LIGNOPHYTA

True roots +; lateral meristems: cork cambium producing cork abaxially, vascular cambium producing phloem abaxially and xylem adaxially.

EXTANT SEED PLANTS/SPERMATOPHYTA

Plant woody, 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, thus containing p-hydroxyphenyl and guaiacyl lignin units, (lignins derived from p-coumaryl alcohol, i.e. S [syringyl] lignin units); true roots present, apex multicellular, xylem exarch, and branching endogenous; arbuscular mycorrhizae +; shoot apical meristem multicellular, interface specific plasmodesmatal network; stem with ectophloic eustele, endodermis 0, xylem endarch, branching exogenous; vascular tissue in t.s. discontinuous by interfascicular regions; vascular cambium + [xylem ("wood") differentiating internally, phloem externally]; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, plastids with starch grains; phloem fibres +; stem cork cambium superficial, root cork cambium deep seated; leaves with single trace from sympodium ["nodes 1:1"]; stomata ?; leaf vascular bundles collateral; leaves megaphyllous [determinancy evolved first, then ad/abaxial symmetry], spiral, simple, lamina with vein density up to 5 mm/mm² [mean for all non-angiosperms 1.8]; axillary buds associated with at most some leaves; prophylls [including bracteoles] two, lateral; plant heterosporous, sporangia eusporangiate, on sporophylls, sporophylls aggregated in indeterminate cones/strobili; true pollen [microspores, i.e. no distal pore for release of gametes] +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, crassinucellate, megaspore tetrad tetrahedral, only one megaspore develops, megasporangium indehiscent; male gametophyte development first endo- then exosporic, tube developing from distal end of grain, to ca 2 mm from receptive surface to egg, gametes two, developing after pollination, with cell walls, with many flagellae; female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large", first cell wall of zygote transverse, embryo straight, endoscopic [suspensor +], short-minute, with morphological dormancy, white, cotyledons 2; plastid transmission maternal; 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.

MAGNOLIOPHYTA

Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, non-hydrolysable tannins, quercetin and/or kaempferol +, 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; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, with gelatinous fibres; 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 cells from same mother cell that gave rise to the sieve tube; sugar transport in phloem passive; nodes unilacunar [1:?]; stomata with ends of guard cells level with pore, paracytic, outer stomatal ledges producing vestibule; leaves petiolate, lamina [formed from the primordial leaf apex], development of venation acropetal, 2ndary veins pinnate, fine venation reticulate, veins (1.7-)4.1(-5.7) mm/mm², endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, polysymmetric, parts spiral [esp. the A], free, numbers unstable, development in general centripetal; P not sharply differentiated, with a single trace, outer members not enclosing the rest of the bud, often smaller than inner members; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], ± embedded in the filament, with at least outer secondary parietal cells dividing, each theca dehiscing longitudinally by action of hypodermal endothecium, endothecial cells elongated at right angles to long axis of anther; tapetum glandular, binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellar, endexine thin, compact, lamellate only in the apertural regions; nectary 0; G free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, 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, megaspore tetrad linear, functional megaspore chalazal, lacking sporopollenin and cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; P deciduous in fruit; seed exotestal; pollen binucleate at dispersal, trinucleate eventually, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing at 80-600 µm/hour, with pectic outer wall, callose inner wall and callose plugs, growing between cells, penetration of ovules via micropyle [porogamous] within ca 18 hours, distance to first ovule 1.1.-2.1 mm, tube moves between nucellar cells; double fertilisation +, endosperm diploid, cellular [micropylar and chalazal domains develop diffently, 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 cellular ab initio, minute; germination hypogeal, seedlings/young plants sympodial; Arabidopsis-type telomeres [(TTTAGGG)_n]; whole genome duplication, 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]].

