EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, not motile, initially ±globular; showing gravitropism; acquisition of phenylalanine lysase [PAL], phenylpropanoid metabolism [lignans +, flavonoids + (absorbtion of UV radiation)], xyloglucans in primary cell wall, side chains charged; plant poikilohydrous [protoplasm dessication tolerant], ectohydrous [free water outside plant physiologically important]; thalloid, leafy, with single-celled apical meristem, tissues little differentiated, rhizoids +, unicellular; chloroplasts several per cell, pyrenoids 0; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles/centrosomes in vegetative cells 0, microtubules with γ-tubulin along its length [?here], interphase microtubules form hoop-like system; metaphase spindle anastral, predictive preprophase band of microtubules [where cell plate will join parental cell wall], phragmoplast + [cell wall deposition spreading from around the spindle fibres], plasmodesmata +; antheridia and archegonia jacketed, surficial; blepharoplast +, centrioles develop de novo, bicentriole pair coaxial, separate at midpoint, centrioles rotate, associated with basal bodies of cilia, multilayered structure + [4 layers: L1, L4, tubules; L2, L3, short vertical lamellae] (0), 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 multicellular, cuticle +, plane of first cell division transverse [with respect to long axis of archegonium/embryo sac], sporangium and upper part of seta developing from epibasal cell [towards the archegonial neck, exoscopic], with at least transient apical cell [?level], initially surrounded by and dependent on gametophyte, placental transfer cells +, in both sporophyte and gametophyte, wall ingrowths develop early; suspensor/foot +, cells at foot tip somewhat haustorial; sporangium +, single, terminal, dehiscence longitudinal; meiosis sporic, monoplastidic, MTOC [MTOC = microtubule organizing centre] associated with plastid, sporocytes 4-lobed, cytokinesis simultaneous, preceding nuclear division, quadripolar microtubule system +; wall development both centripetal and centrifugal, sporopollenin + laid down in association with trilamellar layers [white-line centred lamellae; tripartite lamellae], >1000 spores/sporangium; nuclear genome size <1.4 pg, main telomere sequence motif TTTAGGG, LEAFY and KNOX1 and KNOX2 genes present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes [precursors for starch synthesis], tufA gene moved to nucleus.
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, L- and D-methionine distinguished metabolically; sporophyte with polar transport of auxins, class 1 KNOX genes expressed in sporangium alone; sporangium wall 4≤ cells across [≡ eusporangium], tapetum +, secreting sporopollenin, which obscures outer white-line centred lamellae, columella +, developing from endothecial cells; stomata +, on sporangium, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and of rhizoids/root hairs; spores trilete; shoot meristem patterning gene families expressed; MIKC, MI*K*C* genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns, mitochondrial trnS(gcu) and trnN(guu) genes 0.
[Anthocerophyta + Polysporangiophyta]: gametophyte leafless; archegonia embedded/sunken [on;y neck protruding]; sporophyte long-lived, chlorophyllous; cell walls with xylans.
Sporophyte well developed, branched, branching apical, dichotomous, potentially indeterminate; hydroids +; stomata on stem; sporangia several, terminal; spore walls not multilamellate [?here].
Vascular tissue + [tracheids, walls with bars of secondary thickening].
EXTANT TRACHEOPHYTA / VASCULAR PLANTS
Sporophyte with photosynthetic red light response, stomata open in response to blue light; plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; plant endohydrous [physiologically important free water inside plant]; (condensed or nonhydrolyzable tannins/proanthocyanidins +); xyloglucans with side chains uncharged [?level], in secondary walls of vascular and mechanical tissue; lignins +; stem apex multicellular, with cytohistochemical zonation, plasmodesmata formation based on cell lineage; tracheids +, in both protoxylem and metaxylem, G- and S-types; sieve cells + [nucleus degenerating]; endodermis +; leaves/sporophylls spirally arranged, blades with mean venation density ca 1.8 mm/mm2 [to 5 mm/mm2], all epidermal cells with chloroplasts; sporangia adaxial, columella 0; tapetum glandular; ?position of transfer cells; MTOCs not associated with plastids, basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; suspensor +, shoot apex developing away from micropyle/archegonial neck [from hypobasal cell, endoscopic], root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Sporophyte endomycorrhizal [with Glomeromycota]; growth ± monopodial, branching spiral; roots +, endogenous, positively geotropic, root hairs and root cap +, protoxylem exarch, lateral roots +, endogenous; G-type tracheids +, with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangium dehiscence by a single longitudinal slit; cells polyplastidic, MTOCs diffuse, perinuclear, migratory; 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; stem branching lateral, meristems axillary; lateral root origin from the pericycle; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].
Plants heterosporous; megasporangium surrounded by cupule [i.e. = unitegmic ovule, cupule = integument]; pollen lands on ovule; megaspore germination endosporic [female gametophyte initially retained on the plant].
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]; lignin chains started by monolignol dimerization [resinols common], particularly with guaiacyl and p-hydroxyphenyl [G + H] units [sinapyl units uncommon, no Maüle reaction]; root stele diarch to pentarch, xylem and phloem originating on alternating radii, cork cambium deep seated; stem apical meristem complex [with quiescent centre, etc.], plasmodesma density in SAM 1.6-6.2[mean]/μm2 [interface-specific plasmodesmatal network]; eustele +, protoxylem endarch, endodermis 0; 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; leaf nodes 1:1, a single trace leaving the vascular sympodium; leaf vascular bundles amphicribral; guard cells the only epidermal cells with chloroplasts, stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; axillary buds +, exogenous; prophylls two, lateral; leaves with petiole and lamina, development basipetal, lamina simple; sporangia borne on sporophylls; spores not dormant; microsporophylls aggregated in indeterminate cones/strobili; grains monosulcate, aperture in ana- position [distal], primexine + [involved in exine pattern formation with deposition of sporopollenin from tapetum there], exine and intine homogeneous, exine alveolar/honeycomb; ovules with parietal tissue [= crassinucellate], megaspore tetrad linear, functional megaspore single, chalazal, sporopollenin 0; gametophyte ± wholly dependent on sporophyte, development initially endosporic [apical cell 0, rhizoids 0, etc.]; male gametophyte with tube developing from distal end of grain, male gametes two, developing after pollination, with cell walls; female gametophyte initially syncytial, walls then surrounding individual nuclei; embryo cellular ab initio, suspensor short-minute, embryonic axis straight [shoot and root at opposite ends; plant allorhizic], cotyledons 2; embryo ± dormant; ycf2 gene in inverted repeat, mitochondrial trans- nad2i542g2 and coxIIi3 introns present; whole nuclear genome duplication [ζ - zeta - duplication], two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], 5.8S and 5S rDNA in separate clusters.
