LIGNOPHYTA

Plant a shrub or tree; true roots +, origin endogeneous, root cap +, apex multicellular; endodermis +; shoot apical meristem multicellular; lateral meristems +, cork cambium producing cork abaxially, vascular cambium producing phloem abaxially and xylem adaxially; lamina with mean venation density 1.8 mm/mm² (to 5 mm/mm²).

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, so no Maüle reaction; root xylem exarch, cork cambium deep seated; arbuscular mycorrhizae +; shoot apical meristem interface specific plasmodesmatal network; stem with vascular tissue around central pith [eustele], vascular bundles with interfascicular tissue, ectophloic, endodermis 0, xylem endarch; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; stem cork cambium superficial; branches exogenous; leaves with single trace from vascular sympodium ["nodes 1:1"]; vascular bundles collateral [stem: phloem external; leaf: phloem abaxial]; stomata morphology?, pore opening controlled by abscisic acid; leaves with petiole and lamina, spiral, development basipetal, blade simple; axillary buds +, not associated with all leaves; prophylls two, lateral; plant heterosporous, sporangia borne on sporophylls; microsporophylls aggregated in indeterminate cones/strobili; true pollen +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, parietal tissue 2+ cells across, 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, flagellae numerous; ovules increasing considerably in size between pollination and fertilization, female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large" [ca 8 mm³], but not much bigger than ovule, with morphological dormancy; embryo cellular ab initio, endoscopic, plane of first cleavage of zygote transverse, suspensor +, short-minute, embryo straight, shoot and root at opposite ends [allorrhizic], white, cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, 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, exodermis +; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, associated gelatinous fibres [g-fibres] with innermost layer of secondary cell wall rich in cellulose and poor in lignin; 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 cell and sieve tube from same mother cell; sugar transport in phloem passive; nodes unilacunar [1:?]; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, secondary veins pinnate, overall growth ± diffuse, venation hierarchical, fine venation reticulate, veins (1.7-)4.1(-5.7) mm/mm², endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, ± haplomorphic, 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, endothecium +, endothecial cells elongated at right angles to long axis of anther; tapetum glandular, cells 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 superior, 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]; ovule not increasing in size between pollination and fertilization; pollen binucleate at dispersal, male gametophyte trinucleate, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing between cells, growth rate 20-20,000 µm/hour, outer wall pectic, inner wall callose, with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametes lacking cell walls, flagellae 0, double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; seed exotestal, becoming much larger than ovule at time of fertilization; endosperm diploid, cellular [micropylar and chalazal domains develop differently, 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; embryogenesis cellular; 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. The actual level at 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; pollen monosulcate [anasulcate], tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.

[AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood 0; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; carpels plicate; nucellar cap + [character lost where in eudicots?]; 12BP [4 amino acids] deletion in P1 gene.

[[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]] / MESANGIOSPERMAE: benzylisoquinoline alkaloids +; polyacetate derived anthraquinones + [?level]; outer epidermal walls of root elongation zone with cellulose fibrils oriented transverse to root axis; P more or less whorled, 3-merous [possible positiion]; embryo sac bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid; ?germination.

[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), filaments fairly slender, anthers basifixed; microsporogenesis simultaneous, 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. Tricolpate pollen has been found in the Late Barremian-Early Aptian of the Cretaceous some 127-120 m.y.a., and so an age of some 125 m.y. for the eudicots seems reasonable (e.g. Magallón et al. 1999; Sanderson & Doyle 2001), an age that is also similar to that of the oldest monocot fossils. However, as Smith et al. (2010) noted, when tricolpate pollen first appears in the fossil record it is widely dispersed geographically and quite heterogeneous (see also Friis et al. 2006b). This would imply an earlier origin of the clade and so the fossils are then marks of its "rise to dominance" (Beaulieu et al. 2013), however, a mid-Jurassic age for the clade of 164-127 m.y. was found only when using a broad (15 m.y.) prior on fossil calibrations and so could probably be rejected.

The recent discovery of the fossil Leefructus, dated to at least 122.6 m.y. old and assigned to stem group Ranunculaceae (Sun et al. 2011; c.f. Crepet et al. 2004 for an earlier mesofossil estimate), would also imply a substantially greater age for Ranunculales - and hence the whole eudicot clade - of ca 152-140 m.y. as extrapolated from the ages of various clades in Ranunculales given by Anderson et al. (2005). Although the fossil described by Sun et al. (2011) seems quite well preserved, it is not associated with pollen.

Other estimates of the age of this clade range from (147-)137(-128) m.y. (with eudicot calibration) to (172-)153(-138) m.y. (without: Smith et al. 2010, see also their Table S3), 147-131 m.y. (Wikström et al. 2004), 122-120 m.y. (Anderson et al. 2005), 131.1-118.5 m.y. (Moore et al. 2007), ca 125 m.y. (Magallón & Castillo 2009), (139-)130, 129(-123) m.y. (Bell et al. 2010), (127-)126(-123) m.y. (N. Zhang et al. 2012) and (129.4-)124.8-123.6(-120.2) m.y. (Magallón et al. 2013: with temporal constraints).

Subsequent divergence of eudicot clades like Proteales, Buxales, etc., may have been rapid, occurring 120-116 m.y.a. (Anderson et al. 2005). Note, however, that Wikström et al. (2003) suggested a crown group age of 147-131 m.y. for the clade, clades below core eudicots having diverged by 135-123 m.y.a., while Soltis et al. (2008: a variety of estimates) suggest an age of crown eudicots of 152-110 m.y.; ages of divergence of other eudicot clades below core eudicots are uncertain since the topology there is [Proteaceae [Sabiaceae [Buxaceae [Trochodendraceae + core eudicots]]]], different to that used (tentatively) here.

Pollination Biology. For the possible functional significance of the evolution of triaperturate 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 affect its harmomegathic movements. For pollen aperture development, see Banks et al. (2010). Diversification of eudicots is roughly contemporaneous with that of bees; the latter is estimated to have occurred (132-)123(-113) m.y.a. (Cardinal & Danforth).

