LIGNOPHYTA

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

EXTANT SEED PLANTS/SPERMATOPHYTA

Plant woody, evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins derived from (some) sinapyl and particularly coniferyl alcohols, thus containing p-hydroxyphenyl and guaiacyl lignin units, (lignins derived from p-coumaryl alcohol, i.e. S [syringyl] lignin units); true roots present, apex multicellular, xylem exarch, and branching endogenous; arbuscular mycorrhizae +; shoot apical meristem multicellular, interface specific plasmodesmatal network; stem with ectophloic eustele, endodermis 0, xylem endarch, branching exogenous; vascular tissue in t.s. discontinuous by interfascicular regions; vascular cambium + [xylem ("wood") differentiating internally, phloem externally]; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, plastids with starch grains; phloem fibres +; stem cork cambium superficial, root cork cambium deep seated; leaves with single trace from sympodium ["nodes 1:1"]; stomata ?; leaf vascular bundles collateral; leaves megaphyllous [determinancy evolved first, then ad/abaxial symmetry], spiral, simple, lamina with vein density up to 5 mm/mm² [mean for all non-angiosperms 1.8]; axillary buds associated with at most some leaves; prophylls [including bracteoles] two, lateral; plant heterosporous, sporangia eusporangiate, on sporophylls, sporophylls aggregated in indeterminate cones/strobili; true pollen [microspores, i.e. no distal pore for release of gametes] +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, crassinucellate, megaspore tetrad tetrahedral, only one megaspore develops, megasporangium indehiscent; male gametophyte development first endo- then exosporic, tube developing from distal end of grain, to ca 2 mm from receptive surface to egg, gametes two, developing after pollination, with cell walls, with many flagellae; female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large", first cell wall of zygote transverse, embryo straight, endoscopic [suspensor +], short-minute, with morphological dormancy, white, cotyledons 2; plastid transmission maternal; two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], nrDNA with 5.8S and 5S rDNA in separate clusters; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.

MAGNOLIOPHYTA

Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, non-hydrolysable tannins, quercetin and/or kaempferol +, apigenin and/or luteolin scattered, [cyanogenesis in ANITA grade?], S [syringyl] lignin units common, positive Maüle reaction [syringyl:guaiacyl ratio more than 2-2.5:1], and hemicelluloses as xyloglucans; root apical meristem intermediate-open; root vascular tissue oligarch [di- to pentarch], lateral roots arise opposite or immediately to the side of [when diarch] xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, with gelatinous fibres; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, cytoplasm not occluding pores of sieve plate, companion cells from same mother cell that gave rise to the sieve tube; sugar transport in phloem passive; nodes unilacunar [1:?]; stomata with ends of guard cells level with pore, paracytic, outer stomatal ledges producing vestibule; leaves petiolate, lamina [formed from the primordial leaf apex], development of venation acropetal, 2ndary veins pinnate, fine venation reticulate, veins (1.7-)4.1(-5.7) mm/mm², endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, polysymmetric, parts spiral [esp. the A], free, numbers unstable, development in general centripetal; P not sharply differentiated, with a single trace, outer members not enclosing the rest of the bud, often smaller than inner members; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], ± embedded in the filament, with at least outer secondary parietal cells dividing, each theca dehiscing longitudinally by action of hypodermal endothecium, endothecial cells elongated at right angles to long axis of anther; tapetum glandular, binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellar, endexine thin, compact, lamellate only in the apertural regions; nectary 0; G free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, dry [not secretory]; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across [crassinucellate], nucellar cap?; megasporocyte single, hypodermal, megaspore tetrad linear, functional megaspore chalazal, lacking sporopollenin and cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; P deciduous in fruit; seed exotestal; pollen binucleate at dispersal, trinucleate eventually, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing at 80-600 µm/hour, with pectic outer wall, callose inner wall and callose plugs, growing between cells, penetration of ovules via micropyle [porogamous] within ca 18 hours, distance to first ovule 1.1.-2.1 mm, tube moves between nucellar cells; double fertilisation +, endosperm diploid, cellular [micropylar and chalazal domains develop diffently, first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous, embryo cellular ab initio, minute; germination hypogeal, seedlings/young plants sympodial; Arabidopsis-type telomeres [(TTTAGGG)_n]; whole genome duplication, ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, paleo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]].

