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 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), where on the tree a thicker nucellus and a stylar epidermal layer are acquired has not yet been indicated.

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

[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (veins in lamina often 7-17mm/mm² or more [mean for eudicots 8.0]); (stamens opposite [two whorls of] P); (pollen tube growth fast).   Back to Main Tree

[CERATOPHYLLALES + EUDICOTS]: ethereal oils 0.

EUDICOTS  Back to Main Tree

Myricetin, delphinidin scattered, asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; K/outer P members with three traces, "C" with a single trace; A few, (polyandry widespread, initial primordia 5, 10, or ring, ± centrifugal, numbers of C/G usually not changed), anthers basifixed, filaments fairly slender; microsporogenesis simultaneous, tetrads tetrahedral, pollen tricolpate, apertures in pairs at six points of the young tetrad [Fischer's rule], cleavage centripetal, wall with endexine; G with complete postgenital fusion, stylulus/style solid [?here]; seed coat?

Evolution. Divergence & Distribution. An older meso/megafossil-based estimate for this clade is ca 100 million years (Crepet et al. 2004). However, tricolpate pollen from the Late Barremian-Early Aptian of the Cretaceous some 127-120 million years before present is known, and from that point of view an age of some 125 million years for the eudicots seems reasonable (e.g. Magallón et al. 1999; Sanderson & Doyle 2001), and this age is similar to that of the oldest monocot fossils; Moore et al. (2007) suggest an age of 131.1-118.5 million years for diversification of the eudicot crown group. However, as Smith et al. (2010) note, when tricolpate pollen first appears in the fossil record it is widely dispersed geographically and somewhat heterogeneous (see also Friis et al. 2006b), implying an earlier origin of the clade. Their estimates range from (147-)137(-128) million years old (with eudicot calibration) to (172-)153(-138) million years (without: Smith et al. 2010, see also their Table S3). Other estimates of the age of diversification within the eudicots range from (139-)130, 129(-123) million years (see Bell et al. 2010 for details). The recent discovery of the fossil Leefructus that is at least 122.6 million years old and is assigned to stem group Ranunculaceae (Sun et al. 2011) would also imply a substantially greater age for Ranunculales - and hence the whole eudicot clade - of some ca 152-140 million years or so (this estimate is based the suggestions of the ages of various clades in Ranunculales made by Anderson et al. 2005). Note that although the fossil described by Sun et al. (2011) seems quite well preserved, it is not associated with pollen.

Subsequent divergence of eudicot clades like Proteales, Buxales, etc., was rapid, occurring 120-116 million years before present (Anderson et al. 2005). Note, however, that Wikström et al. (2003) suggest an age of 147-131 million years before present for the clade, while Soltis et al. (2008: a variety of estimates) suggest an age of divergence of Ranunculales from other eudicots of 152-110 million years; ages of divergence of other eudicot clades below core eudicots are uncertain since the topology there is different - [Proteaceae [Sabiaceae [Buxaceae [Trochodendraceae + core eudicots]]]] - from that used (tentatively) here.

Floral Biology. Chanderbali et al. (2010) found that expression of genes active in each floral whorl in flowers of the one Ranunculales they examined (Escholtzia - Papaveraceae) were restricted to that whorl, as in other eudicots, however, expression of genes active in the two outer floral whorls in Delphinium (Ranunculaceae) were not sharply differentiated (Voelckel et al. 2011).

For the possible functional significance of the evolution of triaperturate - or multiaperturate - pollen, see e.g. Dajoz et al. (1991), Halbritter and Hesse (2004), and Furness and Rudall (2004); the occurrence of several apertures on one grain may increase the speed of germination of the pollen but at the same time decrease its viability, and also affect its harmomegathic movements.

Genes & Genomes. Salse et al. (2009) suggest the common ancestor of this clade had seven protochromosomes.

Chemistry, Morphology, etc. Cuticle waxes as clustered tubules, nonacosan-10-ol the main wax, could be optimised to this position, later being lost in Sabiaceae, Platanaceae, Buxales, and perhaps also in core eudicots... (but they are present in a few Santalales, also in woody Saxifragales: see Barthlott et al. 2003). Doyle (2007) scored chloranthoid teeth as plesiomorphous for eudicots; given current ideas of phylogeny, they may be an apomorphy here. He also considered palmate-crowded veins to be an apomorphy for all eudicots, but Sabiaceae were not mentioned. The interpretation of the venation of Euptelea is debatable, as he noted (Doyle 2007), and the palmate venation found in aquatics like Nelumbo further confuses the situation; palmate venation is common in aquatics and seems to be associated with the aquatic life style.

For a valuable survey of floral morphology of the whole eudicot clade, see Endress (2010c); "a first [sic] attempt to characterize the major subclades of eudicots", including other than "conventional features" (ibid. p. 540); characterizations are a mixture or apomorphies and plesiomorphies, with an emphasis on "tendencies". Dimerous flowers are scattered through the basal eudicot grade, but are at least very uncommon in taxa at the node above core eudicots and in monocots (Drinnan et al. 1994; Soltis et al. 2003; Wanntorp & Soltis et al. 2005; Ronse De Craene 2005; Doust & Stevens 2005; Kramer & Zimmer 2006; Moody & Les 2007 [this with examples of variation in the core eudicot Haloragaceae]); Endress 2010 c) also emophasizes that the flowers may be trimerous. Stamens are also quite often inserted opposite the tepals in the basal eudicot grade, even if there is more than a single whorl of tepals (e.g. see Endress 1995a for illustrations of these in Ranunculales; Doust & Stevens 2005); this feature has been placed at the [monocots Cceratophyllales = eudicots]] node here. However, note that Lauraceae (magnoliids) at least have similar flowers. Taxa with androecia that are initiated as antesepalous triplets are scattered throughout the group (Hufford 2001a), although they are really rather uncommon. For aperture development, see Banks et al. (2010).

See Hegnauer (1990) for a discussion of the chemistry of the old grade group Polycarpicae, which includes many Ranunculales, the magnoliids and Austrobaileyales. The Eudicot Evolutionary Research website should also be consulted.

Phylogeny. Within the eudicots, most recent studies place Gunnerales as sister to all other core eudicots, and the support for this position is usually strong (e.g. Senters et al. 2000; Hilu et al. 2001; S. Kim et al. 2004; Qiu et al. 2010 [support weak]; especially D. Soltis et al. 2003a), although there was a weakly supported [Gunnera + Dillenia clade in Zhu et al. (2007). Ranunculales are usually found to be sister to all other eudicots, while recent work suggests that Ceratophyllaceae may be sister to [Ranunculales + all other eudicots] (e.g. Moore et al. 2007: see the discussion immediately preceding the Magnoliales) page.

Beyond this there remains considerable uncertainty. An unresolved Proteales-Sabiaceae group is often sister to eudicots minus Ranunculales (e.g. S. Kim et al. 2004b), and the Proteales and Sabiaceae are sister taxa in an analysis of all 79 protein-coding plastid genes and four mitochondrial genes (Moore et al. 2008, support only moderate: see also Soltis et al. 2011 and Moore et al. 2011: support weak in both cases). Similarly, Savolainen et al. (2000a), Qiu et al. (2006b) and Burleigh et al. (2009) also suggested that there was weak evidence for an association of Sabiaceae with Proteales, and so an expanded Proteales is recognised here (cf. in part the Main Tree). However, Morton (2011: nuclear Xdh gene) found some support for a [Platanaceae + Ranunculales] clade. A three-gene analysis by Soltis et al. (2003) found that that Sabiaceae were near Proteales, Buxales, etc., while a four gene analysis (Kim et al. 2004a) had a weakly supported clade [Trochodendrales [Sabiaceae + Buxales]]. Hilu et al. (2003) suggested that Buxales were sister to core eudicots, although other details of their phylogeny are congruent with those presented here [check this]. Other permutations, none strongly supported, were found by Zhu et al. (2007). Worberg et al. (2006, 2007, Ophiocaryon not included) presented a 3-gene (chloroplast) phylogenetic analysis focusing on the eudicots; some of the relationships they suggest are followed here. They found most of the relationships along the eudicot spine to be strongly (³90% jacknife) supported, although the position of Sabiales as a branch immediately above Ranunculales had only 83% support, of which most came from the matK gene (the other genes examined were petD and trnL-F).

The relationships of Buxales and Trochodendrales are still somewhat unclear. Although Buxales are sister to core eudicots in most analyses, relationships in this general area were scrambled using the PetD marker alone (Worberg et al. 2007). Qiu et al. (2006b) also found an unclear set of relationships in a three-gene analysis of mitochondrial data, but with eight genes a topology similar to that used here was found (see also Qiu et al. 2010, although Sabiaceae very weakly supported as sister to all eudicots minus Ranunculaceae). Moore et al. (2008) also did not find strongly-supported relationships in this part of the tree while Soltis et al. (2008) used the topology [Proteaceae [Sabiaceae [Buxaceae [Trochodendraceae + core eudicots]]]] (see also Goloboff et al. 2009 for other relationships). However, Soltis et al. (2011, see also Moore et al. 2010, but cf. Moore et al. 2011 for position of Buxales and Trochodendrales) in their seventeen-gene analysis found strong ML bootstrap support for the relationships along the basal spine of the eudicots shown in the Summary Tree here.

RANUNCULALES Berchtold & J. Presl  Main Tree, Synapomorphies.

(O-methyl)flavonols, flavonols +; vessel elements?; young stem with separate bundles, vessels only in central part, true tracheids +; rays exclusively wide multiseriate [and in wood, where present, composed mostly of procumbent cells]; (wood fluorescence +); cambium storied; sieve tube plastids large S-type, dispersive P-protein +; petiole bundles annular; leaf cuticle waxes as clustered tubules with nonacosan-10-ol the main wax [?Euptelea]; lamina margins toothed, ?morphology; G opposite P; ovules bistomal; P deciduous in fruit; seed exotestal; endosperm development?, embryo size? - 7 families, 199 genera, 4445 species.

Evolution. Divergence & Distribution. Ranunculales contain ca 1.6% of eudicot diversity.

