EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, thalloid, with single-celled apical meristem, showing gravitropism; rhizoids +, unicellular; acquisition of phenylalanine lysase [PAL], flavonoids [absorbtion of UV radiation], phenylpropanoid metabolism [lignans, also lignins], xyloglucans +; plant poikilohydrous [protoplasm dessication tolerant], ectohydrous; cuticle +; cell wall also with (1->3),(1->4)-ß-D-MLGs [Mixed-Linkage Glucans]; chloroplasts per cell, lacking pyrenoids; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles in vegetative cells 0, metaphase spindle anastral, predictive preprophase band of microtubules, phragmoplast + [cell wall deposition spreading from around the spindle fibres], plasmodesmata +; antheridia and archegonia jacketed, stalked; spermatogenous cells monoplastidic; blepharoplast, bicentriole pair develops de novo in spermatogenous cell, associated with basal bodies of cilia [= flagellum], multilayered structure [4 layers: L1, L4, tubules; L2, L3, short vertical lamellae] + spline [tubules from L1 encircling spermatid], basal body 200-250 nm long, associated with amorphous electron-dense material, microtubules in basal end lacking symmetry, stellate array of filaments in transition zone extended, axonemal cap 0 [microtubules disorganized at apex of cilium]; male gametes [spermatozoids] with a left-handed coil, cilia 2, lateral; oogamy; sporophyte dependent on gametophyte, embryo initially surrounded by haploid gametophytic tissue, plane of first division horizontal [with respect to long axis of archegonium/embryo sac], suspensor/foot +, cell walls with nacreous thickenings; sporophyte multicellular, with at least transient apical cell [?level], sporangium +, single, dehiscence longitudinal; meiosis sporic, monoplastidic, microtubule organizing centre associated with plastid, cytokinesis simultaneous, preceding nuclear division, sporocytes 4-lobed, with a quadripolar microtubule system; spores in tetrads, sporopollenin in the spore wall, wall with several trilamellar layers [white-line centred layers, i.e. walls multilamellate]; nuclear genome size <1.4 pg, LEAFY gene present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes.
Many of the bolded characters in the characterization above are apomorphies of subsets of streptophytes along the lineage leading to the embryophytes, not apomorphies of crown-group embryophytes per se.
All groups below are crown groups, nearly all are extant. Characters mentioned are those of the immediate common ancestor of the group,  contains explanatory material, () features common in clade, exact status unclear.
Abscisic acid, ?D-methionine +; sporangium with seta developing from basal meristem [between epibasal and hypobasal cells], sporangial columella + [developing from endothecial cells]; stomata +, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and in rhizoids/root hairs; spores trilete; polar transport of auxins and class 1 KNOX genes expressed in the sporangium alone; shoot meristem patterning gene families expressed; MIKC, MI*K*C* and class 1 and 2 KNOX genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns.
[Anthocerophyta + Polysporangiophyta]: archegonia embedded/sunken in the gametophyte; sporophyte long-lived, chlorophyllous; sporophyte-gametophyte junction interdigitate, sporophyte cells showing rhizoid-like behaviour.
Sporophyte branched, branching apical, dichotomous; sporangia several, each opening independently; spore walls not multilamellate [?here].
EXTANT TRACHEOPHYTA / VASCULAR PLANTS
Photosynthetic red light response; plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; (condensed or nonhydrolyzable tannins/proanthocyanidins +); sporophyte soon independent, dominant, with basipetal polar auxin transport; vascular tissue +, sieve cells + [nucleus degenerating], tracheids +, in both protoxylem and metaxylem, plant endohydrous; endodermis +; stem with an apical cell; branching dichotomous; leaves spirally arranged, blades with mean venation density 1.8 mm/mm2 [to 5 mm/mm2]; sporangia adaxial on the sporophyll, derived from periclinal divisions of several epidermal cells, wall multilayered [eusporangium]; columella 0; tapetum glandular; gametophytes exosporic, green, photosynthetic; basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; placenta with single layer of transfer cells in both sporophytic and gametophytic generations, root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Sporophyte branching ± indeterminate; root apex multicellular, root cap +, lateral roots +, endogenous; endomycorrhizal associations + [with Glomeromycota]; tracheids with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangia borne in pairs and grouped in terminal trusses, dehiscence longitudinal, a single slit; cells polyplastidic, microtubule organizing centres not associated with plastids, diffuse, perinuclear; blepharoplasts +, paired, with electron-dense material, centrioles on periphery, male gametes multiciliate; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; LITTLE ZIPPER proteins.
Sporophyte woody; lateral root origin from the pericycle; branching lateral, meristems axillary; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].
EXTANT SEED PLANTS / SPERMATOPHYTA
Plant 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 [hence with p-hydroxyphenyl and guaiacyl lignin units, so no Maüle reaction]; root stele with xylem and phloem originating on alternate radii, cork cambium deep seated; shoot apical meristem interface specific plasmodesmatal network; stem with vascular cylinder around central pith [eustele], phloem abaxial [ectophloic], endodermis 0, xylem endarch [development centrifugal]; 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 +; cork cambium superficial; leaves with single trace from vascular sympodium [nodes 1:1]; stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; buds axillary (not associated with all leaves), exogenous; prophylls two, lateral; leaves with petiole and lamina, development basipetal, blade simple; plant heterosporous, sporangia borne on sporophylls, sporophylls spiral; microsporophylls aggregated in indeterminate cones/strobili; grains monosulcate, aperture in ana- position [distal], exine and intine homogeneous; ovules unitegmic, parietal tissue 2+ cells across, megaspore tetrad linear, functional megaspore single, chalazal, lacking sporopollenin, megasporangium indehiscent; pollen grains land on ovule; gametophytes dependent on sporophyte; apical cell 0, rhizoids 0; male gametophyte development initially endosporic, tube developing from distal end of grain, gametes two, developing after pollination, with cell walls; female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; embryo cellular ab initio, endoscopic, plane of first cleavage of zygote transverse, suspensor +, short-minute, embryonic axis straight [shoot and root at opposite ends; plant allorhizic], cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, whole nuclear genome duplication [zeta duplication], 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.