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

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

[PROTEALES [TROCHODENDRALES [BUXALES + CORE EUDICOTS]]]: (axial/receptacular nectary +).

[TROCHODENDRALES [BUXALES + CORE EUDICOTS]]: benzylisoquinoline alkaloids 0; euAP3 + TM6 genes [duplication of paleoAP3 gene: B class], mitochondrial rps2 gene lost.

[BUXALES + CORE EUDICOTS]: ?

Evolution. Divergence & Distribution. Estimates of the age of divergence within this clade (as [Proteales [Sabiales, Buxales [ Trochodendrales....]) range from (145-)134, 121(-116) million years (Bell et al. 2010 for details).

Chemistry, Morphology, etc. For the loss of the rps2 mitochondrial gene, see Adams et al. (2002b), for duplication of the paleoAP3 gene, see Kramer et al. 2006), also the Trochodendrales page.

BUXALES Reveal  Main Tree, Synapomorphies.

Steroidal pregnan pseudoalkaloids +; true tracheids +; compression wood +; ?nodes; stomata cyclocytic; lamina margins entire; inflorescence racemose; flowers small, imperfect; anthers ± dorsifixed; pollen also with endoapertures; styles stigmatic their entire length, with two crests; micropyle bistomal; seed testal, with several cell layers; endosperm development?, embryo size? - 2 families, 5 genera, 72 species.

Evolution. Divergence & Distribution. Stem group Buxales date to 121-117 million years before present (Anderson et al. 2005); Magallón and Castillo (2009: relaxed and constrained penalized likelihood estimates) suggest ages of ca 121.2 and 121.9 million years for the stem group and about 111.2 and 112.9 million years for the crown group.

Chemistry, Morphology, etc. The stomata of Buxaceae, at least, may be described as being laterocytic (Baranova 1983).

Phylogeny. For discussion on the phylogenetic position of Buxales, see the Ranuculales page. Didymelaceae are sister to Buxaceae (representatives of both tribes were included) in the three-gene analysis of Worberg et al. (2007), although Hilu et al. (2003: matK [incomplete sequence] alone) found Didymeles to be embedded in a paraphyletic Buxaceae. Including Didymelaceae in Buxaceae was an option in A.P.G. II (2003). The poorly-known Haptanthaceae was tentatively included in Buxales in early (pre March 2011) versions of the site based on the anatomy of the male flower (Doust & Stevens 200), but a position in Buxaceae sister to Buxus was strongly suggested by analysis of data from the rbcL gene (Shipunov & Shipunova 2011).

Includes Buxaceae, Didymelaceae.

Synonymy: Didymelales Takhtajan - Buxanae Reveal & Doweld

DIDYMELACEAE Leandri   Back to Buxales

Evergreen trees; hairs small, peltate; cork ?; pericyclic fibres 0; pith chambered, nodes ?; fibres +; petiole with three traces, the two lateral inverted; leaves spiral; plant dioecious; staminate flowers: P 0; A 2, connate basally, anthers extrorse; pollen tricolpate with 2-orate colpi; carpellate flowers: ?P 1, scale-like; G 1; ovules 1(2)/carpel, median, epitropous, integuments ± prolonged, protruding into the stylar canal, outer integument fringed apically; fruit a drupelet furrowed on one side; ?rudimentary aril +, testa cell walls thickened; endosperm type?, 0, embryo large; n = ?

1[list]/2. E. Madagascar. [Photos - Inflorescence]

• Didymelaceae may be recognised by their spiral, entire, greenish-drying leaves, indumentum of small scales, and small flowers, the staminate flowers having two extrorse anthers and the carpellate flowers a single carpel with a long, oblique stigma.

Chemistry, Morphology, etc. Iridoids are reported by Sutton (1989); this should be confirmed.