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 is 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; such flowers are founf in the core eudicot Haloragaceae); Endress (2010c) also emphasized 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 [Ceratophyllales + eudicots]] node, but the flowers of Lauraceae (magnoliids) are similar. Taxa with androecia that are initiated as antesepalous triplets are scattered throughout the group (Hufford 2001a), although they are rather uncommon. Although stamen number may be high, development is rarely simply centripetal as in Magnoliaceae, and carpel and petal number seem to be unaffected (c.f. the asterid I + II clade).

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 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 Zhu et al. (2007) found a weakly supported [Gunnera + Dillenia] clade. Ranunculales are usually sister to all other eudicots, and Ceratophyllaceae may be sister to [Ranunculales + all other eudicots] (e.g. Moore et al. 2007), for which, 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; Soltis et al. 2011 and Moore et al. 2011: support weak in both cases). Similarly, Savolainen et al. (2000a), Qiu et al. (2006b), Burleigh et al. (2009) and N. Zhang et al. (2012) have also found some (weak) evidence for an association of Sabiaceae with Proteales, and so an expanded Proteales is recognised here.

A three-gene analysis by Soltis et al. (2003) found that that Sabiaceae were near Proteales, Buxales, etc., while Morton (2011: nuclear Xdh gene) found some support for a [Platanaceae + Ranunculales] clade and 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. 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 Worberg et al. (2007) found that Buxales were sister to core eudicots in most analyses, relationships in this general area were scrambled using the PetD marker alone. 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: 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; Fiz-Palacios et al. 2011 for other relationships). However, Soltis et al. (2011, see also Moore et al. 2010; Xue et al. 2012; Vekemans et al. 2012; c.f. 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 of bundles, 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]; leaves spiral; lamina ?tooth morphology; G opposite P, style 0; ovules 1-2/carpel, bistomal; P deciduous in fruit; seed exotestal; endosperm development?, embryo size? - 7 families, 199 genera, 4445 species.

Note: Possible apomorphies are now being added throughout the site; they are in bold. However, the actual level at which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is because there is very considerable homoplasy, with variation within and between clades, for most characters. Furthermore, the basic information for all too many characters is very incomplete, often coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there is the not-so-trivial issue of how ancestral states are reconstructed...

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

Magallón et al. (1999) suggested a fossil-based age of ca 70 m.y. for the clade, but the fossil was a member of the decidedly non-basal Menispermaceae. Anderson et al. (2005) dated crown group Ranunculales to 121-114 m.y.; all families had diverged before 105 m.y. except Ranunculaceae/Berberidaceae, where divergence occurred 104-90 m.y.a.. Magallón and Castillo (2009: both relaxed and constrained penalized likelihood ages) suggest ages of 113.2-121.9 m.y.. The recent discovery of a fossil assigned to stem group Ranunculaceae (see below) that is at least 122.6 m.y. old (Sun et al. 2011) suggests a decidedly greater age for the clade of ca 152-140 m.y. or so (extrapolating from the suggestions of Anderson et al. 2005). If its identity is confirmed, all age estimates in the order may well have to be revised upwards.

Krassilov and Volynets (2008) discuss a number of fossils from the Early to Middle Albian (ca 105 m.y.a.) of Primorye that they associate with Ranunculidae sensu Takhtajan, specifically comparing some with Ranunculaceae. The morphology of these fossils is odd, some appearing to have abaxially dehiscent follicles (c.f. 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). The Early Cretaceous Archaefructus has also been compared with Delphinium (Becerra et al. 2012).

See W. Wang et al. (2009) for the evolution of characters optimised on to a tree with the same topology as that used here. Optimization is difficult, for example, where should the character 1-2 ovules/carpel be placed? - low ovule numbers are probably plesiomorphic in the order.

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.

Pollination Biology. Endress (2010c) emphasized the several independant origins of wind and especially fly pollination in the clade. 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).

Spurs have evolved four to six times here; they may be on members of the outer (Myosurus) or inner (Aquilegia) perianth whorls, and be five (Aquilegia), two (Dicentra) or one (Delphinium) in number (Damerval & Nadot 2007).

Chemistry, Morphology, etc. See Hegnauer (1990) for a discussion of the chemistry of the Polycarpicae, which also includes the magnoliids and Austrobaileyales. 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?

For dimerous flowers in this part of the tree, see Doyle (2013). The basic pollen type for eudicots seems to be tectate/semitectate-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 additional information, see Ernst (1964: general), Fay and Christenhuz (2012: illustrated summary), Hennig et al. (1994) and Barthlott and Theisen (1995: both cuticle waxes), 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), and Floyd and Friedman (2000: endosperm).

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: four-genes), Kim et al. (2004a), and Worberg et al. (2006, 2007: non-coding chloroplast DNA), all suggest that Eupteleaceae may be sister to the whole of the rest of the order, although support for this position was sometimes 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. W. Wang et al. (2009) found a largely well supported set of relationships within the order, however, purely morphological analyses yielded a hightly pectinate topology, and very few branches had even poor bootstrap support and posterior probabilities were still worse. Analysis of mitochondrial genes suggested a largely rather different set of relationships between the families (Qiu et al. 2010), although support was mostly (very) weak, only the [Berberidaceae + Ranunculaceae] clade 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, containing three families (= Papaveraceae below), were commonly recognised as a separate order next to Ranunculales (Cronquist 1981; Dahlgren 1989), but there is no point in recognising them, especially given that Eupteleaceae appear to be sister to all other families, including the restricted Papaverales.

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 to 10-seriate; nodes 1:many; cuticle wax crystalloids 0; bud scales +; lamina vernation subplicate-conduplicate, margins gland-toothed, secondary veins pinnate; inflorescence axillary, fasciculate or umbellate; P 0; A 6-20, filaments short [much shorter than the anthers], anthers inconspicuously valvate, latrorse, connective prolonged; G 6-31, stipitate, "intermediate ascidiate", stigma brush-like, at most weakly secretory; ovules (-4/carpel), epitropous, outer integument 2-5 cells across, inner integument ca 2 cells across; antipodal cells do not persist; 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 are deciduous trees with short shoots that 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 m.y. 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).