. Magallón et al. (1999) suggested an age of ca 70 million years before present for the clade based on the earliest fossil assignable to it, however, this was a member of the decidedly non-basal Menispermaceae. Anderson et al. (2005) date stem group Ranunculales at 122-120 million years before present, divergence within it beginning 121-114 million years before present; all families diverge before 105 million years before present except Ranunculaceae/Berberidaceae, where divergence occurred 104-90 million years before present (but see below). Magallón and Castillo (2009: both estimates relaxed and constrained penalized likelihood ages) suggest comparable figures of ca 125 and 113.2-121.9 million years respectively. The recent discovery of a fossil assigned to stem group Ranunculaceae (see below) that is at least 122.6 million years old (Sun et al. 2011) would suggest a notably greater age for the clade of ca 152-140 million years or so (extrapolating from the suggestions of Anderson et al. 2005).

Krassilov and Volynets (2008) discuss a number of fossils from the Early to Middle Albian of Primorye that they associate with the Ranunculidae sensu Takhtajan, specifically comparing some with Ranunculaceae. The morphology of these fossils is odd, some appearing to have abaxially dehiscent follicles (cf. Cercidiphyllaceae) and others have axillary fruits associated with nodes from which branches also arise. The plants are very small, and are described as being weedy (Krassilov & Volynets 2008).

See W. Wang et al. (2009) for the evolution of characters optimised on to a tree with the same topology as that used here.

Plant-Animal Interactions. Ranunculales - perhaps especially Menispermaceae and Ranunculaceae - are little used as food plants of butterfly caterpillars (Ehrlich & Raven 1964), probably because alkaloids and other noxious compounds are common in the clade.

Floral Biology. There are a number of reports of delayed fertilisation (up to some two months or more after pollination) in Ranunculales, including Eupteleaceae, Circeasteraceae, Lardizabalaceae, and Ranunculaceae (Sogo & Tobe 2006d for references).

Petals seem to have evolved several times in the order, while at the same time the AP3-III gene appears to be active in the petal-like whorl in Ranunculaceae, Menispermaceae, Berberidaceae and Papaveraceae - possibly these structures are developmentally equivalent (Rasmussen et al. 2009). Note that the petals of Papaveraceae are not associated with nectar secretion, those of the other families tend to be. Endress (2010c) emphasized the several independant origins of wind and especially fly pollination in the clade.

Chemistry, Morphology, etc. Berberin, common in the order, is synthesised via the tyrosine pathway. For wood anatomy, see Carlquist and Zona (1988). Gleissberg and Kadereit (1999) discuss the evolution of leaf form in the order, with polyternate/acropetal/basipetal-pedate leaves perhaps being plesiomorphic. The glandular leaf teeth have a clear, persistent, swollen cap into which higher order lateral veins also run. What is the distribution of colleters? Drinnan et al. (1994) suggest that petals have been derived from stamens several times in the order, examples would include Lardizabalaceae. Tamura (1965) summarizes evidence for the staminal nature of the petals in Ranunculaceae: petals have a single trace, are in the same parastiches as androecial members, are similar to stamens in early development, and are often peltate. Tepalline spurs have evolved four to six times in the order; they may be on members of the outer (Myosurus) or inner (Aquilegia) perianth whorl, and be equal in number as the basic merism of the flower (Dicentra) or single (Delphinium) (Damerval & Nadot 2007).

The basic pollen type for eudicots seems to be tectate/semtitectate-reticulate, the latter being found in Platanacaeae, Menispermacaeae, Hamamelidaceae, Gunneraceae (Denk & Tekleva 2006), Nelumbonaceae, etc. Is the pollen endexine ever lamellate? Antipodal cells are commonly other than simply persistent; data are summarized in Williams and Friedman (2004).

For information, see Ernst (1964: general), Hennig et al. (1994) and Barthlott and Theisen (1995: both cuticle waxes), Drinnan et al. (1994: floral evolution), Behnke (1995b: sieve element plastids and phloem proteins), Carlquist (1995b: wood anatomy), Endress (1995a: floral morphology), Ronse Decraene and Smets (1995b: androecial variation), Blackmore et al. (1995: pollen, very variable), Brückner (1995: summary of seed anatomy), Loconte et al. (1995: morphological phylogeny, Ranunculales paraphyletic...), Floyd et al. (1999: embryology), Floyd and Friedman (2000: endosperm) and Damerval and Nadot (2007: floral evolution).

Phylogeny. Relationships in the order are fairly well understood - see Hoot and Crane (1995), Kadereit et al. (1995), Oxelman and Lidén (1995), Hoot et al. (1999: three genes), Soltis et al. (2011) and especially W. Wang et al. (2009: four genes). Soltis et al. (2003a), a four-gene analysis (Kim et al. 2004a), and a study of non-coding chloroplast DNA (Worberg et al. 2006, 2007), all suggest that Eupteleaceae may be sister to the whole of the rest of the order (in some of these studies the support for this position was only moderate). W. Wang et al. (2009) found a similar position, but support was again only moderate, however, it was strengthened when morphological data were added; interestingly, in purely morphological analyses Euptelea was placed well outside Ranunculales, forming a clade with Nelumbo, Illicium, Paeonia, etc. - but mercifully without any bootstrap support. Some earlier studies have suggested other topologies, such as Ranunculaceae (Soltis et al. 2000; Hilu et al. 2008 - but no strong support for any position of Eupteleaceae) or Papaveraceae (Soltis et al. 2007a; Anderson et al. 2005) sister to all other members of the order. The phylogenies presented by W. Wang et al. (2009) provide a largely well supported set of relationships within the order, however, purely morphological analyses yielded a hightly pectinate topology, even if very few of the branches had even poor bootstrap support and posterior probabilities were still worse (W. Wang et al. 2009). Analysis of mitochondrial genes suggests a rather different set of relationships between the families (Qiu et al. 2010), although support is mostly (very) weak, only the [Berberidaceae + Ranunculaceae] family pair having strong support.

Classification. For our current understanding of relationships within the order and a classification based on this (largely followed here), see W. Wang et al. (2009); they include a convenient summary of earlier phylogenetic work and an extensive morphological data matrix for the whole order.

Previous Relationships. Papaverales, which contain just these three families, are commonly recognised as a separate order next to Ranunculales (Cronquist 1981; Dahlgren 1989), but there is no point in recognising them, especially given the developing support for the position of Eupteleaceae as sister to the rest of Ranunculales.

Includes Berberidaceae, Eupteleaceae, Circaeasteraceae, Lardizabalaceae, Menispermaceae, Papaveraceae (inc. Fumarioideae Papaveroideae, Pteridophylloideae), Ranunculaceae.

Synonymy: Papaverineae Thorne & Reveal, Ranunculinae Bessey - Berberidales Berchtold & J. Presl, Circeasterales Takhtajan, Eupteleales Reveal, Fumariales Link, Glaucidiales Reveal, Helleborales Nakai, Hydrastidales Takhtajan, Lardizabalales Loconte, Menispermales Berchtold & J. Presl, Nandinales Doweld, Papaverales Berchtold & J. Presl, Podophyllales Dumortier - Eupteleineae Shipunov, Lardizabalineae Shipunov - Berberidanae Doweld, Eupteleanae Doweld, Papaveranae Doweld, Ranunculanae Reveal - Ranunculidae Reveal - Berberidopsida Brogniart, Papaveropsida Brongniart, Ranunculopsida Brongniart

EUPTELEACEAE K. Wilhelm   Back to Ranunculales

Deciduous trees; (dihydro)chalcones +; cork cambium deep in cortex; vessel elements with scalariform-reticulate perforations; rays ca 10-seriate; nodes 1:many; idioblasts?; cuticle wax crystalloids 0; bud scales +; lamina vernation subplicate-conduplicate, margins gland-toothed, 2ndary veins pinnate; inflorescence axillary, fasciculate or umbellate; flowers (staminate), disymmetric; P 0; A 6-20, anthers valvate, latrorse, connective prolonged; G 6-31, stipitate, "intermediate ascidiate", stigma at most weakly secretory, brush-like; ovules 1-2(-4)/carpel, epitropous, outer integument 2-5 cells across, inner integument ca 2 cells across; fruit a samara; seed with ± enlarged exotestal cells, (sclerotic mesotesta), endotesta lignified subpalisade; endosperm cellular; n = 14; germination epigeal.

1[list]/2. Temperate South East Asia (map: from Fu & Hong 2000). [Photo - Collection]

• Eupteleaceae can be recognised by their spiral, dentate leaves with strong, ascending, pinnate veins going into the teeth, and excavated petiole bases. The small flowers lack a perianth, the anthers have a long connective, and the carpels are separate, stipitate and have a stigma like a tooth brush. The fruits are small, disc-shaped samaras down one side of which are the remains of the distinctive stigma.

Evolution. Divergence & Distribution. Anderson et al. (2005, but note topology) suggested an age of ca 120-111 million years for stem-group Eupteleaceae.

Chemistry, Morphology, etc. Lateral veins only approach the glandular teeth; the gland itself has an apical cavity. Is the wood storied, what about fluorescence, separate bundles? See Endress (1969, 1993) for some general information, Hegnauer (1973, 1989, 1990) for chemistry, Li and Ren (2005) for wood anatomy, and Ren et al. (2007b) for floral development.

Previous Relationships. Eupteleaceae were placed next to Cercidiphyllaceae in Hamamelidales by Cronquist (1981) or Hamamelididae by Takhtajan (1997). They have been often been linked with Eucommiaceae, for which see Garryales (asterid I!) - coincidentally, Eucommiaceae also have delayed fertilization.

[Papaveraceae [[Circaeasteraceae + Lardizabalaceae] [Menispermaceae [Berberidaceae + Ranunculaceae]]]]: (berberidin +); herbs, shrubs or lianes; vessel elements with simple perforation plates, in diagonal groups; with both vasicentric tracheids and nucleated libriform fibres; leaves (ternately compound or palmately lobed, articulated), 2ndary venation palmate; stigma wet [optimization?].

Evolution. Endress (2011a) suggested that presence of sepals and petals was a key innovation somewhere around here; optimization on the tree is not easy, and it is doubtful if the sepals and petals of Papaveraceae-Papaveroideae and Ranunculaceae-Ranunculoideae have the same origin.