ANGIOSPERMAE / MAGNOLIOPHYTA
Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, 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, hypodermis suberised and with Casparian strip [= 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 1:?; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance to increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, venation hierarchical-reticulate, secondary veins pinnate, veins (1.7-)4.1(-5.7) mm/mm2, endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, ± haplomorphic; protogynous; parts spiral [esp. the A], free, numbers unstable, development in general centripetal; P +, members each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], sporangium pairs dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, 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 columellate, endexine lamellate only in the apertural regions, thin, compact; nectary 0; carpels present, superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus at most short [shorter than ovary], hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, 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, functional megaspore, chalazal, lacking cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; supra-stylar extra-gynoecial compitum +; ovule not increasing in size between pollination and fertilization; pollen grains land on stigma, bicellular at dispersal, mature male gametophyte tricellular, germinating in less than 3 hours, pollen tube elongated, unbranched, growing between cells, growth rate (20-)80-20,000 µm/hour, apex of pectins, wall with callose, lumen 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, cilia 0, siphonogamy; double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; mature seed much larger than ovule when fertilized, small , dry [no sarcotesta], exotestal; endosperm diploid, cellular, heteropolar [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; dark reversal Pfr → Pr; Arabidopsis-type telomeres [(TTTAGGG)n]; nuclear genome size <1.4 pg [1 pg = 109 base pairs], whole nuclear genome duplication [epsilon duplication]; protoplasm dessication tolerant [plant poikilohydric]; 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]]]]]: 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]]]]: vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood +; 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 +; sesquiterpene synthase subfamily a [TPS-a] [?level], 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 position]; pollen tube growth intra-gynoecial; embryo sac bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid.
[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (extra-floral nectaries +); (veins in lamina often 7-17 mm/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 +), asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; (vessel elements with simple perforation plates in primary xylem); nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; protandry common; 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], short [<2 x length of ovary]; seed coat?
Age. Estimates of the age of the crown eudicot clade commonly range from 150-120 m.y.a., e.g. (147-)137(-128) m.y. (with eudicot calibration) to (172-)153(-138) m.y. (without: Smith et al. 2010, see also their Table S3), (153-)147, 131(-125) m.y. (Wikström et al. 2001, 2004), 122-120 m.y. (Anderson et al. 2005; similar in Schwery et al. 2014), 131.1-118.5 m.y. (Moore et al. 2007), ca 125 m.y. (Magallón & Castillo 2009), ca 131.7 m.y. (Magallón et al. 2015), (145-)130, 129(-117) m.y. (or thereabouts: Bell et al. 2010), (127-)126(-123) m.y. (N. Zhang et al. 2012; see also Xue et al. 2012), (129.4-)124.8-123.6(-120.2) m.y. (Magallón et al. 2013). Soltis et al. (2008: a variety of estimates) suggest an age for crown eudicots of 152-110 m.y., a mid-Jurassic age for the clade of 164-127 m.y. was found when using a broad (15 m.y.) prior on fossil calibrations (Beaulieu et al. 2013), a similar age of (161-)156(-146) (or (128-)125.5(-115) m.y.) was found by Zeng et al. (2014), while the age in Z. Wu et al. (2014) is around 197 m.y. ago. See also a variety of ages that depend on whether dating is by phytoliths, nuclear or chloroplast genes, etc., in Christin et al. (2014); a rather unlikely age of (100.4-)96.3(-93) m.y. is suggested by Iles et al. (2014).
Tricolpate pollen has been found in the Late Barremian-Early Aptian of the Cretaceous some 127-120 m.y.a., and so a minimum age of some 125 m.y. for the eudicots is reasonable (e.g. Magallón et al. 1999; Sanderson & Doyle 2001; Friis et al. 2011 for numerous references), an age that is also similar to that of the oldest monocot fossils. However, as Smith et al. (2010) note, when tricolpate pollen first appears in the fossil record it is both widely dispersed geographically and quite heterogeneous (see also Friis et al. 2006b). This would imply an earlier origin of the clade, the fossils then being more marks of its "rise to dominance" than of its origin (Beaulieu et al. 2013: p. 4).
The recent discovery of 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. (age extrapolated from the ages of various clades in Ranunculales given by Anderson et al. ). Although Leefructus seems quite well preserved, it is not associated with pollen (Sun et al. 2011). Friis et al. (2011) discuss a variety of early fossils that are, or from general morphology might be, associated with tricolpate grains.
Evolution. Divergence & Distribution. In the topology found by Zhang et al. (2014) there is a substantial period of 16-26 m.y. (ca 35 m.y. in Zhang et al., but c.f. suppl. Table 6) between the divergence of [Ceratophyllales + Chloranthales] and the eudicots. Subsequent divergence of eudicot clades like Proteales, Buxales, etc., may have been rapid, occurring 120-116 m.y.a. (Anderson et al. 2005), while Wikström et al. (2001) thought that the clades immediately below core eudicots had diverged by (140-)135, 123(-118) m.y. ago.
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 (such waxes 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, and the interpretation of the venation of Euptelea is debatable, as he noted (Doyle 2007). The palmate venation in aquatics like Nelumbo may further confuse the situation; palmate venation is common in aquatics with their broad peltate or cordate-based leaf blades and so 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". For the evolution of syncarpy, see Sokoloff et al. (2013d).
Dimerous flowers are to be found in the basal eudicot grade, but are at most 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; Doyle 2013; such flowers are found 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 is placed at the [monocots [Ceratophyllales + eudicots]] node here, 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 Magnoliales (e.g. Corner 1946b), and carpel and perianth/petal number do not often increase in parallel, unlike in the euasterids. The basic pollen type for eudicots seems to be tectate/semitectate-reticulate, the latter grains being found in e.g. Platanacaeae, Menispermacaeae, Hamamelidaceae, Gunneraceae (Denk & Tekleva 2006) and Nelumbonaceae. For optimisation of syncarpy in this part of the tree, see Sokoloff et al. (2013d).
Ecology & Physiology. Liu et al. (2014) suggest that it is only with the eudicots that we see generally faster litter decomposition with all its implications in terms of nutrient cycling.
Pollination Biology. Diversification of eudicots is roughly contemporaneous with that of bees; the latter is estimated to have begun (132-)123(-113) m.y.a. (Cardinal & Danforth 2013). Protandry is common in eudicots, although aquatic taxa tend to be protogynous, and protogyny is also common in mono- and dioecious taxa (interfloral protogyny: see Bertin & Newman 1993).
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).
