EXTANT SEED PLANTS

Plant woody, evergreen; nicotinic acid metabolised to trigonelline; primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins rich in guaiacyl units; true roots present, xylem exarch; shoot apical meristem complex; arbuscular mycorrhizae +; stem with ectophloic eustele, endodermis 0, xylem endarch; 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 ?; leaf vascular bundles collateral; leaves spiral, simple, axillary buds?, prophylls [including bracteoles] two, lateral; plant heterosporous, sporangia eusporangiate, on sporophylls, sporophylls aggregated in indeterminate cones/strobili; true pollen [microspores] +, mono[ana]sulcate, pollen exine and intine homogeneous, ovules unitegmic, crassinucellate, megaspore tetrad tetrahedral, only one megaspore develops, megasporangium indehiscent; male gametophyte development endo/exosporic, gametes two, with cell walls; female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large", first cell wall of zygote transverse, embryo straight, endoscopic [suspensor +], short-minute, with morphological dormancy, white, cotyledons 2; plastid transmission maternal; two copies of LEAFY gene, PHY gene duplication, mitochondrial nad1 intron 2 and coxIIi3 intron present.

MAGNOLIOPHYTA

Plant woody, evergreen; lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, non-hydrolysable tannins, quercetin and/or kaempferol +, apigenin and/or luteolin scattered, cyanogenesis via tyrosine pathway, lignins derived from both coniferyl and sinapyl alcohols, containing syringaldehyde [in positive Maüle reaction, syringyl:guaiacyl ratio less than 2-2.5:1], and hemicelluloses as xyloglucans; root apical meristem intermediate-open; root vascular tissue oligarch [di- to pentarch], lateral roots arise opposite or immediately to the side of [when diarch] xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0; stem with 2-layered tunica-corpus construction; wood fibers and wood parenchyma +; reaction wood ?, with gelatinous fibres; starch grains simple; primary cell wall mostly with pectic polysaccharides; tracheids +; sieve tubes eunucleate, with sieve plate, companion cells from same mother cell that gave rise to the tube, the sieve tube with P-proteins; nodes unilacunar; stomata with ends of guard cells level with aperture, paracytic; leaves with petiole and lamina [the latter formed from the primordial leaf apex], development of venation acropetal, 2ndary veins pinnate, fine venation reticulate, vein endings free; flowers perfect, polysymmetric, parts spiral [esp. the A], free, numbers unstable, P not differentiated, outer members not enclosing the rest of the bud, A many, development centripetal, 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, pollen subspherical, binucleate at dispersal, trinucleate eventually, tectum continuous, endexine compact, lamellate only in the apertural regions, pollen tube elongated, with callose plugs, penetrating between cells, growth rate moderate, siphonogamy occuring, nectary 0, G free, several, ascidiate, with postgenital occlusion by secretion, few [?1] ovules/carpel, ovules marginal, anatropous, bitegmic, micropyle endostomal, integuments 2-3 cells thick, megasporocyte single, megaspore lacking sporopollenin and cuticle, chalazal, female gametophyte ?type, stylulus short, stigma ± decurrent, wet [secretory]; P deciduous in fruit; seed exotestal; double fertilisation +, endosperm ?diploid, cellular [first division oblique, micropylar end initially with a single large cell, chalazal end more actively dividing], copious, oily and/or proteinaceous, embryo cellular ab initio; germination hypogeal, seedlings/young plants sympodial; Arabidopsis-type telomeres [(TTTAGGG)_n]; whole genome duplication, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, paleo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and PHYA/PHYC gene pairs.

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

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

PROTEALES [TROCHODENDRALES [BUXALES [GUNNERALES + CORE EUDICOTS]]]: ?

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

BUXALES [GUNNERALES + CORE EUDICOTS]: ?

GUNNERALES + CORE EUDICOTS: Ellagic and gallic acids common, cyanogenesis via phenylalanine, isoleucine or valine pathways; micropyle?; PI-dB motif +, small deletion in the 18S ribosomal DNA common.

CORE EUDICOTS: Root apical meristem closed; flowers rather stereotyped: 5-merous, parts whorled, K and C distinct, K with 3 traces, A = 2x K, internal to the C whorl, (numerous, but then often fasciculate and/or centrifugal), pollen tricolporate, (nectary disc +), [G 5], [3] also common, compitum +, placentation axile, stigma not decurrent; endosperm nuclear; fruit dry, dehiscent, loculicidal [when a capsule]; euAP1 + euFUL + AGL79 genes [duplication of AP1/FUL or FUL-like gene], PLE + euAG [duplication of AG-like gene: C class], SEP1 + FBP6 genes [duplication of AGL2/3/4 gene].

SAXIFRAGALES [VITALES + ROSIDS]: stipules +.  Back to Main Tree

A relatively large embryo over half the length of the seed may be a feature of this clade (Forbis et al. 2002), although there is considerable variation in Saxifragales, Vitales have small embryos, and exactly where larger embryos might be placed on the tree is made yet more uncertain because of the uncertain relationships in this area. See also below.

SAXIFRAGALES Dumortier  Main Tree, Synapomorphies.

Ellagic acid, myricetin, flavonols +; (tension wood +); cuticle waxes as clustered tubules, branching from the previous flush [woody members]; leaf teeth with gland broadening distally and apical foramen, higher order lateral veins joining it; anthers basifixed, with basal pit, transversely sagittate, ?pollen morphology, floral apex flat-concave early in development [G often (semi-)inferior], carpels free, at least apically, micropyle bistomal, styles separate, stigmas decurrent, at most slightly wet; fruit dry; seeds ± exotestal; endosperm type?, embryo size?; unique 1 BP insertion in 18S rDNA. - 16 families, 112 genera, 2470 species.

See the Berberidopsidales page for discussion on the relationships of Saxifragales, which have no firm position as yet.

Saxifragales contain ca 1.3% of eudicot diversity. However, they have a very poor representation in the tropics in general and neotropics in particular, which makes the recent inclusion of the tropical Peridiscaceae (see below) the more notable. Wikström et al. (2001) suggest that the age of the clade is some 121-111 my, with diversification within it starting 110-92 million years before present; comparable figures given by Anderson et al. (2005) are ca 108 million years before present and 102 million years before present respectively; Jian et al. (2006) estimate the age of the clade as between 97-72 million years before present, with diversification being rapid; while Hermsen et al. (2006: topology much more resolved than here, but with little support) also find much diversification having occured by 90 million years before present, in the Late Cretaceous.

Roots are diarch (Van Tieghem & Douliot 1888). Saxifragales commonly have scalariform perforation plates, lateral pitting that is mostly scalariform or opposite, bordered pits, etc., but whether these are synapomorphies is unclear (Jian et al. [2006] characterise the largely unresolved woody members and the Saxifraceae + Crassulaceae clades in terms of their wood anatomy). Leaf teeth are basically rosid, although those of Cercidiphyllum are described as being more or less chloranthoid (not very different), while Hamamelidaceae can have teeth with a clear, glandular apex (fothergilloid) and those of Altingiaceae are platanoid (basically, the higher order lateral veins do not quite make it to the tooth - Hickey & Wolfe 1975; Tetracarpaea is similar, also lacking such veins - Hils et al. 1988). Despite appearances, the floral apex in nearly all taxa studied is flat or concave (Fishbein et al. 2000; Soltis & Hufford 2002; D. Soltis et al. 2003b; Soltis et al. 2005b).