Wink (2008) noted that the berberine bridge enzyme, involved in the synthesis of berberidin, an alkaloid found largely in this clade, was in fact quite widely distributed in flowering plants.

Chemistry, Morphology, etc. For features of wood anatomy common in this part of the clade, see Carlquist and Zona (1988); some may be higher-level apomorphies.

PAPAVERACEAE Jussieu, nom. cons.   Back to Ranunculales

Plant herbaceous, non-mycorrhizal [Fumarioideae, too?]; numerous alkaloids [inc. berberin, known from Pteridophylloideae?; protopine], little oxalate accumulation; roots diarch [lateral roots 4-ranked]; cork?; +; laticifers, articulated or not, anastomosing or not; nodes 1:3-5; petiole bundles arcuate; leaves spiral, lamina margins usu. spiny toothed, soft, ± fleshy, quite often glaucous, leaf base broad; inflorescence determinate, terminal; flower parts whorled, dimerous; P fugaceous, = K + C, K 2, median, C 4, anthers extrorse; G [2], collateral, occluded by secretion, placentation (protruding-diffuse) parietal, (carpels gaping apically), (stigmatic lobes commissural); ovules (with zig-zag micropyle), inner integument (2-)3 cells across; antipodal cells endopolypoid, ± persistent; capsule septicidal [= placenticidal], (with persistent placental strands [= replum]); seeds (arillate), curved; endotesta also well developed, with coarse fibrillar network and calcium oxalate crystals, (exo- [and meso-] tegmen fibrous, fibres crossing), endotegmen walls thickened; endosperm nuclear.

44/760 - two subfamilies and six tribes below. Largely N. Temperate, also S. Africa, scattered in South America, etc.

1. Papaveroideae Eaton   Back to Ranunculales

(Small trees); latex + milky; nodes also unilacunar; lamina vernation variable, colleters +; flowers large, K enclosing the bud, lobed [usu. on left], C also 6, crumpled (0); A (4-)many, in multiples of two or three, (placentation ± axile), style usu. 0, stigmas often confluent, dry; many ± anatropous/campyltropous ovules/carpel, outer integument (2-)4-10 cells across, inner integument 2-4 cells across, parietal tissue 2-4 cells across, nucellar cap ca 3 cells across, hypostase +; antipodals also multinucleate; capsule also with transverse dehiscence, (indehiscent, schizocarp), replum +; exotegmen often with thickened outer walls, unlignified, (anticlinal walls sinuous),(endotegmen not persistent); n = 5-10 (14, 19); non-RNase-based gametophytic incompatibility system present; duplication of PAPACYL gene.

23[list]/230 - four tribes below. Largely N. temperate (map: from Ownbey 1958, 1961; Hultén & Fries 1986; Fl. N. Am. III 1997; Fu & Hong 2000; Malyschev & Peschkova 2004). [Photos - Collection (except Dicentra and Corydalis - Fumarioideae)]

1A. Papavereae Dumortier

(Nodes also 1:1, 3:3); hairs multicellular and multiseriate; G [3-24], (style +); epistase, postament +; (megaspore mother cells several); fruits opening by pores.

8/95-125: Papaver (50-80), Meconopsis (50). N. (warm) temperate, Argemone also South America, A. mexicana commonly introduced in the tropics, and southern Africa and Cape Verde Islands (1 sp. in each - Papaver).

1B. Chelidonieae Dumortier

Latex orange, yellow or red; nodes 3-5(-9):3-5(-9); hairs multicellular and terminally uniseriate; pollen also polyporate; G [(3)] (as few as 1 ovule/carpel); fruit elongated, seeds often arillate.

9/48. East Asia and E. North America (also Europe, C. and S. America, West Indies).

Bocconia has a gynophore and basal placentation, Sanguinaria a 2-merous perianth.

Synonymy: Chelidoniaceae Martynov

1C. Eschscholtzieae Baillon

Nodes 1:1(-3); hairs unicellular; subepidermal collenchyma in stem; pollen polycolpate; capsule dehiscing explosively from base.

3/16. W. North America.

Synonymy: Eschscholziaceae Seringe

1D. Platystemoneae Spach

Nodes 1:1; hairs multicellular and multiseriate; G [3(-25 - Platystemon)], styluli +; ?embryology; fruit lacking replum strands.

3/5. W. North America.

Synonymy: Platystemonaceae Lilja

2. Fumarioideae Eaton   Back to Ranunculales

Latex 0; acetylornithine, (berberin) +; nodes uni(-multi)-lacunar; watery sap in often non-articulated sacs; subepidermal collechyma in stem; nodes 1:1+; flowers transversely disymmetric, K and C in 2's, K small, not enclosing C, C 4; A 6, free to connate, secondary pollen presentation common; pollen exine spinose, (3-colporoidate, etc.), nectaries at base of stamens; (placentation axile), style long; ovules 1-many/carpel, campylotropous, outer integument 2-4 cells across, inner integument ca 2 cells across, parietal tissue ca 4 cells across, nucellar cap 0 [?always]; (fruit a lomentum, nutlet); seeds curved; exotesta palisade or not, exotegmen not fibrous, endotesta lacking fibrillar network; (embryo long); n = (6-)8(+).

19/530 - two tribes below. Mostly N. temperate, also S. Africa (map: from Hultén & Lidén 1986; Fries 1986; Hong 1993; Fl. N. Am. III 1997; Fu & Hong 2000; Malyschev & Peschkova 2004; Serban Procheŝ, pers. comm. S. Africa).

2A. Hypecoeae Dumortier

Protopine alkaloids alone; (nodes 1:1); (leaves pinnately lobed - Pteridophyllum); (K petaloid - Pteridophyllum); (outer petals often lobed, inner petals 3-lobed; A 4, two with two vascular strands [each 2 A connate], pollen dicolpate, deposited on inner petals - Hypecoum), (styles 2); (ovules 1 (2)/carpel [Pteridophyllum]), inner integument ca 3 cells across [Hypecoum]; fruit with placentae persistent; (seeds covered with rectangular crystals - Hypecoum); (exotesta ± collapsing), (tegmen thin - Pteridophyllum); suspensor of two massive cells [Hypecoum]; n = 9.

2/18. Mediterranean to W. China, Japan.

Synonymy: Hypecoaceae Willkomm & Lange, Pteridophyllaceae Nakai

2B. Fumarieae Dumortier

(Nodes with up to 5 traces); (inflorescences racemose); (flowers monosymmetric, single spur adaxial), K minute, two (one) outer C spurred, inner C apically coherent, with median joint; A in two groups of three, 2 anthers dithecal and 4 monothecal; style white, caducous (green, persistent), stigma (flattened, with marginal lobes), wet, pollen deposited on stigma; (seed with elaiosome); exotesta usu. pigmented, endotesta not crystaliferous (palisade, crystaliferous); suspensor cells like a small bunch of grapes, (embryo undifferentiated).

19/505: Corydalis (400), Fumaria (55). Eurasia, North America, North and South Africa, mountains of E. Africa; ¾ species in Sino-Himalayan region. [Photo - Corydalis Flower, another, Dicentra Flower.]

Synonymy: Corydalaceae Vest, nom. illeg., Fumariaceae Marquis, nom. cons.

• Papaveraceae are usually herbs with an exudate of some kind whose fleshy leaves have broad bases. The flowers are 2-merous, and the calyx and corolla are clearly distinguishable; the gynoecium has two (or more) carpels, parietal placentation, and usually a short style.

• Papaveroideae are usually herbs that may be recognised by their often soft if rather bristly-hairy leaves, copious latex, and flowers with two, large, fugaceous sepals enclosing the bud, crumpled petals, usually numerous stamens, and syncarpous gynoecium with at most a short style and parietal placentation.

• Fumarioideae are often fleshy herbs with watery sap and distinctive 2-merous mono- or disymmetrical flowers that are usually spurred; the calyx is usually very small or almost invisible, certainly not green and enveloping the flower bud.

Evolution. Divergence & Distribution. Anderson et al. (2005, but note topology) suggested an age of ca 121-114 million years for stem-group and 119-106 million years for crown-group Papaveraceae.

Ecology. Several species of Fumaria and its relatives are chasmophytes in the Old World, growing in the apparently most inhospitable habitats despite their delicate and rather succulent habit.

Floral Biology & Seed Dispersal. For the unusual (transverse) plane of floral monosymmetry in Fumarioideae, see e.g. Troll (1957), Ronse Decraene and Smets (1992a), Endress (1999), etc. Corydalis and some other genera have only a single outer petal spurred and the flower is monosymmetric; there is a 90° rotation of the flower rather late in development so the spur is in the adaxial position (Ronse Decraene & Smets 1992a) and the monosymmetry is functionally vertical. There is a correlation between flowers with monosymmetry and indeterminate inflorescences, a variant on the corrleation of determinate inflorescences and polysymmetric flowers. CYCLOIDEA genes have been duplicated in Papaveraceae s.l., and this may be connected with the development on monosymmetry (Kölsch & Gleissberg 2006; Damerval et al. 2007).

The stigma of Fumaria and relatives, in which the pollen is deposited (secondary pollen presentation), can have a complex morphology; there is also secondary pollen presentation in Hypecoeae, and here the pollen is deposited on the inner petals. Papaveraceae - Papaver rhoeas, at least - have a fast-acting gametophytic self-incompatibility system which, however, is very different from that in core eudicots (Franklin-Tong & Franklin 2003; Charlesworth et al. 2005).

Quite a number of taxa, both forest herbs and chasmophytes and in both subfamilies, are myrmecochorous, the ants being attracted to the arils developed on the seeds (Fukuhara 1999; Lengyel et al. 2009, 2010); these arils probably evolved several times.

Chemistry, Morphology, etc. 1-benzyltetrahydroisoquinoline alkaloids are found only here and in a small group of related genera of Rutaceae-Rutoideae (and in Apiaceae and Asteraceae...: Kubitzki et al. 2011). Acetylornithine, reported from Fumarioideae, is involved in nitrogen transport (Jensen 1995). One species in each subfamily has distinctive UV fluorescence of unlignified cell walls (Hartley & Harris 1981).

