EXTANT SEED PLANTS

Plant woody, evergreen; nicotinic acid metabolised to trigonelline; primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins rich in guaiacyl units; true roots present, xylem exarch, branching endogenous; arbuscular mycorrhizae +; shoot apical meristem complex; 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 +; tracheid/tracheid pits circular, bordered; sieve tube/cell plastids with starch grains; phloem fibers +; stem cork cambium superficial, root cork cambium deep seated; nodes ?; stomata ?; leaf vascular bundles collateral; leaves spiral, simple, axillary buds?, prophylls [including bracteoles] two, lateral, veins -5(-8) mm/mm2; plant heterosporous, sporangia eusporangiate, on sporophylls, sporophylls aggregated in indeterminate cones/strobili; true pollen [microspores] +, 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, 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 duplication, mitochondrial nad1 intron 2 and coxIIi3 intron present.

MAGNOLIOPHYTA

Plant woody, evergreen; lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, non-hydrolysable tannins, quercetin and/or kaempferol +, apigenin and/or luteolin scattered, cyanogenesis via tyrosine pathway [ANITA grade?], lignins derived from both coniferyl and sinapyl alcohols, containing syringaldehyde [in positive Maüle reaction, syringyl:guaiacyl ratio less 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; stem with 2-layered tunica-corpus construction; wood fibers and wood parenchyma +; reaction wood ?, with gelatinous fibres; starch grains simple; primary cell wall mostly with pectic polysaccharides; tracheids +; sieve tubes eunucleate, with sieve plate, companion cells from same mother cell that gave rise to the tube, the sieve tube with P-proteins; nodes unilacunar; stomata with ends of guard cells level with aperture, paracytic; leaves with petiole and lamina [the latter formed from the primordial leaf apex], development of venation acropetal, 2ndary veins pinnate, fine venation reticulate, vein endings free; flowers perfect, polysymmetric, parts spiral [esp. the A], free, development in general centripetal, numbers unstable, P not differentiated, outer members not enclosing the rest of the bud, smaller than inner members, A many, with a single trace, introrse, filaments stout, anther ± embedded in the filament, tetrasporangiate, dithecal, 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, binucleate at dispersal, trinucleate eventually, tectum continuous or microperforate, exine columellar, endexine thin, compact, lamellate only in the apertural regions, pollen germinating in less than 3 hours, tube elongated, growing at 80-600 µm/hour, with callose plugs and callose-based walls, penetrating between cells, siphonogamy, penetration of ovules within ca 18 hours, distance to first ovule 1.1.-2.1 mm, nectary 0, G free, several, ascidiate, with postgenital occlusion by secretion, few [?1] ovules/carpel, ovules marginal, anatropous, bitegmic, [outer integument often largely subdermal in origin, inner integument dermal], micropyle endostomal, integuments 2-3 cells thick, megasporocyte single, megaspore lacking sporopollenin and cuticle, chalazal, female gametophyte ?type, stylulus short, hollow, stigma ± decurrent, wet [secretory]; P deciduous in fruit; seed exotestal; double fertilisation +, endosperm ?diploid, cellular [first division oblique, micropylar end initially with a single large cell, chalazal end more actively dividing], copious, oily and/or proteinaceous, embryo cellular ab initio; germination hypogeal, seedlings/young plants sympodial; Arabidopsis-type telomeres [(TTTAGGG)n]; whole genome duplication, 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 PHYA/PHYC gene pairs.

Possible apomorphies are in bold. Note that the actual level to which many of these features, particularly the more cryptic ones, should be assigned is unclear, because some taxa basal to the [magnoliid + monocot + eudicot] group have been surprisingly little studied. Furthermore, details of relationships among gymnosperms will affect the level at which some of these characters are pegged.

NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: vessels +, elements with scalariform perforation plates; nucleus of egg cell sister to one of the polar nuclei; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes. Back to Main Tree

Presence of vesels is optimised here on the tree. Feild (2005) suggests that vessels may have evolved in plants growing in humid conditions. This is also true of Gnetales and fossil groups with vessels, too, although they are unlikely to have evolved in aquatics. For discussion as to where characters of pollen morphology and development are to be placed on the tree, see Taylor and Osborn (2006); it partly depends on how the characters are defined. For cell lineages in the embryo sac see Huang and Russel (1992) and Friedman (2006); identification of the pattern above apparently goes back to Porsch (1907), although it has been observed for relatively few plants. Whether a monopolar, 4-nuclear embryo sac and diploid endosperm is an autapomorphy for both Nymphaeales and Austrobaileyales or for all angiosperms minus Amborella is unclear. For the possibility of a genome duplication at about this position, see Cui et al. (2006).

NYMPHAEALES Dumortier  Main Tree, Synapomorphies.

Aquatic herbs; cambium 0; 4-celled uniseriate secretory trichomes with a large terminal cell [hydropoten]; starch grains compound; primary root soon aborts, root apex with secondary dermatogen, etc., epidermis derived from outer layer of cortex [unknown from Hydatellaceae], trichoblasts in vertical files, proximal cell smaller, diaphragms in root aerenchyma, mycorrhizae 0; primary stem with ± scattered closed bundles; protoxylem lacunae +; secondary thickening 0; nodes?; aerenchyma common; stomata anomocytic; leaf base broad; bracts 0; pollen boat-shaped; P persistent; seeds operculate, exotestal, ± palisade, hilum outside operculum; endosperm scanty, perisperm copious [starchy], precocious, cells ± multinucleate, suspensor 0, embryo broad; germination hypogeal; intergenic inversion in chloroplast inverted repeat. - 3 families, 6 genera, 74 species.

Wikström et al. (2001) suggested an age for the clade of some 171-153 million years before present. The curious fossil Archaefructus, probably an aquatic plant and ca 124 million years old, has been linked with Hydatellaceae (Doyle & Endress 2007; Doyle 2008b).

Saarela et al. (2007) suggest a few additional possible synapomorphies for Nymphaeales. Hydrolysable tannins in this group (e.g. in Nuphar) are different to those found elsewhere (Gottlieb et al. 1993; Ishimatsu et al. 1989) - although of course Hydatellaceae are here, as in many other features, very poorly known. Although there are minute perforations in the end walls of the cells that make up the water conducting tissues in some Nymphaeaceae, they hardly have the morphology of what are called vessel elements elsewhere, however, there are vessels of a variety of types in the roots in the stems of Brasenia. Hydatellaceae also have vessels with scalariform perforation plates, although these are absent from the leaves. The distinctive uniseriate trichomes found in all groups may secrete nectar or mucilage, or they may be involved in ion exchange (Vogel 1998a); Wilkinson (2006) calls the trichomes on the leaves, hydropotes. It is possible that there are epidermal oil cells in Nymphaeaceae (Wilkinson 2006); do they contain ethereal oils? For discussion as to whether or not Nuphar has bracts, see Schneider et al. (2003). The inner bracts found in some Hydatellaceae and the inner petals of Cabomba are notably slow in developing (Rudall et al. 2007). If the corolla represents sterilised stamens, as is believed, possession of external staminodes will probably be another synapomorphy at least for [Nymphaeaceae + Cabombaceae]. Some genera in all families have exotestal cells that are neither very tall nor much thickened (Hamann et al. 1979; Collinson 1980).