There is a broad pith and at best late-developing cork (Leandri 1937); the axial parenchyma is replaced by lignified cells (Takhtajan 1997). Harms (1893) describes sclereids in the pericyclic position, and also cortical sclereids. Mabberley (1997) describes the family as being glabrous.

Floral morphology has recently been described by von Balthazar and Endress (2002a) and Von Balthazar et al. (2003). In carpellate flowers there is a little scale between the ovule and the bract; its morphological nature is unclear; is it a third integument (Endress 2011b)? The flowers may be borne in pairs with a small hump between them, perhaps the pairs represent a modified cymose unit, the hump being a reduced terminal flower.

For a general summary, see Köhler (2006).

BUXACEAE Dumortier, nom. cons.   Back to Buxales

Small evergreen trees to herbs; raffinose, stachyose + [phloem exudate], tannins 0; cork subepidermal or pericyclic; sieve tube plastids with protein crystalloids; nodes 3:3; secretory cells single or in branching rows; petiole bundles arcuate; cuticle waxes as curled rodlets or irregular platelets; (stomata laterocytic); leaves opposite (spiral), ptyis flat to curved, (2ndary veins subpalmate); plant monoecious (dioecious); staminate flowers: P 2-4(5), not clearly separated from bracteoles, decussate; (A 3-many); carpellate flowers: P 6-20, at least some spiral; G [3], completely fused, with five bundles, styles ± marginal, stigma spreading, ± bilobed, dry or weakly secretory; ovules 2/carpel, apotropous, inner integument 2(-3) cells across, parietal tissue 4-15+ cell layers across, (weak nucellar cap), ovular obturator +; fruit with persistent styles; seed carunculate or not, exotesta lignified, palisade, hypodermis often lignified; endosperm cellular, +, (perisperm +), embryo short to long.

5[list]/70 - two tribes below. ± World-wide, although very scattered, not Arctic (map: see Meusel et al. 1978). [Photo - Inflorescence, Fruits.]

1. Sarcococceae

(Nodes 1:3 - Sarcococca); lamina margins toothed; no tanniniferous tissue in the flowers [?Didymelaceae]; staminate flowers: (A many - Styloceras), filaments conspicuous, pollen pantoporate, with crotonoid exine processes, (pistilode 0); carpellate flowers: bracts many, all spiral; G 2, (loculi divided), not nectariferous; outer integument 2-3 cells across; fruit a drupe; testa multiplicative, endotegmen lignified [Sarcococca]; endosperm nuclear [Sarcococca], embryo with short radicle; n = 12-14.

3/22. E. Asia to W. Malesia, E. North America, N. South America.

Synonymy: Pachysandraceae J. Agardh, Stylocerataceae Reveal & Hoogland

Haptanthus + Buxeae: outer integument ca 5 cells across.

2. Haptanthus>Cork ?; fibres storied; vessel elements with scalariform perforation plates; nodes 1:1 [from bracts]; stomata ?; hairs 0; lamina weakly pli-nerved at the base, margins entire; inflorescences cymose, bracteoles 0; P 0; staminate flowers: P 0; A 2, anthers attached their length, filament broad; pistillode 0; carpellate flowers: P ?4; staminodes 0; G [3], stipitate, placentation parietal, styles stigmatic their entire length; ovules 8-15/carpel; fruit unknown; n = ?

1/1: Haptanthus hazlettii. Central America, Honduras, recently recollected.

Synonymy: Haptanthaceae C. Nelson

3. Buxeae

(Cortical vascular bundles +); staminate flowers: pollen tri- to polycolpate, colpus with 2-4 endoapertures, or polyporate; pistillode with nectary (0); carpellate flowers: inflorescence with basal decussate "bracts"; G 3, median member adaxial, nectary between styles (0); micropyle endostomal, outer integument 5-10 cells across, minute third integument +?; fruit an explosively-dehiscent loculicidal capsule; embryo ± curved, radicle long; n = 14, 20.

2/31. Scattered, inc. Madagasacar, only Central America and West Indies in New World, not Australia nor much of Malesia.