The clade is suggested in molecular phylogenies (e.g. D. Soltis et al. 1997; D. Soltis & P. Soltis 1997). In addition to sequence similarity, members have i.a. an insertion in common. Peridiscaceae were placed in Malpighiales by Savolainen et al. (2000a: see A.P.G. 2003). However, Davis and Chase (2004; see also Soltis et al. 2007a) rather surprisingly found that the family was to be placed here, also adding Soyauxia. Apart from the Crassulaceae/Saxifragaceae clade, relationships within Saxifragales remained largely unresolved for some time, and it has been suggested that they rapidly diversified into several clades, and that they represent a rapid, ancient radiation (Fishbein et al. 2001; cf. Fishbein & Soltis 2004). Note that Hilu et al. (2003: matK) did not recover the Saxifragaceae/Crassulaceae clade, although there was no strong support for an alternative placement; Cercidiphyllaceae and Daphniphyllaceae were sister taxa, with moderate jacknife support. Hermsen et al. (2006b), who included both molecular and morphological (the latter also from selected fossils) data, also recovered a [Crassulaceae et al. + Saxifragaceae et al.] clade, while all other families were in a clade sister to this. [Paeonia + Daphniphyllum] and [Cercidiphyllaceae + Altingiaceae] are clades in this latter; Peridiscaceae were not included. Paeonia was linked with moderate support to the Crassulaceae clade, or, more weakly, with the Crassulaceae + Saxifragaceae clades in some analyses in Fishbein et al. (2001); the latter relationship also appeared in a recent study (Fishbein & Soltis 2004: Peridiscaceae not included), but it was linked with low support to Peridiscus itself by Davis and Chase (2004). DSoltis et al. (2007b) were also unable to recover stable relationships among the woody Saxifragales, long branch attraction (Paeoniaceae, Peridiscaceae) possibly occuring; depending on the analysis, [Peridiscaceae + Paeoniaceae] made Hamamelidaceae paraphyletic, or Peridiscaceae were sister to all other Saxifragales in the study. Despite the addition of more data, Jian et al. (2006) still found it difficult to resolve relationships between the woody members, although it appeared that Peridiscaceae might be sister to the rest of the order, and Paeoniaceae sister to the Crassulaceae and Saxifragaceae clades, however, subsequently they were able to find strong support for the toplogy used here, although Paeonia in particular moved around the tree is some analyses (Jian et al. 2008). Morphological support for this topology is weak.

Molecular analyses have placed the hitherto unplaced Cynomoriaceae in Saxifragales, perhaps in the Crassulaceae area, although with little support (Nickrent 2002; Nickrent et al. 2005; cf. Barkman et al. 2007: no support for a position in this order - or any place in particular). This position is rejected by Jian et al. (2008), who prefered to place them in Santalales; Balanophoraceae, with which Cynomoriaceae were linked in the past, are also to be included in Santalales.

Saxifragales includes Hamamelidaceae, a group classically linking the Englerian Amentiferae (usu. dioecious or monoecious woody plants with an ament, or catkin, with small flowers, and sometimes believed to be primitive), to "dicots" with more conventional flowers. However, Hamamelidae, inc. Amentiferae, are now in several bits, of which one is here - see also Fagales, which constitutes the major part of the Amentiferae, Malpighiales (Salicaceae), Rosales ("Urticales"), etc. (Qiu et al. 1998a). A link between woody Saxifragales and Fagales is still often recognised (e.g. Frohne & Jensen 1992), although there seems little point in continuing to do this. The old woody Saxifragaceae are spread widely through both rosids and asterids (e.g. Morgan & Soltis 1993), e.g. Brexiaceae (Celastrales), Hydrangeaceae (Cornales), Escalloniaceae (unplaced asterid II); most iridoid-negative, herbaceous and/or crassinucellate members remain here. Ironically, three families of Saxifragales are reported to have iridoids (how many origins?), the only families outside asterids reliably reported to have these compounds! Daphniphyllanae, Saxifraganae and Hamamelidanae, in which Takhtajan (1997) placed most of the families in Saxifragales, are all in his Hamamelididae.

For information on the hamamelids as it was beginning to be realised that they might have to be split, see Crane and Blackmore (1989). For pollen, see Hideux and Ferguson (1976), Zavada and Dilcher (1986); floral anatomy and morphology, Gaümann (1919), Bensel and Palser (1975a-d), Hufford and Endress (1989), Drinnan et al. (1995), Fishbein et al. (2000); for chemistry, Giannasi (1986), Jay (1971); for anatomy, Watari (1939), Ramamonjiarisoa (1980), Cutler and Gregory (1998); for seed coat, Krach (1976); and for general morphology, see Hermsen et al. (2006b).

Includes Altingiaceae, Aphanopetalaceae, Cercidiphyllaceae, Crassulaceae, Cynomoriaceae, Daphniphyllaceae, Grossulariaceae, Haloragaceae, Hamamelidaceae, Iteaceae, Paeoniaceae, Penthoraceae, Peridiscaceae, Pterostemonaceae, Saxifragaceae, Tetracarpaeaceae.

Synonymy: Hamamelidineae Thorne & Reveal - Altingiales Doweld, Cercidiphyllales Reveal, Crassulales Lindley, Cynomoriales Burnett, Daphniphyllales Cronquist, Grossulariales Lindley, Haloragales Bromhead, Hamamelidales Grisebach, Iteales Doweld, Paeoniales Heinze, Peridiscales Doweld, Sedales Reichenbach f. - Daphniphyllanae Takhtajan, Hamamelidanae Takhtajan, Paeonianae Doweld, Saxifraganae Reveal - Hamamelididae Takhtajan, Paeoniidae C. Y. Wu - Crassulopsida Brongniart, Hamamelidopsida Brongniart, Saxifragopsida Brongniart

PERIDISCACEAE Kuhlmann, nom. cons.   Back to Saxifragales

Trees; plants Al accumulators; petiole bundles annular with wing bundles [Soyauxia], also an adaxial plate [Peridiscus] or annular bundle [Whittonia]; crystals +; epidermal wax crystals in rosettes; leaves 2-ranked, (2ndary veins palmate, petiole pulvinate - Peridiscus), stipule single, adaxial, or paired, lateral; inflorescences axillary, racemose-spicate or fasciculate, flowers small; P 4-7, A many, at most slightly connate basally, (anthers monothecal), disc large, annular, hairy or not, G [3-4], ± sunken in disc or not, 1-locular, (placentation free central), with 6-8 pendulous apical ovules, ?type, styles short, stigmas punctate; fruit a drupe or capsule, P deciduous; seed 1, coat tanniniferous, walls thin, ± collapsed; endosperm ?development, copious, cell walls thick, pitted, embryo very small, cotyledons foliaceous; n = ?

3[list]/9. South America, tropical W. Africa (Map: from Heywood 2007).

• Peridiscaceae are tropical trees with entire, stipulate leaves. The racemose inflorescences have small flowers, and the gynoecium has a central column and apical ovules; the style or styles are short. The capsular fruit has a single, large seed with a dark-colored but not very hard coat; the embryo is very small and embedded in cartilagineous endosperm.

Peridiscaceae are a very poorly known and superficially heterogeneous group. For epidermal wax crystals, see Ditsch and Barthlott (1997). The bracteoles are often not very conspicuous (cf. Cronquist 1981). I have not seen Whittonia, but Metcalfe (1962) gives some details of its anatomy.

The basic seed morphology/anatomy of Soyauxia and Peridiscus, from either side of the Atlantic, are almost identical, although the two are vegetatively very different (Peridiscus is sometimes even identified as Menispermaceae!). Peridiscus and Whittonia have monothecal anthers, probably derived within the family.

Peridiscaceae were included in Violales-Flacourtiaceae by Takhtajan (1997); Soyauxia has been associated with Medusandraceae or Flacourtiaceae.

See Soltis et al. (2007b) for general information.

[Paeoniaceae [Altingiaceae [Hamamelidaceae [Cercidiphyllaceae + Daphniphyllaceae]]] [[Crassulaceae [Aphanopetalaceae [Tetracarpaeaceae [Haloragaceae + Penthoraceae]]]] [[Iteaceae + Pterostemonaceae] [Grossulariaceae + Saxifragaceae]]]]: ?