Vascularization of the petals of Papaveroideae varies, but even if there is more than a single trace, the traces seem to have a single point of origin (Dickson 1935). I am unsure if all/some Papaveroideae have extrorse anthers, but anthers are clearly extrorse in the other subfamilies (Murbeck 1912). As in Ranunculaceae, the numerous stamens in Papaver, etc., may be derived from a paucistemonous condition. The nature of the androecium of Fumarieae in particular has occasioned much discussion, and it has sometimes been suggested that two anthers have each split into two, monothecal units, so there would be only four stamens altogether. However, it is more likely that the androecium consists of two dithecal and four monothecal stamens, and in Hypecoum the monothecal stamens have fused in pairs, hence the double vascular supply to two of what appear to be ordinary dithecous stamens (see Ronse Decraene & Smets 1992a, for literature). The androecium of Pteridophyllum has also been interpreted as being derived from a flower with six stamens, the lateral stamens having been lost (Ronse Decraene & Smets 1992a); the stamens alternate with the petals and are diagonally arranged.

When there are four carpels (mostly Papaveroideae-Papavereae) they are diagonally arranged (Ronse Decraene & Smets 1997b). The outer integument of Dendromecon is seven cells across. Papaveraceae are described as having hollow styles, although the central space may become occluded by papillae (Hanf 1935). The gametophytic self-incompatibility system of Papaver is associated with a stigma that is dry (Wheeler et al. 2001); Wheeler et al. (2009) suggest that the PrpS gener encoding the pollen S determinant lacks any homologues in other angiosperms that have similar incompatability systems. The ovary of Fumaria has only a single ovule and the fruit is nut-like and indehiscent.

Much work on the group has been carried out by Brückner, e.g. 1982 (fruit, mostly Papaveroideae), 1983 (seed, mostly Papaveroideae), 1984 (stigma and carpel, Fumarioideae), 1993 and references (carpels in Fumarioideae), and 2000 (summary of arguments about carpel number in the family). Some information on Papaveroideae is taken from Dickson (1935: floral vascularization), Sachar (1955), Sachar and Mohan Ram (1958), and Berg (1968), all embryology, Röder ((1958) and particularly Meunier (1891) for seed coat anatomy and development, and Kadereit (1993); see Gleissberg and Kadereit (1999) for the complexities of leaf development interpreted in a phylogenetic context, and Ronse Decraene and Smets (1990) for floral morphology (comparison with Begoniaceae).

For Fumarioideae in general, see also Guignard (1903) for embryology of Hypecoum, Murbeck (1912) for floral morphology, Bersillon (1955) for nodal anatomy and floral vasculature, Hegnauer (1969, 1990) and Preininger (1986) for chemistry, G. Dahlgren (1981) for stigma secretions, and Fukuhara and Lidén (1995) for testa anatomy. For ovule orientation, see Goebel (1932) and Endress (2011b), for style morphology and development, see Kadereit and Erbar (2011), and for general information, see Lidén (1986 [esp. Fumarieae], 1993). General information on Pteridophyllum is taken from Brückner (1985: fruit and seed) and Lidén (1993: general), but it is poorly known, especially anatomically and embryologically; the seeds have a cellulose network in the endotesta like that of some Papaveroideae.

Phylogeny. For general relationships within the family, especially the position of Pteridophyllum, see W. Wang et al. (2009). Within Papaveroideae, Papaver is paraphyletic and Meconopsis polyphyletic; generic limits need adjustment (Kadereit & Sytsma 1992; Kadereit et al. 1997; Carolan et al. 2006). For a phylogeny of Fumarioideae, see Lidén et al. (1997); Dicentra is dismembered and the old Corydaleae becomes paraphyletic. Various other studies have been carried out on the Papaveraceae s.l., and these include Nikolic (1995: numerical taxonomy) and Judd et al. (1994: morphology); the groupings above are taken from Hoot et al. (1997), Kadereit et al. (1994, 1995) and in particular from W. Wang et al. (2009). The latter found Pteridophyllum to link with Fumarioideae in molecular analyses, although without much support for any particular position, but in total evidence analyses there was strong bootstrap and somewhat less strong posterior probability support for a sister group relationship with Hypecoum, and Pteridophyllum is placed there below. In Fumarioideae in particular morphological studies tend to recover a Fumarieae and Corydaleae.

Classification. A.P.G. II allows as an option the possibility of including Papaveraceae, Fumariaceae, and Pteridophyllaceae in an expanded Papaveraceae, which I follow here (see also Judd et al. 2002, 2007; Mabberley 2008; etc.). Pteridophyllum is apparently rather distinct (although included in Fumariaceae by Cronquist 1981), with its rather harsher pinnate and fern-like leaves and indeterminate inflorescences; in versions 8 and earlier of this site it was placed as a monotypic subfamily sister to the rest of Papaveraceae.

Previous Relationships. In some earlier systems, Papaveraceae s.l. were grouped with Brassicaceae, etc., in Parietales, a single-character group characterised by having parietal placentation. Hardly surprisingly, its constituent members are now scattered throughout the tree.

[[Circaeasteraceae + Lardizabalaceae] [Menispermaceae [Berberidaceae + Ranunculaceae]]]: vascular rays broad; flowers 3-merous, K, C and A, or P and A opposite each other, outer P members with three or more vascular traces, "C" (nectariferous), development notably retarded; AP₃ gene triplicated.

Evolution. Divergence & Distribution. Lardizabalaceae and Menispermaceae are both lianes, sometimes vines, and they both have very large sieve tube plastids and unisexual flowers...

Chemistry, Morphology, etc. The sepals/perianth usually have three or more traces (e.g. see Hiepko 1965); for their development, see Zhang et al. (2009 and literature). For pollen morphology, see Nowicke and Skvarla (1982).

[Circaeasteraceae + Lardizabalaceae]: anthers extrorse; endosperm cellular.

CIRCAEASTERACEAE Hutchinson, nom. cons.   Back to Ranunculales

Herbs; chemistry?; cork ?; true tracheids?; nodes 1:1; petiole bundle ?arcuate; prophyll adaxial; lamina margins toothed, venation largely dichotomous; inflorescence terminal, cymose or thyrsoid, or flowers terminal, perfect or not; parts spirally arranged; P with a single trace [no "C"], (A (1-)2-6(-8), not obviously opposite P; pollen exine layered-striate; G 1-9, ascidiate, occlusion by ?secretion; ovules 1-2/carpel, ± apical, unitegmic, tenuinucellate; embryo sac tetrasporic, 4- or 8-nucleate; fruit an achene; seed coat degenerating, thin; embryo relatively large.

2[list]/2. N. India to S.W. and W. China (map: from Fu & Hong 2000).

Circaeaster Maximowicz

Bracteoles 0; P 2-3; A latrorse?, anthers bisporangiate/monothecal; ovule straight, integument ca 2 cells across; n = 15.

1/1: Circaeaster agrestis. India (Himalayas), W. China.[Photo - Circaeaster Habit.]

Kingdonia Balfour f. & W. W. Smith

Annual; leaves two-ranked, palmately compound; P 5(-7), 8-13 clavate glands; G 3-9, ovules hemianatropous, integument 2-5 cells across; n = 9.

1/1: Kingdonia uniflora. W. and N.W. China.

Synonymy: Kingdoniaceae Airy-Shaw

• Circaeasteraceae are easily recognised. They are small herbs, their leaves have largely dichotomous venation, and their rather small flowers have separate carpels.

Evolution. Divergence & Distribution. Anderson et al. (2005) suggested an age of ca 116-107 million years for stem-group and 84-72 million years for crown-group Circeasteraceae.

Chemistry, Morphology, etc. Kingdonia may have up to four bundles departing from the single foliar trace, endotrophic mycorrhizae and, like Circaeaster, several root hair zones on the roots (Ren & Hu 1998). Xylem perforation plates may also be scalariform. Kingdonia at least appears to have an adaxial prophyll (see s.e.m. of axillary buds in Ren et al. 2004 - no comment is made about this).

Circaeasteraceae do not show the regular relationship between the stamens and perianth members of many other Ranunculales. The tepals of Kingdonia have a single trifid vein, indeed, all floral organs are innervated by a single vein, apart from the first tepal, which has two traces (as in some Ranunculaceae, see Ren et al. 2004). The genus also has 8-13 glistening clavate glands immediately inside the perianth whorl; these are described as petals (perhaps unlikely) by Tamura (1993) and as staminodes by Ren et al. (2004) and may secrete nectar. Mesogamy, i.e. the pollen tube entering the ovule laterally by penetrating the integument, is reported for Circaeaster by Junell (1931); Circaeaster also has endosperm with a chalazal haustorium.

General information is taken from Tamura (1993: in Ranunculaceae) and Wu and Kubitzki (1993); see also Nowicke and Skvarla (1981) for pollen, Hu et al. (1990), Ren and Hu (1995) and Tian et al. (2006) for information on Circaeaster agrestis, and Ren et al. (1998, 2004) for information on Kingdonia uniflora. The inside cover of Act. Bot. Bor.-Occid. Sinica 24(1) (2004) has a photograph of Kingdonia uniflora with excellent details of gross morphology.

Classification. Keeping Kingdoniaceae separate from Circaeasteraceae was optional in A.P.G. II (2003).

Previous Relationships. Kingdonia has been placed in the Ranunculaceae-Anemoneae, e.g. by Kosuge et al. (1989). The dichotomous venation of the leaves and the separate carpels of Circaeasteraceae have attracted attention as possibly indicating a very "primitive" group.

LARDIZABALACEAE R. Brown, nom. cons.   Back to Ranunculales

Lianes; benzylisoquinoline alkaloids 0; glabrous or with uniseriate hairs; (plant Al-accumulators); petiole bundles arcuate; bud scales +; leaves trifolioliate, leaflet vernation conduplicate, margins entire; inflorescence axillary, racemose; parts whorled, "K" 6, "C" 6, small, apices nectariferous, both with a single trace; staminate flowers: A 6, connective often prolonged apically; tapetal cells 2-nucleate; pollen exine smooth; carpellate flowers: staminodia +; G 3, also spiral, placentation marginal, carpels with postgenital fusion and secretion, stigma wet, (extragynoecial compitum +); micropyle endostomal; placenta fleshy in fruit; germination phanerocotylar.