Genes & Genomes. Salse et al. (2009) suggested that the common ancestor of this clade had seven chromosomes. Taxa in which GLO-like proteins cannot form heterodimers predominate in this clade (Melzer et al. 2014); DEF-like proteins also cannot do this (see also the [monocot + eudicot] node). Melzer et al. (2014) also suggest that this may contribute to the increasing canalization of floral development.
Chemistry, Morphology, etc. 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. Ranunculales are usually sister to all other eudicots, and Ceratophyllaceae may be sister to eudicots (e.g. Moore et al. 2007); see also the discussion at the mesangiosperm node. The position of Chloranthales, magnoliids, Ceratophyllales and monocots, all somewhere immediately basal to the eudicots, still remains unclear.
There is some uncertainty about basal eudicot relationships. An unresolved Proteales and Sabiaceae are often sister to eudicots minus Ranunculales (e.g. S. Kim et al. 2004b). A position [Ranunculaceae [Sabiaceae [all other eudicots]]] had only 83% support, of which most came from the matK gene (the other genes examined were petD and trnL-F) in analyses by Worberg et al. (2006, 2007); for this topology, see also Qiu et al. (2010: support weak). A three-gene analysis by Soltis et al. (2003) also 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 [Trochodendrales [Sabiaceae + Buxales]] clade. Moore et al. (2008) did not find strongly-supported relationships in this part of the tree, and various permutations of relationships of the groups being discussed, none strongly supported, were found by Zhu et al. (2007). Soltis et al. (2008) used the topology [Proteaceae [Sabiaceae [Buxaceae [Trochodendraceae + core eudicots]]]] in their book (see also Goloboff et al. 2009; Fiz-Palacios et al. 2011 for other relationships).
However, Proteales and Sabiaceae are sister taxa in an analysis of all 79 protein-coding plastid genes and four mitochondrial genes (Moore et al. 2008: support only moderate; see also Soltis et al. 2011 and Moore et al. 2011: support weak in both cases). The two were also sister in the major analyses of chloroplast and nuclear data in Sun et al. (2014), but not in the mitochondrial study and in many of the supplementary trees. Savolainen et al. (2000a), Qiu et al. (2006b, c.f. 2010), Burleigh et al. (2009), N. Zhang et al. (2012); Ruhfel et al. (2014: not all analyses), Z. Wu et al. (2014), and Magallón et al. (2015) have also found (weak) evidence for an association of Sabiaceae with Proteales, and so an expanded Proteales is recognised here. Morphology is consistent with such a position, however, it has been suggested that the pentamerous flowers of Sabiaceae are derived from trimerous ranunculalean flowers, there being some kind of relationship between the two groups (e.g. Endress 2010c; Ronse De Craene et al. 2015).
The relationships of Buxales and Trochodendrales are also 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 uncertain relationships in a three-gene analysis of mitochondrial data, but with eight genes a topology similar to that used in the Summary Tree was found (see also Qiu et al. 2010). Hilu et al. (2003) also suggested that Buxales were sister to core eudicots. Worberg et al. (2006, 2007) presented a 3-gene (chloroplast) phylogenetic analysis focussing on the eudicots; most of the relationships they found along the eudicot spine were strongly (>90% jacknife) supported. Soltis et al. (2011) in their seventeen-gene analysis found strong support for the relationships along the basal spine of the eudicots shown here (see also Moore et al. 2010; Xue et al. 2012; Vekemans et al. 2012; Ruhfel et al. 2014; Z. Wu et al. 2014; Magallón et al. 2015). The positions of Buxales and Trochodendrales was reversed in the study by Wikström et al. (2003; see also Moore et al. 2011 for position of Buxales and Trochodendrales).
RANUNCULALES Berchtold & J. Presl Main Tree.
(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 serrate, ?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.
Age. Crown-group Ranunculales may be (146-)140, 126(-120) m.y. (Wikström et al. 2001: c.f. topology); Anderson et al. (2005) dated them to 121-114 m.y., Magallón and Castillo (2009) to ca 113.2 m.y., while about 114.8 m.y. is the estimate in Magallón et al. (2015).
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. The crown group age suggested by Early Cretaceous fossils from Portugal can perhaps be assigned to this part of the tree - or to Berberidopsidales or Saxifragales (von Balthazar et al. 2005). If the identity of the fossil assigned to stem group Ranunculaceae (see below) that is at least 122.6 m.y. old (Sun et al. 2011) is confirmed, the clade may be 152-140 m.y.o. or so (extrapolating from the dating suggestions of Anderson et al. 2005).
Krassilov and Volynets (2008) discuss a number of fossils from the Early to Middle Albian (ca 105 m.y.a.) of Primorye that they associated 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 at nodes from which branches also arise. The plants are very small, and were described as being weedy (Krassilov & Volynets 2008). The Early Cretaceous Archaefructus has also been compared with Delphinium (Becerra et al. 2012).
Note: Possible apomorphies 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 partly because many characters show considerable homoplasy, in addition, basic information for all too many is very incomplete, frequently 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 (see above).
Evolution. Divergence & Distribution. Ranunculales contain ca 1.6% of eudicot diversity.
Anderson et al. (2005) noted that all families had diverged before 105 m.y. except Ranunculaceae/Berberidaceae, where divergence occurred 104-90 m.y.a. (see also Wikström et al. (2001).
See W. Wang et al. (2009: extensive morphological data matrix) 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.
Ecology & Physiology. Liu et al. (2014) suggest that it is only somewhere around this node that the origin of angiosperm leaves with rather fast decomnposability can be pegged.
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 fertilization (up to some two months or more after pollination) in members of Ranunculales, including Eupteleaceae, Circeasteraceae, Lardizabalaceae, and Ranunculaceae (Sogo & Tobe 2006d for references).
Floral nectar spurs have evolved four to six times in Ranunculales; they may be on members of the outer (Myosurus, Delphinium) or inner (Aquilegia) perianth whorls, and be five (Aquilegia), two (Dicentra) or one (Delphinium) in number (Damerval & Nadot 2007).
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. However, caterpillars of Papilionidae-Parnassiinae are quite common here (Simonsen et al. 2011; Condamine et al. 2011).
Genes & Genomes. For the complex pattern of duplication of APETALA3 and FUL-like genes and their expression in Ranunculales, see Sharma et al. (2011) and Pabón-Mora et al. (2012) and references; where to put these duplications on the tree is unclear.
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 Ranunculales, is synthesised via the tyrosine pathway. Gleissberg and Kadereit (1999) discussed 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?