[Paeoniaceae [Altingiaceae [Hamamelidaceae [Cercidiphyllaceae + Daphniphyllaceae]]]: mitochondrial coxII.i3 intron 0

PAEONIACEAE Rafinesque, nom. cons.   Back to Saxifragales

Herbs to shrubs; iridoids, ethereal oils, flavones +, myricetin and tannins 0; cork "subcortical" [Tiagi 1970]; stem with cortical vascular bundles; vessel elements with simple or scalariform perforations; nodes also 5:5; calcium oxalate as crystals; petiole bundles annular; wax tubules with palmitone predominating; indumentum 0 (hairs unicellular); leaves spiral, compound, ultimately ternate, ptyxis variable, margin toothed, base broad, stipules 0; flowers large, terminal, with cortical vascular system, P spiral, K (3-)5(-7), tough, C 5-8(-13), A many, from 5 trunk bundles continuing spiral of C, centrifugal, basal pits?, pollen colporoid, nectary a lobed disc, G (2) 3-5(-15), usu. many ovules/carpel, outer integument 10-20 cells across, massive nucellar cap +, archesporium multicellular, nucellus absorbed before anthesis, stylodium at most short, stigma expanded, rather oblique, sessile, wet; fruit a follicle, K persistent; funicle fleshy, with apical rim-aril, testa fleshy, vascularised, exotestal cells palisade, variously thickened, the hypodermis palisade, ± lignified, (some mesotesta thickened); endosperm nuclear, with amyloid, chalazal haustorium +, embryo initially coenocytic, minute; n = 5, chromosomes 10-15 µm long; germination hypogeal; mitochondrial coxII.i3 intron 0.

1[list]/33. N. Temperate, especially East Asia (Map: from Stern 1946; Hultén & Fries 1986). [Photo - Fruit]

• Paeoniaceae are perennial herbs or shrublets that are recognisable by their rather large, ± ternately compound, exstipulate leaves, and large flowers. The latter have sepals, petals, numerous centrifugal stamens, a prominent disc, and separate carpels. The fruit is a follicle and the seeds are fleshy.

The disc apparently does not secrete nectar (Tamura 2006). Johri et al. (1992) called the micropyle exostomal, however, the inner integument, too, partly forms the micropyle. The testa is thick, fleshy and colored, in some species contrasting in color with the testa of partly developed and unfertilised seeds (blackish/red). The funicle is also fleshy, and there may be a small rim aril at the apex. There is no tegmen.

Paeoniales were included in Ranunculidae (Takhtajan 1997), and a relationship between Paeoniaceae and Ranunculaceae in particular is often suggested (Mabberley [1997] included Glaucidium [see Ranunculaceae] in Paeoniaceae; Takhtajan 1997) because of gross floral similarities between the two. However, they differ in the nature of the petals and nectaries, the development of the androecium, numerous embryological features, etc. (e.g. Tiagi 1970). Dilleniales, in which Paeoniaceae were placed by Cronquist (1981; see Corner 1946), have multistaminate and centrifugal androecia, but differ in gynoecial development, nectary morphology, etc.

For general information, see Tamura (2006), and for evolution and biogeography, see Sang et al. (1997); Tiagi (1970) and Takhtajan (1988) provide much information on ovules and seeds.

[Altingiaceae [Hamamelidaceae [Cercidiphyllaceae + Daphniphyllaceae]]]: cuticle waxes as tubules, nonacosan-10-ol the main wax; anthers valvate, with protruding connectives; embryo long.

Raffinose and stachyose are common oligosaccharides in phloem exudate (Daphniphyllaceae not studied: Zimmermann & Ziegler 1975). Interestingly, there are a number of reports of delayed fertilisation from members of all four families, although not in Paeonia (Sogo & Tobe 2006d for references).

ALTINGIACAEAE Horaninow, nom. cons.   Back to Saxifragales

Trees; resins, route I iridoids +; secretory canals [resins!] in stem; petiole bundle annular, with medullary bundles; stomata paracytic; bud scales +; leaves spiral, flat, lobes conduplicate, 2ndary veins palmate, stipules on leaf base; plant monoecious, inflorescence ± capitate; P 0; staminate flowers: A 4-10, anthers with slits, pollen spherical, polyporate, fine-reticulate, pistillode +; carpellate flowers: intercarpellary protrusions, etc., representing sterile flowers, G [2], unsealed, (semi)inferior, (transverse), 20< straight [atropous] apotropous ovules/carpel [only the lower ones fertile], (micropyle endostomal), stigmas with multicellular protrusions, but no papillae; fruit a septicidal (and loculicidal) capsule; seeds winged, exotesta lignified or not, mesotesta ± sclerotic, endotestal cells oblong, lignified, [or seed exotegmic]; endosperm slight, nuclear; n = 15, 16.

1[list]/13 (for generic limits, see Ickert-Bond & Wen 2006). E. Mediterranean, East Asia to Malesia, Central America (Map: see Vink 1957; Wood 1972; Rzedowski 1978; esp. Ickert-Bond et al. 2005). [Photos - Collection]

• Altingiaceae are monoecious, deciduous trees that may be recognised by their spirally-arranged, usually palmately-lobed leaves with petiolar stipules and by their capitate inflorescences. The buds have scales, and the plants often produce resins.

The fossil Microaltingia (ca 90 million years before present) has prolate, tricolpate pollen grains with a coarsely reticulate exine, a more or less superior ovary, ovaries with 8 or more ovules per carpel, and perhaps unwinged seeds; it may have been pollinated by insects (Zhou et al. 2001). If correctly assigned here, it is yet another fossil with interestingly plesiomorphous features (see also Calycanthaceae, Platanaceae, Fagaceae, etc.). Ickert-Bond and Wen (2006) give dates for divergence of clades within Altingiaceae; the basal split in the family is between the European + American and East Asian clades, dated somewhere between 19.5 and 54 million years before present...

Secretory canals are also reported from Mytilaria (Hamamelidaceae s. str.). There are strongly vascularised phyllomes interior to the staminal whorl; these may be staminodia, nectaries or organs sui generis. The orientation of the carpels varies (Bogle 1986). For the interpretation of the knobs, etc., surrounding the carpellate flowers, see Ickert-Bond et al. (2005). Endocarpial cells are thickened and elongated transverse to the long axis of the fruit, and they look almost palisade in tranverse section of the cells.

The testa is notably thinner than that of most Hamamelidaceae. Ickert-Bond et al. (2005) suggest that in Liquidambar the exotegmen "constitutes most of the seed coat", although it is absent in most Hamamelidaceae, a point also made by others (e.g. Rao 1974). This is not immediately evident in the sections presented (e.g. Fig. 9, G-J) nor in Melikian (1973), but if confirmed (see e.g. Ickert-Bond et al. 2007) it will indeed be a sharp difference to the mesotestal seeds of most Hamamelidaceae.

Shi et al. (2001) present a molecular phylogeny of Altingiaceae, and this suggests that there is only one genus, in contrast to a morphological phylogenies (Ickert-Bond et al. 2005, 2007), which also places the fossil Microaltingia as sister the the extant representatives.

For information about Hamamelidaceae s.l., see Bogle (1986: floral morphology, etc.), Ferguson (1989: general, esp. fossils), Melikian (1973: seed coat anatomy), Zavada and Dilcher (1986: pollen), and Endress (1993: general). This and Hamamelidaceae - "micropyle faces upwards"?

[Hamamelidaceae [Cercidiphyllaceae + Daphniphyllaceae]]]: ?

HAMAMELIDACEAE R. Brown, nom. cons.   Back to Saxifragales

Trees or shrubs; (C-glycosylflavones +); (vestured pits +; true tracheids +; nodes 5:5); sclereids common; petiole bundles annular (with adaxial bundle; arcuate); stomata variable; hairs usu. stellate; bud scales + (0); leaves 2-ranked (opposite, spiral), ± conduplicate-flat or -plicate, (margins entire), 2ndary veins palmate, or strong veins at the very base of the lamina (pinnate), stipules cauline; flowers (2-)4-5(-7)-merous; K free to connate, (0), C usu. ribbon-like, adaxially circinate (0), A often = and opposite K (3-many), staminodia opposite C, (anthers with slits), basal pit uncommon, connective prolonged (not), (pollen 6-rugate), nectary a disc, staminodial, or on base of C, G [2], usu. ± inferior, several-many often epitropous ovules/carpel, outer integument 6-7 cells across, (micropyle zig-zag), hypostase +, styles ± long, stigmas with multicellular protrusions, but no papillae; fruit a loculicidal and septicidal capsule, K often persistent; testa thick, hard, multiplicative, exotestal cells thickened (not), mesotesta massive, usually of fibrous sclerotic cells, hilum large, often discoloration near the hilum, tegmen tanniniferous; endosperm slight, nuclear (cellular - Parrotiopsis), perisperm +, (polyembryony +).