9[list]/36 - two groups below. South East Asia and Chile (map: see Taylor B. 1967; Ying et al. 1993).

1. Sargentodoxoideae Thorne & Reveal

Triterpenoid saponins 0; cork cambium deep-seated; tanniniferous cells +; plant dioecious (some flowers perfect); carpellate flowers: K 4-9, C 5-7; staminodes "petaloid"; G many, ascidiate; ovule 1/carpel, pendulous, outer integument ca 4 cells across; surface of testa featureless; endosperm reserve?; n = 11.

1/1: Sargentodoxa cuneata. China.

Synonymy: Sargentodoxaceae Hutchinson

2. Lardizabaloideae Kosteletzky

(Shrubs); oleanone triterpenoid saponins +; (vessel elements with scalariform perforation plates); (stomata cyclocytic); leaves (odd-pinnately compound), leaflets (with basal tooth or lobe), (2ndary veins pinnate); plant monoecious (dioecious; flowers perfect): (K 3, C 0); staminate flowers: (A 3, 8), filaments ± connate, (tapetal cells to 4 nucleate); pollen also colporoidate, (trinucleate); carpellate flowers: staminodes +; G (-12), (placentation laminar), (stigma peltate); ovules (few-)many/carpel, (hemitropous), outer integument 3-4+ cells across, inner integument 2-3 cells across, parietal tissue ca 3 cells across; (antipodal cells persistent - Decaisnea); fruit a berrylet or fleshy follicle; testa multiplicative, exotestal cells lignified, elongated, ± oblong [Descaisnea] or unlignified, fibrous [Akebia, Hoelboellia], hypodermal cells thickened; endosperm starchy [Decaisnea] or with hemicellulose, (nuclear - Decaisnea); n = 14-16, ?17, 18.

8/35. South East Asia and Chile (Lardizabala, Boquila). [Photos - Lardizibala Staminate flower, Boquila Flowers, Fruit, Fruit close-up.]

Synonymy: Decaisneaceae Loconte, Sinofranchetiaceae Doweld

• Lardizabalaceae are usually lianes with compound leaves and broad rays in the wood, the plants being monoecious or dioecious. The medium-sized, three-merous flowers have the perianth members and androecium opposite each other. The carpels are free and the fruits are more or less fleshy, although they are sometimes also follicles.

Evolution. Divergence & Distribution. Anderson et al. (2005) suggested an age of ca 116-107 million years for stem-group and 95-66 million years for crown-group Lardizabalaceae.

Chemistry, Morphology, etc. Wood fluorescence? Smets (1986) suggested that the nectaries are staminal nectaries; stamen and petal develop primordia edevlop immediately adjacent to each other in Holboelllia, and the exudate from the stigmas joins them in a hyperstigma (X.-H. Zhang & Ren 2011). X.-H. Zhang and Ren (2011) depict dehiscence of the staminodes of Decaisnea insignis; the pollen looks normal (but are there some kind of viscin strands?). Nowicke and Skvarala (1982) studied the pollen morphology especially of Sargentodoxa; there may be additional apomorphies for that genus. The seeds of Akebia, at least, are embedded in some kind of fleshy tissue.

General information is taken from Wu and Kubitzki (1993) and Qin (1997), chemistry from Hegnauer (1966, 1989, also 1973, as Sargentodoxaceae) and Zheng and Yang (2001), seed surface from Xia and Peng (1989), capel development from van Heel (1983), and some anatomy from Yong and Su (1993); Zhang et al. (2005, 2009) provide detailed studies of Sinofranchetia, H.-F. Wang et al. (2009a) of Sargentodoxa, and H.-F. Wang et al. (2009b) of Decaisnea.

Phylogeny. Sargentodoxa is sister to the rest of the family (Hoot et al. 1995b, see also Hoot 1995a; Kofuji et al. 1994). Decaisnea may be sister to the remainder (Kofuji et al. 1994); it has a number of distinctive (apomorphic) embryological features (H. F. Wang et al. 2009b).

Classification. Although Sargentodoxa has a number of differences (autapomorphies) when compared with the other genera (see also Zhang & Ren 2008), there is no compelling reason to segregate it as a family (H.-F. Wang et al. 2009a).

[Menispermaceae [Berberidaceae + Ranunculaceae]]: (berberin + [a benzylisoquinoline - scraped stems or roots yellow in color]); endosperm nuclear.

Chemistry, Morphology, etc. For alkaloids found in members of these three families, see Aniszewski (2007). For perianth vasculature, see Hiepko (1964a, b).

MENISPERMACEAE Jussieu, nom. cons.   Back to Ranunculales

Often woody lianes (trees; vines); also/or aporphine alkaloids, sesqui- and diterpenoids +, (plant tanniniferous); successive cambia frequent; (rays narrow); secretory cells in files; sclereids common; crystals common; stomata various, often ± cyclocytic; hairs unicellular to uniseriate; leaves simple (compound - Burasia), often peltate or with the lamina base joining the top of the petiole, lamina margins entire (toothed; lobed), petiole often pulvinate at base and apex; plants dioecious; inflorescence axillary; flowers small, parts whorled or spiral, P with a single trace, "K" (1-)6(-12), "C" 0-8, often connate, (clasping A), staminate flowers: A 3, 6, 12 (1-40, if many, not all opposite petals), (connate and ± extrorse), anthers (bisporangiate/monothecal), thecae superposed; pollen tricolporate, endapertures circular; pistillodes +/0; carpellate flowers: staminodes +/0; G (1-)3(-30<), with postgenital fusion and secretion, opposite P [Cissampelos], five bundles per carpel, gynophore common, stigma ± flaring; ovules 1-2/carpel, often unitegmic, hemitropous-campylotropous, micropyle endostomal (zig-zag), integuments folded, outer integument 2-5 cells across, inner integument 2 cells across, (single integument 3-4 cells across); antipodals multiplying, multinucleate; fruit a straight drupelet, 1-seeded; seed with condyle [placentar intrusion], coat undistinguished, (exotesta tabular, lignified); endosperm +, embryo long, cotyledons divaricate, ± foliaceous; n = (9-)11-13(+).

70 (many small)[list]/420: two groups below. Pantropical, usually lowland (map: see van Balgooy 1993; Fu & Hong 2000: Malyschev & Peschkova 2004; Rosa Ortiz-Gentry, pers. comm. 2004). [Photo - Fruit, Fruit.]

1. Tinosporoideae W. Wang & Z. D. Chen: (G several); seed subglobose-reniform, ruminate, (condlye 0); (embryo curved), cotyledons foliaceous, flat and broad.

2. Menispermoideae W. Wang & Z. D. Chen: (anthers connate); (G 1-several), style lateral to basal; seeds variously curved, endocarp often sculpted; (seed ruminate); (endosperm 0), embryo curved, cotyledons fleshy, ± cylindrical.

• Menispermaceae are recognisable by their often viney/lianescent habit, broad rays, petioles pulvinate at both ends, and often coriaceous lamina with palmate venation. The lamina is also often peltate, and even if not, the two sides of the lamina nearly meet on top of the petiole. The plants are dioecious, the often 3-merous flowers are small, and the drupelets often have a distinctively sculpted endocarp and can be strongly curved (hence the "moon-seed" family - also Menispermum canadense).

Evolution. Divergence & Distribution. Anderson et al. (2005) suggested a stem-group age of ca 116-105 million years and a crown-group age of ca 80-70 million years for Menispermaceae, while comparable ages in Jacques et al. (2011) are 125-115.6 and 124.4-103.3 million years respectively. However, if the identity of the ranunculaceous Leefructus from early Cretaceous deposits 125.8-122.6 million years old (Sun et al. 2011) is confirmed, all these estimates may well have to be revised upwards.

Callicrypta, from the mid-Cretaceous of Siberia, has very small flowers (carpellate) with the parts more or less opposite, or forming spirals, and may be Menispermaceae; it is unclear what a link between Menispermaceae and Amborellaceae - hardly close - that the fossil is supposed to represent might consist of (cf. Krassilov & Goloneva 2004). Fossils are known from the Upper Turonian of ca 89.3 million years from the Czech republic and many fossils are known from Lower Ypresian deposits of ca 55.2 million years age (Jacques et al. 2011), but Cretaceous records of Menispermaceae are questionable (Herrera et al. 2011). Jacques (2009a) and Jacques et al. (2011) discuss the whole fossil history of menisperms. Jacques and de Franceschi (2005, and references) reported on some Lower Eocene endocarps assignable to this family, and South American is proving to be quite diverse. Doria et al. (2008) for report on Eocene leaf fossils from northern Colombia, and well preserved endocarps have been reported from two Palaeocene localities in Colombia, one dated to ca 60 million years ago (Herrera et al. 2011). The latter includes material that they identify as Stephania, now known only from the Old World.

Ecology. Menispermaceae can be an important copmponent of the climbing vegetation in the tropics, perhaps especially in the New World (Gentry 1991).

Plant-Animal Interactions. Larvae of the large noctuid moths of the subfamily Catocalinae use Menispermaceae as their major food source throughout the tropics, although they can also be found on other plants like Erythrina (some Menispermeae have pentacyclic Erythrina-type alkaloids). The adult moths, with their saw-like proboscides, attack ripe or ripening fruits and cause a considerable amount of damage to commercial crops (Fay 1996).

Economic Value. The muscle relaxant D-tubocuranine is obtained from Chondrodendrum tomentosum; this is also a major ingredient of the South American poison curare and is put on arrows and darts.

Chemistry, Morphology, etc. There are few records of cork position. Tamaio et al. (2010) did not find serial cambia in the Menispermaceae they examined, but see Tamaio et al. (2009). The tangential cell walls of the rays of Tinomiscium petiolare are oblique to the ray axis when viewed in transverse section; this is uncommon in other Menispermaceae, where the walls are at right angles (Jacques & de Franceschi 2007), but I do not know the distribution of this feature in the outgroups. In at least some Menispermaceae, the presence of laticifers or sclereids is mutually exclusive (Wilkinson 1986). Cocculus has plagiotropic branches (Keller 1996); does it also have two-ranked leaves?

