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 +).

Evolution. Divergence & Distribution. Estimates of the age of divergence within this clade (as [Proteales [Sabiales [Buxales [Trochodendrales....]) range from (143-)129, 126(-116) million years (Bell et al. 2010 for details).

Endress (2011a) suggested that syncarpy was a key innovation somewhere around here; optimization on the tree is not easy.

Chemistry, Morphology, etc. For the distinction between gynoecial (supposedly asterids only) and receptacular nectaries, see Smets (1988) and Smets et al. (2003); for a general survey of nectaries, see Bernadello (2007).

Phylogeny. The position of Sabiaceae has been unclear, but the most recent detailed data-rich analysis suggests a position sister to Proteales, albeit with only weak support (Soltis et al. 2011). For further discussion see the Ranunculales page.

PROTEALES Berchtold & J. Presl  Main Tree, Synapomorphies.

Lamina with teeth; stigma dry; ovules 1-2/carpel, pendulous, apotropous; seed coat?; endosperm development?, slight or 0, embryo long. - 4 families, 85 genera, 1710 species.

Evolution. Divergence & Distribution. Both Nelumbonaceae and Platanaceae are known as fossils from the Albian (the dates are ca 106 and ca 110 million years before present, respectively; for records of the former, see Upchurch & Wolfe 2005). Anderson et al. (2005, using both molecular and fossil data) date stem group Platanales from 121-119 million years before present, divergence beginning 121-115 million years before present. Magallón and Castillo (2009) suggest comparable dates of ca 122.8 and 123.6 (relaxed and constrained penalized likelihood ages) for the stem group and 116.4 and 117.4 (relaxed and constrained ditto) million years for the crown group. From the molecular point of view, at least, both Platanus and Nelumbo can perhaps be thought of as living fossils (Sanderson & Doyle 2001).

Chemistry, Morphology, etc. Barthlott et al. (1996) noted that the cuticle waxes of Platanaceae and Nelumbonaceae were very different. Hayes et al. (2000) emphasise that there are only two sepals in Nelumbo, and possibly the whole order can be characterised as having dimerous flowers (see Doyle & Endress 2000 for Proteaceae). However, fossils assignable to Platanaceae are very variable in their floral morphologies, and some seem to have much more conventional, almost core eudicot-like flowers (von Balthazar & Schönenberger 2009). For variation in microsporogenesis and pollen morphology, see Furness and Rudall (2004) and Denk and Tekleva (2006); successive microsporogenesis has been reported from both Nelumbonaceae and Platanaceae. A number of "basal" taxa in this clade have one or two ovules per carpel, although the ancestral condition may well be two.

Phylogeny. Chase et al. (1993) and Drinnan et al. (1995) found Platanaceae and Nelumbonaceae to be sister taxa. Indeed, although the order is small, it seems uncomfortably heterogeneous; it has moderate support in molecular analyses. For discussion on the phylogenetic position of Proteales and the inclusion of Sabiaceae, see the Ranuculales page.

Previous Relationships. Thorne (2007) includes the order, variously broken up, along with Buxales, in his hetereogeneous Ranunculidae, however, most authors (e.g. Cronquist 1981; Takhtajan 1997) have not seen any connections at all between the four families here.

Classification. The inclusion of Sabiaceae in Proteales seems the sensible thing to do, assuming its relationships hold up; I still have a separate page for the order, but that is simply precautionary... Ovule number and embryo are similar in the combined group.

Includes Nelumbonaceae, Platanaceae, Proteaceae, Sabiaceae.

Synonymy: Meliosmales C. Y. Wu et al., Nelumbonales Martius, Platanales Martius, Sabiales Takhtajan - Nelumbonineae Shipunov - Proteanae Takhtajan, Nelumbonanae Reveal, Sabianae Doweld - Nelumbonidae Takhtajan - Nelumbonopsida Endlicher, Proteopsida Bartling

SABIACEAE Blume, nom. cons.   Back to Main Tree

Evergreen (deciduous) trees or lianes; pentacyclic triterpenoids +, tanniniferous, benzylisoquinoline alkaloids?; vessel elements with simple to scalariform perforation plates, bars few (-30); wood with broad rays (0 - Sabia), (true tracheids +); (pits vestured - Meliosma); secondary phloem with broad or flaring rays; nodes complex unilacunar [Meliosma]; (sieve tube plastids also with protein crystalloids); cuticle wax crystalloids 0; stomata also paracytic; buds perulate or not; leaves spiral or two-ranked, simple to odd-pinnately compound, lamina vernation conduplicate [Meliosma], teeth ± spiny, or 0; flowers poly- or obliquely monosymmetric, (3-)5-merous; calyx and corolla differentiated, K C A opposite each other; A basally adnate to C, Meliosma, Ophiocaryon - 2 A fertile, with 2 basal processes and opposing C small, 2-3 A staminodial, Sabia)- A 5, disporangiate [?Ophioocaryon], dehiscence transverse or valvular; pollen colporate; nectary a thin ± lobed disc; G [2-3], completely closed (also secretory canal), when 2, oblique or median, styluli (marginal - Ophiocaryon) short, stigmas punctate, wet; ovules 1 or 2/carpel, campylotropous, (Sabia - unitegmic, integument 6 cells across), micropyle 0, open; fruit a (bilobed) ± drupelet to ± dry, dehiscent, (styluli excentric), seed with condyle [placental intrusion]; seed coat ?; chalazal endosperm haustoria +, embryo helobial, curved, (± spiral or coiled), cotyledons usually folded; n = 12, 16.