[Papaveraceae [[Circaeasteraceae + Lardizabalaceae] [Menispermaceae [Berberidaceae + Ranunculaceae]]]]: plants shrbby to herbaceous; vessel elements with simple perforation plates, in diagonal groups; with both vasicentric tracheids and nucleated libriform fibres; leaves (ternately compound or palmately lobed), secondary venation palmate; P differentiated into "K" and "C", C ± petal-like; stigma wet [optimization?].

Evolution. Magallón et al. (2013: temporal constraints) estimated an age of around (404-)394.3-389.9(-382) m.y. for this clade, but it is clearly much younger in most other scenarios; N. Zhang et al. (2012) estimate an age of slightly under 100 m.y..

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 unclear at what level/for what purpose the sepals and petals of Papaveraceae-Papaveroideae and Ranunculaceae-Ranunculoideae might be considered to be the "same" (see below).

Chemistry, Morphology, etc. Wink (2008) noted that the berberine bridge enzyme, involved in the synthesis of berberine, a distinctive alkaloid scattered in this clade (but also found in some Rutaceae, etc.), was quite widely distributed in flowering plants.

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

There has been considerable discussion over the identity of the different whorls of the perianth in Ranunculales. Drinnan et al. (1994) suggested that petals have been derived from stamens several times. An inner, more or less petal-like, nectar-secreting whorl, especially obvious in Berberidaceae and Ranuculaceae, is usually interpreted as being derived from stamens. The two have a number of points of similarity, e.g. petals have a single trace, are in the same parastiches as androecial members, are similar to stamens in early development, are often peltate, originate from a primordium that is a mound rather than a ridge, and there are sometimes intermediates (Jäger 1961; Tamura 1965; Kosuge & Tamura 1989; Erbar et al. 1999; Leins 2000; Zhao et al. 2011; c.f. Kosuge 1994). Gene expression patterns in the inner whorl of Ranunculaceae and Berberidaceae are unique, and intermediates cam be explained by the fading boundaries model of development, and at another level petal presence is common to all Ranunculales, perhaps minus Euptelea (Rasmussen et al. 2009). 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). If on occasion I call the outer whorl, "calyx", and the inner whorl, "corolla", it is simply for descriptive purposes.

PAPAVERACEAE Jussieu, nom. cons.   Back to Ranunculales

Plant herbaceous, (annual), mycorrhizae 0; numerous alkaloids [inc. protopine], little oxalate accumulation; roots diarch [lateral roots 4-ranked]; cork?; +; laticifers +, articulated or not, anastomosing or not; nodes 1:3-5; subepidermal collechyma in stem; petiole bundles arcuate; leaves soft, ± fleshy, quite often glaucous, lamina margins usu. spiny toothed, leaf base broad; inflorescence determinate, terminal; flower parts whorled, dimerous; P = calyx + corolla, fugaceous, K 2, median, C 4; anthers extrorse; G connate, [2], collateral, occluded by secretion, placentation parietal (protruding-diffuse), (carpels gaping apically), (stigmatic lobes commissural); ovules (with zig-zag micropyle), inner integument (2-)3 cells across; antipodal cells endopolypoid, ± persistent; capsule septicidal [= placenticidal], (fruit with false [commissural] septum [= replum]), (persistent placental strands +); 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); (berberine + [isoquinoline alkaloid]); latex +, milky; nodes also 1:1; lamina vernation variable, entire to lobed, colleters +; flowers large, K protective, often green, enclosing the bud, lobed [usu. on left], C also 6 (0), crumpled in bud; A (4-)many, in multiples of two or three, (placentation ± axile), stigmas often confluent, dry; ovules many/carpel, ± anatropous/campylotropous, 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); 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 +), (stigmatic lobes commissural); epistase, postament +; (megaspore mother cells several); fruits opening by valves/pores; n = 6-8, 11, 12, 14...

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; n = 5, 6, 9, 10...

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

(Exudate watery); nodes 1:1(-3); hairs unicellular; subepidermal collenchyma in stem; hypanthium ± developed; pollen 4-11-colpate; capsule with 10 conspicuous longitudinal ridges, dehiscing explosively, opening from base; n = 6, 7, 11...

3/16. W. North America.

Synonymy: Eschscholziaceae Seringe

1D. Platystemoneae Spach

Nodes 1:1; hairs multicellular and multiseriate; flowers 3-merous; A 6-many, (filaments expanded, toothed); G [3(-25 - Platystemon)], styluli +; ?embryology; fruit lacking replum strands; seeds not arillate; n = 6-8.

3/5. W. North America, Baja California and Nevada to Oregon.

Synonymy: Platystemonaceae Lilja

2. Fumarioideae Eaton   Back to Ranunculales

Exudate watery; acetylornithine, (berberin) +; nodes uni(-multi)-lacunar; exudate in often non-articulated sacs; nodes 1:1+; leaves to 3X palmately compound/deeply lobed; flowers transversely disymmetric; K and C in 2's, K small, not enclosing C, C 4; nectaries +, at abaxial base of stamens; A 6; secondary pollen presentation common; pollen exine spinose, (3-colporoidate, etc.); (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]; seeds curved; exotesta palisade or not, exotegmen not fibrous, endotesta lacking fibrillar network; (embryo long).

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; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Malyschev & Peschkova 2004; Serban Procheŝ, pers. comm. S. Africa).

2A. Hypecoeae Dumortier

Protopine alkaloids alone; (nodes 1:1); (leaf blade pinnately lobed - Pteridophyllum); (K petal-like - Pteridophyllum); (outer petals often lobed, inner petals 3-lobed; A 4, (two with two vascular strands [each 2 unithecal A connate] - Hypecoum); (pollen dicolpate, deposited on inner petals - Hypecoum); (styluli 2), stigmas commissural; (ovules 1 (2)/carpel [Pteridophyllum]), inner integument ca 3 cells across [Hypecoum]; fruit (a lomentum), placentae persistent; (seeds covered with rectangular crystals - Hypecoum); (exotesta ± collapsing), (tegmen thin - Pteridophyllum); suspensor of two massive cells [Hypecoum]; n = 8, 9; cotyledons long-cylindrical [Hypecoum].