27[list]/82 - three groups below. Tropical to temperate, esp. East Asia to Australia, not South America (Map: from Vester 1940; Vink 1957; Ying et al. 1993; Fl. N. Am. III 1997; Palgrave 2002). [Photos - Collection] [Photo - Flower]

1. Exbucklandoideae Harms

G ± inferior; exotestal cells alone thickened; n = 8, 12.

3/4-14. Exbucklandia, Rhodoleia, Mytilaria. East Asia, to Assam, East Malesia, to Sumatra.

Synonymy: Exbucklandiaceae Reveal & Doweld, Rhodoleiaceae Nakai

2. Disanthoideae Harms

G; n = 8.

1/1: Disanthus cercidifolius. Japan.

Synonymy: Disanthaceae Nakai

3. Hamamelidoideae Burnett

Leaves with craspedodromous venation; anthers with flaps, 1(-3, 2 sterile) ovule/carpel; fruit with ballistic dispersal of seeds; n = 12.

23/78. Tropical to temperate, esp. East Asia to Australia, not South America.

Synonymy: Fothergillaceae Nuttall, Parrotiaceae Horaninow

• Hamamelidaceae are trees or shrubs that may be recognised by their often stellate or tufted hairs, their strongly stipulate leaves which often have ± palmate venation, their smallish flowers borne in rather dense inflorescences, and their bivalved, loculicidal and septicidal capsules with rather large seeds that have a hard, shiny, bicolored testa. The seed are sometimes forcibly ejected. The bases of the branches are often swollen.

The fossil Microaltingia (Altingiaceae) is ca 90 million years old (Zhou et al. 2001), and if Hamamelidaceae are close to Altingiaceae, this also gives a minimum age for Hamamelidaceae. Allonia decandra, a fossil probably to be placed in crown-group Loropetalineae, was collected from the Campanian in the eastern U.S.A., it has twice as many stamens as petals and a lobed disc adaxial to them (Magallón-Puebla et al. 1996); the seeds are rather angled, so there may have been more than one per loculus.

Buds with one bud scale and branches with one or sometimes two prophylls at the very base are common in temperate genera of Hamamelidoideae. Petals vary in shape from rather ordinary looking, to strap-shaped and coiled in bud, to absent; in Parrotiopsis there are showy inflorescence bracts and in Fothergilla plump and showy filaments. Fertilisation is also often much delayed.

Exbucklandioideae in the circumscription adopted here were apparent only in the analysis of ITS data and good sampling (75% bootstrap, better if gaps scored as a fifth character state: Li et al. 1999b; cf. Shi et al. 1998); the three genera have in the past all been placed in separate subfamilies. With rbcL data, Mytilaria alone was rather weakly supported as sister to [Disanthoideae + Hamamelidoideae] (Li et al. 1999a). Within Hamamelidoideae [Corylopsidae (monotypic) + Loropetaleae (weak support)] were sister to the rest, but tribal interrelationships had for the most part only weak support (Li & Bogle 2001).

What is going on with the growth of Exbucklandia? There is variation in the direction of initiation of the stamens in multistaminate androecia (Endress 1976); it can be centripetal (Matudaea) or centrifugal (Fothergilla).

Exbucklandioideae in the circumscription adopted here were apparent only in the analysis of ITS data and good sampling (75% bootstrap, better if gaps scored as a fifth character state: Li et al. 1999b; cf. Shi et al. 1998); the three genera have in the past all been placed in separate subfamilies. With rbcL data, Mytilaria alone was rather weakly supported as sister to [Disanthoideae + Hamamelidoideae] (Li et al. 1999a). Within Hamamelidoideae [Corylopsidae (monotypic) + Loropetaleae (weak support)] were sister to the rest, but tribal interrelationships had for the most part only weak support (Li & Bogle 2001).

Some information is taken from Endress (1970, 1993). For seed anatomy, see Rao (1974) and Zhao and Li (2008), for a classification of Hamamelidoideae, see Li and Bogle (2001), for some distinctive fossils, see Magállon et al. (2001 and references), and for evolution of the flower in Hamamelidoideae, see Magallón (2007; fossils included, optimisation on to more than one topology).

Cercidiphyllaceae + Daphniphyllaceae: plant dioecious, inflorescence racemose; flowers small, K 0; pistillate flowers: G superior.

CERCIDIPHYLLACEAE Engler, nom. cons.   Back to Saxifragales

Deciduous trees; chalcones, dihydrochalcones +; cork in outer cortex; primary stem with continuous cylinder; prophyll adaxial; leaves usu. opposite, involute, (margins entire), 2ndary veins palmate, stipule adaxial-petiolar; P 0, floral apex?; staminate "flower": A 16-34 [= several flowers]; carpellate "flower": G 2-8 [= flowers], each subtended by a bract, suture abaxial, many ovules/carpel, styluli long, stigmas decurrent the entire length; fruit a follicle; seeds winged, chalazal appendage with hair-pin loop vascular bundle, testa undistinguished, exotestal cells enlarged, slightly thickened, tegmen tanniniferous; endosperm development?, slight; n = 19.

1[list]/2. China and Japan (Map: from Heywood 1978; Fu & Hong 2000). [Photos - Collection]

• Cercidiphyllaceae are deciduous trees that may be recognised by the sharp distinction between the very long-lived short shoots and the long shoots; the leaves are more or less opposite, stipulate, and with palmate venation. The plant is dioecious, and what appear to be flowers lack a perianth; staminate flowers have several stamens and carpellate flowers have 2-8 carpels with long, decurrent stigmas. The fruits are follicles.

Palaeocene fossils (Joffrea) have 2-carpellate flowers borne on an elongated axis with the adaxial sutures of the carpels facing each other (Crane & Stockey 1985); the "flowers" of today's species are best interpreted as pseudanthia, indeed, the carpels are sometimes slightly separated from one another on the stout green axis, that of the "pedicel"=inflorescence axis. Both individual carpels and groups of stamens are subtended by bracts and are more or less decussately arranged. Yan et al. (2007) suggest that the bract is really a tepal because it is developmentally so different from the vegetative leaves, although it may have teeth or be almost bilobed; on balance, however, it still seems most likely that the structure is a bract.

Soltis et al. (2005: fig. 6:11) suggest perhaps inadvertently that the gynoecium is partly inferior. Takhtajan (1997) describes the venation of leaves on the long shoots as being pinnate, but the main secondary veins arise within 5(-10) mm of the base. Endosperm type?

For reported variation in nodal anatomy, see Howard (1979), and for general information, see Endress (1993).

DAPHNIPHYLLACEAE Müller Argoviensis, nom. cons.   Back to Saxifragales

Evergreen trees or shrubs; plants Al-accumulators, route I iridoids, triterpene [squalene] alkaloids +, myricetin, hydrolysable tannins, ellagic acid 0; pericyclic fibers 0; pits bordered; true tracheids +; stomata paracytic; plant glabrous; leaves spiral, ± flat, stipules 0; P (0) 2-6; staminate flowers: A 5-12(-24), filaments with 3 traces, ?basal pit, pistillode 0 (+); carpellate flowers: staminodes 0, G [2(-4)], placentation apical-axile to parietal, (1)2 ± apical ovules/carpel, outer integument 5-6 cells and inner integument ca 4 cells across, micropyle zig-zag, hypostase +, styles short, recurved, stigmas rather massive, with multicellular protrusions, but no papillae; fruit a 1-seeded drupe; seed coat persistent but thin-walled and crushed, or endotegmen tanniniferous, walls thickened; endosperm cellular, perisperm slight, embryo short, cotyledons same width as radicle, (polyembryony +); n = 16.

1[list]/10. East Asia to Malesia (Map: from Huang 1997). [Photo - Fruit]

• Daphniphyllaceae are evergreen trees or shrubs that may be recognised by their rather weakly pseudoverticillate, exstipulate, entire leaves which are often glaucous beneath; the petioles of the leaves of a single innovation often vary considerably in length. The subcorymbose, racemose inflorescence with its small flowers with at most inconspicuous perianth is also distinctive.

Some epiplemine Uraniidae (moths) have caterpillars that eat Daphniphyllaceae - and assorted asterids - probably because of the iridoids they have in common (Lees & Smith 1991).