3[list]/100: Meliosma (70). South East Asia to Malesia, tropical America (map: from van Beusekom 1973; Sinimbu, pers. comm. Rafael Sühs). [Photo - Flower, Fruit.]

• Sabiaceae are evergreen trees or lianes that may be recognised by the brochidodromous venation of their leaves or leaflets, their small flowers with the perianth whorls and stamens all opposite, and the more or less flattened and distinctly curved drupes; the surface of the latter is often distinctly venose.

Evolution. Divergence & Distribution. Fossils identified as Sabiaceae are known from the Cretaceous-Cenomanian (ca 98 million years before present, Insitiocarpus, c.f. Meliosma) and -Turonian (Sabia) of Europe (Knobloch & Mai 1986). Anderson et al. (2005) date stem group Sabiaceae to 122-118 million years before present, crown group Sabiaceae 119-91 million years before present, and Magallón and Castillo (2009: Sabiaceae part of the eudicot pectination) offer the figure of ca 123.2 million years for the stem age.

Floral Biology & Seed Dispersal. Sabiaceae are distinctive among members of the eudicot grade in that the perianth is differentiated into a calyx and corolla (Drinnan et al. 1994; Hoot et al. 1999) and there is a nectary that appears to be axial/receptacular. Meliosma has explosively dehiscent anthers that are held under tension by the complex staminodes, but there is also a kind of secondary pollination presentation in which pollen collects on the broad connective between the anthers sacs (Ronse De Craene & Wanntorp 2008 for discussion).

Chemistry, Morphology, etc. There have been arguments over the interpretation of the flower of Meliosma, especially of the nature of the perianth members; two sepals are smaller than the others and have been called bracteoles, as by Endress (2010c), who would then interpret the flower as being basically monosymmetric and trimerous, the calyx whorl and the two whorls of both corolla and androecium as all alternating (one member of each is reduced). According to Baillon (1874), the two carpels of Sabia are median; Warburg (1896) drew the two carpels of Meliosma as being oblique to the vertical axis of the flowers, but median to the plane between the two bracteoles; van Beusekom and van der Water (1989) show the carpels as being oblique both to the vertical axis and to the plane between the bracteoles, and the flower could be called obliquely monosymmetric; Wanntorp and Ronse de Craene (2007) illustrate them as being more or less collateral; Ronse de Craene (2010) as slightly oblique, bracteoles are not shown, but their position is described as being variable. For a careful study, see Wanntorp & Ronse de Craene 2007).

In Meliosma the integument does not grow over the apical part of the nucellus so there is no micropyle. Ophiocaryon paradoxum has a coiled embryo; it is known as the snake nut. For chemistry, see Hegnauer (1973, 1990), and for a general account, see Kubitzki (2006b).

For wood anatomy, which is very variable, see Carlquist et al. (1993).

Classification. For a revision of Sabia, see van de Water (1980).

Synonymy: Meliosmaceae Meiser, Wellingtoniaceae Meisner

[Nelumbonales [Platanales + Proteales]]: epidermal waxes with tubules [2/3], nonacosan-10-ol the main wax; nodes?; lamina teeth morphology?; stipules surrounding stem [2/3].

NELUMBONACEAE A. Richard, nom. cons.   Back to Proteales

Aquatic herbs, rhizomatous; aporphine alkaloids +; radicle aborts; cork?; plant with air canals; vascular bundles scattered, lacking fibrous sheath; tubular P-protein and rod-shaped bodies +; nodes ?; articulated laticifers +; cuticle waxes as clustered tubules; prophyll adaxial; leaves in groups of three along the stem, vertically two-ranked, sheathing cataphyll on one side then cataphyll and expanded leaf on the other side; leaf peltate, lamina with a central disc, vernation involute, venation actinodromous, midrib unbranched, with many primary veins, dichotomising, proceeding to margin, stipule sheathing, open; flowers ?axillary, large, with complex cortical vascular system; K[?] 2, 4, C 10-30, spiral; A many, from a ring meristem, chaotic, at least outer extrorse, connective with a terminal appendage; tapetal cells multinucleate; receptacle massive, with emergent druses; G (2-)10-30, carpels ascidiate, immersed in receptacle, occluded by secretion, pollen canal long-papillate, stylulus 0, stigma expanded, wet; ovule one/carpel, outer integument ca 30 cells across, inner integument 8-10 cells across, parietal tissue 3-5 cells across, nucellar cap ca 4 cells across, chalaza massive, postament +, hypostase +, funicular obturator +; antipodal cells multiplying, multinucleate, persistent; fruit a nutlet, with an apical pore; seed ?pachychalazal, testa undistinguished; embryo green, large, with a tubular but basically double cotyledon, several leaf primordia, radicle aborting, roots adventitious; n = 8.