ANGIOSPERMAE / MAGNOLIOPHYTA
Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANA grade?], lignin also with syringyl units common [G + S lignin, positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], hemicelluloses as xyloglucans; root apical meristem intermediate-open, pith relatively inconspicuous, lateral roots initiated immediately to the side of [when diarch] or opposite 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; 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, not occluding pores of plate, companion cell and sieve tube from same mother cell; ?phloem loading/sugar transport; nodes 1:?; dark reversal Pfr → Pr; protoplasm dessication tolerant [plant poikilohydric]; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance with increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, secondary veins pinnate, fine venation hierarchical-reticulate, (1.7-)4.1(-5.7) mm/mm2, vein endings free; flowers perfect, pedicellate, ± haplomorphic, protogynous; parts free, numbers variable, development centripetal; P +, ?insertion, 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], each theca dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, endothecium +, cells elongated at right angles to long axis of anther; tapetal 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, intine in apertural areas thick, pollenkitt +; nectary 0; carpels present, superior, free, several, ascidiate [postgenital occlusion by secretion], stylulus at most short [shorter than ovary], hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry; suprastylar extragynoecial compitum +; 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, nucellar cap?; megasporocyte single, hypodermal, functional megaspore lacking cuticle; female gametophyte lacking chlorophyll, not photosynthesising, four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; ovule not increasing in size between pollination and fertilization; pollen 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, ciliae 0, siphonogamy; double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; mature seed much larger than fertilized ovule, small , dry [no sarcotesta], exotestal; endosperm +, cellular, development heteropolar [first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous, embryo short [<¼ length of seed]; plastid and mitochondrial transmission maternal; Arabidopsis-type telomeres [(TTTAGGG)n]; nuclear genome very small [1C = <1.4 pg, mean 1C = 18.1 pg, 1 pg = 109 base pairs], whole nuclear genome duplication [ε/epsilon event]; 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, palaeo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]]; chloroplast chlB, -L, -N, trnP-GGG genes 0.
[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]]]]: phloem loading passive, via symplast, plasmodesmata numerous; vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood + [reaction wood: with gelatinous fibres, G-fibres, on adaxial side of branch/stem junction]; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; 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 [?here]; pollen tube growth intra-gynoecial; extragynoecial compitum 0; carpels plicate [?here]; 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).
[CERATOPHYLLALES + EUDICOTS]: ethereal oils 0.
EUDICOTS: (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 ?, filaments fairly slender, anthers basifixed; microsporogenesis simultaneous, pollen tricolpate, apertures in pairs at six points of the young tetrad [Fischer's rule], cleavage centripetal, wall with endexine; G with complete postgenital fusion, stylulus/style solid [?here]; seed coat?
[PROTEALES [TROCHODENDRALES [BUXALES + CORE EUDICOTS]]]: (axial/receptacular nectary +).
[TROCHODENDRALES [BUXALES + CORE EUDICOTS]]: benzylisoquinoline alkaloids 0; euAP3 + TM6 genes [duplication of paleoAP3 gene: B class], mitochondrial rps2 gene lost.
[BUXALES + CORE EUDICOTS]: ?
CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one position]; micropyle?; γ whole nuclear genome duplication [palaeohexaploidy, gamma triplication], PI-dB motif +, small deletion in the 18S ribosomal DNA common.
[ROSIDS ET AL. + ASTERIDS ET AL.] / PENTAPETALAE: root apical meristem closed; (cyanogenesis also via [iso]leucine, valine and phenylalanine pathways); flowers rather stereotyped: 5-merous, parts whorled; P = calyx + corolla, calyx enclosing the flower in bud, sepals with three or more traces, petals with a single trace; stamens = 2x K/C, in two whorls, internal/adaxial to the corolla whorl, alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G , G  also common, when [G 2], carpels superposed, placentation axile, style +, stigma not decurrent; compitum +; endosperm nuclear; fruit dry, dehiscent, loculicidal [when a capsule]; RNase-based gametophytic incompatibility system present; floral nectaries with CRABSCLAW expression; (monosymmetric flowers with adaxial/dorsal CYC expression).
Age. Soltis et al. (2008: a variety of estimates) suggested that these two large clades diverged 128-114(-84) m.y.a., and similar ages of (131-)120, 117(-112) and (132-)125, 101(-97) m.y. are proposed by Bell et al. (2010). Wikström et al. (2001) suggested ages of (130-)125, 114(-109) m.y., while (128-)127(-124) m.y. is the estimate in Wikström et al. (2015: no Dillenia).
Evolution. Divergence & Distribution. Doyle (2013) suggested that the distinctive pentapetalous flower descibed above evolved from a wind-pollinated, probably dimerous morphology.
Harmomegathic movements of triaperturate pollen grains are discussed by Halbritter and Hesse (2004).
Pollination Biology. For the evolution of the gametophytic incompatibility system, perhaps a precursor to the sporophytic system (although the two may in fact merely be qualitatively different), see Igic and Kohn (2001: phylogeny of RNases), Steinbachs and Holsinger (2002), Igic et al. (2006), Franklin-Tong and Franklin (2003), Charlesworth et al. (2005) and Hiscock and Tabah (2003).
Genes & Genomes. There has been duplication of all four MADS-box gene classes (A, B, C, E) somewhere around here, and also the floral symmetry genes CYCLOIDEA and DIVARICATA (e.g. Boyden et al. 2010).
Chemistry, Morphology, etc. Both sepals and petals of core eudicots may be derived from bracts, bracts and sepals often having three or more traces, petals a single trace (Ronse de Craene (2007); only cases where the vasculature is other than this are mentioned below.
[DILLENIALES [SAXIFRAGALES [VITALES + ROSIDS s. str.]]]: stipules + [usually apparently inserted on the stem].
Age. Moore et al. (2010) suggest an age of (112-)108(103) m.y. for this node (if it exists).
[SAXIFRAGALES [VITALES + ROSIDS]] / ROSANAE Takhtajan / SUPERROSIDAE: ? Back to Main Tree
Age. The age of this node has been estimated at (125-)121, 111(-107) m.y. (Wikstr&m et al. 2004); the age in Anderson et al. (2005: see positions of Crossosomatales included) is ca 108 m.y. and it is ca 160 m.y. in Z. Wu et al. (2014: [Vitales + Saxifragales] sister to rest, ca 151 m.y.a. divergence between the two). Magallón and Castillo (2009) provide estimates of around 114.5 m.y., Moore et al. (2010: 95% highest posterior density) an age of (111-)108(-103) m.y.; ages of (135-)128, 117(-111) m.y. are suggested by Bell et al. (2010), (112-)107(-101) m.y. by N. Zhang et al. (2012), 110.5 m.y. by Magallón et al. (2013), 114-111 m.y. by M. Sun et al. (2014) and ca 117.7 m.y. by Tank et al. (2015: Table S1) - or ca 58 m.y. (Palazzesi et al. 2012, but c.f. Sytsma et al. 2014 - ca 104 m.y.).
Fossils are somewhat younger, and those assignable to rosids as a whole are ca 94 m.y.o., and those to Saxifragales ca 90 m.y. old (Crepet et al. 2004).
Evolution. Divergence & Distribution. Much crown group diversification within this clade probably occurred within a narrow time interval of 5-15 m.y. around 117-93 m.y.a. in the late Aptian early Turonian (Wang et al. 2009).
