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, 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]; 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. The actual level at 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. 2009b for a discussion), it effectively makes the pollen morphology of the common ancestor of all angiosperms ambiguous... Ther are other features such as a nucellus only one (Nymphaeales) to three cells thick above the embryo sac and a stylar canal lacking an epidermal layer that appear to be plesiomorphous for basal grade angiosperms (Williams 2009), however, where on the tree a thicker nucellus and a stylar epidermal layer are acquired has not been indicated.

[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. Back to Main Tree

Evolution. Divergence & Distribution. A fossil-based estimate of the age of this node is ca 113 m.y. (Crepet et al. 2004), while Soltis et al. (2008: a variety of estimates) give an age of 180-132 m.y. Magallón and Castillo (2009) offer still other ages - ca 229 m.y. for relaxed and 127 m.y. for constrained penalized likelihood datings, while Moore et al. (2010: 95% HPD) suggest an age of (162-)155(-145) m.y., Clarke et al. (2011: 95% credibility intervals) ages of (231-)197(-169) m.y., towards the upper end of the various suggestions, N. Zhang et al. (2012) ages of (211-)179(-158) m.y., and Magallón et al. (2013) an age of around 183.4 m.y..

Presence of vessels is optimised here, however, given their distinctive morphology in at least some Nypmphaeales (Carlquist & Schneider 2009; Schneider & Carlquist 2009) and in Amborella (Feild et al. 2000b), they may have arisen three times in this part of the tree. Feild (2005) suggests that vessels may have evolved in plants growing in humid conditions, and Amborella, Gnetales and fossil groups with vessels have/may have been growing in such conditions. However, it would seem unlikely for vessels to have evolved in aquatics, and members of all three nymphaealean families have vessels in at least some parts of the plant. Sperry et al. (2007) discuss features of what they call "basal vessels"; these include little difference between pitting of the end and lateral walls, incomplete break-down of the pit membranes, etc. Bannan (1934) and Mauseth (2009) describe the major features of angiosperm and gymnosperm wood; despite lacking vessels, as in most gymnosperms, the wood of Amborella does have a small amount of parenchyma (Carlquist & Schneider 2001); it of course lacks bordered pits with margo-torus construction.

For discussion as to where characters of pollen morphology and development are to be placed on the tree, see Taylor and Osborn (2006) and also Friis et al. (2009b); it partly depends on how the characters are defined and partly on the recent discovery of fossil Nymphaeales that do not have the pollen characteristics of extant members of the clade.

Chemistry, Morphology, etc. 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. For embryo sac evolution, see Friedman and Ryerson (2009). For the possibility of a genome duplication at about this position, see Cui et al. (2006) and dePamphilis et al. (2009).

NYMPHAEALES Dumortier  Main Tree, Synapomorphies.

Aquatic herbs, plant rhizomatous; 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 vascular bundles; protoxylem lacunae +; vascular cambium 0; nodes?; aerenchyma common; stomata anomocytic; ?lamina margins, leaf base broad; bracts 0; pollen boat-shaped, tectum continuous; ovule with semi-annular [hood-shaped] outer integument; first division of endosperm transverse, chalazal cell undivided, ± enlarged and elongated, haustorial; P persistent; fruit maturation underwater; seeds exotestal, exotesta ± palisade, operculum +, operculum endotegmic [?all], hilum outside operculum; endosperm scanty, perisperm +, starchy, precocious, cells ± multinucleate, embryo broad, cotyledons connate; suspensor 0; germination hypogeal; intergenic inversion in chloroplast inverted repeat. - 3 families, 6 genera, 74 species.

Evolution. Divergence & Distribution. Magallón and Castillo (2009) suggested an age of ca 112 m.y. for the crown group.

Cretaceous fossils assignable to Nymphaeaceae are quite common, and it has been suggested that Nymphaeales were "the first globally diverse clade" (Borsch " Soltis 2008: p. 1051; see also Sender et al. 2010). They are a highly derived aquatic clade, so it is unclear to what extent Cabomba or any other member of the order can serve as a model for understanding early angiosperm evolution (c.f. Vialette-Guiraud et al. 2011).

The curious fossil Archaefructus, probably an aquatic plant and about 124 m.y. old, has been linked with Hydatellaceae in morphological analyses (Doyle & Endress 2007, 2010; Doyle 2008b). Although they have little in common in terms of overall appearance, Archaefructus may be another aquatic angiosperm with very unconventional floral morphology.

Saarela et al. (2007) suggest a few additional possible synapomorphies for Nymphaeales, and Borsch et al. (2007) discuss the evolution of a number of floral characters.