1[list]/1-2. Temperate, E. North America and E. Asia (map: from Fl. N. Am. III 1997; Fu & Hong 2000; Sculthorpe 1987; Wu 1983 [the last two include all Malesia and N. Australia, but not there in NW Australia, at least, in FloraBase 2006, the former also includes the Antilles and NW South America...]). [Photo - Nelumbo Flower © J. Manhart, Collection.]

• Nelumbonaceae are water plants that are easily recognised by their peltate leaves with dichotomous main venation that are held above the water surface like parasols, and their flowers which are like those of water lilies but have free carpels immersed in a large, obconical receptacle.

Evolution. Divergence & Distribution. Stem group Nelumbonaceae have been dated from 121-115 million years before the present (Anderson et al. 2005). Fossils of Nelumbonaceae - as Nelumbites, the leaves with rather different venation but the flowers with the distinctive expanded floral receptacle of extant Nelumbo - are reported from the early Cretaceous from the mid to late Albian (Upchurch & Wolfe 2005); Doyle and Endress (2010) placed the fossil sister to Nelumbonaceae. Fossils - leaves and fruits, although not connected - are known from southern Argentina in rocks of Campanian-Maastrichtian (Upper Cretaceous) age (Gandolfo & Cuneo 2005). Other fossils are discussed by Estrada-Ruiz et al. (2011).

Ecology & Physiology. Vogel (2004a) provides a fascinating account of air circulation in Nelumbo, i.a. suggesting the air flows in different halves of the leaf in different directions, similarly in the petiole. The central disc has many stomata and is the site of air exchange for the petiolar canals (see also Estrada-Ruiz et al. 2011); if covered by water, air from the petiolar canals bubbles up through it.

Floral Biology & Seed Dispersal. The flowers are thermogenic, with breakdown of starch in the expanded receptacle (Vogel & Hadacek 2004; Watling et al. 2006; Li & Huang 2009). The progamic phase, the time between pollination and fertilization, is notably short, as in at least some other aquatic angiosperms (including Nymphaea: see Williams et al. 2010). The sharp-pointed and often six-rayed epidermal druses on the surface of the receptacle may protect it against herbivores (Vogel 2004b).

Lotus fruits are noted for their longevity, and fruits 1350 ± 220 yrs have been germinated (Shen-Miller et al. 1995). This may be connected with the chemical composition of the fruit wall which is distinctive in its high polysaccharide (galactose, mannose) and tannin content, compared to the lignin + cellulose composition of (e.g.) the seed coat of Nymphaeaceae (ven Bergen et al. 1997).

Chemistry, Morphology, etc. Understanding how Nelumbo grows is difficult. The cataphylls more or less surround the stem and presumably represent the stipular portion of the leaf. Axillary branches show the same arrangement of leaves as described above, but with the addition of the prophyll which is on the same side of the branch as the first cataphyll. Flower buds develop in the axis of the second cataphyll, axillary branches in the axil of the expanded leaf, however, other interpretations are also possible. The sheathing stipule associated with the foliage leaf is open on the side of the stem opposite to the leaf insertion. For some literature on the growth pattern of Nelumbo, see Eichler (1878), Wignand and Dennert (1888), Miki (1926), Esau and Kosakai (1975), etc.

Vessels arise first in the roots, but are also found in the rhizome, and the trend of their specialisation is similar; this is the monocot pattern. Details of the root cortex of Nelumbonaceae differ considerably from those in Nymphaeales (Seago 2002). Although the vascular bundles are scattered in the stem, there is an endodermis present.

Hayes et al. (2000) note that the two sepals are inserted in the vertical plane; Moseley and Uhl (1985) note that there may be four, c=decussating sepals. Although the floral vasculature is complex because of the presence of rings of cortical bundles, the basic vascular supply to floral parts is like that of other flowers - the sepals may, however, have but a single trace that quickly divides (Moseley & Uhl 1985). The stamens develop from an androecial ring, and they and the carpels may be irregularly whorled (Hayes et al. 2000). Cronquist (1981) described the stamens as being introrse-latrose; Endress (1995) as extrorse, Takhtajan (1997) as extrorse (the outer members) and introrse (the others). There is also disagreement over endosperm development which has been variously described as nuclear, cellular, or helobial and over pollen morphology (Kreunen & Osborne 1999).