The pith is at least sometimes septate. The flowers may be secondarily superior (D. Soltis et al. 2003b); staminodes can be found in both staminate and carpellate flowers. Bhatnagar and Kapil (1982) describe the endotegmic cells as being thickened and variously cutinised or sclerotic.

Balanopaceae (see Malpighiales) were included in a bigeneric Daphniphyllanae (Takhtajan 1997); Daphniphyllaceae have been difficult to place, sometimes being associated with Euphorbiaceae, etc.

For information on flower, fruit and embryology, see Bhatnagar and Kapil (1982) and for general information, see Zhang and Lu (1989) and especially Kubitzki (2006b).

[Crassulaceae [Aphanopetalaceae [Tetracarpaeaceae [Haloragaceae + Penthoraceae]]]] [[Iteaceae + Pterostemonaceae] [Grossulariaceae + Saxifragaceae]]: cork superficial; petiole bundle(s) arcuate; cuticle waxes not tubular; ovules apotropous [all?]; K persistent, withered; endosperm cellular.

[Crassulaceae [Tetracarpaeaceae [Haloragaceae + Penthoraceae]] [[Saxifragaceae [Iteaceae + Pterostemonaceae]] Grossulariaceae]] - from Morgan & Soltis (1993); Aphanopetalum (ex Cunoniaceae) is to be placed in the first major clade. Mauritzon (1933) provides information on the ovules and endosperm development for many taxa in this clade.

Crassulaceae [Aphanopetalaceae [Tetracarpaeaceae [Haloragaceae + Penthoraceae]]]: stem with endodermis; nodes 1:1; stipules 0; pollen 3-colporate.

CRASSULACEAE Jaume Saint-Hilaire, nom. cons.   Back to Saxifragales

Succulent herbs to soft-stemmed shrubs, often crassulacean acid metabolism; flavones, acylated flavonol glycosides, sedoheptulose [sugar reserve], non-hydrolysable tannins +, hydrolyzable tannins 0; red pigment common, even in roots; (cork cortical); vessel elements with simple perforations; young stem with separate bundles; (medullary bundles +); sieve tube plastids lacking starch grains [and protein inclusions]; rays 0; nodes also 1:1-3, 3:3, etc.; cuticle waxes very variable; stomata usu. anisocytic; leaves succulent, ptyxis flat to curved, margins entire (serrate), hydathodes +; inflorescence cymose; A obdiplostemonous, anthers median sagittate, latrorse, G 3-10(+), ± free, (placentation parietal), opposite C, nectaries [ougrowths of carpels] at base, 1-many ovules/carpel, micropyle bistomal, outer and inner integuments 2 cells across, styles usu. short, stigmas not to moderately capitate; fruit a follicle; exotestal cells with outer wall ± thickened, inner pigmented layer +; endosperm mostly cellular and variants, chalazal haustorium +, embryo long, suspensor uniseriate, basal cell with mycelium-like haustorial branches; x = 8; germination epigeal and phanerocotylar.

34[list]/1370 - three subfamilies below. Cosmopolitan, esp. the Cape region and Mexico, but few in S. South America and Australia, not in Polynesia, frequently in drier regions. (Map: incomplete - see Hultén 1958; Bywater & Wickens 1983; Jürgens 1995; Thiede 1995). [Photo - Flower]

1. Crassuloideae Burnett

Leaves opposite, with several marginal hydathodes only; A = K, slightly introrse, (odd carpel abaxial - Tillaea), ovules tenuinucellate, (archesporium multicellular); follicles releasing seeds through apical pore; testa sinuate-unipapillate; first division of micropylar endosperm cell in horizontal plane; n = 7, 8.

2/196: Crassula (195). Southern Africa, to S.W. Arabia, "Tillaea" more or less world-wide, the only representative of the family in Australia.

The testal cells often have a single papilla and sinuous anticlinal walls (e.g. Bywater & Wickens 1983).

Kalanchoideae + Sempervivoideae: lamina with single (sub)apical hydathode; (placentae lobed); seeds costate; first division of micropylar endosperm cell in vertical plane.

2. Kalanchoideae A. Berger

Plant ± woody; bufadienolides +; crystal sand +; C connate, A with spherical connective prolongation, (style +); seeds 4-6-costate, with a micropylar corona; x = 9 [n = 9, 17 (18)].

4/200: Kalanchoe (145), Tylecodon (46). Old World, especially the Karroo in southern Africa, but extending to South East Asia and Malesia, not Australasia.

3. Sempervivoideae Arnott

(Pyrrolidine and piperidine alkaloids +, nonhydrolyzable tannins 0 - esp. Sedum acre group); leaves (opposite); flower 4-32-merous, (C connate), nucellus elongated; (follicle with abaxial dehiscence in Diamorpha); seeds >6-costate; suspensor with vertical division in micropylar cell; n = 5<, much variation.

28/975: Sedum (420), Echeveria (140), Sempervivum (65), Rhodiola (60), Dudleya (47). Largely N. hemisphere.

All ca 200 species of the Echeveria group appear to be interfertile, a remarkable situation apparently without parallel in flowering plants (Uhl 1992). Moreover, generic limits are unclear, and many genera, some previously placed in what were considered to be different subfamilies, e.g. Sedoideae and Echeverioideae, hybridise (e.g. Uhl 1976; 't Hart et al. 1999). However, Sedum itself occurs in five of the seven main clades apparent in phylogenetic analyses (van Ham 1995; van Ham & 't Hart 1998; Mayuzumi & Ohba 2004); Graptopetalum is also very difficult (Acevedo-Rosas et al. 2004). Thiede and Eggli (2006) provide a guide through the chaos; note that they prefer to retain a paraphyletic Sedum.

There have been several origins of sympetaly in Sedoideae ('t Hart et al. 1999); both it and epipetaly tend to be weak.

• Crassulaceae are recognisable by their succulent herbaceous or soft-stemmed habit, and their flowers, which have the same number of sepals, petals and carpels; the latter are more or less free and have nectariferous scales at their bases. The fruits are usually follicles.

Crassulaceae may be some 77-69 million years old, with diversification beginning 41-39 million years before present (Wikstöm et al. 2001). The distinctive wood, which lacks rays and has very short vessel elements with annular and helical thickening, is probably paedomorphic (t'Hart & Koek-Noorman 1989); plant chemistry, in particular the presence of hydrolyzable tannins and the absence of non-hydrolyzable tannins, as in other woody Saxifragales, is consistent with this idea (Thiede & Eggli 2006). Crassulacean acid metabolism (CAM) is common throughout the family (e.g. references in Winter & Smith 1996a). Some species of Kalanchoe produce plantlets, foliar embryos (Yarborough 1932), in notches at the margin of the leaf blade. Both embryogenetic and organogenetic pathways have been coopted, and the young plantlets have cotyledon-like first leaves; species in which development of plantlets is consitutive do not produce viable seed (Garcês et al. 2007).

The basic phylogenetic structure of the family seems fairly well established (e.g. van Ham 1995; van Ham & 't Hart 1998; Mort et al. 2001; Mayuzumi & Ohba 2004). The rather highly derived Crassuloideae are sister to the rest of the family; Kalanchoe and relatives are sister to the rest of Sedoideae, and this is in some respects a rather plesiomorphous group (e.g. Mort et al. 2001; Mort 2002; Thiede & Eggli 2006). For the phylogeny of Kalanchoe and variation of CAM within it, see Gehrig et al. (2001) and Kluge and Brulfert (1996).

Anthocyanin is also found in the roots of Saxifragaceae, as well as Melastomataceae, Balsaminaceae, Asteraceae, Droseraceae, and Francoaceae (Krach 1976; Molisch 1928). Sedoheptulose is the most abundant sugar in Crassulaceae; isocitrate is common, unlike other succulents (Thiede & Eggli 2006). The sieve tube plastids are in the form of a distinctive variant, lacking starch, the S₀ type (Behnke 1988). The increase in numbers of flower parts in Sedoideae - some have a multistaminate androecium - is in the context of an increased merousness of the whole flower; the relation between the number of parts of each whorl is unchanged from that of a basic core eudicot flower (see also the asterid I + II clade).