Chemistry, Morphology, etc. 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 vessel elements 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). For the distinctive single-celled chalazal haustorium, see Rudall et al. (2009b).

Phylogeny. 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 the distinctive 4-celled embryo sac of other Nymphaeales and Austrobaileyales.

Previous Relationships. 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, it makes them 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 (see above).

Includes Cabombaceae, Hydatellaceae, Nymphaeaceae.

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

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

Hydatellaceae

(Plant annual), growth sympodial, rhizome short, erect; chemistry?; mycorrhizae 0; vessels 0; cuticular waxes 0; leaves linear, with a single vein, margins entire; plant monoecious; inflorescence axillary, scapose (sessile), capitate, with involucral bracts; P 0; staminate flowers: A 1, filaments long, slender; endothecium 0; tapetal cells?; pollen with spinules; carpellate flowers: pedicel articulated; G 1, three vascular bundles equidistant (2, 1), stigma penicillate, of rows of plump cells; ovule 1/carpel, pendulous, anatropous, apotropous, micropyle bistomal, parietal tissue ca 2 cells across (?0), nucellar cap +/0; (two embryo sacs developing); fruit splitting into three valves or an achene; apart from exotesta, other layers ± collapsed, tanniniferous; embryo barely differentiated; n = ?; seedling - see below.

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

Evolution. Divergence & Distribution. The pollen fossils, Monosulcites riparius, from Eastern Siberia of ca 75-70 m.y. age have been identified as Trithuria, but the family may be represented in the pollen record from the Isle of Wight in rocks of some 130 m.y. of age (Hoffmann & Zetter 2010).

Pollination Biology & Seed Dispersal. For reproductive ecology - wind pollination, self pollination - see Taylor et al. (2010); the pollen tubes grow down the multicellular hairs under the cuticle (Prychid et al. 2011).

Chemistry, Morphology, etc. The sieve tube plastids were reported as having triangular proteinaceous inclusions, but these inclusions appear to be of the starchy type as are more to be expected in this part of the tree (Tratt et al. 2009). 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, 2009a). 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. Microsporogenesis may be simultaneous (Remizowa et al. 2008b). 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) compared it with that of a monocot, describing collar rhizoids, a coleoptile, two cotyledonary sheath lobes, and a haustorium. Sokoloff et al. (2008a) suggested that the sheathing structure with its bilobed apex that is found in some species could be interpreted as two, more or less completely connate cotyledons. The rest of the seed is attached to the sheathing structure, and a layer of endosperm is the intermediary between the embryo and perisperm (Friedman et al. 2012). In some taxa there is apparently no sheathing structure at all, only a lateral outgrowth (cotyledonary) that goes into the seed. Sokoloff et al. (2008a) suggested that Hydatellaceae showed how monocot-like embryos/seedlings might have originated. Both Tillich et al. (2007) and Sokoloff et al. (2008a) examined largely surface morphology, neither looked in any detail at anatomy (c.f. Friedman et al. 2012: superb micrographs). Tuckett et al. (2010: discussion of "ancestral" embryo type for angiosperms must include Amborellaceae, at least) found that differentiation of the embryo and appearance of the shoot and root occurred only after germination.

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), Remizova et al. (2008b: pollen), Friedman (2008a) and Rudall et al. (2008a), both embryology, Sokoloff et al. (2009a: growth patterns of the perennial species, 2013: fruit anatomy), Taylor et al. (2010: pollination) and Friedman et al. (2012: perisperm/endosperm interactions).

Classification. Sokoloff et al. (2008b) monographed the family.

Previous Relationships. Hydatellaceae have been considered to be monocots, albeit rather odd, and perhaps close to Poales-Centrolepidaceae (see above).

[Cabombaceae + Nymphaeaceae]: plant monopodial, rhizome/stolon elongated; hydroyzable [ellagi]tannins +; vessel elements in roots, with extensive fibrillar network in the end plates; pit membranes of tracheids with two thick layers of large fibrils; minute rhombic crystals on stellate cells [astrosclereids, stellate parenchyma cells]; leaves peltate, (divided), lamina vernation involute, secondary veins palmate, actinodromous, festoon brochidodromous, margin toothed, crenate or entire, (hydathodes +); flowers single; receptacle with cortical vascular system; P whorled, (outer [inner] whorls in 3's), outer members enclosing the rest of the bud; A whorled; tapetal cells multinucleate; pollen tube growth moderately fast; carpel margins with postgenital fusion, placentation ± laminar; parietal tissue ca 1 cell across; embryo sac very small relative to nucellus; mesocarp ± aerenchymatous; exotesta with anticlinal walls sinuous; embryo suspensor 0 [?level].