Some general information is taken from Williamson and Schneider (1993) and Hayes et al. (2000), for embryology, etc., see Khanna (1965) and Batygina et al. (1982), chemistry, see Hegnauer (1969, 1990 - under Nymphaeaceae), for floral anatomy, see Mosely and Uhl (1985), and for the receptacular druses, see Vogel (2004b).

Previous Relationships. In the past, Nelumbonaceae were usually associated with Nymphaeaceae (e.g. Cronquist 1981), the two having superficially similar flowers and vegetative body (both are "water lilies") - and it turns out that floral gene expression patterns in Nymphaea and Nelumbo are remarkably similar (Yoo et al. 2010)! Takhtajan (1997) removed Nelumbonaceae from the vicinity of Nymphaeales, but considered it to be a very isolated group and placed it alone in his subclass Nelumbonidae. Both the morphology of the cuticle waxes and plant chemistry suggest a relationship with Ranunculales, but there the waxes are nonacosan-10-ol rather than 4-10- or 5-10-diol (Barthlott et al. 1996, the difference not emphasised by Barthlott et al. 2003).

[Platanaceae + Proteaceae]: woody; non-hydrolysable tannins, myricetin +, benzylisoquinoline alkaloids 0; (pits vestured); wood with broad rays [8+-seriate]; stomata laterocytic; flowers 4-merous [see fossil Platanaceae], stamens equal and opposite perianth members; carpels with 5 vascular bundles, hairy, postgenital fusion complete, stylulus long; ovules straight, inner integument 3-5 cells across; endosperm nuclear.

Evolution. Divergence & Distribution. That Platanaceae and Proteaceae are sister taxa may explain why there are so many leaf fossils from the southern hemisphere that are "platanoid" in their general aspect (K. Johnason, in Drinnan et al. 1994; Hoot et al. 1999).

Chemistry, Morphology, etc. The wood anatomy of Proteaceae and Platanaceae is very different, although the former have concave vessel-parenchyma festoons and the latter concave growth ring boundaries in common, in addition to their broad rays. These differences may be connected with the different climatic conditions under which the two groups grow (Baas et al. 2003). For stomatal morphology, see Carpenter et al. (2005). Although flowers of Platanaceae and Proteaceae look very different, von Balthazar and Schönenberger (2009) suggest similarities; both consist of perianth, stamens, and fleshy structures. In Platanaceae the latter may represent an outer staminal whorl, in Proteaceae an inner whorl. This hypothesis needs further study, but in either case they are positionally different and so are unlikely to form an apomorphy for the clade.

PLATANACEAE T. Lestibudois, nom. cons.   Back to Proteales

Growth sympodial; cork in outer cortex; nodes multilacunar; petiole bundle annular, wing bundles +; hairs candelabriform; leaves two-ranked (spiral), lamina vernation plicate, teeth glandular, with a terminal cavity, higher order veins approach but do not enter it, (margin entire), 2 strong 2ndary veins near base (venation pinnate; also seedlings), petiole enclosing the axillary bud (not), stipule tubular, closed (adaxial-sheathing, open); plant monoecious; inflorescences capitate; flowers with odd member of outer whorl abaxial, P connate or not, often lacking vasculature; staminate flowers: P ca 3, tiny, free; "ridged staminodes" +; anthers valvate, connective with subpeltate continuation above the anther; pollen semitectate-reticulate, 16-22 µm long; (pistillodes +); carpellate flowers: P 3-4; "ridged staminodes" +, staminodes +; G (3-)5-8(-9), two-whorled, stigma long, decurrent in two crests, ± dry; ovules 1(-2)/carpel, outer integument 3-4 cells across; antipodals persistent; fruit an achene, with tuft of basal hairs; testa with hypodermal layer of thickened cells; seed reserves hemicellulosic, endosperm moderate; n = 16-21.

1[list]/10. North Temperate (map: from Fl. N. Am. III 1997; Jalas et al. 1999 [Europe]; Feng et al. 2005). [Photo - Leaves & Stipules, Collection.]

• Platanaceae are a distinctive family. The bark commonly exfoliates with characteristic plates, the leaves have leaf-like stipules completely surrounding the stem, the petiole base encloses the axillary bud, and the blades have subpalmate venation. However, Platanus kerrii is rather different vegetatively from the other species, having stipules that are more or less scarious, an axillary bud that is not enclosed by the petiole base, and pinnate venation. In all species, the inflorescences are capitate and made up of numerous small flowers: the fruits are small achenes with tufts of basal hairs.