Ecology & Physiology. Increase in seed size is especially distinctive at this node, and this is associated with large leaf size; plants commonly grow in equatorial areas that are both warm and well-watered (Cornwell et al. 2014: c.f. Saxifragales).
Smets et al. (2003) characterise the rosids as having receptacular nectaries; but Vitales have gynoecial nectaries and Proteaceae, and perhaps Sabiaceae, have receptacular nectaries (Smets 1988). For CRABSCLAW expression in the floral nectaries, see Damerval et al. (2013). A relatively large embryo over half the length of the seed may be a feature of this clade (Forbis et al. 2002), although there is considerable variation in Saxifragales and Vitales have small embryos. Here this character has been pegged at a lower level in the phylogeny (see core rosids).
Plant-Animal Interactions. Butterfly caterpillars are common on members of the group, occurring about twice as frequently as might be expected going by species number alone, but the tree habit is also common here, and trees perhaps can support a correspondingly disproportionately large number of larvae (Janz & Nylin 1998). However, Menken et al. (2009; see also Ward et al. 2003) reported on an extensive survey of larval host plants of British lepidoptera which they thought could be extended - with care - more globally, noting that caterpillars of basal Lepidoptera-Glossata (butterflies and moths with a coilable proboscis) tended to be found on woody rosid I (Fabidae) plants, normally as leaf miners or other non-exposed life styles (see also Ward et al. 2003). Since mines attributed to basal glossatan Neptulicidae have been reported from fossil magnoliid and protealean leaves, among others (see Menken et al. 2009), and these plants have a rather different chemistry from that of the rosids, the deep history of such lepidoptera-plant associations is unclear.
Genes & Genomes. For a possible genome duplication, see Tuskan et al. (2006) and Jaillon, Eury et al. (2007); it is probably to be placed immediately basal to the core eudicot node. Where the loss of the chloroplast infA gene is to be placed is unclear (see Millen et al. 2001).
Chemistry, Morphology, etc. Taxa that have cuticle wax platelets as rosettes are scattered through this group, but they are especially common in Fabaceae and there are also several Malpighiales (see Ditsch & Barthlott 1997 for details). Distinctive mucilage cells with a much thickened mucilaginous inner periclinal wall and distinct cytoplasm are found in flowers especially in this broader group, but they are not yet reported from Geraniales (Matthews & Endress 2006b). The sepals characteristically have three traces from three gaps; in several more basal eudicot clades the outer perianth/sepals have only a single gap (von Balthazar and Endress 2002 - see also Ranunculales). Petal development is often retarded relative to that of other parts of the flower (also in Cabomba and Saruma).
Phylogeny. Basal relationships within rosids remain somewhat unclear, particularly the positions of Vitales and Saxifragales (N. Zhang et al. 2016: Fig. 1 for four common hypotheses, fabids include the COM clade). Hilu et al. (2003: matK analysis, Schumacheria [the one Dilleniaceae included] was firmly associated with Ericales...) found a possible set of relationships [Rosids [[Dilleniacaeae + Vitaceae] [Saxifragales [Santalales [Berberidopsidales [Caryophyllales + Asterids]]]]]]. Nickrent et al. (2005) found the position of Saxifragales to be particularly uncertain, although Vitales again tended to go with rosids. Soltis et al. (2007a) found a grouping [Saxifragales [Vitales + rosids]], both groupings with 1.0 p.p. (see also Zhu et al 2007, but little support). Earlier work had suggested similar relationships, thus Saxifragales were sister to the rest of the group (e.g. P. Soltis et al. 1999: Vitales not included), albeit with little support.
Moore et al. (2010, 2011) found that although [Saxifragales, Vitales, rosids] formed a strongly-supported clade, it was unclear whether Vitales were sister to Saxifragales, to rosids, or to [Saxifragales + rosids]; support for the latter position increased with reduced taxon sampling. Moore et al. (2010) also recovered a [Saxifragales + Vitales] clade sister to rosids in maximum likelihood but not in maximum parsimony analyses, and this also appeared in most analyses in Ruhfel et al. (2014), in both nuclear and chloroplast, but not in mitochondrial, analyses in M. Sun et al. (2014: divergence 114-110 m.y.a., 2015), and in the chloroplast genome analyses of Z. Wu et al. (2014) and N. Zhang et al. (2016: good support). Zhang et al. (2016; see also Soltis et al. 2013) suggested that a bicarpellate gynpoecium might be a synapomorphy for the clade, but support for this must at best be weak.
Hengcheng Wang et al. (2009: Dilleniales not included) in a 43,000 bp analysis, largely of chloroplast sequences, found substantial resolution within rosids s.l., and the relationships that they suggest, [Saxifragales [Vitales [rosid I/fabids + rosid II/malvids]]], are followed here (but maybe not for much longer), although the position of Vitales is only moderately supported (72% bootstrap in a ML analysis); they analysed a twelve-gene and inverted repeat data sets separately and in combination, preferring ML over MP analyses. The topology in Davies et al. (2004), Bell et al. (2010) and Soltis et al. (2011) is similar. Saxifragales are also well supported as sister to [Vitales + rosids] in the 12-gene plus plastid inverted repeat analyses of Wang et al. (2009). Vitales may well be sister to the other rosids s. str. (e.g. Jansen et al. 2007), although support was only weak in Wang et al. (2009). A palaeohexaploidy event seemed to link Vitales with rosids, but the sampling in major core eudicot clades was very poor (Jaillon, Eury et al. 2007), and that event may be a synapomorphy for core eudicots (see above).
Studies on the duplication of the RPB2 gene and subsequent loss of one of the copies (Oxelman et al. 2004; Luo et al. 2007) suggest that Saxifragales and Rosids are linked by loss of the -I copy, which also has occurred in Santalales and Caryophyllales, but not Vitales, Berberidopsidales, Gunnerales or Dilleniales, which have all lost the RPB2-D copy. Saxifragales and Vitales were found to be successively sister to all eudicots minus Gunnerales (mitochondrial gene only), or to all rosids, but with little support (Zhu et al. 2007).
Finally, Saxifragales have sometimes been found to be sister to a [Berberidopsidales ... asterid] clade, although with vanishingly low support, and Vitales sister to a rosid clade, but with scarcely any stronger support (Qiu et al. 2010). What are essentially the reverse positions of these two problematic orders were recovered by Soltis et al. (2015, in N. Zhang et al. 2016). Crossosomatales were in a clade basal to Caryophyllales, while other relationships in the rosid II clade were somewhat scrambled, although again with little support (Qiu et al. 2010). The relationships [[Vitaceae + Saxifragales] [Caryophyllales + rosids]] have also popped up (N. Zhang et al. 2012; M. Sun et al. 2104: mitochondrial and nuclear data) as have the relationships [Vitales [rosids + asterids]] (Wickett et al. 2014: transcriptome analyses), but this latter may be a sampling problem, since no Saxifragales, Dilleniales, etc., were included.
