here, see Doyle and Upchurch (2014).

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.

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, pendant, straight, nucellar cap +; fruit indehiscent (see in part also Duvall et al. 2006; Endress & Doyle 2009). 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).

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 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. Indeed, 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 thus differs somewhat from that in A.P.G. II (2003). For further information, see the discussion at the mesangiosperm node. Chloranthales, magnoliids, and monocots are the other clades immediately basal to the eudicots whose position is 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; flowers extra-axillary, alternating with leaves; P [?or bracts] not vascularized; anthers extrorse, arrangement unclear, tapetum amoeboid; microsporogenesis ?successive; pollen inaperturate, exine 0, pollen tubes branched; G 1, postgenital fusion by secretion; ovule 1/carpel, straight, apical, pendulous, unitegmic; seed coat ± obliterated; endosperm 0, embryo large, suspensor 0. - 1 family, 1 genus, 1-2+ species.

Note: Possible apomorphies are in bold. However, the actual level at which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is partly because many characters show considerable homoplasy, in addition, basic information for all too many is very incomplete, frequently coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there is the not-so-trivial issue of how ancestral states are reconstructed (see above).

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.

Synonymy: Ceratophyllanae Reveal & Doweld

CERATOPHYLLACEAE Gray, nom. cons.   Back to Ceratophyllales

Ceratophyllaceae

Cuticle wax crystalloids 0; leaves dichotomously divided or not; vegetative bud one per node; P 6-13, whorled, glandular at the apex, basally ± connate; A 3(?)-46, ± sessile, connective with ephemeral gland at apex, also two pointed productions, staminodes +; tapetal cells uninucleate; style quite long, stigma small, at base of lateral groove; funicle lacking vascular tissue, nucellar cap +; fruit achenial, spiny; endosperm 0, embryo green, 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 leaves are whorled, there is only a single vegetative bud and usually only a single floral bud 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). Shamrov (2009) described the gynoecium as being two-carpellate and syncarpous.

Some information is taken from Les (1993); see Batygina et al. (1982) for embryology, Floyd and Friedman (2000) for endosperm development, and Endress (1994) and Iwamoto et al. (2003) for floral morphology.

Phylogeny. See Les (1989 and references) for species limits (unclear) and sectional groupings.