Evolution. Divergence & Distribution. Platanaceae are known fossil from the Lower Cretaceous, 98-113 million years before present (Platanocarpus - Crane et al. 1993), and other fossils are associated with Platanaceae in the constrained morphological analysis of Doyle and Endress (2010). Anderson et al. (2005) date stem group Platanaceae to 119-110 million years before present. Fossils with the distinctive petiole bases of subgenus Platanus are abundant in the Palaeocene some 60 million years before present (Feng et al. 2005: note that subgenus Castaneophyllum [P. kerrii] lacks them), although fossil leaves with such petioles may have small, fugaceous triangular stipules (Wang et al. 2011).

As already suggested, the morphology of these fossil plants differs in several respects from that of their extant relatives. Thus inflorescences in Upper Cretaceous plants may have sessile or pedunculate heads, in staminate flowers P 4, basally connate, stamens equal and opposite perianth members and arising from a short ring of tissue, alternating with ?staminodes, perhaps of an inner whorl, or two 4- or 5-membered whorls of perianth present, pistillode consistently present; in carpellate flowers often 4-5-merous. In other flowers the P is in 2 whorls, connate, outer more or less completely so, or free; G 8, 2 opposite each member of inner perianth, ovules perhaps anatropous, stylulus 0, no achenial hairs, etc. Fossils assigned to Platanus may have trifoliolate leaves (Kvacek et al. 2001a), while other fossils have somewhat smaller pollen that that of extant taxa - are they wind-pollinated? - and tricolporate pollen has even been found in situ in fossils assigned to Platanaceae (e.g. Manchester 1986; Crane et al. 1993; Pedersen et al. 1994; Friis et al. 1988; Magallón-Puebla et al. 1997: Mindell et al. 2006: Crepet et al. 2004; von Balthazar & Schönenberger 2009; Taylor et al. 2009 for other references). Fossil Platanaceae do not have hairy fruits (von Balthazar & Schönenberger 2009). Finally, there is some evidence from stomatal size of fossils that polyploidization occurred within this clade (Masterson 2004).

Floral Biology & Seed Dispersal. There is about five weeks between pollination and fertilization in Platanus racemosa, at least (Floyd et al. 1999).

Chemistry, Morphology, etc. Hennig et al. (1994) describe the cuticle wax as lacking crystalloids, Fehrenbach and Barthlott (1988) as having rodlets and platelets. There is some variation in stomatal morphology (Carpenter et al. 2005). Smets (1986) mentions the presence of nectaries; Melikian (1973) and Takhtajan (1991) describe testa anatomy; Floyd et al. (1999) describe the embryology; for chemistry, see Hegnauer (1969, 1990). Endress (1971) describes the flower as having the odd perianth member abaxial; he also describes the 6 carpels as being opposite sepals and corolla. However, there is clearly plenty of room for differences in the interpretation of floral morphology; von Balthazar and Schönenberger (2009) suggest that the parts of the flower alternate regularly and that the androecium is biseriate (see also above). Developmental studies suggest that flowers of Platanus are basically 4-merous (A. Douglas in Hoot et al. 1999).

Some information is taken from Kubitzki (1993b); see Floyd et al. (1999) and Floyd and Friedman (2000: complex cellularization pattern in the endosperm) for embryology, while Denk and Tekleva (2006) discuss pollen morphology of extant and fossil representatives.

Phylogeny. For a phylogeny of Platanus, see Grimm and Denk (2008).

Previous Relationships. Platanaceae were included in Hamamelidales by both Cronquist (1981) and Takhtajan (1997).

PROTEACEAE Jussieu, nom. cons.   Back to Proteales

Trees or (acaulescent) shrubs; lateral roots of limited growth, forming clusters [proteoid roots], plant rarely mycorrhizal; cyanogenic glycosides +; vessel elements with simple perforation plates (scalariform, bars few); true tracheids and libriform fibres +; phloem stratified or not; nodes (1:1), 3:3; petiole bundles numerous, pattern complex; sclereids common; hairs with 2 short cells, one in epidermis, apical cell elongated, bifid or not; leaves spiral (opposite), (odd-pinnately, rarely palmately, compound or lobed), lamina often coriaceous, vernation usu. conduplicate, margins spiny toothed to entire, base of petiole often swollen, stipules 0; inflorescence various; flowers 4-merous; P valvate, diagonal; pollen triangular in polar view, oblate, triporate, pores broadly operculate, apertures in three's at four points of the young tetrad [Garside's Rule], cleavage centrifugal, (colpate), exine with ektexine only; nectary receptacular, vascularized; G 1, orientation adaxial, stigma terminal or lateral, often slit-like, secretory; ovules long, with vascular bundles forming a ring in the chalazal region, outer integument 2-9 cells across, nucellar cap ca 4 cells across, ± endothelial; (antipodals ± persistent); endotesta palisade, crystalliferous, (exotegmen fibrous); cotyledons large, cordate, suspensor 0.