For (mistaken) reports of cortical vascular bundles, see Thiede and Eggli (2006). The lamina usually lacks palisade tissue, and the stomata are often on both sides. The stomata may also be heliocytic, with an additional ring of distinct cells outside a basically anisocytic configuration. There is sometimes only a single vascular trace to the calyx (t'Hart & Koek-Noorman 1989). The ovary is secondarily superior (D. Soltis et al. 2003b). The nucellar epidermal cells seem to be large and more or less radially elongated in Crassuloideae and Kalanchoideae (Mauritzon 1933). There is no tegmen. Spongberg (1977) notes that the endosperm is usually scanty, while Mabberley (1997) describes it as being copious; the former is correct. For the base chromosome number of the family and of its major clades, see Mort et al. (2001).

Some general information is taken from Spongberg (1977); for embryology, etc., see Mauritzon (1933) and Subramanyam (1970), for chemistry, see Stevens (1995), for general recent accounts of the family, see Eggli (2003: enumeration of all species) and in particular Thiede and Eggli (2006).

Synonymy: Cotyledonaceae Martynov, Rhodiolaceae Martynov, Sedaceae Adanson, Sempervivaceae Durande, Tillaeaceae Martynov

Aphanopetalaceae [Tetracarpaeaceae [Haloragaceae + Penthoraceae]]: ?

APHANOPETALACEAE Doweld   Back to Saxifragales

Viny shrub; chemistry?; pericyclic fibers 0; petiole with 3 (1) bundles; leaves opposite, leaf teeth with a single vein, stipules +, looking like teeth; inflorescence cymose or flowers solitary; flowers 4-merous, hypanthium short, C 0 [rudiments visible only when very young], pollen with rugulate-stellate surface, G seminferior, opposite C, 1 apical epitropous ovule/carpel, micropyle bistomal, style +, with four canals, styles short; fruit a nut, K enlarging; seed coat?; endosperm development?, embryo curved, size?; n = ?

1/2. W. and E. Australia (Map: partly from FloraBase 2004). [Photo - Flower.]

• Aphanopetalaceae are scrambling shrubs with prominently lenticellate stems, opposite and more or less serrate leaves with minute "stipules", and axillary inflorescences. the flowers are apetalous and have a spreading calyx that enlarges in fruit; the fruit itself has a single seed.

The ray parenchyma stores starch. Two small bundles soon diverge from the main leaf trace. It is unclear if the stipules "are" stipules or colleters (Kubitzki 2006b). As in Saxifragaceae and Iteaceae, the vascular trace in the petal plane gives a branch to the lateral sepal position, also carpel wall and lateral carpel traces and a single stamen trace; the trace in the sepal plane supplies the carpel wall and median carpel bundle and stamen trace.

Some information is taken from Jensen (1968: vascular system), Bensel and Palser (1975b: floral anatomy), Dickison (1980b: nodal anatomy), Dickison et al. (1994: anatomy) and Kubitzki (2006b: general).

Tetracarpaeaceae [Haloragaceae + Penthoraceae]: ?

Although combination of these three rather small families is an option in A.P.G. II (2003), there seems to be little or nothing holding them together (see also Moody & Les 2007).

TETRACARPAEACEAE Nakai   Back to Saxifragales

Evergreen shrub; chemistry?; plant glabrous; leaves spiral, petiole short; inflorescence racemose; floral apex convex; flowers 4(-5)-merous, C spatulate, A 4-8, basal pits?, fibrous endothecium 0, nectary 0, G 4 (5), opposite C, many ovules/carpel, micropyle exostomal, stigmas sessile, not expanded; fruit a follicle; exotestal cells ± elongated longitudinally, outer walls thickened, no mechanical layer; endosperm development?, embryo size?; n = ?

1/1 (Tetracarpaea tasmannica). Tasmania. [Photo - Habit]

The teeth are perhaps hydathodeal, but there are no water pores. The ovary is apparently secondarily superior (D. Soltis et al. 2003b).

See Hils et al. (1988: anatomy) and Kubitzki (2006b: general) for information.

Penthoraceae + Haloragaceae: ?

PENTHORACEAE Britton, nom. cons.   Back to Saxifragales

Rhizomatous herbs; flavonoids +, flavones, myricetin, non-hydrolysable tannins 0; cork ?; young stem with pseudosiphonostele; endodermoid layer?; pericyclic fibers 0; leaves spiral, supervolute, amphistomatic, teeth hydathodal, colleters +; inflorescence cymose, flowers 5-7-merous; hypanthium +, C 0(-7), A 2x K, lacking a basal pit, latrorse, G [5-8], half inferior, apical parts free, opposite K, becoming superior, many ovules/carpel, placentae intrusive, adaxial, micropyle?, funicles long, styluli submarginal, short, stigmas capitate; free part of each carpel basally circumscissile in fruit; exotestal cells with outer wall ± thickened, micropylar operculum endostomal, tegmen otherwise crushed; suspensor large, embryo large; n = 8 (9).

1[list]/2. East and South East Asia, E. North America (Map: from Hong 1993). [Photo - Penthorum Inflorescence]

• Penthoraceae are rather fleshy herbs with spiral, entire leaves. They may be recognised by their few-branched, monochasial cymose inflorescence, and often apetalous flowers with partly connate carpels with submarginal styles. The fruits are distinctive since the free part of each carpel splits circumscissilely at the base.

Although stem group Penthoraceae have been dated to 77-69 million years before present (Wikström et al. 2001), the E. North American/East Asian disjunction is dated to 6.5-2.4 million years before present (Thiede 2006 for references).

Cork in the root is initiated in a superficial position (van Tieghem 1899). The sepals are unequal in size and the bracts are lateral to the pedicels. There is a much-enlarged but non-dividing micropylar cell in the embryo suspensor - cf. Haloragaceae and their haustorial suspensor. Danilova (1996) shows the carpels opposite the calyx. The first two pair of seedling leaves are opposite.

See Spongberg (1972, in Saxifragaceae: general), Haskins and Hayden (1987: anatomy), Gornall (1998: as Saxifragaceae) and Thiede (2006: general) for information.

HALORAGACEAE R. Brown, nom. cons.   Back to Saxifragales

Aquatic or amphibious to shrublets (small trees); flavones +, flavonols 0; cork ?; vessel elements with simple perforations; often calcium oxalate crystals in hair-like cortical cells; cuticle waxes 0 (parallel platelets); leaves opposite (spiral), conduplicate-flat, (pinnately compound), colleters +?; plant monoecious (dioecious; flowers perfect), inflorescence dichasial, cymose or fasciculate, or flowers solitary; flowers small, (2-)4-merous, K valvate, C deciduous (0), A 8 (= and opposite K), (anthers apiculate), basal pits?, pollen trinucleate, 4-6(-20-colpate or -porate, G inferior (sub 1-locular), opposite C or odd member adaxial, 1 (2) pendulous ovules/carpel, nucellar cap, hypostase and poorly developed funicular obturator +, styles (0) with swollen bases, stigmas capitate or not, penicillate, dry; fruit nut-like, (schizocarpic), exocarp often ornamented, stones 1- or 4-seeded; exotesta (and hypodermal layer) persistent, thin-walled, rest obliterated; endosperm +, (nuclear), starchy, haustorial suspensor +, embryo long (short); n = 6, 7 (8).

8[list]/145: Myriophyllum (60). World-wide, but especially Australia (Map: from van Steenis 1962; Hultén 1958, 1971; van der Meijden 1971; Wood 1972). Proserpinacea is a common fossil in Europe and Asia, but the genus is no longer found there. [Photo - Collection.]

• Haloragaceae are rather small, usually monoecious, often more or less herbaceous plants. Their leaves are serrate or deeply lobed, small, and often opposite or whorled, and their flowers are small (Haloragodendron is an exception) and have penicillate stigmas.

Hernández-Castillo and Cevallos-Ferriz (1999) suggest that the fossil Tarahumara sophiae (found in Mexico in deposits laid down ca 70 million years before present) had carpels free from one another but adnate to a hypanthial wall, while its fruit is described as being drupe-like, so its morphology is unlike that of any extant member of the family.