Flowers can be monosymmetric, as in the carpellate flowers of Stephania dielsiana, where there are 1 + 2 or 1 + 3 sepals and petals and a single carpel (Wang et al. 2006); the staminate flowers are always polysymmetric. Tepals in e.g. Menispermum canadense have only a single trace (Smith 1928). There is considerable variation in pollen morphology in the family (Harley & Ferguson 1982 and references) which needs to be integrated with the clades that are becoming evident. The upper of the two ovules is epitropous and fertile, the lower is apotropous (Mauritzon 1936). Does Tinomiscium have a condyle (see Jacques 2006 - no)? There is apparently a period of 6-8 weeks between fertilization and first division of the zygote in Tinospora cordifolia (Sastri 1964). Jacques and Zhou (2010) used Procrustes analysis to understand variation in endocarp morphology; they placed this in the context of a molecular tree rather than in that of an independent analysis.

Some general information is taken from Kessler (1993), Harley (1985 and references) surveyed pollen morphology, Wilkinson (1986) described leaf anatomy, Réaubourg (1906) provided a morphological and anatomical study of the family, Hegnauer (1969, 1990) summarized information on chemistry, Jacques and de Franceschi (2007), wood anatomy; see also Jacques (2006: much useful information, inc. phylogeny, 2009b: endocarp morphology).

Phylogeny. Although Tinomiscium is strongly supported as sister to all other Menispermaceae (Ortiz et al. 2007), the sequences were corrupt (R. Ortiz, pers. comm.). Rather, Tinomiscium belongs in the [Tinosporeae + Coscinieae] clade, Tinosporoideae, although this is a group with only moderate to weak bootstrap support (Ortiz et al. 2007). A large clade, Menispermoideae, includes the rest of the family and is well supported. Within Menispermoideae Menispermum is sister to other taxa, again with strong support, and there are other well supported relationships (Ortiz et al. 2007: cf. Jacques et al. 2007, morphological data only, variously treated; Jacques & Bertolino 2008, but some samples mislabelled, see Jacques et al. 2011). The old Menispermeae, Fibraureae and Peniantheae are polyphyletic (see also Wang et al. 2007a). Hoot et al. (2009: three chloroplast genes) found that Menispermum and Sinomenium formed a clade sister to all the rest of the family in two gene analyses, but with little support (see also Ahmad et al. 2009; Jacques et al. 2011), although in three gene analyses they were in a position like that found by Ortiz et al. (2007); Hoot et al. (2009) optimized characters on a tree with the first topology. W. Wang et al. (2009: three chloroplast and one nuclear genes, morphology) recovered a topology similar to that found by Ortiz et al. (2007), but support was weak and the sampling of Menispermaceae was poor. ,/P.

Hong et al. (2001) discuss phylogenetic relationships within Menispermeae.

Synonymy: Pseliaceae Rafinesque

[Berberidaceae + Ranunculaceae]: herbs (woody), rhizomatous, rhizome not tuberous; nodes also multilacunar; vascular bundles V-shaped, in herbaceous taxa often closed, scattered or in concentric rings; leaf base broad, (paired petiolar stipules +); ± petaloid staminodial nectaries +; outer integument at least 4 cells thick, nucellar cap +; endosperm reserves other than oil or protein.

Chemistry, Morphology, etc. Nowicke and Skvarla (1981) suggested that aperture columellae might be a synapomorphy for the two families. For general information, see Janchen (1949).

BERBERIDACEAE Jussieu, nom. cons.   Back to Ranunculales

Myricetin, isoprenylated flavonoids +, tanniniferous; cork also pericyclic; hairs 0 (unicellular or -seriate); lamina vernation curved or conduplicate (complex in Podophyllum, etc.), margins gland- or spiny-toothed (entire), (2ndary venation pinnate), stipules common; inflorescence terminal (axillary), often racemose; flowers (2-)3(-5)-merous, parts whorled, with cortical vascular system; P single trace, = "K" + 6 nectariferous "C"; A 6, with flaps; tapetal cells multinucleate; G 1, ascidiate, postgenital occlusion by secretion, stigma broad, dry or wet; (micropyle zig-zag), outer integument 5-11 cells across, inner integument 3-5 cells across; antipodal cells endopolypolypoid; exotestal cells lignified, oblong-fibrous (cuboid); endosperm with hemicellulose; embryo minute.

14/701 [list] - three clades below. Mostly East Asia and E. North America, also South America, N. Africa, general N. temperate (map: from Ahrendt 1961; Hong 1993; Fl. N. Am. III 1997; Malyschev & Peschkova 2004).[Photos - Collection]

1. Podophylloideae Eaton

Lowermost branch of inflorescence from axil of reduced leaf; K (0 - Achlys), 4-18, vascular supply 3:3, C vascular supply 1:1, (0; 4, with nectar spurs; 7-9; nectary 0); A (-19, Podophyllum, Achlys; dehiscence by slits); microsporogenesis successive [?all], pollen wall development by centripetal furrowing, striate, (spiny; diads; tetrads); ovules 1-many/carpel, (micropyle bistomal), (integuments lobed), inner integument 2-3 cells across, parietal tissue 0-2 cells across, (postament +); (megaspore mother cells several - Diphylleia); fruit an achene, berry, or a follicle also with transverse dehiscence; (seeds arillate); outer integument multiplicative [?all]; n = 6.

8/75: Epimedium (55). Mostly (Europe to) East Asia (some desert xerophytes) and W. or E. North America. [Photo - Podophyllum Flower © R. Kowal, Fruit, Ripe Fruit.]

Synonymy: Diphylleiaceae Schultz-Schultzenstein, Epimediaceae Menge, Leonticaceae Airy Shaw, Podophyllaceae Candolle, nom. cons., Razaniaceae Takhtajan

[Nandinoideae + Berberidoideae]: K + C with 1 trace; stigma wet.

2. Nandinoideae Heintze

(Woody); petiole concave at the base; lowermost branch of inflorescence from axil of ± expanded leaf; (P many, nectary 0 - Nandina); (A dehiscence by slits); ovules 1-2 (4) carpel; fruit a berry or pericarp evanescent or bladder-like; funicle swollen, (testal cells thin-walled, endotegmic cells large, lignified - Nandina); n = 8, 10.

4/15. E. Europe to Japan.

Synonymy: Nandinaceae Horaninow

3. Berberidoideae Kosteletzky

(Plant woody;) (vessel elements with scalariform perforations, petiole bundles arcuate - Berberis); leaves odd-pinnate or unifoliolate; lowermost branch of inflorescence from axil of reduced leaf; K 3-12, "C"/staminodia with paired basal nectaries; stamens sensitive; tapetum plasmodial; pollen 6-12 colpate, or apertures irregular (spiraperturate), wall undifferentiated; ovules 1-many/carpel, parietal tissue ca 2 cells across; (megaspore mother cells several); fruit a berry; endosperm cellular [Mahonia], embryo long; n = 7.

2/601: Berberis (600). General N. temperate, also South America, N. Africa.

• Berberidaceae are herbs or shrubs that may be recognised by their often yellow-colored secondary tissue (most obvious in the roots) and their often compound, stipulate leaves with palmate venation and sharply toothed or spiny margins. Their flowers are usually 3-merous, the perianth is often multiseriate, the stamens are often opposite the perianth members (there are sometimes more), and anther dehiscence may be valvate; there is always a single carpel.

Evolution. Divergence & Distribution. Anderson et al. (2005) suggested a stem-group age of ca 104-90 million years and a crown-group age of ca 88-72 million years for Berberidaceae.

Within the family, Berberis is by far the most widely distributed genus, and fossils have been reported from Palaeocene deposits ca 60 million years old in northeast China; Oligocene and younger fossils are known from elsewhere in the Northern Hemisphere (Y.-L. Li et al. 2010). Several genera in Berberidaceae are disjunct and/or occupy only limited areas, and many of the taxa involved may have originated in East Asia. Despite the age of the family - probably late Cretaceous - these disjunctions may be relatively recent, forming within the last 10 million years, although the desert xerophytes Bongardia and Leontice are probably rather older (Donoghue & Smith 2004; Wang et al. 2007b).

Seed Dispersal. Seeds of a number of taxa, both forest herbs and desert xerophytes, have elaiosomes/are arillate (not necessarily different things) and are myrmecochorous (Lengyel et al. 2009, 2010); Berberidoideae, however, have berries.

Bacterial/Fungal Associations. Some seventy species of Berberis (inc. Mahonia) are alternate hosts for Puccinia graminis, the economically very important black stem rust of wheat and other grain crops in Pooideae.

Chemistry, Morphology, etc. In Podophyllum the epidermal waxes are solid rods. The leaves on long shoots of Berberis s. str. are mostly modified as trifid spines that represent leaf blades; there are usually simple but articulated photosynthetic leaves (i.e. they are unifoliate) on short shoots while the cataphyls are basically stipular (Gonzalez & Pabon Mora 2009). Mahonia s. str. (with ca 100 species) has compound leaves, but the two hybridise.

Epimedium has four nectar spurs coming from the four inner tepals, and even in Podophyllum single stamens or groups of stamens are opposite the innermost perianth members (Schmidt 1928). Successive microsporogenesis has been reported (Min et al. 1995). The carpels in Berberidaceae vary in their orientation. According to Chapman (1925, cf. e.g. Feng & Lu 1998), the gynoecium is derived from two or three carpels, with the gynoecia of the n = 6 clade alone being derived from two carpels (Kim & Jansen 1998), however, the gynoecium is probably unicarpellate throughout the family (Brückner 2000 for a summary). Ghimire et al. (2010) describe the thinly crassinucellate ovules of Gymnopsermium (Podophylloideae) as having a well-developed endothelium. In genera like Caulophyllum the carpel walls do not surround the maturing blue seeds, so the plant is a kind of gymnosperm!

Some general information is taken from Schmidt (1928) and Loconte (1993) and chemistry from Hegnauer (1964, 1989); see Nowicke and Skarvla (1981) for pollen and Furness (2008b) for microsporogenesis. Stearn (2002) provides much information on herbaceous Berberidaceae. For floral development of Caulophyllum (with common stamen-nectary primordia), see Brett and Posluszny (1982), for the chaotic arrangement of the androecium in Achlys, see Endress (1989), for spore/gamete development in Diphylleia, see Huang et al. (2010), and for the female gametophyte, see Huss (1906), for that of Podophyllum, see Sreenivasulu et al. (2010).