80[list]/1600 - five subfamilies below. Largely southern hemisphere, esp. Australia and S. Africa (map: from Johnson & Briggs 1975; Weston 2006; Prance et al. 2007).

1. Bellendenoideae P. H. Weston

Plants Al-accumulators; inflorescence terminal, bracts 0; ovules 2/carpel; fruit dry, indehiscent, 2-winged; endosperm at most slight; n = 5, chromosomes ca 6.7 µm long (mean).

1/1: Bellendena montana. Australia (Tasmania).

[Persoonioideae [Grevilleoideae + Symphionematoideae + Proteoideae]]: stomata brachyparacytic; P connate; A adnate to P, more or less sessile, (connective appendage +); usu. 4 nectary lobes; stylulus long; endosperm +; (cotyledonary blade cordate).

2. Persoonioideae L. A. S. Johnson & B. Briggs

(Plants Al-accumulators - Placospermum); proteoid roots 0; tepals with Vorlaüferspitze, 1-2(+) ovules carpel; fruit a drupe (follicle - Placospermum); cotyledons obreniform; n = 7, chromosomes 9.1-14.4 µm long (mean).

5/110: Persoonia (100). Mostly Australia, also New Caledonia and New Zealand.

[Grevilleoideae + Symphionematoideae + Proteoideae]: flowers vertically or obliquely monosymmetric [P split to base on one side (4:0), or 3 P connate, 1 free (3:1)]; (secondary pollen presentation, the apex of the style bearing the pollen); (ovules anatropous); x = 14, chromosomes 0.5-5 µm long (mean).

3. Grevilleoideae Engler

Plants Al accumulators; sieve elements with rosette-like non-dispersive protein bodies; paired flowers subtended by a common bract very common; T orthogonal; pollen biporate, also with abundant endexine, also in the apertural region; (carpel orientation other than adaxial); ovules (1-)2+/carpel; fruit a drupe or follicle, the latter with winged seeds; (seeds pachychalazal); endosperm with chalazal ± nuclear haustorium; cotyledons basally auriculate; n = (10-)14(-15).

45/855: Grevillea (515, inc. Hakea, Finschia), Helicia (100), Banksia (175: inc. Dryandra, see Mast et al. 2005). Australia and the S.E. Pacific to Southeast Asia, S. India and Sri Lanka, South America, South Africa (Brabejum) and Madagascar (Madagascaria). [Photos - Grevillea Flower, Embothrium Flower, Fruit, Habit.]

Synonymy: Banksiaceae Berchtold & J. Presl

[Symphionematoideae + Proteoideae]: fruit indehiscent.

4. Symphionematoideae P. H. Weston & N. P. Barker

Proteoid roots 0; nectaries 0; ovules 1-2/carpel; fruit dry; n = also 10.

2/3. S.E. Australia, inc. Tasmania.

5. Proteoideae Eaton

(Herbaceous), (plants Al-accumulators); sieve elements with non-dispersive protein bodies; flowers sessile; (hypanthium +); T orthogonal [level?]; (A monothecal; 1-3); ovules 1(2)/carpel; fruit often single-seeded, drupe or nut; n = (10-)11-13(-14).

25/640: Protea (115), Leucadendron (80), Conospermum (55), Petrophile (55), Synaphea (55), Serruria (50). Africa S. of the Sahara, esp. the Cape region, Australia.

Synonymy: Lepidocarpaceae Schultz Schultestein

• Proteaceae are woody plants that may be recognised vegetatively by the broad rays in the wood, the surface of which is often furrowed even in the twigs, the often rather scleromorphic and coriaceous leaf blades with rather distant (or no) teeth and prominent reticulum, the swollen leaf base and the sometimes rather short petiole (which is then bottle-shaped), and the brown indumentum. The 4-merous flowers are often aggregated into conspicuous inflorescences; the perianth has a single whorl and may be monosymmetric and curved and the stamens are opposite the perianth members; the single carpel often has a long style.

Evolution. Divergence & Distribution. Hill et al. (1995) and Weston (2006) summarize the fossil record of the family. Molecular estimates such as those of Anderson et al. (2005, see also Barker et al. 2007b) date stem group Proteaceae at 119-110 million years before present, the crown group at 96-85 million years before present while Barker et al. (2007b) estimate stem Proteaceae at (126.7-)118.5(-110.3) million years ago. Leng et al. (2005) discuss small but mature capsular fruits from late Cretaceous (late Santonian/early Campanian) Sweden which have several attributes of Proteaceae, e.g. the flowers are paired, the stigma is somewhat abaxial on the fruit, however, there are also differences, including the fact that there are only three vascular bundles per carpel and there seems to be little in the way of a perianth; one species has the most remarkable papillate seeds.

