EXTANT SEED PLANTS

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 rich in guaiacyl units; true roots present, apex multicellular, xylem exarch, 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 +; 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 mm/mm² [mean for all non-angiosperms 1.8]; 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, 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 [N/O//A/C and P//BE lines], 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 in 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 a sieve plate and cytoplasm with P-proteins, companion cells from same mother cell that gave rise to the sieve tube; nodes unilacunar [1:?]; stomata with ends of guard cells level with pore, paracytic, outer stomatal ledges producing vestibule; leaves with petiole and lamina [the latter 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; flowers perfect, polysymmetric, parts spiral [esp. the A], free, development in general centripetal, numbers unstable; P not sharply 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, ektexine columellar, endexine thin, compact, lamellate only in the apertural regions; 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 four-celled [one-modular, nucleus of egg cell sister to one of the polar nuclei], stylulus short, hollow, stigma ± decurrent, dry [not secretory]; P deciduous in fruit; seed exotestal; 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; 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, minute; 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 + C/PHYB + E gene pairs.

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, because some taxa basal to the [magnoliid + monocot + eudicot] group have been surprisingly little studied, there is considerable variation between families 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....

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

ERICALES [ASTERID I + II]: ovules tenuinucellate.

ASTERID I + II: Ellagic acid 0, proanthocyanidins not common; inflorescence cymose; C forming a distinct tube; A epipetalous, = and opposite sepals or P [polyandry (secondary) very uncommon indeed].

ASTERID II Back to Main Tree

Myricetin 0; vessel elements with scalariform perforation plates; flowers rather small, style short; endosperm copious, embryo short/very short.

Chemistry, Morphology, etc. Another synapomorphy for the asterid II clade may be a valvate corolla. The feature "small(!) flowers" may be assignable to the asterid node, since the first nodes of both the asterid I and II clades may have this feature, but I have tentatively assigned it to this node. The asterid II clade as a whole certainly has many taxa with small flowers (but cf. Campanulaceae, etc.) that are often aggregated into conspicuous inflorescences, and the fruits have few seeds; the apices of the petals tend to be pointed.

Phylogeny. Within the asterid II clade there is moderate (Olmstead et al. 2000; Soltis et al. 2000) to strong (B. Bremer et al. 2002; Janssens et al. 2009) support for Aquifoliales as being sister to the rest, and then Asterales may be sister to Apiales + Dipsacales (e.g. Olmstead et al. 2000; Lens et al. 2008a). Note, however, that studies on the duplication of the RPB2 gene suggest a relationship between the asterid I clade and Aquifoliaceae in particular (Oxelman et al. 2004b), and Aquifoliaceae also seem to lack the PI duplication of other members of the asterid I + II clade (Viaene et al. 2009), so the other Aquifoliales may need to be sampled. A relationship between Apiales and Dipsacales has quite often been suggested, as by Nandi et al. (1998), Lundberg (2001c), Winkworth et al. (2008), etc.

Recent work is clarifying relationships within the whole clade (as the Campanulid clade, see Winkworth et al. 2008a). The basic relationships are [Asterales [Apiales + Dipsacales]], Aquifoliales being the out-group, although with little support in analyses of non-coding chloroplast genes. Paracryphiaceae, Quintiniaceae and relatives (only Paracryphia and Quintinia were studied) are probably sister to Dipsacales, although not in analyses that included coding chloroplast genes (Winkworth et al. 2008a). Bruniaceae are sister to [Columelliaceae + Desfontainiaceae], although not in analyses of non-coding chloroplast sequences, and in turn may be associated with Escalloniaceae and Asterales. Janssens et al. (2009: two genes) found weak support for a [Dipsacales [Asterales + Apiales]] set of relationships. Analyses by Tank and Donoghue (2009) suggest the relationships followed here, although the position of Escalloniales is still rather poorly supported.

Classification. This group is also called campanulids (B. Bremer et al. 2002).

AQUIFOLIALES Senft  Main Tree, Synapomorphies.

Iridoids?; petiole bundles arcuate; C valvate, free, ?development; A free from P/C, ?disc, 1-2 apical apotropous ovules/carpel; fruit a drupe, stones one-seeded. - 5 families, 21 genera, 536 species.

Evolution. Janssens et al. (2009) date stem group Aquifoliales to 113±9.8 million years ago.

Chemistry, Morphology, etc. With the partial exception of Aquifoliaceae, embryology, testa anatomy, and chemistry of this order are little known, and the polarity of features for and within the order is very unclear.