Phylogeny. Nandina is a very distinctive plant, and in the past it has been segregated as a separate family or subfamily (as in versions 7 and earlier of this site). However, Nickol (1995) had suggested on morphological grounds that it was close to Caulophyllum, although it was sister to the rest of the family in the most parsimonious tree that he found. Early molecular studies (e.g. Adachi 1995) found similar relationships, and these have since been confirmed, as by Kim et al. (2004), but Nandina did tend to wander in the tree (e.g. Kim & Jansen 1996, 1998). The three groupings above, which more or less form a trichotomy, appear in the analyses carried out by Kim et al. (2004); Podophylloideae have only moderate support (see also Wang et al. 2007b). W. Wang et al. (2009) confirmed these groupings, and although molecular support for a clade [Nandinoideae + Berberidoideae] was weak, it was much strengthened in analyses that included morophological data.

For Nandina: K many, spiral, nectaries absent, [C and A develop from the splitting of a single primordium], pollen with massive endexine, nectary 0, nucellus early absorbed, endothelium ?+; fruit a berry, seed concave; endotestal cells crystalliferous, but otherwise testa crushed, endotegmic cells enlarged, lignified, thickened esp. internally, crystalliferous. For its floral development, see Feng and Lu (1998); the flower is basically trimerous-whorled, sepals are borne in slightly-spiralling lines up the receptacle, and all perianth parts have similar vasculature, having ca 3 traces.

Classification. For an infra-familial classification, see W. Wang et al. (2009).

Previous Relationships. Fruit dehiscence in at least some Berberidaceae and Papaveraceae is transverse, at least in part. Although it has been suggested that on this account these families are similar (e.g. Endress 1995a), there is little other evidence indicating immediate phylogenetic relationships.

RANUNCULACEAE Jussieu, nom. cons.   Back to Ranunculales

Tannin 0, little oxalate accumulation; cork deep-seated, rarely developed; when woody with broad primary rays persisting and cambium developing in the primary vascular bundles; vessel elements with simple and/or scalariform perforation plates; (nodes 1:1, 2:2); (cuticle waxes as platelets); stomata also paracytic; leaves (opposite, two-ranked), quite often simple, lamina vernation variable, margins usu. gland-toothed; inflorescence terminal, often cymose, or flowers single; flowers medium to large, parts spiral or whorled, K, "C", and A not opposite each other, K (2-)5(-6), often petaloid, three-trace; A many, spiral, extrose or introrse; (pollen inaperturate); G (1-)many, usually with complete postgenital fusion, (ascidiate), when 3, orientation variable, stigma ± dry; ovules several/carpel, apotropous, micropyle endostomal, obturators various; antipodal cells persistent, multiply or not; fruit a follicle; exotestal cells often thickened, unlignified, or seed ± pachychalazal, coat thin; endosperm starchy (0), embryo minute to long, cotyledons connate or not, cotyledonary tube common; chromosomes small, straight, stout; germination epigeal.

62[list]/2525 - five subfamilies below. ± World-wide, but esp. (N.) temperate, not lowland tropics (map: from Vester 1940; Hultén 1971; Wilson 2007). [Photo - Flower]

[Glaucidioideae + Hydrastidoideae]: vessel elements with simple and scalariform perforation plates; medullary bundles +; vascular bundles flat; also medullary petiole bundles; palisade mesophyll 0; leaves two-ranked; flowers single, terminal; nectaries 0; stigma bilobed; outer integument 4-13 cells across, inner integument 2-5 cells across; antipodals unmodified; follicle dehiscing abaxially as well.

The rhizome is an irregular sympodium. Soltis et al. (2003a) suggest that both Glaucidium and Hydrastis have a bimerous perianth.

For much information, see Tobe and Keating (1985).

Synonymy: Hydrastidaceae Martynov

1. Glaucidioideae Loconte

Coumarin +, alkaloids, berberin 0; lamina supervolute-curved and plicate; flowers with cortical vascular system; P 4, petaloid; A centrifugal; G 2, basally connate, opposite outer P [transverse], plicate; ovules many/carpel, tenuinucellate, nucellar cap massive; megaspore mother cells several; fruit with stigma on lower abaxial surface; seeds winged, outer integument vascularized; polyembryony common, embryo long, cotyledons foliaceous; n = 10, chromosomes 1.5-2.5 µm long.

1/1: Glaucidium palmatum. Japan (map: from Li 1952, blue).

Synonymy: Glaucidiaceae Tamura

2. Hydrastidoideae Martynov

Roots bright yellow; nodes on erect stem swollen, multilacunar; lamina vernation plicate, petiole base on rhizome encircling stem; P (2)3(4), with a single trace; pollen tectum striate-reticulate; G several, stigma with multicellular projections; ovules 1-4/carpel, micropyle zig-zag follicle rather fleshy; exotesta strongly palisade, exotegmen lignified, both testa and tegmen multiplicative; embryo minute; n = 13.

1/1: Hydrastis canadense. C. and E. North America (map: from Li 1952, red).

Synonymy: Hydrastidaceae Martinov

[Coptoideae [Thalictroideae + Ranunculoideae]]: xylem surrounding phloem [cf. Takhtajan 1997], paratracheal parenchyma ± absent; petiole bundles with associated lignification; P 5-merous, ± petaloid, "C" 0-13, usu. obviously nectariferous, very diverse in form, with a single trace; outer integument?; antipodal cells large, (multinucleate), persistent.

3. Coptoideae Tamura

Woody or perennial herb; nectaries 5-10, petaloid, thick, stalked; carpels stipitate; n = (8) 9, small, rod-like.

3/17. East Asia, E. and W. North America.

Wand and Ren (2008) describe a rather obscure annular structure that surrounds the ovule in Coptis.

[Thalictroideae + Ranunculoideae]: ovules apotropous [when single], outer integument 2-10 cells across, inner integument 2-3 cells across, (integument single); postament + (0); (fruit an achene).

4. Thalictroideae Rafinesque

Tyrosine derived cyanogenic compounds, 18:3[d]5t,9c,12c, also 18:1[d]5t, 18:2[d]5t,9c fatty acids +; hairs capitate; lamina segments ± curved-involute, papillate, (stipules + - Thalictrum); (plant dioecious), nectaries ± petaloid and stalked, (internal staminodes +); integument single, 7-8 cells across; n = 7, small, bean-shaped.

9/450: Thalictrum (330: wind pollinated), Aquilegia (80). N. temperate, also South America, Africa and New Guinea.

Tucker and Hodges (2005) discuss floral development in Aquilegia and its immediate relatives, Wang and Chen (2007) discuss phylogenetic relationships and petal evolution in the whole subfamily.

Synonymy: Aquilegiaceae Lilja, Thalictraceae Rafinesque

5. Ranunculoideae Arnott

Lactone-forming glycosides [ranunculin], (20:3[d]5c,11c,14c fatty acid), (cardenolides; bufadienolides) +, benzylisoquinoline alkaloids few or usu. 0, berberin 0; stomata ³35 µm long; (petiole bundles arcuate; wing bundles +; medullary bundles +); hairs clavate; (leaves opposite - Clametis), lamina segments ± involute (supervolute and/or curved), (stipules + - Caltha); (flowers vertically monosymmetric); (pollen multicolpate/porate); ovule (often single, median [lateral - Adonidae]), (micropyle bistomal), {single integument 6-12 cells across), parietal tissue 1-2 cells across, or 0, incompletely tenuinucellate, (nucellar cap 0); (postament +); (fruit a berrylet - some Actaea); (exotesta short-palisade; endotesta ± developed; testa vascularized); endosperm nuclear, (embryo undifferentiated); n = (6-)8(-9), R-type chromosomes [Ranunculus type - large, long, 2-armed, often curved]; (germination hypogeal - some Clematis).

46/2025: Ranunculus (600), Delphinium s.l. (400), Aconitum (300), Clematis (325), Anemone s.l. (190). Worldwide, but few in lowland tropics.

Synonymy: Aconitaceae Berchtold & J. C. Presl, Actaeaceae Berchtold & J. C. Presl, Anemonaceae Vest, Calthaceae Martynov, Cimicifugaceae Bromhead, Clematidaceae Martynov, Delphiniaceae Brenner, Helleboraceae Vest, Nigellaceae J. Agardh

• Ranunculaceae can be recognised by their usually herbaceous habit and spiral, usually exstipulate, lobed leaves with broad bases. The flowers have large and often petaloid sepals, nectariferous "petals", spiral, usually numerous stamens, and separate carpels borne on a well-developed receptacle.

Evolution. Divergence & Distribution. It had been noted that there were Pre-Campanian fossils possibly identifiable as the family (Pigg & deVore 2005), but the recent discovery of Leefructus from early Cretaceous deposits 125.8-122.6 million years old in China and assigned to stem Ranunculaceae (Sun et al. 2011) will, if confirmed, very much change our ideas of the evolution of the clade. Earlier estimates of the age of Ranunculaceae were considerably younger; thus Anderson et al. (2005) had suggested a stem-group age of ca 104-90 million years and a crown-group age of ca 87-73 million years for Ranunculaceae. Paleoactaea, from the Late Palaeocene some 58 million years ago, has fruits very similar to those of Actaea down to the palisade tissue in the testa (Pigg & deVore 2005). Somewhat older Eocaltha has seeds rather like those of extant Caltha, i.a. both having a flotation chamber; this fossil is from the Mexican Campanian (Cretaceous) of some ca 77 million years ago (Rodríguez de la Rosa et al. 1998).

The beginning of diversification within the speciose Clematis has been dated to as recently as (13.1-)7.8(-4.0 million years ago, however, the stem age is considerably older, being some (43.8-)26(-9.2) million years (Miikeda et al. 2006; Xie et al. 2011: HPD). For the evolution of Arctic Ranunculaceae, see Hoffmann et al. (2010), while Emadzade et al. (2010, 2011) and Hörandl and Emadze (2011) show that there has been a substantial amount of dispersal in tropical and subtropical mountains and in the Sothern Hemisphere - even between southern Africa and America - often followed by radiations, in the widely-distributed Ranunculus. Diversification within Aquilegia has been much studied, the nectar spurs that characterise most of the genus being considered a key innovation that spurred recent and rapid diversification in the clade (Hodges & Arnold 1995 and references). There are only ca 80 species in the clade, but they show little molecular differentiation (Whittall et al. 2006).