Geranium, the only representative of Geraniales included, was sister to all other rosids except Vitaceae in a study by Zhu et al. (2007, support weak); their position is also unstable in a rbcL analysis of all angiosperms (Hilu et al. 2003). In some earlier trees, Crossosoma (Crossosomatales) was also included or was nearby, see e.g. Morgan and Soltis (1993), Chase et al. (1993), while in Price and Palmer (1993: rbcL analysis) Biebersteinia (see Sapindales here) was still tentatively included in Geraniales. Savolainen et al. (2000a) found Geraniales to be monophyletic, but with only 52% support (see also Savolainen et al. 2000b); Crossosomatales were still its sister group, but with still less support. However, Soltis et al. (2011, see also Moore et al. 2011) find strong support for relationships in the clade as shown in the Summary Tree, those for [Malvales + Brassicales] at 85% ML bootstrap and for [Geraniales + Myrtales] at 79% being the weakest; all other rleationships along the spine have ³99% ML bootstrap (see also Ruhfel et al. 2014; M. Sun et al. et al. 2016: support for the two basal internodes weak). Relationships [Geraniales [Myrtales [ Sapindales etc.]]] were recovered by Hohmann et al. (2015).
Fernando et al. (1995) placed Picramniaceae, ex Simaroubaceae, between the [Fabid + COM] clade, which includes Surianaceae (fabid) and Irvingiaceae (COM clade), both ex Simaroubaceae, and malvids, which include Simaroubaceae themselves, but a position along the spine of the malvid clade is best.
Using mitochondrial and chloroplast genes, Zhu et al. (2007) found that Myrtales and Geraniales were successively sister to all other rosids - but with little support (Zhu et al. 2007). S.-B. Lee et al. (2006) found some support for the clade [Geraniales + Myrtales] sister to the rosid I clade, although sampling was poor. Jansen et al. (2007; see also Z. Wu et al. 2014) recovered this [Myrtales + Geraniales] clade as sister to the malvids, albeit with weak support. Xi et al. (2014) found that Eucalyptus was weakly supported as sister to all rosids in analyses using nuclear data, while in those using chloroplast data, the genus was sister to the malvids, and with strong support, however, representatives of Geraniales were not included and sampling in general was a bit sketchy (this was not the main focus of their work). There is a fair amount of variation in relationships in this area in the trees provided by M. Sun et al. (2014).
See the Dilleniales page for further discussion on major patterns of relationships within Pentapetalae and the rosid node for major patterns in relationships within the rosids.
Classification. The circumscription of the rosids could usefully be expanded to include both Saxifragales and Vitales if they form a single clade (see above); they are morphologically quite similar.
SAXIFRAGALES Berchtold & J. Presl Main Tree.
Ellagic acid, myricetin, flavonols +, (silicon concentration high [?level]); (tension wood +); branching from the previous flush [woody members]; cuticle waxes as clustered tubules; petiole bundle annular; lamina margins serrate, teeth with gland broadening distally and with apical foramen, higher order lateral veins joining it; A ?, anthers basifixed, with basal pit, sagittate; carpels free, at least apically, styluli short, stigmas decurrent, at most slightly wet; ovules ³2/carpel, with bistomal micropyle, (outer integument largely dermal in origin); fruit dry; seeds ± exotestal; embryo size?; unique 1 BP [adenosine] insertion in 18S rDNA. - 15 families, 112 genera, 2,500 species.
Age. Jian et al. (2006, esp. 2008) estimate the crown-group age for Saxifragales at 103-83 m.y.; ca 108 m.y. is the age in Tank et al. (2015: Table S1, S2) .
Note: Boldface denotes possible apomorphies, (....) denotes a feature common in the clade, exact status uncertain, [....] includes explanatory material. Note that the particular node to which many characters, particularly the more cryptic ones, should be assigned is unclear. This is partly because homoplasy is very common, in addition, basic information for all too many characters 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 are the not-so-trivial issues of how character states are delimited and ancestral states are reconstructed (see above).
Evolution. Divergence & Distribution. Saxifragales contain ca 1.3% of eudicot diversity. They have a very poor representation in the tropics in general, which makes the inclusion of the small but lowland tropical Peridiscaceae as sister to the rest (see below) the more notable. D. Soltis et al. (2013) looked at diversification in Saxifragales in the context of a 900+-species supermatrix, focusing particularly on woody<->herbaceous and annual<->perennial transitions, while Rubio de Casas et al. (2016) looked at the relationship between habitat and diversification, finding the ancestral habitat to be forest and shifts to the tundra habitat in particular, but also to cliffs and shrublands, to be accompanied by high net diversification rates.
Because many relationships within Saxifragales were difficult to resolve, it was suggested that they represented an ancient and rapid radiation (Fishbein et al. 2001; Fishbein & Soltis 2004). More recently Jian et al. (2006, esp. 2008) estimated that early diversification in the clade perhaps occurred over a period as short as 3-6 m.y., while Hermsen et al. (2006b: topology quite resolved, different in detail from that adopted here, support slight) thought that much diversification occurred around 90-84 m.y.a. in the Late Cretaceous.
Saxifragales have notably small seeds compared with those of other angiosperms (Linkies et al. 2010), although this is not so for Peridiscaceae, not included in that study, so this character is pegged at the next node up here.
D. Soltis et al. (2007b), Endress (2010c) and Carlsward et al. (2011) have all suggested possible apomorphies for the clade - or at least features common in the clade - other than those given above, while Hermsen et al. (2006b, see list of characters there) thought that Saxifragales lacked any "diagnostic" morphological features. Carlsward et al. (2011) suggest apomorphies for all internal branches of Saxifragales, and many of these are flagged as such below (pollen characters are not yet included). Doyle (2012) suggested that tricolpate pollen was "retained" in many Saxifragales.
Plant-Animal Interactions. Caterpillars of Papilionidae-Parnassiinae are quite common here (Simonsen et al. 2011; Condamine et al. 2011).
Chemistry, Morphology, etc. Roots are diarch (Van Tieghem & Douliot 1888). Saxifragales commonly have scalariform perforation plates, lateral pitting that is mostly scalariform or opposite, bordered pits, etc., but whether these are synapomorphies is unclear (Jian et al.  characterise the largely unresolved woody members and the Saxifraceae + Crassulaceae clades in terms of their wood anatomy). Leaf teeth are basically rosid, although those of Cercidiphyllum are described as being more or less chloranthoid (not very different), while Hamamelidaceae can have teeth with a clear, glandular apex (fothergilloid) and those of Altingiaceae are platanoid (basically, the higher order lateral veins do not quite make it to the tooth - Hickey & Wolfe 1975; Tetracarpaea is similar, also lacking such veins - Hils et al. 1988). Despite appearances, the floral apex in nearly all taxa studied is reportesd to be flat or concave (Fishbein et al. 2000; Soltis & Hufford 2002; D. Soltis et al. 2003b; Soltis et al. 2005b), although Wurdack and Davis (2009) suggested that this was not the case for Peridiscaceae.