Evolution. Possible apomorphies for flowering plants are in bold. Note that the actual level to which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is because some taxa basal to the [magnoliid + monocot + eudicot] group have been surprisingly little studied, there is considerable homoplasy as well as variation within and between families of the ANITA grade in particular for several of these characters, and also because details of relationships among gymnosperms will affect the level at which some of these characters are pegged. For example, if reticulate-perforate pollen is optimized to the next node on the tree (see Friis et al. 2009 for a discussion), it effectively makes the pollen morphology of the common ancestor of all angiosperms ambiguous... For other features such as details of sugar transport in the phloem, their placement on the tree is frankly speculative. Finally, for features such as parietal tissue/a nucellus only one (Nymphaeales) to three cells thick above the embryo sac and a stylar canal lacking an epidermal layer, although plesiomorphous for basal grade angiosperms (Williams 2009), I am unsure where on the tree a thicker nucellus and a stylar epidermal layer are acquired.

NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: vessels +, elements with elongated scalariform perforation plates; wood fibres +; axial parenchyma diffuse or diffuse-in-aggregates; tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.

[[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]] / MESANGIOSPERMAE: benzylisoquinoline alkaloids +; outer epidermal walls of root elongation zone with cellulose fibrils oriented transverse to root axis; P more or less whorled, 3-merous [possible position]; carpels plicate; embryo sac bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid; ?germination.

[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (veins in lamina often 7-17mm/mm² or more [mean for eudicots 8.0]); (stamens opposite [two whorls of] P); (pollen tube growth fast).

[CERATOPHYLLALES + EUDICOTS]: ethereal oils 0.

Evolution. Divergence & Distribution. Bell et al. (2010) suggest ages of (168-)156(-146) or (142-)136(-130) million years depending on the method used. Soltis et al. (2008: a variety of estimates) suggest an age of divergence of Ceratophyllales and eudicots of 160-123 million years, Magallón and Castillo (2009) give ages of ca 201.4 and 128 million years for relaxed and constrained penalized likelihood datings respectively for stem Ceratophyllales, and Moore et al. (2010: 95% highest posterior density) suggest ages of (140-)132(-125) million years. A fossil-based estimate for the age of this clade is ca 100 million years (Crepet et al. 2004).

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 their common ancestor 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 an ancient aquatic lineage, Ceratophyllaceae have a very derived morphology. Thus it has been suggested that Ceratophyllaceae are sister to Chloranthaceae, see e.g. Duvall et al. (2006). Features common to that clade include: Leaves opposite, margin toothed; flowers small; G 1, ovule 1, pendant, straight, nucellar cap +; fruit indehiscent (see also Duvall et al. 2006). If Ceratophyllaceae were 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. However, if Ceratophyllaceae are sister to eudicots, as now seems likely (Jansen et al. 2007; Saarela et al. 2007; Moore et al. 2007), any similarity in characters between Ceratophyllaceae and monocots that could be linked with a more or less aquatic habitat are likely to be parallelisms - and there are no morphological characters in particular linking Ceratophyllaceae with eudicots. One might almost expect a submerged aquatic plant to lack ethereal oils, and to have an otherwise highly unconventional morphology.

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).

CERATOPHYLLALES Link  Main Tree, Synapomorphies.

Herbaceous, aquatic; mycorrhizae absent; delphinidin +, alkaloids 0; roots 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, connective apically produced, tapetum amoeboid; microsporogenesis ?successive; pollen inaperturate, exine much reduced, 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.

Evolution. Divergence & Distribution. The distinctive fruits (with associated leaves) of Ceratophyllum are known from the Aptian and Albian onwards and are widely distributed (see Dilcher & Wang 2009 for references). Dilcher and Wang (2009) describe Donlesia, from deposits in Kansas of the end-Albian age some 100 million years ago, a plant that they think may be sister to Ceratophyllum; note that it has a basal rather than an apical ovule, not a basal ovule, as in extant Ceratophyllaceae.

Synonymy: Ceratophyllanae Reveal & Doweld

CERATOPHYLLACEAE Gray, nom. cons.   Back to Ceratophyllales

Cuticle wax crystalloids 0; leaves dichotomously divided or not; vegetative bud one per node; P 6-13, whorled, basally connate; A 3(?)-46, ± sessile; 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]

• Ceratophyllaceae may be recognised by their whorled, spiny-toothed, often dichotomously-branched leaves; their small, sessile flowers (even the perianth and connective have spiny teeth); and their distinctive, spiny, achenial fruits.

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, Iwamoto et al. (2003) for floral morphology.

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