There has been considerable discussion over the identity of the different petal/tepal/sepal/stamen parts of the flower in Ranunculales. Almost all Ranunculales, perhaps minus Euptelea, have petals, that is, more or less expanded and attractive parts of the flower (Rasmussen et al. 2009). An inner, more or less petal-like, nectar-secreting whorl is especially obvious in Berberidaceae and Ranuculaceae, and is usually interpreted as being derived from stamens, and Drinnan et al. (1994) suggested that petals had been derived from stamens several times. However, Sharma et al. (2014 and references) found no developmental evidence for a connection between more or less petal-like nectaries and stamens in Ranunculaceae, at least.
This next paragraph to be reworked: Gene expression patterns in the inner perianth whorl of Ranunculaceae and Berberidaceae are unique, and intermediates can be explained by the fading boundaries model of development (ref.). Chanderbali et al. (2010) found that expression of genes active in each floral whorl in flowers of the one member of Ranunculales they examined (Escholtzia) were restricted to that whorl, as in other eudicots; within Ranunculales, Papaveraceae-Papaveroideae, to which Escholtzia belongs, have a perianth that is apparently made up of a rather conventional calyx and corolla. On the other hand, in Delphinium (Ranunculaceae) expression patterns of genes active in the two outer floral whorls 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.
Monosymmetry has evolved at least twice in this clade, and i>Cycloidea genes are involved. However, they are variously expressed, ad- or abaxially or laterally, in the flower, and may also be expressed in the outer whorl (Jabbour et al. 2014 and references: see Papaveraceae-Fumarioideae and Ranunculaceae below). This is unlike the consistent adaxial expression in Pentapetalae studied (Hileman 2014 and references).
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 tube plastids and phloem proteins), Carlquist and Zona (1988) and 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), 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. 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; Bell et al. 2010) sister to all other members of the order.
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 (W. Wang et al. 2009); the topology was hightly pectinate, and very few branches had even poor bootstrap support and posterior probabilities were still worse. Loconte et al. (1995) found Ranunculales to be paraphyletic in a morphological phylogeny. 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 a classification of the order, largely followed here, see W. Wang et al. (2009).
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, i.e. including Papaverales.
Includes Berberidaceae, Eupteleaceae, Circaeasteraceae, Lardizabalaceae, Menispermaceae, Papaveraceae (inc. Fumarioideae, Papaveroideae), 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 1:5(-9); cuticle wax crystalloids 0; buds perulate; 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]
Evolution. Divergence & Distribution. Anderson et al. (2005) suggested an age of ca 120-111 m.y. for stem-group Eupteleaceae, and Wikström et al. (2001) an age of (141-)135, 122(-116) m.y., but note topologies. Euptelea represents a very old and species-poor clade.
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]]]]: 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?].
Age. Magallón et al. (2013) estimated an age of around (404-)394.3-389.9(-382) m.y. for this clade, but it is much younger in most other scenarios; N. Zhang et al. (2012) estimate an age of slightly under 100 m.y., while about 112.9 m.y. is the age in Magallón et al. (2015).
Evolution. Divergence & Distribution. 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). For features of wood anatomy common in this part of the clade, see Carlquist and Zona (1988); some may be higher-level apomorphies.
Chemistry, Morphology, etc. Wink (2008) noted that the berberine bridge enzyme (BBE), involved in the synthesis of berberine and other distinctive alkaloids from this clade (Kutchan 1998: berberine is also found in some Rutaceae, etc.) was quite widely distributed in flowering plants. Another gene in this pathway, FAD-dependent (S)-tetrahydroprotoberberine oxidase (STOX), is at least scattered in Ranunculales, and the different forms are quite similar in their activities if with different substrate specificities (Gesell et al 2011). STOX and BBE genes were members of different clades of FAD-dependent oxidases (Gesell et al. 2011).
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, , 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] - ?level), (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.
Age. Anderson et al. (2005) suggested an age of ca 119-106 m.y. for crown-group Papaveraceae.
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)], (gynophore + - Bocconia); ovules (as few as 1/carpel), (basal - Bocconia); 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).
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).
Age. Bell et al. (2010) offered an age for crown-group Fumarioideae of (106-)88, 82(-61) m.y.; (129-)123, 110(-104) m.y. is the age suggested by Wikström et al. (2001: note topology1).
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 [Pteridophyllum], two with two vascular strands [= 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, (palisade, crystaliferous), endotesta not 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.
Evolution. Divergence & Distribution. Kadereit et al. (2011) discuss evolution within Papavereae, offering some dates. Gleissberg and Kadereit (1999) discuss the complexities of leaf development and interpret them in a phylogenetic context.
Ecology & Physiology. Several species of Fumaria and its relatives are chasmophytes. They grow in the apparently most inhospitable habitats from North Africa and the Mediterranean region eastwards 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.
Economic Importance. For Papaver, see Bernáth (1998).
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). The single species in each subfamily examined had 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.; asymmetry of expression of the CYC gene is in the transverse plane here, and is rather late (Damerval et al. 2013; Hileman 2014). CYCLOIDEA genes have been duplicated in Papaveraceae s.l., and this may be connected with the development of monosymmetry (Kölsch & Gleissberg 2006; Damerval et al. 2007; see Jabbour et al. 2014 for analogous happenings in Ranunculaceae). 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.
Vascularization of the petals of Papaveroideae varies, but even if there is more than a single trace entering the base of the petals, 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.
Interestingly, nectary development is associated with the expression of CRABSCLAW genes, unlike the development of nectaries in monocots and Ranunculaceae, but like that in core eudicots (Damerval et al. 2013).
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. 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 gene 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),Mikhailova (2015: rootstock variation in Corydalis, 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 Ronse Decraene and Smets (1990) for floral morphology (comparison with Begoniaceae), and Becker et al. (2005: floral development of Eschscholzia).
For general information about Fumarioideae, see Lidén (1986: esp. Fumarieae), Hegnauer (1969, 1990) and Preininger (1986) for chemistry, Bersillon (1955) for nodal anatomy and floral vasculature, Murbeck (1912) for floral morphology, Guignard (1903) for the embryology of Hypecoum, G. Dahlgren (1981) for stigma secretions, Tarasevich (2014) for pollen, 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). Additional information on Pteridophyllum is taken from Brückner (1985: fruit and seed); the seeds have a cellulose network in the endotesta like that of some Papaveroideae.