Proteaceae fossils are known from sediments ca 94 million years old in Australia, i.e., shortly after the separatiion of Australia from Antarctica some 97 million years ago (Hill & Brodribb 2006). There is a great diversity of proteaceous pollen from the late Cretaceous (Campanian-Maastrichtian) in southeast Australia (Dettmann & Jarzen 1991, 1998). The stem age of the very largely Australian Bansieae is estimated at (94.9-)87.9(-80.9) million years (Barker et al. 2007b, q.v. for other ages). Although some transoceanic disjunctions in the family, for example, that of the sister taxa Cardwellia in Australia and Gevuina in South America, are possibly caused by vicariance/continental drift events, others, like Brabejum in Africa which is sister to Panopsis in South America, involve genera whose estimated time of divergence is later than the geological events that from their distribution patterns might seem to have caused them (Barker et al. 2007b). There has been extensive extinction of Proteaceae in New Zealand (Lee et al. 2001).

Some more recent diversifications may have been instigated by vicariance events, such as that of some Banksia that is perhaps associated with the aridification of the Nullarbor Plain some 14-13 million years ago leading to the separation of what became eastern and western clades (Crisp & Cook 2007), however, the genus itself may be ca 61 million years old (He et al. 2011). Several lines of molecular evidence suggest that there may have been a rapid diversification within Grevilleoideae (Hoot & Douglas 1998); crown group Hakea s. str. may have diversified within the last 10 million years (Mast et al. 2009). The diversification of Protea, notably speciose in southern Africa with some 70 out of its 115 species being restricted to the Cape, has been studied by Barraclough and Reeves (2005), although they find it difficult to pin down the timing of this; however, Sauquet et al. (2009a, b) suggest that it may have diversified within the last 18 million years, while Leucadendrinae started diversifying there as much as 39 million years ago, even though they have been in the Cape region for a shorter time than Protea itself. On the other hand, Schnitzler et al. (2011) suggest that diversification began ca 28 million years ago in the middle of the Oligocene and is connected with changes in soil preferences of related species; rates of diversification throughout its range may be similar (Valente et al. 2010b; see also Silvestro et al. 2011).

Plant-Animal Interactions. Given the size of the family, caterpillars of Lycaenidae butterflies seem to eat its members quite frequently (see Fiedler 1991).

Floral Biology & Seed Dispersal. Pollination in Proteaceae has been studied in some detail, and in both Australia and southern Africa non-flying mammals (rodents, marsupials) are among the pollinators (Collins & Rebelo 1987). Secondary pollen presentation by regions at the apex of the style is common, and the pollen may even cover the stigmatic area (Ladd et al. 1996), but selfing is uncommon, the stigma often being slit- or groove-like; Proteaceae show very great variation in these pollen presenting areas (Ladd 1994). Bernhardt and Weston (1996) studied pollination of Persoonia, which lacks secondary pollen presentation; it was by bees. Monosymmetric flowers are common the family, but the Cape species Mimetes cucullatus has monosymmetric groups of flowers, the flowers being borne under a more or less brightly coloured inflorescence bract. The inflorescences of some species of the Australian Conospermum (Proteoideae) in particular look rather like those of Anigozanthus (Haemodoraceae), and there is considerable developmental variation in the flowers of Conospermeae (Douglas & Tucker 1997).

Serotiny is scattered in the family, the follicles opening only after a fire. A number of the taxa involved have massive fruits, but with only two seeds; Banksia is a major serotinous clade, although with some reversals (He et al. 2011: Dryandra not included, other features associated with serotiny also examined). For myrmecochory in Grevillea, Leucadendron, etc., i.e. Grevilleoideae and Proteoideae, see Lengyel et al. (2009, 2010).

Ecology & Physiology. Proteoid roots are short lived clusters of roots of determinate growth that have densely set root hairs; they may account for over 50% of the mass of all roots at any one time (Shane & Lambers 2008). They exude organic acids, especially as tricarboxylates, into the soil and mobilize phosphate, and perhaps other nutrients like manganese that are at a premium in the phosphorous-poor soils on which members of the family are often found (Weston 2006); they are phosophorous miners. Many but not all members of the family develop phosphorous toxicity when growing on relatively phosphorous-rich soils; phosphorous uptake cannot be down-regulated and it eventually starts accumulating in palisade mesophyll cells in particular, eventually causing their death (Shane et al. 2004; Shane & Lambers 2008; see also Lambers et al. 2011 for a general summary). (Interestingly, proteoid roots develop in Lupinus and Arabidopsis under conditions of low phosoporous [López-Bucio et al. 2003 for references]).

For the evolution of scleromorphic leaf anatomy in the family, see Jordan et al. (2005, 2008); some of the structures involved are implicated in photoprotection and also are associated with some combination of open, oligotrophic, cold and dry conditions. In general, Proteaceae are most diverse in rather dry climates in Australia and southern Africa; lignotubers have evolved several times. See also Purnell (1960) and Dinkelaker et al. (1995) for information.