Phylogeny Aquifoliaceae were included in Asteridae II by Gustafsson et al. (1996) and B. Bremer (1996). rbcL and other data suggested the following relationships: Phyllonoma (Hellwingia + Ilex) (Morgan & Soltis 1993; see also Soltis & Soltis 1997; Olmstead et al. 2000; Kårehed 2002b; Whitworth et al. 2008). It seemed a little odd that there was little evidence that the two taxa with epiphyllous inflorescences form a monophyletic clade - they also have fimbriate stipules, brochidodromous venation, absence of hairs, etc., in common - but recent comprehensive analyses of the asterid II clade (Tank et al. 2007) recovered a sister group relationship (1.0 p.p.). Irvingbaileya + Gomphandra were placed with strong support in Aquifoliales (D. Soltis et al. 2000), and the group expanded by Kårehed (2001). Cardiopteridaceae are sister to Stemonuraceae, in turn sister to Ilex (one species!), Phyllonoma and Helwingia, with very strong support for this basic structure (Kårehed 2001 - see tree). The grouping (Cardiopteridaceae + Pentaphylacaceae) had weak support in a single gene analysis (Savolainen et al. 2000b); for the latter family, see Ericales.

Includes Aquifoliaceae, Cardiopteridaceae, Helwingiaceae, Phyllonomaceae, Stemonuraceae.

Synonymy: Cardiopteridales Takhtajan, Helwingiales Takhtajan, Ilicales Brongniart

Cardiopteridaceae + Stemonuraceae: Vessel elements with simple and scalariform perforation plates; pits usually not bordered; apotracheal parenchyma and variants common; (crystal sand in wood rays); nodes 3:3; stomata cyclocytic to anisocytic; hairs unicellular (adpressed); leaves two-ranked or spiral, margins entire; (plant dioecious); petals inflexed at apex, (ridged adaxially); A basifixed; G [?2], unilocular, with 2 apical crassinucellate ovules, funicular obturator +; fruit a 1-seeded drupe (pseudoloculus +); testa vascularised; embryo very short.

Chemistry, Morphology, etc. For other information, see Bailey and Howard (1941, their group II: anatomy), Fagerlind (1945: embryology), Heintzelmann and Howard (1948), Padmanabhan (1961: embryology), Sleumer (1971a: general), van Staveren and Baas (1973: epidermis), Baas (1973: epidermis, 1974: stomata), Lobreau-Callen (1980: pollen), Kaplan et al. (1991: chemistry), Teo and Haron (1999: anatomy). Kårehed (2001, 2002b) discusses the taxa in their current circumscriptions, while Lens et al. (2008a) provide a detailed anatomical survey in a phylogenetic context.

Classification. These two families have quite a lot in common, however, Kårehed (2002c) recognised them as separate.

Previous Relationships. For the other genera that were until recently included in Icacinaceae s.l., see Icacinaceae themselves and relatives (near Garryales) and Pennatiaceae (Apiales).

CARDIOPTERIDACEAE Blume, nom. cons.   Back to Aquifoliales

(Twining vine); plants Al accumulators [?all], iridoids?; (vessel elements with scalariform perforation plates only); petiole bundles annular (+ medullary); (articulated laticifers + - Cardiopteris); stomata also anomocytic and paracytic; (leaves toothed; 2ndary veins palmate); (plant dioecious, andromonoecious), (inflorescence branched, ultimate units clearly cymose or not), (bracts 0); K, C usu. ± connate, (C imbricate); A often adnate to C, also dorsifixed, disc 0 (+), (ovule 1), style usu. slender, stigma truncate or capitate, (styles 2, heteromorphic, one stout, lobed and grooved, the other slender, with capitate stigma – Cardiopteris); (pseudoloculus - Pseudobotrys, Citronella); (fruit 2-winged samara, wings horizontally striate, stout style accrescent – Cardiopteris); endosperm ?development, (ruminate; embryo long, with foliaceous cotyledons); n = 14 [Leptaulus].

5(?6)[list]/43(45): Citronella (21). Tropics, inc. the Pacific, to Taiwan (map: from Sleumer 1971a, c; Utteridge & Brummitt 2007).

·        Cardiopteridaceae are a rather heterogeneous group of genera, although one or sometimes two rather slender styles are usually evident. The fruits are more or less flattened and/or ridged drupes.

Chemistry, Morphology, etc. Cardiopteris itself looks rather like Dioscorea, but the latter has three-merous flowers and an inferior ovary. Leptaulus has a violet-colored flavonoid; in L. daphnoides the shoot apex aborts. Kong et al. (2002) described the ovules of Cardiopteris as being ategmic, straight, tenuinucellate and with the egg at the chalazal end; the ovules may in fact be anatropous.

For additional literature, see above, also Lobreau-Callen (1982 - pollen, Peripterygium), and Vera-Caletti and Wendt (2001).