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, resupinate, single spur adaxial); K minute, two outer C spurred, (one spurred), inner C apically coherent, with median joint; A in two groups of three, 1 anther dithecal and 2 monothecal, endothecium from outer secondary parietal cell layer, inner layer dividing; style white, caducous, (green, persistent), stigma (flattened, with marginal lobes), wet, pollen deposited on stigma; (fruit indehiscent, a nutlet); (seed with elaiosome); exotesta usu. pigmented, endotesta not crystaliferous (exotesta palisade, crystaliferous); suspensor cells like a small bunch of grapes, (embryo undifferentiated); n = (6-)8(+).

19/505: Corydalis (400), Fumaria (55). Eurasia, North America, North and South Africa, mountains of E. Africa; three quarters of the 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 disymmetric flowers that are usually spurred; the calyx is usually very small or almost invisible, certainly not green and enveloping the flower bud, and there are usually six stamens.

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

Kadereit et al. (2011) discuss evolution within Papavereae, offering some dates.

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.

Pollination Biology & Seed Dispersal. The stigma of Fumaria and relatives, in which the pollen is deposited for secondary pollen presentation, can be complex; there is also secondary pollen presentation in Hypecoum, and here the pollen is deposited on the central lobe of 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 have 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).

For the unusual (transverse) plane of floral monosymmetry in Fumarioideae, see e.g. Troll (1957), Ronse Decraene and Smets (1992a), Endress (1999), etc. In Corydalis and some other genera only a single outer petal is 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 correlation of determinate inflorescences and polysymmetric flowers. CYCLOIDEA genes have been duplicated in Papaveraceae s.l., and this may be connected with the development of monosymmetry here (Kölsch & Gleissberg 2006; Damerval et al. 2007). Interestingly, nectary development is associated with the expression of CRABSCLAW genes, unlike nectaries in monocots and Ranunculaceae, but like the expression in core eudicots (Damerval et al. 2013).

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 Fumarioideae (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, but it is likely that the androecium consists of two dithecal and four monothecal stamens, the dithecal stamens being opposite the outer petals and the monothecal stamens on either side of the insertion of the inner petals (e.g. Brückner 1992; Damerval et al. 2013). In Hypecoum the monothecal stamens have fused in pairs, hence the double vascular supply to two of what appear to be ordinary dithecal stamens (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 dithecal stamens alternate with the petals and are diagonally arranged. Has the distinctive androecium of Fumarieae and of Hypecoum evolved independently?

When there are four carpels (mostly Papaveroideae-Papavereae) they are diagonally arranged (Ronse Decraene & Smets 1997b); see Brückner (2000) for discussion of carpel numbers in Fumarioideae. 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 incompatibility systems. The ovary of Fumaria has only a single ovule and the fruit is nut-like and indehiscent.

For information, see Léger (1895: vegetative morphology and anatomy), Brückner, e.g. 1982 (fruit, mostly Papaveroideae), 1983 (seed, mostly Papaveroideae), 1984 (stigma and carpel, Fumarioideae), 1992 (Pseudofumaria), and 1993 and references (carpels in Fumarioideae), and there is much general information in J. W. Kadereit (1993: as Papaveraceae) and Lidén (1993: as Fumariaceae and Pteridophyllaceae). 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 Ernst (1967: Platystemoneae); see Gleissberg and Kadereit (1999) for the complexities of leaf development interpreted in a phylogenetic context, Ronse Decraene and Smets (1990) for floral morphology (comparison with Begoniaceae), and Becker et al. (2005: floral development of Eschscholzia).

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). Additional information on Pteridophyllum is taken from Brückner (1985: fruit and seed), but the genus is poorly known; the seeds have a cellulose network in the endotesta like that of some Papaveroideae.

Phylogeny. 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 in particular. See also Judd et al. (1994) and Nikolic (1995) for earlier studies.

Within Papaveroideae, Papaver is paraphyletic and Meconopsis polyphyletic (Kadereit & Sytsma 1992; Kadereit et al. 1997, 2011; Carolan et al. 2006). For a phylogeny of Fumarioideae, see Lidén et al. (1997); Dicentra is dismembered and the old Corydaleae becomes paraphyletic. In Fumarioideae in particular morphological studies tend to recover a Fumarieae and Corydaleae; for relationships within the former, see Pérez-Gutiérrez et al. (2012).

Classification. A.P.G. II (2003) 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 harsh pinnate and fern-like leaves; in versions 8 and earlier of this site it was placed as a monotypic subfamily sister to the rest of Papaveraceae.

Within Papaveroideae, generic limits need major adjustments (e.g. Kadereit & Baldwin 2011; Kadereit et al. 2011).

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 members are now scattered throughout the tree.

[[Circaeasteraceae + Lardizabalaceae] [Menispermaceae [Berberidaceae + Ranunculaceae]]]: vascular rays broad; flowers often 3-merous, K, C and A opposite each other, K with three or more vascular traces, ± petal-like, 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. For the vasculature of the sepals/outer tepals,see Hiepko (1965); for their development, see Zhang et al. (2009 and literature). For pollen morphology, see Nowicke and Skvarla (1982).

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

Evolution. Divergence & Distribution. Anderson et al. (2005) suggested an age of ca 116-107 m.y. for this node.

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, ?stylulus; ovules ± apical, unitegmic, parietal tissue 0; 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

Leaves simple; bracteoles 0; P +, small, ± green, 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; K 5(-7), C = 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 84-72 m.y. for the divergence of these genera.

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 (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 +; leaflet vernation conduplicate, margins entire; inflorescence axillary, racemose; flowers six-merous; K with a single trace, C small, apices nectariferous; 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; germination phanerocotylar.