Other. In Australia, the fungal pathogen Phytophthora cinnamomi is proving especially destructive to members of this family in the Mediterranean climates of the southwest.

Chemistry, Morphology, etc. For distinctive fatty acids in the seeds, see Badami and Patil (1981). Sieve tubes have sieve areas for most of their length. The roots have 4-7 protoxylem poles. Nodes in Panopsis appear to be pentalacunar, while those of Finschia are trilacunar, although with some variation in the number of traces departing from each gap (Catling 2010). Cotyledonary nodes commonly have split laterals (Naubauer 1991), however, the distribution of this character is unclear. The lenticels are often horizontally elongated (Keller 1996). Foliar anatomy is notably variable within Grevilleoideae.

For flower pairs, which represent reduced inflorescence branches, see Douglas and Tucker (1996a), for the variable floral orientation, see Douglas and Tucker (1996a, b); the flowers may be mirror images, as in Orites (image at: www.anbg.gov.au/proteaceae/illustrations.html). In Grevilleoideae, the basical floral orientation is orthogonal to the bract immediately subtending the flower, but the position of this bract relative to the axis that bears it varies (Douglas & Tucker 1996a). There is no evidence that the uniseriate perianth is derived from a biseriate structure, and the individual perianth members - of Macadamia, at least - have three traces; for the family, 1-5 bundles supplying each tepal are reported (Weston 2006). A small, almost spine-like process that is described as a Vorlaüferspitze (Douglas & Tucker 1996c) occurs just abaxial to the apex of the perianth members (see Kaplan 1973) in Persoonioideae, but it is also found elsewhere in the family. The nectary has very variable vasculature and is best considered an enation rather than a modified stamen, etc. (Douglas & Tucker 1996c). The position of the embryo sac in the ovule varies considerably (Venkata Rao 1971). The stigma may be papillate, or it is more or less enclosed, with exudate (Matthews et al. 1999); due to the early growth of the carpel, it may be in a more or less abaxial position on the carpel/style. Testa and tegmen variation is considerable, parly because the fruits are sometimes indehiscent, and both testa and tegmen may sometimes be multiplicative (Venkata Rao 1971; Corner 1976); however, the ovary wall and integuments may be adnate (so the fruit is a caryopsis??!!) and there has been much misinterpretation of fruit/seed anatomy (Manning & Brits 1993: their interpretation is followed here). Testa anatomy is similar to that in Papaveraceae, Chloranthaceae, and Aristolochiaceae, for what that is worth. Cotyledons of Bellendena are not cordate are they often are elsewhere in the family. That 'palaeo-polyploidy' has been involved in the evolution of chromosome number in the family is questionable (Stace et al. 1998).

For life history of Grevillea, see Brough (1933), for Al-accumulation, see Webb (1954), for general chemistry, see Hegnauer (1969, 1990), for polyol distribution, see Bieleski and Briggs (2005), for floral morphology in Conospermeae, see Douglas and Tucker (1997), for pollen development, see Blackmore and Barnes (1995: Garside's Rule), for general information, see Johnson & Briggs (1963, 1975: including chromosome lengths) and Venkata Rao (1971), for nodes, Catling and Gates (1998), for a survey of seed coat anatomy, Takhtajan (2000), for pollen, see Dettmann (1998), Sauquet et al. (2006) and Sauquet and Cantrill (2007), and for general information see especially Weston (2006).

Phylogeny. For phylogeny, see Hoot and Douglas (1998) and Weston and Barker (2006). Although the subfamilies recognised here seem to be fairly solidly supported, relationships between them are less clear. Thus the summary tree in Weston and Barker (2006) and Weston (2006) suggests that Bellendenoideae and Persoonioideae are sister taxa. Carnarvonia and Sphalmium, sometimes segregated as subfamilies, may be immediately related, and although definitely in Grevilleoideae, relationships within that clade are unclear.

For relationships in Proteoideae, see Barker et al. (2002); the Australian Isopogon and Adenanthos are sister to a clade that represents most of the subfamily, but not including Protea and Faurea (support strong for this set of relationships); unfortunately Eidothea, a distinctive genus and is segregated as Eidotheoideae in The Flora of Australia, was not included. However, the biogeography of the subfamily is clearly interesting.

Classification. For a new classification, the outlines of which are followed here, and a generic checklist, see Weston and Barker (2006) and Weston (2006). Carnarvonia and Sphalmium are both morphologically very distinctive, the first having fully compound leaves and the latter only a short stylulus, and are segregated as Carnarvonioideae L. A. S. Johnson & B. Briggs and Sphalmioideae L. A. S. Johnson & B. Briggs in The Flora of Australia), but they are included in Grevilleoideae here.