Pteridophyllum is particularly poorly known.
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). 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. However, W. Wang et al. (2009) 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; A.P.G. III 2009).
Within Papaveroideae, generic limits need major adjustments (e.g. Kadereit & Baldwin 2011; Kadereit et al. 2011), as they do around Dicentra.
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/P ± petal-like, "C" +, nectariferous, development notably retarded; AP3 gene triplicated.
Age. Bell et al. (2010) suggested an age for this node of (106-)92, 85(-71) m.y.; ages of (126-)120, 111(-105) m.y. were suggested by Wikström et al. (2001) and of about 98.2 m.y. by Magallón et al. (2015).
Evolution. Ecology & Physiology. Lardizabalaceae and Menispermaceae are both lianes, sometimes vines, and they both have very large sieve tube plastids. Fossil woods of lianes that can be identified as belonging somewhere in this part of the tree are relatively common in woods Cretaceous-Palaeogene age; woods of Vitaceae-Vitoideae are first known from the Palaeogene (Smith et al. 2013a).
If the evolution of nectaries/nectariferous petals can be placed at this node, details of the pattern of expresssion of AP3-III petal identity genes become interesting (see also Sharma et al. 2011). Nectariferous petals seem not to be staminodial in origin (Sharma et al. 2014). The duplication of Cycloidea genes can be pegged to this node (Jabbour et al. 2014); they are involved in the development of monosymmetric flowers in Ranunculaceae (see below).
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). For chromosome size, see Langlet (1928, 1931) and Okada and Tamura (1979).
[Circaeasteraceae + Lardizabalaceae]: leaves palmately compound; K/P with a single trace; anthers extrorse; endosperm cellular.
Evolution. Divergence & Distribution. Anderson et al. (2005) suggested an age of ca 116-107 m.y. for this node, Bell et al. (2010) ages of (102-)87, 81(-66) m.y., Wikström et al. (2001) ages of (121-)115, 106(-100) m.y., and Magallón et al. (2015) an age of about 86.3 m.y. ago.
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; A (1-)2-6(-8), not obviously opposite P; pollen exine layered-striate; G 1-9, ascidiate, occlusion by ?secretion; 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).
Age. Anderson et al. (2005) suggested an age of ca 84-72 m.y. for the divergence of these genera, Bell et al. (2010) ages of (65-)48, 45(-30) m.y., and Wikström et al. (2001) ages of (72-)68, 54(-50) m.y..
1. Circaeaster Maximowicz
Leaves simple; bracteoles 0; P +, uniseriate, small, ± green and ± sepal-like, 2-3; A latrorse?, anthers bisporangiate, ?thecae, monothecal; ovule straight, integument ca 2 cells across; n = 15, chromosomes "Ranunculus type".
1/1: Circaeaster agrestis. India (Himalayas), W. China.[Photo - Circaeaster Habit.]
2. Kingdonia Balfour f. & W. W. Smith
Annual; leaves two-ranked; K 5(-7), "C" of 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
Chemistry, Morphology, etc. Kingdonia may have up to four bundles departing from the single foliar trace 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 same relationship between the stamens and perianth members of many other Ranunculales. The perianth members of Kingdonia have a single trifid vein, indeed, all floral organs are innervated by a single vein, apart from the first perianth member, 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 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, and the mature endosperm is differentiated into two zones; Circaeaster also has endosperm with a chalazal haustorium (see Junell 1931).
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 K. uniflora flowers 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; (plant Al-accumulators); petiole bundles arcuate; plant glabrous or hairs uniseriate; buds perulate; leaflet vernation conduplicate, margins entire; inflorescence axillary, racemose; flowers six-merous; "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, (supra-stylar extra-gynoecial compitum/pollen tube growth); micropyle endostomal; fruit a berrylet; germination phanerocotylar; chromosomes "small".
7[list]/40 - two groups below. South East Asia and Chile (map: see Taylor B. 1967; Ying et al. 1993).
Age. Anderson et al. (2005) suggested an age of 95-66 m.y. for crown-group Lardizabalaceae, Bell et al. (2010) ages of (51-)38, 35(-23) m.y., and Wikström et al. (2001) ages of (88-)81, 76(-67) m.y..
Kajanthus has receently been described from Portugese Cretaceous deposits around 113 m.y.a. and the charaters available for it are identical to those of Sinofranchetia, so it may even be assignable to crown-group Lardizabalaceae (Mendes et al. 2014).
1. Sargentodoxoideae Thorne & Reveal
Triterpenoid saponins 0; cork cambium deep-seated; tanniniferous cells +; leaves ternate; plant dioecious (some flowers perfect); carpellate flowers: K 4-9, C 5-7; staminodes +, like inner T; G 40<, ascidiate, stipitate; ovule 1/carpel, pendulous, outer integument ca 4 cells across; receptacle becoming fleshy; 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 - Decaisnea), petiolules long (terminal leaflet only), (leaflets with basal tooth or lobe), (secondary veins pinnate); plant monoecious (dioecious; flowers perfect): (outer T 3), ("C" 0); staminate flowers: (A 3, 8), filaments connate (not); (tapetal cells to 4 nucleate); (pollen grains colporoidate), (tricellular); carpellate flowers: staminodes +; G 3-12, (placentation laminar), (stigma peltate); ovules many/carpel (few), (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 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.]
Age. Wikström et al. (2001: Decaisnea sister to rest) suggested ages of (69-)61, 51(-42) m.y. for crown-group Lardizabaloideae.
Synonymy: Decaisneaceae Loconte, Sinofranchetiaceae Doweld
Evolution. Pollination Biology. In some taxa, at least, stigma exudate spreads and joins adjacent stigmas in a hyperstigma (Wu and Kubitzki 1993; X.-H. Zhang & Ren 2011).
Chemistry, Morphology, etc. Wood fluorescence? The leaves of Akebia pentaphylla, at least, are peltately palmate (Kim et al. 2003).
Smets (1986) suggested that the nectaries are staminal nectaries; stamen and petal develop primordia develop immediately adjacent to each other in Holboelllia (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 additional general information, see Wu and Kubitzki (1993), Qin (1997), Christenhuz (2012) and other 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.
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). However, based on the recent discovery of the fossil Kajanthus, very similar to Sinofranchetia, Mendes et al. (2014) suggest that the root may be misplaced, Sargentodoxa being nested within the crown group.