See Moody and Les (2001, 2004 and especially 2007, note that in the latter study the nuclear ITS was in some conflict with chloroplast genes) for relationships within the family, which may have an Australian origin. The woody [Glischrocaryon + Haloragodendron] clade is sister to other Haloragaceae (the monophyly of the two genera themselves is not certain), and although much of the rest of the family forms a clade (the trimerous Trihaloragis is sister to all other members of this clade), relationships of this clade are uncertain, Meionectes and Proserpinaca in particular being of uncertain position (Moody & Les 2007). Moody and Les (2007) point out the extensive variation in floral meristicity in the family.

Nodal anatomy was observed in Haloragis erecta and Laurembergia, ptyxis in the first. Pelargonidin occurs in leaves, as in Saxifragaceae (Doyle & Sogin 1988). Adventitious roots arise between the leaves in Haloragis. Myriophyllum appears to have endostomal ovules (Batygina et al. 1985), while Bawa (1970) noted that the archesporial cell is hypodermal, i.e. the ovules is tenuinucellate. Corner (1976) describes the endosperm as being starchy.

The monotypic Haloragales were placed near Saxifragales by Takhtajan (1997). Historically Gunneraceae and Haloragaceae have been associated, although their pollen is quite different (e.g. Praglowski 1970), the perianth of Gunneraceae is not differentiated into two whorls of sepals and petals, etc.; for the former, see Gunnerales.

Some information is taken from Orchard and Keighery (1993: Meziella), Orchard (1975) provided a partial monograph of the family (Antipodean taxa), with much detail on floral anatomy, etc., and Kubitzki (2006b) summarized what is known about it; see Praglowski (1970) for pollen.

Synonymy: Cercodiaceae A.-L. de Jussieu, Myriophyllaceae Schultz-Schultzenstein

[Iteaceae + Pterostemonaceae] [Grossulariaceae + Saxifragaceae]: leaves spiral; hypanthium +, A = and opposite K; fruit septicidal.

Iteaceae + Pterostemonaceae: C-glycosylflavones +; stipules +; placentation axile, micropyle?, style +; endosperm sparse.

Fossils assignable to this clade are ca 90 my old (Crepet et al. 2004 for references).

Combination of the two families is optional (as Iteaceae s.l.), see A.P.G. II. For the chemistry of these families, see Bohm et al. (1999). Pterostemon also has flavones, in this being like other Saxifragales.

ITEACEAE J. Agardh, nom. cons.   Back to Saxifragales

Trees to shrubs; allitol +, flavonols, ellagic acid 0; hairs unicellular; young stem with separate bundles; pith chambered; leaves conduplicate, margins spiny- or gland-toothed, stipules small, on leaf base or adjacent stem; inflorescence axillary, racemose to paniculate, flowers rather small; C valvate, anthers lacking basal pits, connective forming apical protrusion, pollen bilateral, 2-porate, ektexine homogeneous, disc or nectary lining hypanthium, G [2] to subinferior, many ovules/carpel, stigma punctate-lobed, wet; fruit valves often attached by the stigma; exotestal cells with outer walls thickened; (endosperm moderate - I. rhamnoides); n = 11.

1[list]/18. South East Asia to W. Malesia, E. North America, E. and S. Africa (Map: from Mai 1985; Aubréville 1974a; Palgrave 2002; Heywood 2007). [Photo - Itea Flower]

• Iteaceae may be recognised by their stems with chambered pith, spirally-arranged serrate leaves with superposed axillary buds, paniculate to racemose inflorescences with rather small flowers, and septicidal fruits the valves of which often remain attached by the stigma. The flowers have a hypanthium, the corolla is valvate, and there are only two carpels.

The fossil Divisestylus, from the late Cretaceous some 90 million years before present, has five stamens opposite the sepals and ovaries and stigmas fused, but there are separate styles; however, the pollen is tricolpate and striate, suggesting that the 2-porate pollen mentioned above is not a synapomorphy for the whole clade (Hermsen et al. 2003), merely for the crown group.

Choristylis (= Itea) lacks axial parenchyma. It is sometimes described as being unitegmic, with the integument 6-7 cells across, but this appears to be incorrect (Kubitzki 2006b). Although the carpels are free initially, they become connate, even along the style (Ge et al. 2002 - so perhaps techically the styles really are simply postgenitally connate styles). The distinctive pollen is known fossil in Europe. Interestingly, Ribes divaricatum has pentacolpo-di-orate pollen (Weigend 2006).

For additional information is taken from Spongberg (1972: general), Bensel and Palser (1975b: floral anatomy), Ramamonjiarisoa (1980: anatomy), Gornall et al. (1998: general), Ge et al. (2002: floral development) and Kubitzki (2006b: general).

PTEROSTEMONACEAE Small, nom. cons.   Back to Saxifragales

Shrubs; conical to peltate glandular hairs +; vessel elements also with simple perforations; stipules cauline, minute; inflorescence a corymbose cyme; hypanthium?, K valvate, A 5, opposite K, filaments flattened, toothed, anthers with basal pits?, pollen 3-colporate, 5 staminodes opposite C, disc 0, G [5], largely inferior, orientation?, 4-6 ascending ovules/carpel, (± radiating styles +), stigma capitate, ?type; C also persistent in fruit; seed coat "cartilaginous"; n = ?

1[list]/3. Mexico (Map: from Smith et al. 2004).

• Pterostemonaceae look rather like Rosaceae, both being woody and having spiral, serrate, stipulate leaves, although the leaf blades of Pterostemonaceae tend to be notably shiny. However, the distinctive conical to peltate glandular hairs, the exudate of which produces the shiny leaf surface, and the flowers, each with a whorl of five stamens that have winged and toothed filaments and a whorl of five staminodes, allow the family to be recognised.

The pericyclic fibers seem to be weakly developed and the androecium is obdiplostemonous. Similar peltate glandular hairs are known from Grossulariaceae.

For information, see Goldberg (1986), Wilkinson (1994, 1998) and especially Kubitzki (2006b), but the family is not well known.

Grossulariaceae + Saxifragaceae: G [2-3]; (endosperm helobial).

GROSSULARIACEAE de Candolle, nom. cons.   Back to Saxifragales

Shrubs; cork outer cortex/pericyclic; (vessel elements with simple perforations); underground stems with endodermis; pericyclic fibers 0; leaves conduplicate-plicate, margins also lobed, teeth hyadthodal, 2ndary veins palmate, leaf bases broad and with thin margins (paired prickles at the nodes); inflorescence racemose, (flowers 4-merous); nectary at base of well-developed hypanthium, C small, open, (staminodes +; A 10), pollen 5-15-porate, with distinctively rugose ectoapertures, tectum complete, G inferior, usu. median, placentation parietal, many ovules/carpel, outer integument 3-5 layers across, hypostase +, style +, styles ± developed, stigma capitate, wet; fruit baccate; seeds hard, arillate, exotestal cells palisade, mucilaginous [all told this layer 3-6 cells thick], endotestal cells crystalliferous, radial and inner walls lignified, ?tegmen cells elongated, tanniniferous; endosperm hemicellulosic, embryo short; n = 8, chromosomes 1.5-2.5 µm long; germination epigeal.

1[list]/150: Ribes. Temperate N. hemisphere, also along the Andes (Map: see Hultén & Fries 1986; Jalas et al. 1999; Malyschev & Peschkova 2004 - incomplete). [Photos - Collection.]

• Grossulariaceae may be recognised by their lobed, spiral leaves with broad bases, and flowers with a well-developed hypanthium, relatively large and colored sepals and smaller petals, a usually bicarpellate gynoecium, and parietal placentation; the fruit is baccate.

The fruits of Ribes are an important food for Andean frugivorous birds. A number of fungi, including the white pine blister rust (the basidiomycete Cronartium ribicola), spend part of their life cycles on the plants of this genus, and a number of insects eat them (Weigend 2006).

Stem collenchyma is well developed. Nectar glands are reported from the anthers in some species.

Some information is taken from Cutler and Gregory (1998: anatomy); see Weigend et al. (2002) and Senters and Soltis (2003) for phylogenies of Ribes, and Weigend (2006) for a general account.