Hydatellaceae are superficially like Centrolepidaceae, both being very reduced morphologically, and indeed Hydatellaceae have been misidentified as that family. It is unclear if the gynoecium is 1- or 3-carpellate; the fruits of Trithuria open by three valves, so they look rather monocot-like. Although Hydatellaceae have long been considered to be monocots, largely because of this superficial similarity to Centrolepidaceae, the combination of characters they show has been recognised as being unique in that group, indeed, very distinctive within monocots as a whole (e.g. Hamann et al. 1979; Dahlgren et al. 1985). Hydatellaceae are sister to Xyridaceae in Stevenson et al. (2000; see also Stevenson & Loconte 1995); both have latrorse anthers and an operculum "stopper" that is tegmic in origin. Trithuria and Xyris appear as sister taxa (weak support) and in turn sister to Mayaca (still weaker support), although other Xyridaceae are not immediately related (Michelangeli et al. 2003). However, although Bremer (2002) noted that Mayacaceae and Hydatellaceae might be weakly associated with Xyridaceae or Eriocaulaceae, depending on what taxa were included in the analysis, there were a number of long branches in this area and he excluded the first two families from his final analysis, while Janssen and Bremer (2004) suggested that the association of Hydatellaceae with Mayacaceae was probably an artefact (see also Chase et al. 2006).

This last suggestion was correct. Recent studies (Saarela et al. 2006, esp. 2007, several genes from two compartments, morphology: Friis & Crane 2007 [commentary]) place Hydatellaceae firmly with Nymphaeales, and sister to [Cabombaceae + Nymphaeaceae]; the sequence that placed Hydatellaceae in Poales was a chimaeric pcr recombinant involving a grass and a moss. Many of the morphological features of Hydatellaceae that made it so different from other monocots are consistent with this new position - Hamann (1998) even noted that the antipodal cells were absent or degenerated early, and absence of these cells would almost be expected if Hydatellaceae were placed here, indeed, recent work (Friedman 2008a; Rudall et al. 2008) shows it has a 4-celled embryo sac like other Nymphaeales and Austrobaileyales.

Includes Cabombaceae, Hydatellaceae, Nymphaeaceae.

Synonymy: Barclayales Doweld, Euryalales H. L. Li, Hydropeltidales Spenner - Nymphaeanae Reveal - Nymphaeidae Takhtajan - Hydropeltopsida Bartling, Nymphaeopsida Horaninow

HYDATELLACEAE U. Hamann, nom. cons.   Back to Nymphaeales

Plant caespitose; chemistry?; vessels in leaf 0; sieve tube plastids with triangular proteinaceous inclusions; leaves linear, with a single vein; plant monoecious; inflorescence axillary, scapose, capitate, with involucral bracts, (sessile); flowers imperfect; P 0; staminate flowers: A 1, filaments long, slender, endothecium 0, tapetal cells?, pollen tectate, with spinules; carpellate flowers: G 1, three vascular bundles equidistant, with 1 pendulous anatropous apotropous ovule, micropyle bistomal, ovule tenuinucellate, nucellar cap +, semi-annular [hood-shaped] outer integument, stigma penicillate, of rows of plump cells; fruit dehiscent or and achene; apart from exotesta, other layers ± collapsed, tanniniferous; embryo undifferentiated; n = ?; seedling - see below.

Hydatellaceae

1[list]/10. India, New Zealand and Australia (Map: from Cooke 1987; FloraBase 2004).

The inflorescence is described as being cymose and capitate, although bractless and with highly reduced flowers, i.e., it is a sort of pseudanthium, although alternative interpretations are possible (Rudall et al. 2007a). Early work suggested that the carpels might be initiated outside the stamens, and this has been confirmed (Rudall et al. 2007a); staminate flowers are the first to be initiated in the cymose inflorescence (see also Begoniaceae!). Hairs with possible apical secretory cells are known only from the inflorescences. The pedicels seem at least sometimes to be articulated. The fruit opens along three lines as the three vascular bundles separate from the rest of the pericarp. Both integuments have two cell layers; the operculum is formed from enlarged cells of the inner integument. Starch deposition in tissues that will become perisperm begins before fertilization (Friedman 2008a).