For information on the hamamelids as it was beginning to be realised that they might have to be split, see Crane and Blackmore (1989). For pollen, see Hideux and Ferguson (1976), Zavada and Dilcher (1986); floral anatomy and morphology, Gaümann (1919), Bensel and Palser (1975a-d), Hufford and Endress (1989), Drinnan et al. (1995), Fishbein et al. (2000); for chemistry, Giannasi (1986), Jay (1971); for anatomy, Watari (1939), Ramamonjiarisoa (1980), Cutler and Gregory (1998); for seed coat, Krach (1976); and for general morphology, see Hermsen et al. (2006b).
Phylogeny. Most of Saxifragales as circumscribed here have long been apparent in molecular phylogenies (e.g. D. Soltis et al. 1997; D. Soltis & P. Soltis 1997), although support for the clade is not always very strong (D. Soltis et al. 2013). Within Saxifragales relationships other than the Saxifragaceae/Crassulaceae clade ("S.-C. clade" below) have been unclear for some time, and even now many of the deeper nodes remain poorly supported (D. Soltis et al. 2013). However, support for the S.-C. clade and relationships within it is generally strong. The relationships [[Crassulaceae [Tetracarpaeaceae [Penthoraceae + Haloragaceae]] [[Saxifragaceae [Iteaceae + Pterostemonaceae]]] Grossulariaceae]] were found by Morgan & Soltis (1993); support for a [Pterostemon + Itea] clade (= Iteaceae) is strong (e.g. Soltis et al. 2007a: see below). Aphanopetalum (ex Cunoniaceae) is to be included in the Crassulaceae et al. clade.
Although Hilu et al. (2003: matK) did not recover the S.-C. clade, there was no strong support for alternative placements; Cercidiphyllaceae and Daphniphyllaceae were sister taxa, with moderate jacknife support. Hermsen et al. (2006b), who included both molecular and morphological (the latter also from selected fossils) data, also recovered a S.-C. clade, while all other families were in a clade sister to this. [Paeonia + Daphniphyllum] and [Cercidiphyllaceae + Altingiaceae] were clades, but with very weak support (<50% bootstrap). Paeonia was linked with moderate support to the Crassulaceae clade, or, more weakly, with the S.-C. clade in some analyses in Fishbein et al. (2001); the latter relationship also appeared in a study by Fishbein and Soltis (2004), while Z.-D. Chen et al. (2016) found some support for a position as sister to [Cercidiphyllaceae [Dapniphyllaceae [Altingiaceae + Hamamelidaceae]]], relationships with even less support.
In none of these analyses were Peridiscaceae included. This family was an unexpected addition to Saxifragales, and they had been placed in Malpighiales by Savolainen et al. (2000a: see A.P.G. II 2003). However, Davis and Chase (2004; see also Soltis et al. 2007a) found that the family belonged here, adding Soyauxia, previously placed in Medusandraceae, while Wurdack and Davis (2009) added Medusandra itself. Paeonia was linked with low support to Peridiscus itself by Davis and Chase (2004). D. Soltis et al. (2007b) were unable to recover stable relationships among the woody Saxifragales, long branch attraction (to Paeoniaceae and Peridiscaceae) possibly occurring; depending on the analysis, a [Peridiscaceae + Paeoniaceae] clade made Hamamelidaceae paraphyletic, or Peridiscaceae were sister to all other Saxifragales. Despite the addition of more data, Jian et al. (2006) still found it difficult to resolve relationships between the woody members, although it appeared that Peridiscaceae might be sister to the rest of the order, and Paeoniaceae sister to the S.-C. clade. Similar relationships were recovered by Soltis et al. (2011, see also Moore et al. 2011), but support for the position of Paeoniaceae was weak; other relationships with Saxifragales that they found agree with the topology described below. Li (2008) also found little support for many relationships in the order, including the association of Paeoniaceae with the Crassulaceae group that appeared in some analyses, while Paeoniaceae were again associated with the S.-C. clade, but with litttle support, by M. Sun et al. (2016).
However, Jian et al. (2008: see also Qiu et al. 2010, slight differences [placement of Hamamelidaceae]), using a variety of large data sets (some with over 50,000 bp) and analyeses, found strong maximum likelihood and Bayesian support for the topology used here, although Paeonia in particular moved around the tree in some parsimony analyses. There is little morphological support for the basal branches, pretty much par for the course, although characters can be optimised to positions on a number of the shallower branches (c.f. Hermsen et al. 2006b). A study by Qi et al. (2012) that focused on Cercidiphyllum found a rather different set of relationships, including the paraphyly of Hamamelidaceae, but posterior probabilities were low, while in a rbcL analysis by Breteler et al. (2015), with a focus on Medusandraceae, but not including Paeonia, not only were Medusandraceae not basal (but there was no particular support for an alternative position), but Leea was placed within the order....
Some molecular analyses have placed the hitherto unplaced Cynomoriaceae in Saxifragales, perhaps in the Crassulaceae area, although with little support (Nickrent 2002; Nickrent et al. 2005), however, Barkman et al. (2007) found no support for a position in this order - but none for any particular position at all. A position in Saxifragales was rejected by Jian et al. (2008), who preferred to place them in Santalales; Balanophoraceae, with which Cynomoriaceae were linked in the past, are certainly to be included there (see also Nickrent et al. 2005). Recently Cynomoriaceae have been placed in Rosales as sister to Rosaceae based on analysis of chloroplast inverted repeat sequences (Moraceae were the only other family in the order examined), and with strong support; Cynomoriaceae were certainly to be excluded from Saxifragales (good sampling) and several other rosid orders (Z.-H. Zhang et al. 2009; see also Moore et al. 2011). Depending on the mitochondrial gene analyzed by Qiu et al. (2010), Cynomoriaceae were placed with Saxifragales (matR, nad5) or Sapindales (atp1, rps3). Naumann et al. (2013) placed Cynomoriaceae in Saxifragales as sister to [Paeoniaceae + Altingiaceae], the only other Saxifragales in the study, but representatives of the other clades to which Cynomoriaceae might be related were also included, while they are sister to the S.-C. clade in Z.-D. Chen et al. (2016), but with little support. The inclusion of Cynomoriaceae in Saxifragales has been confirmed by.
Previous Relationships. Saxifragales include Hamamelidaceae, thought to be a key group classically linking the Englerian Amentiferae (usually dioecious or monoecious woody plants with an ament, or catkin, with small flowers, and sometimes believed to be primitive), to "dicots" with more conventional flowers (e.g. Endress 1967; Frohne & Jensen 1992). However, the old Amentiferae, included in Cronquist's (1981) Hamamelidae, are now in several bits, mostly in the rosids, of which one is here - see also Fagales, the major part of Amentiferae, Malpighiales (Salicaceae), Rosales ("Urticales"), etc. (Qiu et al. 1998a). For the woody Saxifragaceae, now similarly widely distributed, see below; many iridoid-positive and/or tenuinucellate members are now in the asterids, but most iridoid-negative, herbaceous and/or crassinucellate members remain here. Ironically, three families of Saxifragales s. str. are reliably reported to have iridoids (how many origins?) and are the only families outside asterids with them. Daphniphyllanae, Saxifraganae and Hamamelidanae, in which Takhtajan (1997) placed most of the families that are in Saxifragales here, are all in his Hamamelididae.