7[list]/40 - 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 +, like inner T; G 40<, ascidiate, stipitate; ovule pendulous, outer integument ca 4 cells across; fruit a berrylet; 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), (secondary veins pinnate); plant monoecious (dioecious; flowers perfect): (K 3); staminate flowers: (A 3, 8), filaments connate (not); (tapetal cells to 4 nucleate); pollen also colporoidate, (trinucleate); carpellate flowers: staminodes +; G 3-12, (placentation laminar), (stigma peltate); ovules (few-)many/carpel, (hemitropous), outer integument 3-4+ cells across, inner integument 2-3 cells across, parietal tissue 3-8 cells across, (nucellar cap ca 2 cells across); (antipodal cells persistent - Decaisnea); fruit a berrylet or fleshy follicle, placenta fleshy in fruit; 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.

6/39: Stauntonia (28). 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, usually six--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 95-66 m.y. for the crown-group clade.

Chemistry, Morphology, etc. Wood fluorescence? Smets (1986) suggested that the nectaries are staminal nectaries; stamen and petal develop primordia deevlop 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.

For general information, see Wu and Kubitzki (1993), Qin (1997) and the papers in Bot. Mag. 29(3). 2012, for chemistry, see Hegnauer (1966, 1989, also 1973, as Sargentodoxaceae) and Zheng and Yang (2001), seed surface, Xia and Peng (1989), carpel development, van Heel (1983), and some anatomy, Yong and Su (1993); X.-H. Zhang et al. (2005, 2009, 2012) 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 X.-H. Zhang & Ren 2008), there is no compelling reason to segregate it as a family (H.-F. Wang et al. 2009a). See Christenhuz (2012) for a summary of the family.

[Menispermaceae [Berberidaceae + Ranunculaceae]]: (berberine + [isoquinoline alkaloid]); nucellar cap +; endosperm nuclear.

Evolution. Divergence & Distribution. The age of this node may be 113-103 m.y. (Wikström et al. 2004); on the other hand, Magallón et al. (2013) estimate an age of around 65.9 m.y., Anderson et al. (2005; the estimate in Wikström et al. 2004 is similar) an age of 116-105 m.y., and Jacques et al. (2011) 125-115.6 m.y..

• The scraped stems or roots are yellow in colour in plants that have berberine.

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

Lianes (vines), climbing by twining, (shrubs, trees); 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; b class="apo">leaves simple (compound - Burasia), lamina ± peltate [at least with the base joining the top of the petiole], margins entire (toothed; lobed), petiole often pulvinate at base and apex; plants dioecious; inflorescence axillary; flowers small, parts whorled or spiral; K with a single trace, (1-)6(-12), "C" 0-8, often connate, (clasping A); staminate flowers: A 3, 6, 12 (1-40, if many, not all opposite petals), 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 2/carpel, 1 fertile, often unitegmic, hemitropous-campylotropous, micropyle endostomal (zig-zag), integuments folded, outer integument 2-5 cells across, inner integument 2-3 cells across, (single integument 3-6 cells across), parietal tissue 2-11 cells across, chalazal part large to massive; antipodals multiplying, multinucleate; fruit a drupelet, 1-seeded, style (sub)basal, endocarp dorsoventrally curved (not), (with longitudinal ridging); seed with condyle [placentar intrusion], curved, coat undistinguished, (exotesta tabular, lignified); endosperm + (0), variously ruminate (smooth), embryo long; n = (9-)11-13(+).

70 (many small)[list]/442: two groups below. Pantropical, usually lowland (map: see Wickens 1976; Frankenberg & Klaus 1980; van Balgooy 1993; Fu & Hong 2000; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Malyschev & Peschkova 2004; Rosa Ortiz-Gentry, pers. comm. 2004; Australia's Virtual Herbarium i.2013). [Photo - Fruit, Fruit.]

1. Tinosporoideae W. Wang & Z. D. Chen

(G several); seed subglobose-reniform, ruminate, (condyle 0); (style terminal), endocarp bilaterally curved; condyle ± boat-shaped or a ventral groove; cotyledons foliaceous, divaricate/imbricate (fleshy, accumbent).

27/142: Tinospora (32), Odontocarya (30). Pantropical, Atlantic North America.

2. Menispermoideae W. Wang & Z. D. Chen

Staminate flowers: (anthers connate, extrorse; pistillode 0); carpellate flowers: (staminodes 0; G 1), style lateral to basal; endocarp not bilaterally curved, condyle bilaterally and/or dorsoventrally compressed (not), often with transverse ridging as well; embryo curved, cotyledons strap-like/subterete (fleshy), accumbent (incumbent).

44/300: Abuta (21), Cyclea (30), Stephania (30). Pantropical, east North America, eastern Asia

• 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; the estimate in Wikström et al. 2004 is similar) though that the crown-group was ca 80-70 m.y.o., Jacques et al. (2011) estimated 124.4-103.3 m.y., while Wang et al. (2012: calibration using Menispermaceae fossils) suggested ages of (115.2-)109.1, 106.3(-101.7) m.y..

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; however, it is unclear what a link between Menispermaceae and Amborellaceae - hardly close - that the fossil is supposed to represent might look like (c.f. Krassilov & Goloneva 2004). Fossils are known from the Upper Turonian of ca 89.3 m.y. from the Czech republic and many fossils are known from Lower Ypresian deposits of ca 55.2 m.y. age (Jacques et al. 2011; see also Jacques 2009a). Although Cretaceous records of Menispermaceae seemed questionable to Herrera et al. (2011), Wang et al. (2012) accepted that of Prototinomiscium vangerowii, from the Turonian of the Czech Republic (Knobloch & Mai 1986; see also Anderson et al. 2005). South American is proving to be quite diverse. Doria et al. (2008) found Eocene leaf fossils from northern Colombia, and well preserved endocarps have been recorded from two Palaeocene localities in Colombia, one dated to ca 60 m.y.a. (Herrera et al. 2011); some have been identified as Stephania, now known only from the Old World.

Major clades within the family diverged during the late Cretaceous (Jacques et al. 2011: Table 5 for dates). Indeed, extensive diversification and migration in the family, which is probably Laurasian in origin, occured around the K/T boundary during a period spanning (82.2-)71.7, 60.3(-45.3 m.y.a. (W. Wang et al. 2012).

For character distributions of fruit and seed that allow their optimization on the tree, see Wefferling et al. (2013); polarization of the variation is not so easy.