Delphinium, Aconitum, and relatives (Delphinieae), which between them account for about a quarter of the diversity in the family as a whole, have monosymmetric flowers, the monosymmetry becoming apparent rather late in development after organ initiation (Jabbour et al. 2009). Aconitella is derived from within Consolida, and the combined clade is included within Delphinium (Jabbour & Renner 2011), the whole being largely Mediterranean-Turanian in distribution.

Floral Biology & Seed Dispersal. Many Ranunculaceae have nectaries, sometimes quite elaborate beaker-shaped structures, which are usually interpreted as being derived from stamens, with which they have a number of points of similarity, e.g. origination from a primordium that is a mound rather than a ridge, etc. (Jäger 1961; Tamura 1965; Kosuge & Tamura 1989; Erbar et al. 1999; Leins 2000; Zhao et al. 2011; cf. Kosuge 1994); gene expression data, however, suggest a rather different explanation in which stamens do not play a role (Rasmussen et al. 2009). The five nectar spurs of Aquilegia occurring in a radially symmetrical flower are very unusual in flowering plants, while Delphinium the nectary spurs are paired, being borne inside a spurred perianth member, so from the point of view of the pollinator the flower has a single spur. In Ranunculus there are small nectaries at base of the petals and the outer perianth members are very sepal-like while in Laccopetalum and relatives there are a number of nectary ridges on the "petals", but normally the nectaries are rather different morphologically from the other perianth members, the latter being petaloid and visually attractive (see Kramer & Hodges 2010 for a review of the evolution of "petals" in Aquilegia).

A number of forest herbs in Ranunculoideae in particular are myrmecochorous, the attractive outgrowths developing either from seed or fruit (Lengyel et al. 2009, 2010).

Plant-Animal Interactions. North temperate Ranunculaceae are hosts to over 110 species of dipteran agromyzid leaf miners (Phytomyza: Spencer 1990; see also Jensen 1995), which for the size of the family may be the most diverse assemblage in flowering plants; there are no agromyzids on Paeoniaceae! Agromyzids moved on to Ranunculaceae from asterids, perhaps in the late Oligocene and diversified there as the climate cooled; subsequent diversification was on asterid clades (Winkler et al. 2009). For the intimate association between Trollius and its pollinators/seed parasites, the fly Chiastochaeta, see Pellmyr (1992).

Chemistry, Morphology, etc. Benzylisoquinoline alkaloids are largely absent from Ranunculaceae, although present in Coptis and Isopyyrum (Jensen 1995), which makes placing this feature on the tree difficult (lost and regained versus two losses). Ruijgrok (1966) clarified the distribution of the lactone ranunculin and of cyanogenic compounds. Clematis, secondarily woody, has storied wood (see Carlquist 1995a for wood and bark anatomy); it also has opposite leaves with sensitive petioles. There are cortical bundles in the erect stem of Hydrastis, but not in the rhizome. There is extensive variation in petiole anatomy in the family (Tamura 1995).

In Anemone s.l. the bracts tend to be calycine, and this is especially evident in the Hepatica group where the bracts are borne immediately underneath the flower, although not particularly closely enveloping it - and here the androecium appears to be secondarily spiral and multistaminate. Phyllotaxy in Anemoneae is particularly variable (Ren et al. 2010). There is a great deal of variation in the innervation of the perianth and petals/nectariferous appendages. Thus in Hepatica s. str. the perianth may have only a single trace, while in Laccopetalum both petals and stamens may have three traces (Hiepko 1964a). In Aquilegia the stamens are in ten vertically-arranged two-ranked series, each opposite an internal staminode; the basal member of alternating rows is a spur which has three vascular traces running into it. For an earlier discussion on stamens and nectaries, and a suggestion that the flower of Ranunculaceae might be fundamentally 3-merous, see Salisbury (1919).

Laccopetalum has huge flowers up to 15 cm across and with ca 10,000 carpels. In Caltha there are nectariferous hairs on the carpels. Although the carpels of Nigella are connate, no compitum is developed (Erbar 1998). There are often five traces to each carpel. When there is only one ovule/carpel, it is the basal member of the series (cf. Rosaceae, with which Ranunculaceae share superficial similarity, but where the single ovule is the apical member of the series). Uniovulate taxa are usually also unitegmic and with a nucellar cap (Philipson 1974). Bouman and Calis (1977) give details of the integuments of some Ranunculoideae; Wang and Ren (2008) suggest that unitegmic ovules have arisen in different ways, the single integument being either the outer (e.g. Clematis) or the inner integument (e.g. Ranunculus). The adaxial side of the carpels of Glaucidium expands more than the abaxial during the development of the fruit, so the stigma ends up on the "lower" surface. The embryo is shown as being long by Tamura (1972) and Takhtajan (1988), but it is described as being minute by Takhtajan (1997). There is extensive variation in seedling morphology, and the development of a cotyledonary tube is quite common; in a few species, e.g. Ranunculus ficaria, there is only a single cotyledon (Förster 1997).

For additional information see Schöfel (1932: esp. floral diagrams), Brouland (1935: floral vasculature), Kumazawa (1937: vernation), Tamura (1962: petiole anatomy, 1965: flower, etc., 1993: a summary of the cytology, 1995: general account, including infrageneric groupings), Rohweder (1967a: carpels), Huss (1906) and Bhandari (1967 and references), both embryology, Hegnauer (1969, 1990: chemistry), van Heel (1981, 1983: carpel development), Trifonova (1990 and references: petiole anatomy; seed anatomy), Jensen (1995: chemistry), Tobe and Keating (1985: Hydrastis), Hegnauer (1986: chemistry), Weberling (1989: nectaries), Engell (1995: considerable variation in embryo and suspensor morphology), Endress (1995a), Leins and Erbar (2010), Ren et al. (2009: Adonidae, 2011: Thalictroideae), and Zhao et al. (2011: some Ranunculoideae), all floral morphology, Johri et al. (1992: general), Aizetmüller (1995 and references, 1996, 1999: fatty acids, very variable in Ranunculaceae), Tobe (2002: general, as Hydrastidaceae), Ren et al. (2009: floral development of Adonidae, 2011: floral development of Thalictroideae), and Heiss et al. (2011: seed anatomy of Nigella). See Tamura (1972) for much information on Glaucidium, embryological data for that genus are taken mostly from Tobe (1981).

Phylogeny. The clade [Hydrastis + Glaucidium] was found to be sister to the rest of the family by Hoot et al. (1998). This and other major phylogenetic structure within the family - [Coptoideae [Thalictroideae + Ranunculoideae]] - seems quite well established (cf. also in part Ro et al. 1997). However, W. Wang et al. (2009) found strong molecular support for the relationships [Glaucidium [Hydrastis + rest of Ranunculaceae]], that for [Hydrastis + rest of Ranunculaceae] being weakened slightly by the addition of morphological data to the analysis, while Soltis et al. (2011) found weak support for a topology [Hydrastis [Glaucidium + Ranunculus]] (only three taxa of Ranunculaceae in the analysis). Indeed, the similarities between Glaucidium and Hydrastis are quite extensive, and if the two do not form a clade, using simply parsimony (ACCTRAN) one could argue that their similarities would be apomorphies for the whole Ranunculaceae... Glaucidium has quite often been placed in its own family, but this would make Ranunculaceae paraphyletic in some of these phylogenetic reconstructions, including the one preferred here; even if sister to the rest of Ranunculaceae, if recognized as a family, it would be monotypic. It is a distinctive genus; Tamura (1996) described its androecial development as being centrifugal and the androecium as being innervated by branches of staminal trunk bundles, very like the androecial development common in polystaminate core eudicots.

For relationships within Thalictroideae, see Ro and McPheron (1997). Relationships around Ranunculus are interesting. Ficaria, as well as Myosurus, with its very elongated receptacle and a flower that as a result looks like the inflorescence of Houttuynia (Saururaceae), and [Laccopetalum + Krapfia], with large flowers, many carpels, polyporate pollen, an androgynophore, etc. (Lehnebach et al. 2007), are in a strongly supported clade with a monophyletic Ranunculus - see Hörandl et al. (2005), Paun et al. (2005), Hoot et al. (2008), Gehrke and Linder (2009: esp. African montane taxa), and especially Emadzade et al. (2011). Hoot and Palmer (1994), Hoot et al. (1994), Hoot et al. (2004), Schuettpelz et al. (2002) and Meyer et al. (2010) discuss relationships in Anemone s.l., which includes Hepatica, Pulsatilla, etc.; there is a considerable amount of pollen variation in the clade (e.g. Ehrendorfer et al. 2009). Actaea is to include Cimicifuga (Compton et al. 1998). Luo et al. (2005) discuss the phylogeny of Aconitum subgenus Aconitum, Jabbour and Renner focus on Delphinium s.l., and it is clear that generic limits in Delphinieae are in need of attention. and W. Wang et al. (2010) discuss relationships in Adonidae. Xie et al. (2011; see also Miikeda et al. 2006) provde a fairly comprehensive analysis of Clematis. Unfortunately, several of the deeper bracnhes in the genus are poorly supported, but the main clades that are evident neither correlate very well with previous infrageneric taxa nor have much morphological support.

Classification. Ranunculus could perhaps include Myosurus, with its very elongated receptacle, and in particular Laccopetalum and Krapfia, which have a number of morphological similarities with Ranunculus s. str. (Lehnebach et al. 2007), but its limits are drawn slightly more narrowly by Emadzade et al. (2010). For generic limits in Adonidae, see W. Wang et al. (2010).

Previous Relationships. Ranunculaceae are a classic example of a "famille par enchaînement", nothing in particular seeming to hold them together, but work over the last two decades suggests that they are largely monophyletic (Hoot 1991, 1995; Jensen et al. 1995). However, Paeonia, frequently associated with Ranunculaceae in the past, is now included in Saxifragales as Paeoniaceae.