Includes Altingiaceae, Aphanopetalaceae, Cercidiphyllaceae, Crassulaceae, Cynomoriaceae, Daphniphyllaceae, Grossulariaceae, Haloragaceae, Hamamelidaceae, Iteaceae, Paeoniaceae, Penthoraceae, Peridiscaceae, Saxifragaceae, Tetracarpaeaceae.
Synonymy: Hamamelidineae Thorne & Reveal - Altingiales Doweld, Cercidiphyllales Reveal, Crassulales Link, Cynomoriales Burnett, Daphniphyllales Hurusawa, Fothergillales Link, Grossulariales Berchtold & J. Presl, Haloragales Link, Hamamelidales Link, Iteales Doweld, Medusandrales Brenan, Paeoniales Heinze, Peridiscales Doweld, Sedales Reichenbach f., Sempervivales Berchtold & J. Presl - Daphniphyllanae Takhtajan, Hamamelidanae Takhtajan, Paeonianae Doweld, Saxifraganae Reveal - Hamamelididae Takhtajan, Paeoniidae C. Y. Wu - Crassulopsida Brongniart, Hamamelidopsida Brongniart, Saxifragopsida Brongniart
PERIDISCACEAE Kuhlmann, nom. cons. Back to Saxifragales
Trees; plants Al-accumulators, ?chemistry; vessel elements with scalariform perforation plates; apotracheal (paratracheal, diffuse) parenchya +; secretory canals + [Medusandra]; petiole bundles with wing bundles [Soyauxia], also an adaxial plate [Peridiscus] or an adaxial [Whittonia] or medullary [Medusandra] annular bundle; crystals +; hairs unicellular, lignified [Medusandra]; epidermal wax crystals in rosettes; leaves two-ranked, (spiral), lamina margin serrate [?tooth morphology], (entire), (secondary veins palmate, petiole pulvinate - Peridiscus, Medusandra), stipule single and adaxial, or paired and lateral; inflorescences axillary, racemose(-spicate) or fasciculate, flowers small; P 4-7, or K 5(-6), C 5(-6); A many, at most slightly connate basally, (anthers monothecal); nectary ?large, annular, hairy, or 0, (or: A 5, opposite C, staminodes 5, long, hairy, opposite K; nectary 0 - Medusandra); G [3-4], 1-locular, (with central column), stigmas punctate; ovules 1-2(-3)/carpel [6-8 in total], apical, pendulous, epitropous; fruit a drupe or capsule, 3-4-valved, wall expanding early [Medusandra], P deciduous or K much enlarged, accrescent, recurved (Medusandra); seed 1, large, coat tanniniferous, walls thin, ± collapsed; endosperm ?development, copious, cell walls thick, pitted, embryo very small, cotyledons foliaceous; n = ?
4[list]/11: Soyauxia (7). South America, tropical W. Africa (map: from Heywood 2007; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010).
Chemistry, Morphology, etc. Peridiscaceae are a very poorly known and superficially heterogeneous group; I have not seen Whittonia, but Metcalfe (1962) gives some details of its anatomy. The vascular pitting of Medusandra is scalariform and the pits are bordered (Metcalfe 1952). Note that the leaves are almost certainly simple, not unifolioliate (c.f. Brenan 1952; Hutchinson 1973); the rather swollen apex of the petiole is like that of many Euphorbiaceae, Hydnocarpus, Octoknema, etc., which are not usually described as being possibly unifoliolate. Petiole anatomy in the region of the pulvinus is complex. For epidermal wax crystals, see Ditsch and Barthlott (1997). The bracteoles are often inconspicuous (c.f. Cronquist 1981).
Peridiscus and Whittonia have monothecal anthers, probably derived within the family. The flowers of Medusandra have long and conspicuous staminodes borne opposite the sepals, hence the generic name. Breteler et al. (2015) discuss stamninodes and nectaries in Peridiscaceae; they suggest that in Soyauxia, at least, what had been called a disc is staminodial. The basic seed morphology/anatomy of Soyauxia and Peridiscus, from either side of the Atlantic, are almost identical, although the two are vegetatively very different - Peridiscus is sometimes even identified as Menispermaceae!
See Metcalfe (1952b, 1962) and Miller (1975) for anatomy and Soltis et al. (2007b) and Bayer and Dressler (2014) for general information.
Phylogeny. Relationships are [Medusandra [Peridiscus + Soyauxia]] (Wurdack & Davies 2009; Breteler et al. 2015).
Previous Relationships. Peridiscaceae were included in Violales-Flacourtiaceae by Takhtajan (1997), and a similar position was suggested by A.P.G. III (2003); Soyauxia in particular has been associated with Medusandraceae or with Flacourtiaceae (Malpighiales). Medusandra itself was tentatively included in Malpighiales by Soltis et al. (2005b), certainly, the serrate leaf blades and the cauline stipules suggest relationships other than to Santalales or Santalanae (c.f. Cronquist 1981; Takhtajan 1997; Thorne 2007).
Synonymy: Medusandraceae Brenan, nom. cons.
[[Paeoniaceae [Altingiaceae [Hamamelidaceae [Cercidiphyllaceae + Daphniphyllaceae]]]] [[Crassulaceae [Aphanopetalaceae [Tetracarpaeaceae [Haloragaceae + Penthoraceae]]]] [[Iteaceae [Grossulariaceae + Saxifragaceae]]]: floral apex flat-concave early in development; hypanthium +/G often (semi-)inferior.
Age. Magallón and Castillo (2009) estimated an age of ca 106.7 m.y. for this node, Bell et al. (2010) an age of (111-)103, 95(-92) m. years. Other estimates are from Wikström et al. (2001, 2004) at (116-)111, 92(-87) m.y. and Anderson et al. (2005) at ca 102 m.y., while 109-107 m.y. is the age suggested by M. Sun et al. (2014).
Evolution. Divergence & Distribution. This clade is characterised by having notably small seeds (Moles et al. 2005a; Sims 2012: as Saxifragales, but Peridiscaceae not included).
[Paeoniaceae [Altingiaceae [Hamamelidaceae [Cercidiphyllaceae + Daphniphyllaceae]]]]: buds perulate; leaves with basically palmate venation; stigma ± decurrent; mitochondrial coxII.i3 intron 0.
Age. The age of this clade is estimated to be around 72.6 m.y. by Naumann et al. (2013) and ca 103.3-103.6 m.y. by Tank et al. (2015: Table S1 and S2).