Ecology. Menispermaceae are an important component 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 Importance. 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 (W. Wang et al. 2006; Meng et al. 2012); 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; Joshi 1939). Joshi (1939) suggested that in the unitegmic Tinospora cordifolia, the thinner upper part of the integument represented the outer integument. 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.

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, and Jacques and de Franceschi (2007), wood anatomy; see also Jacques (2006: much useful information). Much work has recently been carried out on the complex drupelets of the family; see Jacques (2009b), Jacques and Zhou (2010), Ortiz (2012: curved embryos develop in different ways) and Wefferkling et al. (2013: also terminology).

Phylogeny. Although Tinomiscium was strongly supported as sister to all other Menispermaceae (Ortiz et al. 2007), the sequences were corrupt (R. Ortiz, pers. comm.). The genus belongs in the [Tinosporeae + Coscinieae] clade, Tinosporoideae, a clade that had at most moderate bootstrap support (Ortiz et al. 2007; see also Ortiz 2012), but the monophyly of the subfamily was well supported in the analyses described by Wefferling et al. (2013). The tropical Coscinieae are sister to the rest of the subfamily (W. Wang et al. 2012; Wefferling et al. 2013). Menispermoideae includes the rest of the family and is well supported (but less supported in Wefferling et al. 2013). Within Menispermoideae the temperate Menispermum and relatives (Menispermeae) are sister to the other taxa, again with strong support, and there are other well supported relationships (Ortiz et al. 2007; Wang et al. 2012; Wefferling et al. 2013: c.f. Jacques et al. 2007: morphological data only, variously treated; Jacques & Bertolino 2008, some samples mislabelled, see Jacques et al. 2011). The old Menispermeae, Fibraureae and Peniantheae are polyphyletic (see also Wang et al. 2007a). 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 sampling poor.

Hoot et al. (2009: three chloroplast genes) had 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. Optimization of characters in Wefferling et al. (2013) of course was carried out in the context of the topology described in the previous paragraph.

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

Thanks. To Rosa Ortiz, for discussion and information.

Synonymy: Pseliaceae Rafinesque

[Berberidaceae + Ranunculaceae]: perennial herbs, rhizomatous; nodes also multilacunar; vascular bundles V-shaped, in herbaceous taxa often closed, scattered or in concentric rings; leaf base broad, (paired petiolar stipules +); AP3-III gene expressed in P whorl alone; outer integument at least 4 cells thick; endosperm reserves other than oil or protein.

Evolution. Divergence & Distribution. Anderson et al. (2005) had suggested an age of ca 104-90 m.y. for this node.

Chemistry, Morphology, etc. Nowicke and Skvarla (1981) thought 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 variously toothed (entire), (secondary venation pinnate), stipules common; inflorescence terminal (axillary), often racemose; flowers (2-)3(-5)-merous, parts whorled, cortical vascular system; C 6; A 6, opening by flaps; tapetal cells multinucleate; G 1, ascidiate, postgenital occlusion by secretion, stigma broad, dry or wet; (micropyle zig-zag), outer integument 4-12 cells across, inner integument 2-5 cells across; antipodal cells endopolypolypoid, persistent or not; exotestal cells lignified, oblong-fibrous to 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; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Malyschev & Peschkova 2004). [Photos - Collection]

1. Podophylloideae Eaton

Leaves palmate, 2-foliate, simple and ± deeply lobed; lowermost branch of inflorescence subtended by reduced leaf; K (0 - Achlys), 4-18, C (0; 4, with nectar spurs; 7-9; petal-like, but nectary 0); (stamens sensitive), (-19, Podophyllum, Achlys), (dehiscence by slits); microsporogenesis successive [?all], pollen wall striate (spiny), (diads; tetrads); ovules 1-many/carpel, (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], (undifferentiated - Gymnospermium); 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 with 1 trace; stigma wet.

2. Nandinoideae Heintze

(Shrubby); leaves to 3x palmately compound, petiole concave at the base; lowermost branch of inflorescence subtended by ± leaf-like inflorescence bract; (K many, C 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

Shrubby; (vessel elements with scalariform perforations, petiole bundles arcuate - Berberis); leaves odd-pinnate (unifoliolate), margins spiny-toothed; lowermost branch of inflorescence subtended by reduced inflorescence bract; K 3-12, petal-nectaries paired, basal; stamens sensitive; tapetum plasmodial, tapetal cells 4-8-nucleate; microspore tetrads isobilateral, 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. and E. 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. In their flowers 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 crown-group age of ca 88-72 m.y. for Berberidaceae.

Within the family, Berberis is by far the most widely distributed genus, and fossils have been reported from Palaeocene deposits ca 60 m.y. 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 m.y., although disjunctions in 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 unifolioliate) on short shoots while the scale leaves are basically stipular (Gonzalez & Pabon Mora 2009). Mahonia s. str. (with ca 100 species) has compound leaves, but it hybridises with Berberis.

In Epimedium there are nectaries are spurs coming from the four inner tepals. Although Podophyllum has many stames, single stamens or groups of stamens are opposite the innermost perianth members (Schmidt 1928). Ghimire and Heo (2012) described the anther tapetum of Berberidoideae as being glandular; if true, multinucleate tapetal cells would still separate Berberidoideae from other Berberidaceae. Successive microsporogenesis has been reported (Min et al. 1995). The carpel in Berberidaceae varies in its orientation. According to Chapman (1925, c.f. 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) described 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, M.-Y. Zhang et al. (2012) for pollen evolution, 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 monotypic 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 placed sister to the rest of the family in the most parsimonious tree that he found. Early molecular studies (e.g. Adachi 1995) found relationships between the two genera, and these have since been confirmed, as by Kim et al. (2004), if Nandina did sometimes tend to wander about 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 the [Nandinoideae + Berberidoideae] clade was weak, it was much strengthened in analyses that included morphological data.

• Nandina: K many; nectaries 0; K and A develop from the splitting of a single primordium; pollen with massive endexin; 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 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 ca 3 traces.