There is some disagreement over the interpretation of the morphology of the embryo. Tillich et al. (2007) compare it with that of a monocot, describing collar rhizoids, a coleoptile, two cotyledonary sheath lobes, and a haustorium. Sokoloff et al. (2008a) suggest that the sheathing structure with its bilobed apex that is found in some species can be interpreted as more or less completely connate cotyledons. The seed attaches to the sheathing structure, although details of exactly how are unclear (or bifacial hyperphyll and unifacial hypophyll?!). In some taxa there is no sheathing structure at all and have only a lateral outgrowth that goes into the seed. Sokoloff et al. (2008a) suggest that Hydatellaceae may show how monocot-like embryos/seedlings might have originated. Both studies examined largely surface morphology, neither looked in any detail at anatomy.

Some information is taken from Cutler (1969: vegetative anatomy), Hamann (1975, 1998 - embryology and general respectively), Cook (1983: germination), Hamann et al. (1979: seed anatomy), Rudall et al. (2007a: flower/inflorescence development), Sokoloff et al. (2008b: monograph), and Friedman (2008a) and Rudall et al. (2008a), both embryology.

Cabombaceae + Nymphaeaceae: stem rhizomatous; leaves involute, peltate, (divided), 2ndary veins palmate, actinodromous, festoon brochidodromous, margin toothed or entire; flowers single along stem, with cortical vascular system, P whorled (outer [inner] whorls in 3's), outer members enclosing the rest of the bud, A whorled, pollen tube growth moderately fast, placentation ± laminar, carpel margins with postgenital fusion; anticlinal walls of exotesta sinuous; suspensor 0 [?level].

Fossils of both Nymphaeaceae and Cabombaceae are known from the Lower Cretaceous (D. W. Taylor et al. 2001). Although other fossils possibly of this group (to a certain extent characters of the two families are combined) are known from the Barremian-Aptian 125-113 million years before present in Portugal (Friis et al. 2001; see also von Balthazar et al. 2008 for another fossil perhaps assignable to this general [Nymphaeales-Austrobaileyales] area), they may be from a member of Austrobaileyales (Gandolfo et al. 2004), and there is considerable discussion over when diversification within Nympahaeales and Nymphaeaceae occured (Nixon 2008). Wikström et al. (2001) suggest that divergence of Nymphaeaceae and Cabombaceae occured 144-111 million years before present, although details of relationships within the clade differ from those given here, and of course Hydatellaceae were not included. On the other hand, Yoo et al. (2005) dated divergence within the crown group to only 44.6 ± 7.9 million years before present; they suggested that the fossil Microvictoria was perhaps stem group Nymphaeales (cf. Gandolfo et al. 2004). D. W. Taylor et al. (2008) discuss the vegetative evolution of the group (see some of the characters above), noting how inclusion of diverse fossils affects relationships and hence evolutionary interpretations.

There is the option of combining the two families as Nymphaeaceae s.l. (see A.P.G. II 2003).

Note that Carpenter (2005) describes stomata as being largely variants of the actino/stephanocytic types; only one member of Cabombaceae was studied.

For information on anatomy, see Gwynne-Vaughan (1897), for root epidermis, see Voronkina (1974: ordinal characterisation above), for pollen morphology, see Osborn et al. (1991), for the development of the embryo sac, Orban and Bouharmont (1998), for the chloroplast inverted repeat, Graham and Olmstead (2000), for endosperm evolution, Floyd and Friedman (2001), for ovule development, see Yamada et al. (2001b), for root anatomy, see Seago (2002), for seed anatomy, see Collinson (1980) and Chen et al. (2004), and for general information, Les et al. (1999) and Schneider et al (2003).