Classification. Although Sargentodoxa has a number of autapomorphies (see above, 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.
Age. The age of this node may be (119-)113, 103(-97) m.y. (Wikström et al. 2001); on the other hand, Magallón et al. (2013) estimate an age of around 65.9 m.y., Magallón et al. (2015) an age of ca 89.9 m.y., Anderson et al. (2005) an age of 116-105 m.y., Bell et al. (2010) an age of (99-)83, 77(-63) m.y., and Jacques et al. (2011) an age of 125-115.6 m.y..
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; leaves simple (compound - Burasia), lamina ± peltate [at least with the base joining the top of the petiole], margins entire (toothed; lobed), petiole 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, ± petal-like and nectariferous, (clasping A); staminate flowers: A 3, 6, 12 (1-40, if many, not all opposite petals), anthers with superposed thecae, (bisporangiate, monothecal); 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, (supra-stylar extra-gynoecial compitum/pollen tube growth); 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 [placental intrusion], curved, coat undistinguished, (exotesta tabular, lignified); endosperm + (0), variously ruminate (smooth), embryo long; n = (9-)11-13(+); chromosomes small.
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.]
Age. Anderson et al. (2005) thought that the crown-group was ca 80-70 m.y.o., Wikström et al. (2001) gave a rather younger age of (59-)53, 48(-42) m.y., while that Bell et al. (2010) at (52-)35, 33(-18) m.y. is even younger. However, Jacques et al. (2011) estimated an age of 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 menisperms are reported 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).
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 Arnott
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
Evolution. Divergence & Distribution. Major clades within the family diverged during the late Cretaceous (Jacques et al. 2011: Table 5 for dates, Menispermeae sister to rest). Indeed, extensive diversification and migration in the family, which is probably Laurasian in origin, may have occurred 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).
South American is proving to be quite diverse in fossils. 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. If the identification is correct, the younger ages for crown-group Menispermaceae above are incorrect.
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. Hoot et al. (2009) optimized characters on a tree with Menispermum and immediate relatives (Menispermeae) sister to the rest of the family.
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, the thicker part, both integuments fused. 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 analyses to understand variation in endocarp morphology; they placed this in the context of a molecular tree.
Additional general information is taken from Réaubourg (1906), Kessler (1993), and Jacques (2006); Hegnauer (1969, 1990) summarized information on chemistry, Wilkinson (1986) described leaf anatomy, and Jacques and de Franceschi (2007), wood anatomy, and Harley (1985 and references) surveyed pollen morphology. Much work has recently been carried out on the complex drupelets of the family; see also Jacques (2009b), Jacques and Zhou (2010), and Ortiz (2012: curved embryos develop in different ways).
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 W. Wang et al. 2009: three chloroplast and one nuclear genes, morphology, support weak, sampling poor; Ortiz 2012). The monophyly of Tinosporoideae 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). 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).
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, not in a single ring [scattered or in concentric rings]; leaf base broad, (paired petiolar stipules +); inflorescence terminal; K with three or more vascular traces; AP3-III gene expressed in P whorl alone; outer integument at least 4 cells thick; endosperm reserves other than oil or protein.
Age. Anderson et al. (2005) suggested an age of ca 104-90 m.y. for this node, Bell et al. (2010) an age of (87-)72, 67(-54) m.y., Xue et al. (2012) an age of ca 77.8 or 89.1 m.y., Magallón et al. (2015) an age of about 80.3 m.y., and Wikström et al. (2001) an age of (106-)100, 84(-78) m.y.; the ca 128 m.y. in Z. Wu et al. (2014) is dramatically older (but see fossils attributed to Ranunculaceae).
Chemistry, Morphology, etc. Nowicke and Skvarla (1981) thought that aperture columellae might be a synapomorphy for the two families. For the expression of the AP3-III gene, see Sharma et al. (2011).
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 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; ovules (with zig-zag micropyle), outer integument 4-12 cells across, inner integument 2-5 cells across; antipodal cells endopolyploid, persistent or not; fruit a berrylet; exotestal cells lignified, oblong-fibrous to cuboid; endosperm with hemicellulose; embryo minute; chromosomes large.
14/701 [list] - three clades below. Mostly East Asia and E. North America, also South America, a few species general N. temperate, scattered in Africa (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 palmately compound, 2-foliolate, or simple and ± deeply lobed; lowermost branch of inflorescence subtended by reduced leaf; K (0 - Achlys), 4-18, "C" (0, 7-9), (4, with nectar spurs), (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 also an achene, or 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, green, C 0 - Nandina); (A dehiscence by slits); ovules 1-2 (4) carpel; (fruit with 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 (herbaceous); (vessel elements with scalariform perforations, petiole bundles arcuate - Berberis); leaves palmate, odd-pinnate, (unifoliolate), (reduced to spines), margins often spiny-toothed; (inflorescence axillary), lowermost branch subtended by reduced inflorescence bract; K 3-12, "C" nectaries basal; stamens sensitive; tapetum amoeboid, 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); endosperm cellular [Mahonia], embryo long; n = 7.
2/601: Berberis (600). General N. temperate, also South America, N. and E. Africa.
Age. Anderson et al. (2005) suggested a crown-group age of ca 88-72 m.y. for Berberidaceae.
Evolution. Divergence & Distribution. 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). The genus may have originated in North America, with one move to South America and two to Eurasia (Adhikari et al. 2015). 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 probably late Cretaceous age of the family, 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 in particular 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 unifoliolate) 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 the nectaries are inside spurs coming from the four inner tepals. Although Podophyllum has many stamens, single stamens or groups of stamens are opposite the innermost perianth members (Schmidt 1928); Zhao et al. (2014) described all floral organs (except the carpel) as originating in whorls of three in the related Dysosma, and, unlike elsewhere in the family, there were no C-A primordia. 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 Gymnospermium (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), even 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 three main clades, and although molecular support for a [Nandinoideae + Berberidoideae] clade was weak, it was much strengthened in analyses that included morphological data.
For relationships within Berberis, see Adhikari et al. (2015); relationships are [B. higginsae [B. nivenii + The Rest]].
Classification. For an infra-familial classification, see W. Wang et al. (2009); Berberis is to include Mahonia.
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), little else indicates 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; flowers medium to large, parts spiral or whorled, K, C, and A not opposite each other, K petal like; 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 short [0.5-2.5 µm long], ± rod-like [T(Thalictrum)-type; germination epigeal.