Evolution. Divergence & Distribution. There has been much discussion over the timing of diversification within the Cabombaceae-Nymphaeaceae clade (e.g. Nixon 2008). Early fossil-based estimates for the age of this group were only ca 90 m.y. (Crepet et al. 2004), but substantially earlier dates are likely (Friis et al. 2009b). Fossils assigned to Nymphaeaceae, Cabombaceae and/or stem-group Nymphaeales (i.e. Nymphaeaceae + Cabombaceae) are known from the Lower Cretaceous and from several parts of the world (e.g. D. W. Taylor et al. 2001, 2008). Although other fossils possibly of this group (to a certain extent characters of the two families are combined) are known from the Barremian-Aptian deposits 125-113 m.y.o. in Portugal (Friis et al. 2001), they may also be from a member of Austrobaileyales (Gandolfo et al. 2004); see also von Balthazar et al. (2008) for another fossil perhaps assignable to this general [Nymphaeales-Austrobaileyales] area.

Recently, fossils assignable to crown group Nymphaeaceae (as Jaguariba) found in the Aptian Crato flora, some 115 m.y.o. in northeast Brazil (Coiffard et al. 2013) while Pluricarpellatia, probably Cabombaceae, is known from the same rocks (Mohr et al. 2008). Morphological analyses placed the Early Cretaceous Monetanthus in an embedded position within Nymphaeaceae (Friis et al. 2009b). The distinctive reticulate-perforate pollen of Monetanthus would then be independently derived within Nymphaeales, but analyses also placed the genus at the node above Nymphaeales along the spine of the angiosperm tree (Friis et al. 2009b).

Dates from molecular analyses in part conflict strongly. Wikström et al. (2001) early suggested that divergence of the two families occurred 144-111 m.y.a. (details of relationships within the clade differ from those given here), and Magallón et al. (2013) suggested an age of around 122.7 m.y.. However, Löhne et al. (2008) thought that divergence was only Palaeocene in age, (75-)56.4(-38) m.y.a., while Yoo et al. (2005) offered a still younger date, pegging the crown group age to only 44.6 ± 7.9 m.y.; the fossil Microvictoria was perhaps stem group Nymphaeales (c.f. Gandolfo et al. 2004).

Nymphaeales, along with other angiosperms, may have dominated aquatic habitats in Europe by the Albian ca 105 m.y.a. (Sender et al. 2010). D. W. Taylor et al. (2008, see also Taylor 2008) discuss the vegetative evolution of the group (see some of the characters above). They noted how inclusion of different fossils affected relationships, and hence evolutionary interpretations, in analyses of morphological variation.

Chemistry, Morphology, etc. For micromorphological details of vessels and tracheids, see Carlquist and Schneider (2009) and Schneider et al. (2009); details of the wall structure of tracheids, at least, are very distinctive. Note that Carpenter (2005) described stomata as being largely variants of the actino/stephanocytic types; only one member of Cabombaceae was studied. Taylor (2008) outlined the vegetative morphology of this clade; Nymphaea s. str. appeared as monophyletic in a phylogenetic analysis of these characters, but without much support. Warner et al. (2008) discuss perianth evolution; they provide a useful summary on the literature on perianth morphology.

For information on anatomy, see Gwynne-Vaughan (1897), for root epidermis, see Voronkina (1974: ordinal characterisation above), for perianth venation, see Hiepko (1965b), 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), for more on vessels and tracheids, see Schneider and Carlquist (2009a, b), for tapetum development, see Taylor et al. (2012), for pericarp anatomy, Yatzenko et al. (2012), and for general information, Les et al. (1999) and Schneider et al (2003).

CABOMBACEAE A. Richard   Back to Nymphaeales

Cabombaceae

Plant floating, rhizome/stem horizontal; alkaloids 0; stem vascular tissue with two pairs of bundles; internodes long; (leaves opposite), (lamina with semidichotomous venation); flowers rather small, parts whorled, (2)3(4)-merous; P two-whorled, tepaloid, hexamerous, members with single trace, (inner whorl somewhat delayed in development, with nectaries - Cabomba); A (3, 6), extrorse to latrorse, filaments moderately slender; tapetum more or less amoeboid; pollen (trichotomocolpate, tectum continuous, striate - Cabomba), endexine lamellate when young, not when mature; G (1-)3-18(-22), when 3 or more, inner whorl of three ± opposite petals, three vascular bundles equidistant, stylar neck +, stigma terminal, capitate, (elongate - Brasenia); ovules 1-3(-5)/carpel, attached variously, outer integument semi-annular [hood-shaped], nucellar epidermal cells ± radially elongated, hypostase +; fruits follicles or achenes; hilum and micropyle sharing same opening in center of operculum; endosperm helobial [micropylar cell alone with free-nuclear division]; n = 40, 48, 52; germination?.