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

Previous Relationships. Fruit dehiscence in some Berberidaceae and Papaveraceae is transverse, at least in part. Although 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; (cuticle waxes as platelets); stomata also paracytic; lamina margins usu. gland-toothed; inflorescence terminal; flowers medium to large, parts spiral or whorled, K, C, and A not opposite each other, A many, spiral; receptacle well developed, stigma ± dry; ovules several/carpel, apotropous, micropyle endostomal, obturators various; fruit a follicle; exotestal cells often thickened, unlignified, or seed ± pachychalazal, coat thin; endosperm starchy, embryo minute to short, cotyledons connate or not, cotyledonary tube common; chromosomes small, straight, stout; germination epigeal.

62[list]/2525 - five subfamilies below. ± World-wide, but mainly temperate.

[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, lamina simple, vernation plicate, margin deeply palmately lobed; flowers single, terminal; P +, nectaries 0; stigma bilobed; outer integument 4-13 cells across, inner integument 2-5 cells across.

Synonymy: Hydrastidaceae Martynov

1. Glaucidioideae Loconte

Coumarin +, alkaloids, berberin 0; lamina vernation also supervolute-curved; flowers with cortical vascular system; P 4, large, petal-like; A development centrifugal; G 2, basally connate, opposite outer P [transverse], plicate; ovules many/carpel, parietal tissue 0, nucellar cap massive; megaspore mother cells several; follicle with stigma on lower abaxial surface, also dehiscing abaxially; 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; erect stem with cortical vascular bundles, nodes swollen, multilacunar; petiole base on rhizome encircling stem; P inconspicuous, (2)3(4), with a single trace; A ?development; pollen tectum striate-reticulate; G several, stigma with multicellular projections; ovules 1-2(-4)/carpel, micropyle zig-zag; fruit a little berry; exotesta strongly palisade, exotegmen lignified, testa and tegmen multiplicative; embryo minute; n = 13.

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

Synonymy: Hydrastidaceae Martinov

[Coptoideae [Thalictroideae + Ranunculoideae]]: vascular bundles with xylem surrounding phloem [c.f. Takhtajan 1997], vessel elements with simple perforation plates [usu.]; paratracheal parenchyma ± absent; (nodes 1:1, 2:2); petiole bundles with associated lignification; leaves (opposite, two-ranked), palmately compound, lamina vernation variable; inflorescence often cymose, or flowers single; P 5-merous, ± petal-like, petals 0-13, usu. obviously nectariferous, very diverse in form; A development centripetal, extrose or introrse; (pollen inaperturate); G (1-)many, usually with complete postgenital fusion, (ascidiate), when 3, orientation variable; ovules 1-15/carpel; outer integument?; (endosperm 0).

60/2523. ± World-wide, but especially northern and montane (map: from Vester 1940; Hultén 1971; Frankenberg & Klaus 1980; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Wilson 2007).

3. Coptoideae Tamura

Small shrub or perennial herbs; nectaries 5-10, petal-like, thick, stalked; carpels stipitate; n = (8) 9, chromosomes small, rod-like.

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

[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), (embryo medium).

54/2475.

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; leaves to 3x compound, lamina segments ± curved-involute, papillate, ([adaxial] stipules + - Thalictrum); (plant dioecious); flower parts ± whorled; nectaries ± petal-like and stalked, (internal staminodes +); integument single, 7-8 cells across; n = 7, chromosomes small, bean-shaped.

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

Synonymy: Aquilegiaceae Lilja, Thalictraceae Rafinesque

5. Ranunculoideae Arnott

(Liane), (annual herbs); lactone-forming glycosides [ranunculin], (20:3[d]5c,11c,14c fatty acid), (cardenolides; bufadienolides [cardiac glycosides]) +, benzylisoquinoline alkaloids usu. 0, berberine 0; stomata ³35 µm long; (petiole bundles arcuate; wing bundles +; medullary bundles +); hairs clavate; (leaves opposite - Clematis), (simple), (pedate), lamina segments ± involute (supervolute and/or curved), (stipule adaxial - Caltha); (flowers vertically monosymmetric), (flower parts ± whorled); (K sepal-like), (nectaries 0), (staminodes surrounding G); (pollen multicolpate/porate); ovule often 1/carpel, median (lateral - Adonidae), (micropyle ?endostomal), (integument single, 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), (cotyledon 1), (cotyledons connate); n = (6-)8(-9), chromosomes large, long, 2-armed, often curved [R-/Ranunculus-type]; (germination hypogeal - some Clematis).

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

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 petal-like sepals, nectariferous "petals", spiral, usually numerous stamens, and separate carpels borne on a well-developed receptacle.

Evolution. Divergence & Distribution. Anderson et al. (2005) estimated a crown-group age of ca 87-73 m.y. for Ranunculaceae.

There are 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 m.y. old in China and assigned to stem Ranunculaceae (Sun et al. 2011) will, if confirmed, very much change our ideas of the evolution of eudicots as a whole. Paleoactaea, from the Late Palaeocene some 58 m.y.a., 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 m.y.a. (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 m.y.a., however, the stem age is some (43.8-)26(-9.2) m.y. (Miikeda et al. 2006; Xie et al. 2011: HPD). Diversification within Delphinieae began early in the Oligocene (41.8-)32.3(-23.0) m.y.a. (Jabbour & Renner 2012).

For the evolution of Arctic Ranunculaceae, see Hoffmann et al. (2010). In the widely-distributed Ranunculus tthere has been a substantial amount of dispersal in tropical and subtropical mountains and in the Southern Hemisphere - even between southern Africa and America - often followed by radiations (Emadzade et al. 2010, 2011; Hörandl & Emadze 2011). 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 and they show little molecular differentiation (Whittall et al. 2006).

Delphinium s.l., Aconitum, and relatives (Delphinieae) between them account for about a quarter of the diversity in the family. Delphinium s.l. is largely Mediterranean-Turanian in distribution, but with forays into Africa and North America. Delphinieae began diversifying about 32.5 m.y.a.; interestingly, the transition from a short-lived (± annual) to a perennial habit in Delphinium is associated with bursts of diversification (Jabbour & Renner 2011, 2012a).