PAEONIACEAE Rafinesque, nom. cons. Back to Saxifragales
Perennial herbs, shortly rhizomatous to shrublets; ethereal oils, flavones +, hydrolysable and non-hydrolysable tannins 0; cork "subcortical" [Tiagi 1970]; stem with cortical vascular bundles; vessel elements with simple or scalariform perforation plates; nodes also 5:5; calcium oxalate as crystals; wax tubules with palmitone predominating; palisade mesophyll with arm cells; indumentum 0 (hairs +, unicellular); leaves spiral, compound, ultimately ternate, lamina vernation variable, leaf base broad, stipules 0; inflorescence terminal, flowers 1-few; flowers large [³5 cm across], with cortical vascular system; P +, spiral, 3:3 vascularization, "K" (3-)5(-7), tough, "C" 5-8(-13), not sharply distinguished; A many, from 5 trunk bundles continuing spiral of P, centrifugal, anthers with basal pits?; receptacular nectary +; G free, (2) 3-5(-15), stylulus 0, stigma expanded, rather oblique, wet; ovules usu. many/carpel, micropyle exo-/bistomal, outer integument 10-20 cells across, inner integument 3-4 cells across, endothelium +, parietal tissue ca 5 cells across, nucellar cap ca 12 cells across, nucellus mostly absorbed before anthesis; megaspore mother cells several, embryo sac often more than 1, elongate; fruit a follicle, K persistent; funicle fleshy, with apical rim-aril (0); testa fleshy, vascularized, exotestal cells palisade, variously thickened, the hypodermis palisade, ± lignified, (some mesotesta thickened); endosperm cell walls with xyloglucans [thick, pitted - amyloid], chalazal endosperm haustorium +, zygote initially coenocytic, several embryos initially developing, one matures, minute; n = 5, chromosomes 10-15 µm long; germination hypogeal; mitochondrial coxII.i3 intron 0.
1[list]/33. N. Temperate, especially East Asia (map: from Stern 1946; Hultén & Fries 1986). [Photo - Fruit]
Evolution. Divergence & Distribution. For the evolution and biogeography of the genus, see Sang et al. (1997).
Seed Dispersal. The testa is thick, fleshy and coloured, and in at least some species (Paeonia anomala, P. mlokosewitschii) its blackish colour contrasts with the red of the testa of partly developed and unfertilized seeds when the follicle opens. The funicle is also fleshy.
Chemistry, Morphology, etc. According to Hiepko (1965, see also Endress 2010c) Paeonia lacks petals - presumably because of the spiral arrangement and vasculature of the perianth members. There is a prominent lobed disc, but in P. officinalis, not other species, it does not secrete nectar (Hiepko 1966; Erbar 2014 and references). Johri et al. (1992) called the micropyle exostomal, however, the inner integument, too, partly forms the micropyle.
Both embryo sac and embryo development are very distinctive. The embryo sacs (there is often more than one per ovule) develop from megaspore mother cells that are deeply embedded in a massive nucellus plus nucellar cap, and they elongate considerably towards the micropyle as they develop; the secondary endosperm nucleus is huge (see e.g. Yakovlev & Yoffe 1957; Cave et al. 1961; Walters 1962). The funicle is also fleshy, and there may be a small rim aril at the apex. There is no tegmen.
For general information, see Tamura (2006), for the perianth, see also Brouland (1935); for general floral morphology, see Hiepko (1964, 1966) and Leins and Erbar (1991); Yakovlev and Yoffe (1957), Tiagi (1970) and Takhtajan (1988) provide much information on ovules and seeds. For an account of the genus, see Hong (2012).
Previous Relationships. Paeoniales were included in Ranunculidae (Takhtajan 1997), and a relationship between Paeoniaceae and Ranunculaceae in particular has often been suggested (Takhtajan 1997; Mabberley 1997 included Glaucidium [see Ranunculaceae here] in Paeoniaceae) because of gross floral similarities between the two. However, they differ in the nature of the petals and nectaries, the development of the androecium, numerous embryological features, etc. (e.g. Tiagi 1970); there are no dipteran agromyzid leaf miners on Paeoniaceae, although they are common on Ranunculaceae. Dilleniales, in which Paeoniaceae were placed by Cronquist (1981; see Corner 1946), have multistaminate and centrifugal androecia, but differ in gynoecial development, nectary morphology, etc.
[Altingiaceae [Hamamelidaceae [Cercidiphyllaceae + Daphniphyllaceae]]]: (route I iridoids +); cuticle waxes as tubules, nonacosan-10-ol the main wax; buds perulate; inflorescence racemose, flowers sessile; anthers ± valvate, connectives apically protruding; seeds winged; embryo long; germination epigeal and phanerocotylar.
Age. Moore et al. (2010: 95% HPD) suggested crown group ages of (103-)98(-94) m.y. for this node; aroud 98.7 m.y. is the age in Tank et al. (2015: Table S2)..
Evolution. Divergence & Distribution. Maslova (2010; see also Maslova et al. 2012) saw fossil Platanaceae and Hamamelidaceae, in particular Hamamelidaceae-Altingioideae, as being related and springing from a polymorphic ancestral group. Maslova's Hamamelidales included Hamamelidaceae, with a number of fossil genera, Platanaceae and several more fossil genera, and Bogutchantaceae (for further details, see Platanaceae) while Sarbaicarpaceae N. Maslova and Kasicarpaceae N. Maslova were both placed in the extinct order Sarbaicarpales N. Maslova, part of the immediately larger group.
Variation in this whole group is complex, and whether some characters reflected common ancestry or parallel variation was unclear (Maslova 2010: p. 1456 for a summary). Vavilov's Law of parallel variation was invoked (Maslova 2010: table 2), and it helped explain the "isomorphic polymorphisms" observed in platanoids and altingioids. Maslova (2010) was inclined to reject molecule-based hypotheses of relationships, and Proteaceae barely entered into the discussion; it is unclear what to make of these fossils and ideas.
Pollination Biology. There are a number of reports of delayed fertilization from members of all four families, although not in Paeonia (Endress 2110c, but esp. Sogo & Tobe 2006d and references), hence the placement of this feature here.
Chemistry, Morphology, etc. Raffinose and stachyose are common oligosaccharides in phloem exudate in this clade (Daphniphyllaceae not studied: Zimmermann & Ziegler 1975). Hufford and Endress (1989; see also Hersen et al. 2006b) discuss anather morphology and anatomy in detail; members of this clade can have obviously valvate anthers, as in Hamamelidoideae, or the stomium may simply divide at the two ends of the theca, or at least at the base of the theca. Wheeler et al. (2011) summarize what is known of wood anatomy in the clade.
ALTINGIACAEAE Horaninow, nom. cons. Back to Saxifragales
Trees, evergreen or deciduous; resins, route I iridoids +; secretory canals + [containing terpenoid resins]; petiole with 3-5 annular bundles (with medullary bundles); stomata paracytic; leaves spiral, lamina lobed, vernation flat, lobes conduplicate, stipules on leaf base; plant monoecious, inflorescence ± capitate; P 0; staminate flowers: A 4-10, (anthers with longitudinal slits), ?filament length; pollen grains polyporate, spherical, surface fine-reticulate; pistillode +; carpellate flowers: intercarpellary protrusions + [= sterile flowers]; G , unsealed, (semi)inferior, (transverse), styles short to quite long, stigmatic their entire length, with multicellular protrusions, but no papillae; ovules 20</carpel [only the lower ones fertile], straight, (micropyle endostomal), outer integument ca 2 cells across, inner integument ca 5 cells across; fruit a septicidal (and loculicidal or ventricidal) capsule; exotesta lignified or not, mesotesta ± sclerotic, endotestal cells oblong, lignified; endosperm slight; n = 15, 16.
