LIGNOPHYTA

Plant a shrub or tree; true roots +, origin endogeneous, root cap +, apex multicellular; endodermis +; shoot apical meristem multicellular; lateral meristems +, cork cambium producing cork abaxially, vascular cambium producing phloem abaxially and xylem adaxially; lamina with mean venation density 1.8 mm/mm² (to 5 mm/mm²).

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, so no Maüle reaction; root xylem exarch, cork cambium deep seated; arbuscular mycorrhizae +; shoot apical meristem interface specific plasmodesmatal network; stem with vascular tissue around central pith [eustele], vascular bundles with interfascicular tissue, ectophloic, endodermis 0, xylem endarch; 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 +; stem cork cambium superficial; branches exogenous; leaves with single trace from vascular sympodium ["nodes 1:1"]; vascular bundles collateral [stem: phloem external; leaf: phloem abaxial]; stomata morphology?, pore opening controlled by abscisic acid; leaves with petiole and lamina, spiral, development basipetal, blade simple; axillary buds +, not associated with all leaves; prophylls two, lateral; plant heterosporous, sporangia borne on sporophylls; microsporophylls aggregated in indeterminate cones/strobili; true pollen +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, parietal tissue 2+ cells across, 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, flagellae numerous; ovules increasing considerably in size between pollination and fertilization, female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large" [ca 8 mm³], but not much bigger than ovule, with morphological dormancy; embryo cellular ab initio, endoscopic, plane of first cleavage of zygote transverse, suspensor +, short-minute, embryo straight, shoot and root at opposite ends [allorrhizic], white, cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, 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, 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 unilacunar [1:?]; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, secondary veins pinnate, overall growth ± diffuse, venation hierarchical, fine venation reticulate, veins (1.7-)4.1(-5.7) mm/mm², endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, ± haplomorphic, 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, 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 columellar, endexine thin, compact, lamellate only in the apertural regions; nectary 0; G superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, 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, 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]; ovule not increasing in size between pollination and fertilization; pollen binucleate at dispersal, male gametophyte trinucleate, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing between cells, growth rate 20-20,000 µm/hour, outer wall pectic, inner wall callose, 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, flagellae 0, double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; seed exotestal, becoming much larger than ovule at time of fertilization; endosperm diploid, cellular [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; embryogenesis cellular; germination hypogeal, seedlings/young plants sympodial; Arabidopsis-type telomeres [(TTTAGGG)_n]; 2C genome size 1-8.2 pg [1 pg = 10⁹ base pairs], 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]].

[NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]]: vessels +, elements with elongated scalariform perforation plates; 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]]]]: essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood 0; 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 +; 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 positiion]; 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) suggested ages of (168-)156(-146) or (142-)136(-130) m.y. for the divergence of Ceratophyllum and the eudicots depending on the method used. Wikström et al. (2004) suggested ages of 155-144 m.y., Soltis et al. (2008: a variety of estimates), 160-123 m.y., Magallón and Castillo (2009) 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., and Magallón et al. (2013) suggested an age of about 132.5 m.y.. A fossil-based estimate for the age of this clade is ca 100 m.y. (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 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 an ancient aquatic lineage, Ceratophyllaceae have a very derived morphology, and relationships suggested by morphology are likely to be ambiguous../p> If Ceratophyllaceae are sister to Chloranthaceae, see e.g. Duvall et al. (2006), features common to the combined 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. 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 especially the discussion immediately preceding the Magnoliales, i.e. the magnoliid clade; eudicots and monocots are the other main clades involved, q.v. for more discussion.

CERATOPHYLLALES Link  Main Tree, Synapomorphies.

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 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.

Note: Possible apomorphies are now being added throughout the site; they 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 because there is very considerable homoplasy for many characters, with with variation within and between clades. Furthermore, basic information for all too many characters is very incomplete, often 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...

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 m.y.a., 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, 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]

• 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, and Endress (1994) and Iwamoto et al. (2003) for floral morphology.

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