62[list]/2525 - five subfamilies below. ± World-wide, but mainly temperate.
Age. Anderson et al. (2005) estimated a crown-group age of ca 87-73 m.y. for Ranunculaceae, Bell et al. (2010) ages of (73-)59, 55(-41) m.y., and Wikström et al. (2001) ages of (91-)85, 65(-59) m.y..
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, but there may be some question about "the authenticity of the specimen" (Z. Zhou 2014: p. 553).
[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; C 0, nectaries 0; stigma bilobed; outer integument 4-13 cells across, inner integument 2-5 cells across.
Age. Bell et al. (2010) estimated crown-group ages for this clade of (66-)51, 48(-34) m.y. and Wikström et al. (2001) ages of (80-)74, 47(-41) m.y. ago.
1. Glaucidioideae Loconte
Coumarin +, alkaloids, berberin 0; lamina vernation also supervolute-curved; flowers with cortical vascular system; K 4; 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.
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; K 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 berrylet; 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 [= amphivasal], 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; K 5-merous, "C" 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).
Age. Bell et al. (2010) estimated crown-group ages for this clade of (59-)45, 42(-30) m.y. and Wikström et al. (2001) ages of (71-)66, 51(-46) m.y..
3. Coptoideae Tamura
Small shrub or perennial herbs; "C" nectaries 5-10, petal-like, thick, stalked; carpels stipitate; n = (8) 9.
3/17. East Asia, E. and W. North America.
Age. Crown-group ages for this clade of (20-)17, 12(-9) m.y. and Wikström et al. (2001: Cop. Xan.).
[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).
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, leaflet vernation ± curved-involute, ([adaxial] stipules + - Thalictrum); (plant dioecious); flower parts ± whorled; nectaries ± petal-like and stalked, (internal staminodes +); integument single, 7-8 cells across; n = (6) 7.
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; (palisade mesophyll with arm cells); 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), (parts ± whorled); (K sepal-like), "C" various, (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, (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 long [(3-)4.1-10.5(-12) µm 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.]
Age. 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, e.g. both have a flotation chamber. This fossil is from the Mexican Campanian (Cretaceous) some ca 77 m.y. old (Rodríguez de la Rosa et al. 1998; see also Pigg & deVore 2005 for early records), but its identity needs confirmation (Friis et al. 2011).
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
Evolution. Divergence & Distribution. 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, e.g. both have a flotation chamber; this fossil is from the Mexican Campanian (Cretaceous) some ca 77 m.y. old (Rodríguez de la Rosa et al. 1998; see also Pigg & deVore 2005 for early records). If crown-group ages of these fossils is confirmed, they will i.a. constrain the age of the family as a whole.
The beginning of diversification within the speciose Clematis clade 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. (Mikeda et al. 2006; Xie et al. 2011: HPD).
For the evolution of Arctic Ranunculaceae, see Hoffmann et al. (2010). In the widely-distributed Ranunculus there 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 (Thalictroideae) 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 (Ranunculoideae-Delphinieae) have monosymmetric flowers and 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 early in the Oligocene (41.8-)32.3(-23.0) 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). There has been duplication of Cycloidea genes involved in this monosymmetry, and they are variously expressed, ad- or abaxially, in the flower, and also in the outer whorl of petaloid sepals (Jabbour et al. 2014; c.f. Hileman 2014).
Expression of a duplicated A-class gene, APETALA 3, is intimately involved in the development of the nectariferous petals found in Delphinieae and many other Ranunculaceae. Absence of the gene has been linked to the loss of the nectarial function, and these nectary-type structures then look much more like the petaloid sepals (R. Zhang et al. 2013; Gonçalves et al. 2013; Sharma et al. 2014).
Pollination Biology & Seed Dispersal. One commonly thinks of Ranunculaceae as having rather unspecialized flowers, and in an analysis of European members of the family Waser et al. (1996) found as many as 53 species of pollinator from 29 genera visiting a single species - and as few as one. Many Ranunculaceae have distinctive nectaries which can be more or less like petals, and some species have complex flowers in which these nectaries take very different forms. Thus Delphinieae have monosymmetric flowers with paired nectary spurs that are borne inside a spurred petaloid member of the outer floral whorl; Renner and Jabbour (2012b) discuss the evolution of this unusual pollination morphology. Bumble bees are the predominant pollinators of the 600-700 species of this tribe, which is very speciose in the Himalayas (Renner & Jabbour 2012b). Diversification of bumble bees, generalist bees that handle specialized flowers quite easily (see below, probably occurred 40-25 m.y.a. (Hines 2008 and references), i.e., about the same time as that of Delphinieae. Rather unusually for a bumble bee, Bombus consobrinus has specialized on Aconitum, especially on A. septentrionale, although several other bumble bees also pollinate members of that genus (Laverty & Plowright 1988; Thostesen & Olesen 1996); Kronfeld (1890: p. 19) early declared Aconitum to be an excellent example of an insect-adapted flower.
The five, coloured nectar spurs of the polysymmetric flowers of Aquilegia are very unusual in flowering plants; nectar spurs are usually associated with monosymmetry. Pollen deposition on the pollinator may be quite precise here (Kay et al. 2006b); Kramer and Hodges (2010) review the evolution of these "petals".
For the intimate association between Old World Trollius and its pollinators/seed parasites, the fly Chiastocheta (close to Botanophila), see Pellmyr (1992) and Ibanez et al. (2013: plant volatiles). Caltha has nectariferous hairs on the carpels, while taxa like Clematis and Ranunculus have apparently unspecialized flowers and may be visited by many species of pollinators (Waser et al. 1996).
Many species of Thalictrum are wind-pollinated, and some of these species are monoecious or dioecious. Monoecy and dioecy are restricted to and predominate in New World species; wind pollination may reverse to animal pollination (Soza et al. 2012).
A number of forest herbs in Ranunculoideae in particular are myrmecochorous, the outgrowths that attract ants developing either from the seed or the 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 number of species of Ranunculaceae involved may be the most diverse assemblage in flowering plants. Phytomyza (well over 700 species) may have moved on to Ranunculaceae from asterids, perhaps in the late Oligocene ca 24.5 m.y.a., and diversified there as the climate cooled; they have since moved back to asterids, especially to campanulid groups (Winkler et al. 2009).