CABOMBACEAE A. Richard   Back to Nymphaeales

Floating and rhizomatous; alkaloids 0; stem vascular tissue with two pairs of bundles; leaves (opposite, with semidichotomous venation); flowers rather small, parts whorled, (2)3(4)-merous; K & C 3(-4) (subequal; with nectaries), A (3, 6), extrorse to latrorse, filaments slender, tapetum more or less amoeboid, (pollen trichotomocolpate; striate - Cabomba), endexine lamellate when young, not when mature, G (1-)3-18(-22), when 3 ± opposite petals [Cabomba], 1-3(-5) ovules/carpel, attached variously, outer integument semi-annular [hood-shaped], (stigma terminal, capitate); fruits follicles or achenes; hilum and micropyle sharing same opening in center of operculum; endosperm helobial [first division transverse, micropylar cell free-nuclear, chalazal cell ± enlarged]; n = 40, 48, 52; germination?.

Cabombaceae

2[list]/6. World-wide, Brasenia schreberi subfossil remains show it to be far more widespread in Europe than at present (Map: from Raymond & Dansereau 1949; Fassett 1953; Ørgaard et al. 1992; Hultén 1961; Fl. N. Am. III 1997; Wilson 2007). [Photo - Brasenia Habit] [Photo - Flower]

Brasenia is wind pollinated, while Cabomba has paired nectaries on its inner tepals and is pollinated by insects. Stamens are sometimes physically close to each nectary and then they appear paired (Ørgaard et al. 1992).

The root endodermis has a Casparian strip and suberin lamellae. It is unclear how to interpret nodal anatomy. In Cambomba a trace leaves from each member of a vascular budle pair which shortly thereafter fuse commissurally, creating a nodal plexus; the foliar traces fuse and then divide, providing two petiolar bundles (Moseley et al. 1984). Brasenia has stems that are encased in a thick layer of mucilage; there are paired, glandular patches at the nodes. Peltate leaves are spiral, although in some taxa they are uncommon; the more or less dichotomously-divided submerged leaves are opposite. There are five vascular bundles in the sepals and three vascular bundles in the petals of Cambomba, in both cases there is a single trace leaving the floral axis (Moseley et al. 1984). Pollen of Cabomba has striate exine. Although the endexine of mature pollen of Brasenia schreberi is not lamellate, it is laid down in plates (M. L. Taylor & Osborn 2006).

The granular infratectum of Podostemaceae has been compared with that of Cabombaceae; both are aquatics (Passarelli et al. 2002).

Some information is taken from Richardson (1969: development of Brasenia flowers), Schneider and Jeter (1982: pollination of Cabomba), Williamson and Schneider (1993: general), Floyd and Friedman (2000: embryo sac), D. W. Taylor et al. (2001: fossils) and M. L. Taylor et al. (2008: esp. pollen).

Synonymy: Hydropeltidaceae Dumortier

NYMPHAEACEAE Salisbury   Back to Nymphaeales

Rhizomatous to tuberous perennials, stem not floating; a root arises below each leaf; myricetin, sesquiterpene [pseud]alkaloids, hydrolyzable [elagi-]tannins +; stem vascular tissue complex, (in concentric rings), axial bundles concentric; astrosclereids +; nodes 3:3; stipules adaxial or none; flowers and buds not in normal axillary position [often replace leaf in spiral], flowers large, C petaloid or not, (0- [some Ondinea])4-many, A often whorled, laminar, 3-veined, (filaments stout), connective produced or not, tapetum both glandular and amoeboid, microsporogenesis simultaneous, pollen trinucleate, ektexine homogeneous-granulate, (no exine), (endexine lamellate), staminodes inside (outside), G laterally connate only and floral axis often projecting in the middle, whorled, margin fusion also postgenital, (3-)many (atropous) ovules/carpel, outer integument variable, stigma dry; fruit baccate; (exotesta not palisade; anticlinal walls not sinuous); embryo green or white, plug-like, cotyledons basally connate or not.

Nymphaeaceae

3[list]/58. World-wide (Map: from Vester 1940; Wickens 1976; Hultén 1961; Heywood 2007; Wilson 2007). [Photo - Leaf, Flower.]

1. Nupharoideae Ito

Rhizomes stout, creeping; roots with 10-18 xylem poles, pith large; bracts +; K 5-14, spiral, nectary on abaxial surface of inner tepals [= petals], pollen spiny, G 5-23(-30); fruit emergent; n = 17.