• Buxaceae are generally monoecious evergreen herbs to small trees with exstipulate and often opposite leaves and rather small flowers with an inconspicuous perianth. The stamens are opposite the perianth members, and the styles, stigmatic their entire length, are conspicuous. The fruit is few-seeded, the mesocarp and endocarp separate, and the latter splits septicidally as well; the persistent styles are conspicuous. In flower and fruit Buxaceae look rather like Euphorbiaceae s.l., but there is no columella in the fruit, unlike Euphorbiaceae.

Evolution. Divergence & Distribution. Drinnan et al. (1991) described the fossil Spanomera from east North American deposits of Albian age, some 98-113 million years before present; it is perhaps a member of stem group Buxaceae (see also Crepet et al. 2004; Doyle & Endress 2010). Lusistemon, also with striate pollen (but with different anther insertion and arrangement) from deposits in Portugal of about the same age seems to be a related group (Pedersen et al. 2007), indeed, there are a number of distinctive tricolpate-striate pollen types also perhaps assignable to plants of this relationship that are widely distributed in early Cretaceous rocks (Pedersen et al. 2007 and references). Anderson et al. (2005) suggest that stem group Buxaceae date from 118-99 million years before present, crown group Buxaceae date from 111-63 million years before present. Krutzsch (1989) discussed the later pollen record of the family, widespread in the northern hemisphere in the early Tertiary.

Floral Biology & Seed Dispersal. Members of Buxeae are myrmecochorous (Lengyel et al. 2010).

Chemistry, Morphology, etc. Buxus often has fibre strands in stem. All genera (but Styloceras is unknown) have three vascular bundles in the upper part of the petiole.

The carpellate flowers have spirally inserted parts, but the basical floral construction of the family is perhaps dimerous (note that in the fossil Spanomera the carpellate flowers, too, may be dimerous, but there may also be five stamens opposite five tepals - Drinnan et al. 1991); this also suggests relationships with Trochodendraceae (Doyle 1999). However, as von Balthazar and Endress (2002) show, interpretation of inflorescence morphology is not easy, indeed, the nature of the paired "bracts" (?prophylls?!) below the carpellate flowers of Buxus is particularly unclear. Perianth parts have a single vascular bundle, however, the staminate flowers of Styloceras lack a perianth. Some species of Buxus have distinctive pollen with two or more orae per colpus that is rather like that of Didymelaceae; pollen in the family is variable (Köhler 2006 for references). Both Styloceras and Pachysandra have subdivided carpels; the relative poisitions of the carpels and perianth is unclear (Wiger 1935).

Haptanthus has parietal placentation and odd staminate flowers that were originally described as consisting of a single stamen (Goldberg & Nelson S. 1989). However, these flowers have two lateral anthers each with two thecae attached their length to an elliptic structure with a single arcuate vascular bundle (?very broad filament; ?prophyll - the former is the preferred interpretaion, see Shipunov & Oskolski 2011); the endothecium is massive (Doust & Stevens 2005), as it is inStyloceras, the genus most similar to Haptanthus (Shipunov & Oskolski 2011). The staminate flowers are borne in a two-ranked arrangement along the two branches of the inflorescence, the carpellate flower being central; this inflorescence is unlike any others in angiosperms, although the first/central flowers in cymose inflorescences in Euphorbia-Euphorbiaceae, for example, may be the only carpellate flower in the inflorescence.

For nectary types, see Vogel (1998b), for fossil pollen, Doyle (1999), for inflorescence morphology, von Balthazar and Endress (2001, 2002a), for floral morphology, von Balthazar and Endress (2001, 2002b), and for a general summary, see Köhler (2006).

Phylogeny. For relationships in the family, see von Balthazar et al. (2000), von Balthazar and Endress (2002b), and Shipunov and Shipunova (2011); the latter found that Haptanthus as sister to Buxeae in maximum likelihood but not maximum parsimony analyses.

Previous Relationships. Buxaceae have often been associated with Euphorbiaceae s.l. in the past. When the very distinctive Haptanthus was first described, it was not assigned a family. Shipunov (2003) placed Haptanthaceae in his Violales (= Malpighiales here), close to Salicaceae and Lacistemataceae (see also Goldberg & Alden 2005), probably because of its parietal placentation.