Synonymy: Ribesiaceae Marquand

SAXIFRAGACEAE Jussieu, nom. cons.   Back to Saxifragales

Largely herbs; cork also pericyclic; vessel elements usu. with simple perforations; young stem with separate bundles [pseudosiphonostele]; nodes also 1:1, 1:2 and 3<:3<; petiole bundles also annular (with medullary or adaxial bundles); hairs (uni-)multiseriate with multicellular glandular head; leaves (opposite), (bases sheathing), ptyxis variable, (margins entire), 2ndary veins usu. palmate, stipules basal or sub-basal on petiole, persistent, or cauline [Astilbe], or 0, colleters +; (flowers obliquely monosymmetric); pollen colpate, colporate, or 6-9-porate, nectariferous disc + (0), G to inferior, (free, or apical parts quite often free), orientation variable, placentation parietal to axile, many ovules/carpel, styles + [no compitum], stigmas spatulate to capitate, wet or dry; fruit also a follicle; exotestal cells with outer wall (radial walls) ± thickened, inner pigmented layer + (endotegmen thick-walled [Heuchera, Tolmeia]; crystalliferous); endosperm moderate, embryo medium (large); n = (5-)7(+); chloroplast rpl2 intron 0.

Ca 33[list]/540 - two groups below. Mostly N. temperate and Arctic (S. temperate, tropical mountains) (Map: from Hultén 1958, 1971; Meusel et al. 1965 - incomplete). [Photos - Collection]

1. Saxifraga s. str.

1/370. Mostly Arctic and tropical montane.

2. The Rest

Flowers (3-10)-merous; (hypanthium 0), C morphology variable, (0), A (3-10, (ob)haplostemonous, pollen colpate, colporate, or 6-9-porate, disc + (0), G [(3-5)], ovules unitegmic.

Ca 32/170: Micranthes (70), Chrysosplenium (55), Heuchera (35). Mostly N. temperate (tropical montane and Arctic).

• Saxifragaceae can be recognised by their herbaceous habit and gland-toothed leaves; stipules, when present, are often on the petiole near the base. The flowers often have 2-3 carpels that are basally connate, although the styluli are clearly free, a nectariferous disc is common, and the fruit is a follicle or septicidal capsule.

Short-cycle Puccinia rusts are frequently found on Saxifragaceae s. str. (Savile 1979a, b). The moth Greya (Prodoxidae), related to Tegeticula, of yucca moth fame, is both a seed predator and pollinator of some Saxifragaceae (Segraves & Thompson 1999); this association is being studied in considerable detail, clarifying the diversification of both plant and pollinating seed parasite (Rich et al. 2008 and references). It has even been suggested that the general lability of ovary position in the family is connected by selection by such pollinators (Soltis & Hufford 2002). Mitella (and a few other Saxifragaceae) is very largely pollinated by fungus gnats, and this association seems to have evolved in parallel; since taxonomists have classified on pollination syndrome (and there are also similarities in fruit type, etc., involved), Mitella has turned out to be polyphyletic (Okuyama et al. 2008). Flowers involved are often more or less broadly saucer-shaped and the petals have very narrow lobes. A number of forest-dwelling Saxifragaceae are pollinated by rain, whether by a splash cup mechanism, as in Mitella, or by the seeds being thrown from the fruit as it moves violently after being hit by a drop of water.

Saxifragaceae can be confused with Rosaceae (Astilbe [Saxifragaceae] and Aruncus [Rosaceae - Rosales] are particularly similar), however, the carpels of former are usually two and basally connate rather than several to many and free, and they have five or ten rather than fifteen to many stamens. The two families are not close.

Over 50 vascular bundles may enter the petiole base in some taxa! Hydathodes are common. In at least some species of Saxifraga, and in Astilbe and Rodgersia, the two carpels are oblique, but in the latter two this is associated with inverted floral orientation, the odd K being abaxial. Many other taxa have median carpels, and the androecium is obdiplostemonous (Eichler 1878; Engler 1930a; Eckert 1966). Variation in ovary position within the family is extreme, even occuring within genera and between the different morphs of heterostylous flowers (e.g. Kuzoff et al. 2001; Soltis & Hufford 2002). Darmera (see below) has only one integument that is 4-6 cells thick (Gornall 1989).

There are two major clades in Saxifragaceae, Saxifraga s. str., largely arctic-alpine, and the Heuchera clade, the rest of the family and predominantly temperate. Members of the latter clade contain the bulk of the floral variation in the family (Soltis et al. 2001). Generic limits in this latter group are unclear (Soltis et al. 1996, and refs.; Okuyama et al. 2008); hybridisation is extensive and there are various combinations of chloroplast and nuclear genomes. For example, the chloroplast genome of Tellima is also found in Mitella (e.g. Soltis et al. 1993).

The distribution of druses and acicular crystals is of systematic interest (Gornall 1987); only Saxifraga s.l. has been studied in detail. In Saxifraga s. str. the diploid chromosome number varies from 12-ca 200, in Micranthes from 10-120. The inflorescence of Saxifraga s. str. often has cauline bracts, however, that of Darmera is scapose, and there are pollen and testa surface differences between the two.

In the past, "intermediate" genera were kept in Saxifragaceae because the inclusion of more odd genera had little effect on the family description since it already included so much variation, but if placed in Crassulaceae, for example, they would greatly affect its description and hence make that family less discrete. Many woody, tenuinucellate and unitegmic members in particular ithat used to be included in Saxifragaceae are entirely unrelated to that family and to each other. Of Saxifragaceae in the old and broad sense, Escallonia (unplaced asterid II), Hydrangea (Cornales) and many other woody taxa are asterids, while Parnassia is Parnassiaceae-Celastrales (a conclusion in agreement with data from floral anatomy - e.g. Bensel & Palser 1975a, d). A division between Saxifragaceae + Grossulariaceae, with their petals that remain very small for quite some time during development, and Hydrangeaceae, with their large petals and septicidal capsules, was evident (Gelius 1967). However, the unitegmic Darmera is properly to be retained in Saxifragaceae (Gornall 1989). Fehrenbach and Barthlott (1988) included Dichroa (Hydrangeaceae-Cornales), Francoa (Francoaceae-Geraniales), and Vahlia (unplaced asterid I) as well as Penthorum (Penthoraceae) and Saxifragaceae s. str. in their survey of cuticle waxes, but no significant differences between the species in these very different groups were noted.

Some information is taken from Morf (1950) and Spongberg (1972), details of vegetative anatomy from Thouvenin (1890) and Gornall (1998) and details of floral anatomy from Bensel & Palser (1975b).

Synonymy: Brachycaulaceae Panigrahi & Dikshit, Pectiantiaceae Rafinesque

CYNOMORIACEAE (Schott & Endlicher) Lindley, nom. cons.   Back to Saxifragales

Echlorophyllous root parasite; vessel elements?; cork?; hairs 0; leaves spiral; plant monoecious, inflorescence capitate; flowers minute, P (1)4-5(-8), basally connate or not; staminate flowers: A 1, adnate to P, pollen colporate, ?nectary-stylodium +; carpellate flowers: staminodia 0, G 1, inferior, 1 pendulous straight [atropous] unitegmic ovule, integument 5-7 cells thick, nucellar cap +?, style long, channeled; fruit an achene; testa ca 7 cells across, persistent, cells little thickened; endosperm cellular, copious, thick-walled, embryo undifferentiated; n = 12, size strongly bimodal.

1[list]/2. Mediterranean to C. Asia (Map: from Jalas & Suominen 1976; the Parasitic Plants Website 2004). [Photo - Habit © D.L. Nickrent]

The host is often a member of Cistaceae; the root has root hairs.

Perfect flowers are also known. The perianth is less well developed in pistillate than in staminate flowers, and there is debate as to its morphological nature. The pistillode in staminate flowers may be superior or inferior, according to Hooker (1856). The channeled style has two vascular bundles, together a rather odd combination.

A number of other Saxifragales have cellular endosperm.

Cynomoriaceae have usually been included in Balanophoraceae or Balanophoranae (e.g. Cronquist 1968; Takhtajan 1997).

For details of seed anatomy, see Takhtajan (2000), for morphology, see Weddell (1860), for ovule, etc., see Juel (1902) and Teryokhin et al. (1975), and for general information, see the Parasitic Plants website (Nickrent 1998 onwards).