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; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003, 6. 2011; Löhne et al. 2008). [Photo - Brasenia Habit] [Photo - Flower.]

Evolution. Divergence & Distribution. Pluricarpellatia, probably Cabombaceae, is known from rocks 115 m.y.o. in northeast Brazil (Mohr et al. 2008).

Pollination Biology & Seed Dispersal. Brasenia is wind pollinated, while Cabomba has paired nectaries on its inner tepals and is pollinated by flies; Taylor and Williams (2009) describe details of reproduction from pollination to fertlization in considerable detail.

Chemistry, Morphology, etc. 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. The peltate leaves are spirally arranged, 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). Stamens are sometimes physically close to each nectary and then they appear paired (Ørgaard et al. 1992). 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 Khanna (1965) and Batygina et al. (1982), both embryology, Richardson (1969: development of Brasenia flowers), Schneider and Jeter (1982: pollination of Cabomba), Williamson and Schneider (1993: general), Floyd and Friedman (2000: endosperm development), D. W. Taylor et al. (2001: fossils) and M. L. Taylor et al. (2008: esp. pollen).

Synonymy: Hydropeltidaceae Dumortier

NYMPHAEACEAE Salisbury   Back to Nymphaeales

Nymphaeaceae

Perennials (annuals); myricetin, sesquiterpene [pseud]alkaloids; a root arises below each leaf; stem vascular tissue complex, (in concentric rings), axial bundles concentric; astrosclereids +; nodes 3:3; flowers neither terminal nor axillary [often replace leaf in spiral]; flowers large, haplomorphic; P members usu. with sepaloid and petal-like areas, (0- [some Ondinea])4-many; A many, often whorled, laminar, staminodes +, next to G (also next to P), (filaments stout), connective produced or not; tapetum both glandular and amoeboid; microsporogenesis simultaneous, pollen trinucleate, (zona-aperturate), ektexine homogeneous-granulate, (no exine), (endexine lamellate); G laterally connate only, whorled, margin fusion also postgenital, stigma dry; ovules (3-)many/carpel, not filling the locule, (straight), outer integument also cap-shaped [annular]; fruit baccate; (exotesta not palisade; anticlinal walls not sinuous); endosperm scanty, embryo green or white, plug-like, (large).

3[list]/58. World-wide (map: from Vester 1940; Wickens 1976; Hultén 1961; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Heywood 2007; Löhne et al. 2008). [Photo - Leaf, Flower.]

1. Nupharoideae Ito

Rhizomes stout, horizontal, creeping; indolizidine alkaloids +; roots with 10-18 xylem poles, pith large; bracts +; P members 1-veined, K 5-14, spiral, outer greenish, inner coloured, inner tepals many, small, petal-like, somewhat delayed in development; nectary on abaxial surface of inner tepals; pollen trinucleate, spiny, tectum continuous; G 5-23(-36); outer integument 4-6 cells across, parietal tissue ca 2 cells across, nucellar cap ca 4 cells across, hypostase, postament +; fruit emergent; n = 17.

1/11. North Temperate.

Synonymy: Nupharaceae A. Kerner

2. Nymphaeoideae

(Rhizome short, erect); roots with 5-9 xylem poles, pith at most small; vegetative buds not axillary; stipules +, adaxial or lateral; inner satellite peduncle bundle +; bracts 0; hypanthium ± developed; P members 3-veined, K 4-5, spiral, (C 0); staminodes showy, (larger peripheral A with three traces); pollen (trinucleate), with encircling sulcus (inaperturate), surface various, inc. tectum continuous; 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, floral axis projecting in the middle [not Barclaya], stigmatic surface continuous, extragynoecial compitum +; ovules (straight - Barclaya), (micropyle bistomal), (outer integument to 20 cells across - Euryale), (parietal tissue 3-4 cells across - Victoria); seeds arillate (not, but spiny - Barclaya), (exotesta cells cuboid - Euryale); n = 10, 12, 14-18.