Previous Relationships The relationships of Cardiopteris itself were previously obscure. It was included in Celastrales by Cronquist (1981), near there by Takhtajan (1997), and placed as sister to Pentaphylacaceae (Ericales), but with weak support, by Savolainen et al. (2000b).

Synonymy: Leptaulaceae van Tieghem, Peripterygiaceae F. Williams

STEMONURACEAE Kårehed   Back to Aquifoliales

Iridoids +; petiole bundles arcuate + wing or annular + medullary; sclereids +/0; plant dioecious (flowers perfect), pedicels articulated; flowers 4-5(-7) merous; K ± connate, (C connate; keeled), nectary (semi)annular (0), staminate flowers: filaments often stout and with club-shaped hairs, connective well developed, tapetum multinucleate, pollen usu. colpate or 2-6 porate, pistillode +; carpellate flowers: staminodes +/0, style 0, stigma broad; drupe compressed dorsi-ventrally (rounded), often sulcate, the two sides sometimes very different and one with a fleshy "appendage" developing over the sulcus, (pseudoloculus – Cantleya), endocarp with ridges and grooves on the side of the appendage, when present; testa thick, outer cells thick-walled, elongate, inner cells not thickened, post-chalazal bundle +; endosperm free-nuclear; n = 22. ILLUSTRATION.

12[list]/95: Gomphandra (55), Stemonurus (15). Tropics, esp. Indo-Malesia to Australia (Queensland) (map: from Sleumer 1971a; Utteridge & Brummitt 2007).

• Stemonuraceae are woody plants whose entire, exstipulate leaves can lack much in the way of venation when dry. The flowers are rather small and are borne in cymose inflorescences; the usually free petals are inflexed at the apex, stout filaments are often conspicuously hairy, the broad stigma is sessile, and the gynoecium appears to have a single carpel. The fruit is a more or less flattened and ridged drupe with one side sometimes very different in appearance, both in colour and texture, from the other, as in Medusanthera.

Chemistry, Morphology, etc. Schori et al. (2009) discuss fruit variation in the family; for additional literature, see above. I am grateful to Melanie Schori for comments.

Phylogeny. Note that Lasianthera, with colporate pollen, is sister to the other Stemonuraceae, but only five genera were sampled (Kårehed 2001). Still…

Aquifoliaceae [Phyllonomaceae + Helwingiaceae]: nodes 1:1; petiole bundle arcuate; leaves spiral, lamina margins toothed, stipules +, small, cauline; drupe with separate pyrenes.

Evolution. Janssens et al. (2009) dated the crown group in this part of Aquifoliales to 62±11.9 million years.

AQUIFOLIACEAE A. Richard, nom. cons.   Back to Aquifoliales

Evergreen (deciduous) trees or shrubs (climbers); tanniniferous, iridoids 0; resiniferous, laticiferous idioblasts +; nodes also 3:3, etc.; petiole bundles arcuate to annular and complex; branching from previous flush; (leaves opposite; two-ranked), supervolute (conduplicate), teeth with single vein and opaque, glandular deciduous apex (margins entire; stipules 0); plants often dioecious; flowers 4-9-merous, C imbricate, often connate basally, nectaries at base; A adnate to base of C (free), pollen conspicuously gemmate/clavate; G [(2-)4-6(-many)], opposite petals, placentation axile basally, becoming free-central, 1 (2) crassi(tenui)nucellate ovules/carpel, papillate funicular obturator + (0), stigma broad, wet; stones several, stigma prominent, K deciduous (semipersistent); exotestal cells cuboid, tangentially elongated, inner walls lignified, rest crushed, endotesta tanniniferous; endosperm hemicellulosic; n = 9, 10; mitochondrial coxII.i3 intron 0.

1[list]/405: Ilex. ± World-wide, esp. America and South East Asia-Malesia, one species in Africa (map: see Meusel et al. 1978; Loiseau et al. 2005). [Photo - Staminate Flower, Carpellate Flower.]

• The family may be recognised by its usually spiral, toothed leaves which may have small cork-warts on the lower surface of the lamina; the stipules are minute and blackish. The inflorescence is cymose and frequently subumbellate. The fruits often dry broadly bottle-shaped, being capped by the distinctive, sessile, broad, black stigma; there are several stones.

Evolution. The distinctive pollen is known from Turonian deposits ca 80 million years before present in S.E. Australia (Martin 1977; Loizeau et al. 2005).