Genes & Genomes. It is over 80 years since Langlet (1932) realized that the cytological variation in the family has a stong systematic signal, with genera having large R(anunculus)- or small T(halictrum)-type chromosomes, a finding that was at odds with the then-accepted classification. Okada and Tamura (1979) note characters other than gross size and shape that also separate the two chromosome types (see also Tamura 1993). However, the correlation between chromosome morphology and taxonomy does break down; Chung et al. (2013: note lengths given for the two types) found that the chromosomes of some species of Ranunculus like the annual R. sceleratus were quite small, rather like those of the Thalictrum type.
Chemistry, Morphology, etc. Benzylisoquinoline alkaloids are largely absent from Ranunculaceae, although present in Coptis and Isopyyrum (Coptoideae: 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. The vascular bundles often have xylem surrounding the phloem, but c.f. Takhtajan (1997). 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 of Glaucidium is an irregular sympodium. Variation in petiole anatomy is extensive (Tamura 1962, 1995) and adaxial/intrapetiolar stipules occur sporadically in the family (Hagemann 1970).
Monosymmetry in flowers of Delphinieae becomes apparent only rather late in development after organ initiation (Jabbour et al. 2009a). Soltis et al. (2003a) suggest that both Glaucidium and Hydrastis have a bimerous perianth. Floral phyllotaxy in Anemoneae is particularly variable (Ren et al. 2010).
For an early discussion on stamens and nectaries in Ranunculaceae, and a suggestion that the flower here might be fundamentally 3-merous, see Salisbury (1919). Nectaries in the family vary greatly in morphology, and they were generally thought to be modified stamens. The two have a number of points of similarity, e.g. the "petals" have a single trace, although in some Delphinieae they have two traces (Novikoff & Jabbour 2014). They 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). Normally the nectaries are rather different morphologically from the sepals and are sometimes quite elaborate beaker- or hood-shaped structures; the sepals are more consistently petal-like and visually attractive. However, in Ranunculus and Ficaria sepals are green and protective, while the nectaries are very petal-like, the nectary proper being a small scale at the base of what otherwise appears to be an ordinary petal, while in Laccopetalum and relatives there are a number of nectary ridges on the petals; in the latter both petals and stamens may have three traces (Hiepko 1964a). Pabón-Mora et al. (2013) suggested that aspects of floral development in Aquilegia differed from those in other members of the family. There the basal/abaxial member of alternating staminal rows is a spurred petal/nectary which has three vascular traces running into it. Recent work does not confirm a stamen identity for the nectaries (see above). Genera like Clematis, Thalictrum and Anemone s.l. lack nectaries/petal-like structures inside the petal-like sepals.
In Anemone s.l. the floral bracts/bracteoles tend to be calycine, and this is especially evident in the Hepatica group where the bracts are borne immediately underneath the flower with its petal-like sepals, although they do not particularly closely envelop the rest of the flower. There the sepals have only a single trace and there are no nectaries. Wang and Chen (2007) discuss "petal" evolution in Thalictroideae; see also above, again, petals/nectaries have been lost. In Aquilegia the stamens are in ten vertically-arranged two-ranked series, each opposite an internal staminode, unique to Ranunculales (see Sharma & Kramer 2012 for their development). Insertion of the stamens, etc., can be spiral or whorled (Gonçalves et al. 2013).
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. 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 the family, while Ranunculus ficaria, for example, has only a single cotyledon (Förster 1997).
For general information, see Johri et al. (1992) and Tamura (1993, 1995: including infrageneric groupings), Hegnauer (1969, 1986, 1990) and Jensen (1995), all chemistry, Aizetmüller (1995, 1996, 1999 (fatty acids), Kumazawa (1937: leaf vernation), Schöfel (1932: esp. floral diagrams), Brouland (1935: floral vasculature), Rohweder (1967a: carpels), Huss (1906), Bhandari (1967 and references), and Engell (1995), all embryology, van Heel (1981, 1983: carpel development), Trifonova (1990 and references: petiole and seed anatomy), Weberling (1989: nectaries), Endress (1995a), Tucker and Hodges (2005: Aquilegia and immediate relatives), 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, Ren et al. (2009: floral development of Adonidae, 2011: floral development of Thalictroideae), and Heiss et al. (2011: seed anatomy of Nigella). See Tobe and Keating (1985) and Tobe (2002) for Hydrastis and Tamura (1972) for much information on Glaucidium, embryology mostly from Tobe (1981).
Phylogeny. The clade [Hydrastis + Glaucidium] has been found to be sister to the rest of the family by Hoot et al. (1998) and others since. 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; W. Wang et al. 2005). 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, while Soltis et al. (2011) found weak support for a topology [Hydrastis [Glaucidium + Ranunculus]] (only three taxa of Ranunculaceae in the analysis). Indeed, the vegetative and anatomical 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 these would be apomorphies for the whole family... For other early work on the family, see Hoot (1991, 1995) and Jensen et al. (1995), and more recently, Cai et al. (2009, 2010).
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, Myosurus, with its very elongated receptacle and as a result a flower that 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 two, a clade having x = 7 (inc. Hepatica) and another with x = 8 (see also Zhang et al. 2015); there is certainly a lot of variation around here in bracteole morphology, staminode presence/absence, pollen morphology, etc. (see also Ziman et al. 2008 and references). 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, 2012a) focused on the speciose Delphinieae, and the clades they found only partly mappped on to previously-recognized genera, while Aconitum gymnandrum, although belonging there, did not link with any major clade. There was little resolution of relationships within the speciose Delphinium section Diedropetala (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, and the main clades that are evident neither correlate very well with previous infrageneric taxa nor have much morphological support.
Classification. The classification above is largely based on that in Tamura (1993). Glaucidium has quite often been placed in its own family (indeed, it was excluded from Ranunculaceae by Tamura), but it would be monotypic; although a distinctive plant, it has quite a lot in common with Hydrastis (see also Cai et al. 2010, c.f. in part Cai et al. 2009).
For generic limits around Ranunculus, see Emadzade et al. (2010), in Adonidae, see W. Wang et al. (2010), and around 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, quite often associated with Ranunculaceae in the past, is now included in Saxifragales as Paeoniaceae, while Tamura (1972) thought that Glaucidium was close to Hypericales.
Botanical Trivia. The zygote of Anemone flaccida is undivided at the time of seed dispersal (Tamura & Mizumoto 1972).