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

Synonymy: Barclayaceae H.-L. Li, Euryalaceae J. Agardh

Evolution. Divergence & Distribution. The family is thought to have been much more diverse in earlier epochs, with distinctive seeds with a micropylar and palisade exotesta with sinuous anticlinal walls that can be assigned here being common in the Cretaceous (Friis et al. 2009b for references). The Late Aptian/Early Albian Cretaceous Monetianthus, from Portugal, is embedded in Nymphaeaceae in morphological analyses (Friis et al. 2009b). Microvictoria, a somewhat later fossil from the Turonian ca 90 m.y. old and found in New Jersey, U.S.A., is very like Victoria (= Nymphaea). Victoria has "paracarpels" immediately surrounding the gynoecium, and these are also found in Microvictoria; indeed, flowers of this latter are like those of Victoria in almost all respects, although they are less than 1/10th their size (Gandolfo et al. 2004). Jaguariba is assignable to crown group Nymphaeaceae; it is from the Aptian Crato flora of northeast Brazil and is some 115 m.y.o. (Coiffard et al. 2013). Schneider et al. (2004) suggested an age for the family of ca 121 m.y.

Although the family is widespread and probably very old, individual clades within it are relatively localized, and crown group diversification may have occurred in the northern hemisphere as late as the early Tertiary (Löhne et al. 2008); Magallón et al. (2013), however, suggested a crown-group age of around 100.1 m.y..

Plant-Animal Interactions. Nymphaeaceae are host plants of reed beetles, Chrysomelidae-Donaciinae (see also Poales: Kölsch & Pedersen 2008: much discussion on the age and evolution of the group). Interestingly, Enterobacteriaceae near Buchnera are believed to produce the material that makes up the cocoon that characterises Donaciinae, a group that is also noted for the ability of the larvae to grow under water (Kölsch & Pedersen 2010).

Pollination Biology & Seed Dispersal. Thermogenesis has been detected in the flowers of some Nymphaeaceae (Seymour 2001; Seymour & Matthews 2006). Beetles and a variety of other insects may be pollinators (e.g. see Padgett 2007). Scarab beetles (Cyclocephalini) may have pollinated night-flowering water lilies for some 100 m.y., pollinating species both in America, where the beetles are common, and in Africa, where the beetles are otherwise very uncommon (Ervik & Knudsen 2003). The distinctive flowers of Ondinea, wind pollinated, are derived from Nymphaea-type flowers (Löhne et al. 2009). Schneider (1979) summarizes information about the pollination biology of the family.

The progamic phase, the time between pollination and fertilization, is notably short, up to a mere 8 hours, as in at least some other aquatic angiosperms (including Nelumbo: see Williams et al. 2010).

Dehiscence of the fruit of Nymphaeaoideae is by swelling of the mucilage inside it, whereupon the wall splits irregularly.

Chemistry, Morphology, etc. 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). Schneider et al. (2008, 2009) and Schneider and Carlquist (2009) discuss stem tracheids and root vessels, emphasizing the rather arbitrary distinction between vessels and tracheids; Carlquist (2012c) suggested that there were no vessels. 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. Cutter 1957a, b; Groß et al. 2006). Cutter (1957b) noted that the leaf apparently subtending the flower of Nuphar was in fact born on the flower stalk; if a prophyll, it should be noted that it is abaxial in position!

Flower parts are generally whorled (e.g. ). Yoo et al. (2010) discuss the evolutionary/developmental relationship between sepals and petals; see also Doyle and Endress (2011), who suggest that Nuphar has both tepals and petals. Schneider (1976) and Moseley and Uhl (1985) note that the vascular suppy to perianth and androecial members consists of two radially associated bundles. 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 - see also Kanna 1964, 1967 for endosperm development in the family). 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. Weberling (1989) also described how in Nuphar 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), its gynoecium would be very similar to that of other Nymphaeaceae; Padgett (2007) described dehiscence as being along lines in the septal and ovarian walls where aerenchymatous tissue had developed. 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, Khanna (1964, 1967) described embryology (8-nucleate embryo sacs...), Tillich (1990) information on seedling morphology, Shamrov (1998) on the ovule of Nuphar, Floyd and Friedman (2001) on endosperm development, and Yao et al. (2004) some information on pollen morphology.

Phylogeny. 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, 2012); the genus definitely includes the wind-pollinated and usually apetalous Ondinea, but some relationships lacked much support, e.g. the position of [Euryale + Victoria] as sister to Nymphaea s.l. However, in some studies the spiny Victoria and Euryale are embedded in Nymphaea s.l., as of course is Ondinea (Löhne et al. 2007, 2009; Borsch et al. 2008).

Taxonomy. For a revision of Nuphar, see Padgett (2007).