Chemistry, Morphology, etc. Pallisade glandular tissues with protein rich secretions are found on the leaf teeth and stipules; the latter have been called colleters as a result (Gonzalez & Tarragó 2009). Spiral strands may join the two halves of a tranversely-torn leaf. The integument is about 15 cells across (van Tieghem 1898). The embryo is often minute and barely developed when the fruit is dispersed, only slowly maturing afterwards (Herr 1965, for references).

See Baas (1975) for vegetative anatomy, Martin (1977) for pollen, and Galle (1997) for an account of the cultivated members of the family.

Phylogeny. Cuénoud et al. (2000) found several clades correlating with geography/morphology in their study of Ilex s. str., however, support for some was weak; Ilex canariensis was not associated with any of these clades. However, a South American group may be sister to the rest of the genus, including that species (Selbach-Schnadelbach et al. 2009). The erstwhile genus Nemopanthus is deeply embedded in Ilex (Powell et al. 2000).

Previous Relationships. Phelline and Sphenostemon have sometimes been included in Aquifoliaceae (e.g. Mabberley 1997), but are here recognised as a separate family in Asterales (Phellinaceae) while Sphenostemon is in Paracryphiaceae (Paracryphiales).

Synonymy: Ilicaceae Berchtold & J. S. Presl

Phyllonomaceae + Helwingiaceae: hairs 0; lamina with brochidodromous venation, stipules fimbriate; inflorescence epiphyllous, on adaxial side of lamina.

PHYLLONOMACEAE Small   Back to Aquifoliales

Trees or shrubs; plants Al accumulators; cork ?; young stem with separate bundles; petiole bundle annular; plant glabrous, leaves ?two-ranked; inflorescences usu. branched; flowers perfect; K 4-5, open, C 3-5; G [2], inferior, nectary +, placentation parietal, many ovules/carpel, stigmas recurved; fruit a few-seeded berry; testa multilayered, exotestal cells large, thick-walled, mucilaginous, 2-3 layers of flattened cells; endosperm hemicellulosic; n = ?

1/4. Mexico to Peru (map: see Mori & Kallunki 1977). [Photo - Leaves, Flowers]

• Phyllonomaceae are shrubs or small trees that may be recognised by their leaves which have epiphyllous inflorescences borne on the upper surface of the lamina towards the apex; the stipules are minute. The ovary is inferior and has a prominent nectariferous disc on top; the baccate fruit contains only a few seeds.

Although the inflorescence of Phyllonoma has been described as being "truly phyllogenous", it appears to be produced from a displaced axillary shoot, as in Helwingia (Weber 2004c, and references).

Krach (1977) suggested that the seeds of Phyllonoma and those of Grossulariaceae were similar. Phyllonoma was included in Grossulariaceae by Cronquist (1981), and as Phyllonomaceae, in Hydrangeales, by Takhtajan (1997).

See Thouvenin (1890) and Dickinson and Sattler (1974) for inflorescence and general information, Krach (1976) and Takhtajan (2000) for seed anatomy, Mori and Kallunki (1977) for a revision.

Synonymy: Dulongiaceae J. G. Agardh, nom. illeg.

HELWINGIACEAE Decaisne   Back to Aquifoliales

Trees or shrubs; flavones, chlorogenic acid, unidentified iridoids +; cork?; cuticle wax crystalloids 0; leaf ptyxis supervolute-curved; plant dioecious, inflorescence fasciculate; P 3-5, valvate; staminate flowers: stamens = and alternating with P, pollen with diffuse endoapertures; carpellate flowers: staminodes 0, G [2-4], alternating with P, one incompletely tenuinucellate ovule/carpel, stigma dry; stones few; testa thin; endosperm weakly ruminate, ?development; n = 19.

1/3. Himalayas to Japan (map: from Hara 1972). [Photo - Fruit]

• Helwingiaceae are evergreen shrubs or small trees that may be recognised by their leaves which have epiphyllous fasciculate inflorescences on the upper surface of the blade; the stipules are small and fimbriate. The flowers have only a single perianth whorl, the ovary is superior, and the fruit is a drupe.

Chemistry, Morphology, etc. The fasciculate inflorescence is clearly cymose (Weber 2004c). Helwingiaceae may be interpreted as lacking a calyx, and so anthers and corolla alternate (Takhtajan 1997); however, external morphology shows no trace of a missing calyx, so is the corolla absent (the interpretation prefered here)? The carpel ventral bundles are central.

Previous Relationships. Helwingiales were included in Aralianae by Takhtajan (1997); Helwingia was included in Cornaceae by Cronquist (1981) and Mabberley (1997 - but with hesitation).

For chemistry, see Iwashina et al. (1997), for embryo and seed, see Korobova (1980), while some other information is taken from Horne (1914), Dickinson and Sattler (1975) and Hara and Kurosawa (1975: revision).