Pollination Biology & Seed Dispersal. Bumble bees are the predominant pollinators of the 600-700 species of Delphinieae, a group that is very speciose in the Himalayas (Renner & Jabbour 2012b), and diversification of bumblebees probably occured 40-25 m.y.a. (Hines 2008 and references), i.e., about the same time as that of Delphinieae. Delphinieae have paired nectary spurs of the inner floral whorl that are borne inside a spurred petaloid member of the outer floral whorl; Renner and Jabbour (2012b) discuss the evolution of this unusual pollination mechanism. The monosymmetry of Delphinieae becomes apparent only rather late in development after organ initiation (Jabbour et al. 2009). Other Ranunculaceae like Clematis and Ranunculus have apparently unspecialized flowers and may be visited by many species of pollinators (Waser et al. 1996).

Many other Ranunculaceae also have distinctive nectaries which are more or less petaloid. The five, coloured nectar spurs of Aquilegia are very unusual in flowering plants; nectar spurs are usually associated with monosymmetry. In Ranunculus there are small nectaries at base of the petal-like inner whorl; the outer whorl is very sepal-like, while in Laccopetalum and relatives there are a number of nectary ridges on the petals. Normally, however, the nectaries are rather different morphologically from ordinary petals and are sometimes quite elaborate beaker-shaped structures; it is the sepals that are petal-like and visually attractive. Kramer and Hodges (2010) review the evolution of "petals" in Aquilegia and Wang and Chen (2007) discuss "petal" evolution in Thalictroideae; see also above.

Many species of Thalictrum are wind-pollinated, and some of these species are monoecious or diocious; monoecy and dioecy are restricted to and predominate in New World species (Soza et al. 2012).

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. Agromyzids may have 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 is a liane with opposite leaves with sensitive, twining petioles. There are cortical bundles in the erect stem of Hydrastis, but not in the rhizome, the rhizome, and that of Glaucidium, is an irregular sympodium. Variation in petiole anatomy is extensive (Tamura 1995) and adaxial/intrapetiolar stipules occur sporadically in the family (Hagemann 1970).

Soltis et al. (2003a) suggest that both Glaucidium and Hydrastis have a bimerous perianth. Tucker and Hodges (2005) discuss floral development in Aquilegia and its immediate relatives. 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. Phyllotaxy in Anemoneae is particularly variable (Ren et al. 2010). There is a great deal of variation in the innervation of the sepals and petals/nectariferous appendages. Thus in Hepatica s. str. the sepals 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 (for the development of these unusual internal staminodes, see Sharma & Kramer 2012); the basal member of alternating rows is the spurred petal 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). Tamura (1996) described the androecial development of Glaucidium 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.

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 (c.f. Rosaceae, with which Ranunculaceae share a superficial similarity, but where the single ovule is the apical member of the series). Uniovulate taxa are usually also unitegmic and have a nucellar cap (Philipson 1974). Bouman and Calis (1977) give details of the integuments of some Ranunculoideae. Z.-F. Wang and Ren (2008) suggested 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); they also described a rather obscure annular structure that surrounds the ovule in Coptis. The adaxial side of the carpels of Glaucidium grows more than the abaxial as the fruit develops, so the stigma ends up on the "lower" surface; there 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 embryo size (Tamura & Mizumoto 1972) and seedling morphology, and the development of a cotyledonary tube is quite common; in some 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, 1993: summary of cytology, 1995: general account, including infrageneric groupings), Rohweder (1967a: carpels), Huss (1906) and Bhandari (1967 and references), both embryology, Hegnauer (1969, 1986, 1990) and Jensen (1995), all chemistry, Aizetmüller (1995, 1996, 1999 (fatty acids), van Heel (1981, 1983: carpel development), Trifonova (1990 and references: petiole anatomy; seed anatomy), Tobe and Keating (1985: Hydrastis), Weberling (1989: nectaries), Engell (1995: embryo and suspensor morphology, considerable variation), Endress (1995a), Leins and Erbar (2010), Ren et al. (2009: Adonidae, 2011: Thalictroideae), and Zhao et al. (2011, 2012: some Ranunculoideae), all floral (and some inflorescence) morphology, Johri et al. (1992: general), 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 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 (c.f. 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... For other early work on the family, see Hoot (1991, 1995) and Jensen et al. (1995)

For relationships within Thalictroideae, see Ro and McPheron (1997) and especially Wang and Chen (2007). Relationships along the spine of Thalictrum are for the most part poorly supported, but an insect-pollinated clade is sister to the rest; current sections seem largely useless (Soza et al. 2012).

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 to huge 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: 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). However, Pfosser et al. (2011) suggests that Anemone may be best divided up into x = 7 (inc. Hepatica) and x = 8 clades. For the phylogeny of Actaea, see Compton et al. (1998). Luo et al. (2005) discuss the phylogeny of Aconitum subgenus Aconitum. Jabbour and Renner (2011, 2012) focused on the speciose Delphinieae, and the clades they found only partly mappped on to previously-recognized genera while Aconitum gymnandrum was unplaced. There was little resolution of relationships within the speciose Delphinium section Diedropetela (Koontz et al. 2004). W. Wang et al. (2010) discuss relationships in Adonidae. Xie et al. (2011; see also Miikeda et al. 2006) provide a fairly comprehensive analysis of Clematis, unfortunately, several of the deeper branches 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. The classification above is based on that in . Glaucidium has quite often been placed in its own family, but it would be monotypic; although a distinctive genus, it has quite a lot in common with Hydrastis.

For generic limits around Ranunculus, see Emadzade et al. (2010), in Adonidae, see W. Wang et al. (2010), and aorund Anemone, see Pfosser et al. (2011). In the Delphinium area, Aconitella is derived from within Consolida, and the combined clade is to be included within Delphinium (Jabbour & Renner 2012; see also Jabbour et al. 2011). Actaea is to include Cimicifuga (Compton et al. 1998)

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. However, Paeonia, frequently associated with Ranunculaceae in the past, is now included in Saxifragales as Paeoniaceae. On the other hand, Tamura (1972) thought that Glaucidium was close to Hypericales.

Botanical Trivia. The zygote of Aneomne flaccida is undivided when the seed is dispersed (Tamura & Mizumoto 1972).