1/ca 10. North Temperate.

Weberling (1989) describes how axial tissue separates from the gynoecium when the fruits are ripe, so exposing the basically free carpels; if this is correct (but it seems rather unlikely), the gynoecium of Nuphar would be very similar to that of other Nymphaeaceae.

2. Nymphaeoideae

Roots with 5-9 xylem poles, pith at most small; inner satellite peduncle bundle +; K 4-5, (C 0), staminodes showy, (larger peripheral A with three traces), pollen zonasulcate (inaperturate), surface various, G 3-many, more or less inferior [A alone on top of G, K and "C" also often on top; A also adnate to "C"], with inter-carpel septal slits, micropyle bistomal, (ovules straight [atropous] - Barclaya; outer integument to 20 cells across - Euryale), stigmatic surface continuous; fruit maturation underwater; seeds arillate (not, but spiny - Barclaya), (exotesta cells cuboid - Euryale); n = 10, 12, 14-18.

2/48: Nymphaea (46). World-wide.

In Euryale the filaments are quite slender and are basally adnate to the staminodes; it is unclear if it has free nuclear endosperm (Floyd & Friedman 2001). Dehiscence of the fruit is by swelling of the mucilage inside it, whereupon the wall splits irregularly.

The family was previously much more diverse and its first known fossil is from the Turonian (ca 90 million years before present: New Jersey, U.S.A.). Victoria has "paracarpels" immediately surrounding the gynoecium, and these are also found in the Turonian Microvictoria; indeed, this latter is like flowers of Victoria in almost all respects, except being less than 1/10th the size (Gandolfo et al. 2004, see also above, and for early Cretaceous nymphaeaceous flowers).

Thermogenesis has been detected in the flowers of some Nymphaeaceae (Seymour 2001).

Liu et al. (2005) provide an ITS phylogeny of the family, but with some rather surprising relationships - Nuphar [Cabomba + Brasenia] [Nymphaea [Euryale + Victoria]]. Nelumbo, which was included in the analysis, did at least stay outside this clade... For a phylogeny of Nymphaea, see Borsch et al. (2007); it definitely includes the wind-pollinated and usually apetalous Ondinea, but lacked much support. However, in a study with more complete sampling the results suggest that it seems very likely that the spiny Victoria and Euryale should also be included (as sister taxa - see LÖhne et al. 2007).

The root endodermis has a Casparian strip. There are sometimes sclerenchymatous diaphragms in the pith. The vasculature of the stem is exceedingly complex, especially at the node, with peduncular complexes forming internally, however, basic stem structure is unlike that of monocotyledons; the primary xylem is mesarch (Weidlich 1980 and references). The astrosclereids of Nuphar and Nymphaea, at least, have calcium oxalate crystals in the walls (Fink 1991). Stipules may be adaxial and bicarinate or paired and lateral. In both Nuphar and Nymphaea flowers and even branches may replace leaves in the genetic spiral (e.g. Groß et al. 2006); within the flowers themselves, however, parts are generally whorled (e.g. ). Weberling (1989) suggested that in at least some Nymphaeaceae the individual carpels were free laterally, if adnate to the central axis inside and to "hypanthial" tissue outside (see also von Balthazar et al. 2008). Zhou and Fu (2008) found that at anthesis, but not before or after, the micropyle of Nuphar was bistomal, not endostomal. The seedling axis of some species of Nymphaea have a lateral projection.

Some information is taken from Schneider and Williamson (1993: general); Takhtajan (1988) provides much information on ovules and seeds, Tillich (1990) on seedling morphology, Yao et al. (2004) some information on pollen morphology, and Schneider et al. (2008) on stem tracheids.

Synonymy: Barclayaceae (Endlicher) H.-L. Li, Euryalaceae J. Agardh, Nupharaceae A. Kerner