1[list]/13. E. Mediterranean, East Asia to Malesia, Central America (map: see Vink 1957; Wood 1972; Rzedowski 1978; esp. Ickert-Bond et al. 2005). [Photos - Collection]
Age. Ickert-Bond and Wen (2006) suggested that the crown-group age for the family can be dated to somewhere between 54 and 19.5 m.y. ago.
The fossil Microaltingia (ca 90 m.y.o.) has prolate, tricolpate pollen grains with a coarsely reticulate exine, a more or less superior ovary, ovaries with 8 or more ovules per carpel, and perhaps unwinged seeds; it may have been pollinated by insects (Z.-K. Zhou et al. 2001). If correctly assigned here - sister to the extant representatives of the family (Ickert-Bond et al. 2005, 2007) - it is yet another fossil with interestingly plesiomorphous features (see also Calycanthaceae, Platanaceae, Fagaceae, etc.). See also Friis et al. (2011) for discussion; i.a. they note that there are 2-3 series of sterile organs on the ovary, and prefer to think of the fossil as stem Altingiaceae.
Evolution. Divergence & Distribution. Ickert-Bond and Wen (2006) give dates for divergence of clades within Altingiaceae; the basal split in the family is between the European + American and East Asian clades.
Chemistry, Morphology, etc. There can be confusion between the exudates of Styracaceae, and the genus Styrax in particular (form which benzoin oil, gum benjamin, etc.), and Altingiaceae (from which, storax) - not to mention Lindera benzoin (Lauraceae). Secretory canals are also reported from Mytilaria (Hamamelidaceae s. str.).
There are strongly vascularized structures ("phyllomes") interior to the staminal whorl; these may be staminodia, nectaries or organs sui generis. The orientation of the carpels varies (Bogle 1986). For the interpretation of the knobs, etc., surrounding the carpellate flowers, see Ickert-Bond et al. (2005). This and Hamamelidaceae - "micropyle faces upwards"?
Endocarpial cells are thickened and elongated transverse to the long axis of the fruit, and they look almost palisade in transverse section. The testa is notably thinner than that of most Hamamelidaceae. Ickert-Bond et al. (2005) suggest that in Liquidambar the exotegmen "constitutes most of the seed coat", although it is absent in most Hamamelidaceae, a point also made by others (e.g. Mohana Rao 1974). This is not immediately evident in the sections presented (e.g. Fig. 9, G-J) nor in Melikian (1973) and Z.-Y. Zhang and Wen (1996), but if confirmed (see e.g. Ickert-Bond et al. 2007) it will be another sharp difference from the more or less massively mesotestal seeds of most Hamamelidaceae.
For information about Hamamelidaceae s.l., see Bogle (1986: floral morphology, etc.), Ferguson (1989: general, esp. fossils), Skvortsova (1960: petiole), Melikian (1973: seed coat anatomy), Zavada and Dilcher (1986: pollen), and Endress (1993: general).
Phylogeny. Shi et al. (2001) present a molecular phylogeny of Altingiaceae, and this suggests that there is only one genus, in contrast to morphological phylogenies (Ickert-Bond et al. 2005, 2007).
Classification. It is best that a single genus be recognised, both because of phylogeny (e.g. Ickert-Bond & Wen 2006) and because species of the two genera that have been recognized, Liquidambar and Altingia, can hybridize (Wu et al. 2010). See Ickert-Bond and Wen (2013) for a taxonomic synopsis of the family.
Previous Relationships. Altingiaceae have often been included in Hamamelidaceae (e.g. Cronquist 1981).
[Hamamelidaceae [Cercidiphyllaceae + Daphniphyllaceae]]: ?
Age. The age of this node is ca 98.2 m.y. (Tank et al. 2015: Table S2).
HAMAMELIDACEAE R. Brown, nom. cons. Back to Saxifragales
Trees or shrubs, evergreen; (C-glycosylflavones +); (vestured pits +; true tracheids +); sclereids common; petiole bundle (±) annular (with adaxial bundle; arcuate); stomata often paracytic, but variable, inc. laterocytic; hairs stellate (other); leaves two-ranked (opposite, spiral), lamina vernation ± conduplicate-flat or -plicate, (margins entire), stipules cauline; flowers (2-)4-5(-7)-merous; K free to connate; A = and opposite sepals (3-many); staminodia opposite petals, anthers with two pairs of valves, (connective not prolonged); pollen tricolpate, (6-rugate); nectary ± annular, staminodial, or on base of C; G , styluli ± long, stigmas with multicellular protrusions, but no papillae; ovules ca 6/carpel, often epitropous, outer integument 6-12 cells across, inner integument 2-3 cells across, (micropyle zig-zag), hypostase +; fruit a loculicidal and septicidal capsule, K often persistent; hilum large, coat often with often discoloration near the hilum, testa thick, hard, multiplicative, exotestal cells thickened (not), mesotesta massive, usually of ± fibrous sclerotic cells, tegmen tanniniferous; endosperm slight, perisperm +, (polyembryony +).
27[list]/82 - four groups below. Tropical to temperate, esp. East Asia to Australia, not South America (map: from Vester 1940; Vink 1957; Ying et al. 1993; Fl. N. Am. 3, 1997; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Coates Palgrave 2002). [Photos - Collection] [Photo - Flower]
Age. An estimate of the crown-group age of Hamamelidaceae is a mere (42-)27, 25(-13) m.y. (Bell et al. 2010) or a very different (110-)104, 87(-81) m.y. (Wikström et al. 2001), but both these ages are in the context of relationships in the order that are very different from those followed here.
Archamamelis has 6-7-merous flowers, rather small, almost triangular petals, anthers with flaps, and a tricarpellate gynoecium, and may be stem-group Hamamelidaceae (Endress & Friis 1991; Friis et al. 2011).
1. Exbucklandoideae Harms
(Venation pinnate), (stipules 0); inflorescence capitate; (C 0); G half inferior, (styluli long); (ovules to 20/carpel); outer integument ca 2 cells across [Exbucklandia]; exotestal cells alone thickened; n = 12, 16.
2/ca 7. East Himalayas and South China to Sumatra.
Synonymy: Exbucklandiaceae Reveal & Doweld, Rhodoleiaceae Nakai
[Mytilarioideae [Disanthoideae + Hamamelidoideae]]: seeds not winged.
2. Mytilarioideae H. D. Chang
(Secretory canals +); nodes 5:5; (stipule 1, tubular - Chunia); (K 0, C 0 - Chunia); (C and A basally fused, forming a tube); G ± inferior; ovules 2/carpel; n = ?
2/2. Kwangsi, Laos, Hainan.
[Disanthoideae + Hamamelidoideae]: C ribbon-like, adaxially circinate.
Age.The age of this node is estimated at (92-)84, 61(-53) m.y. (Wikström et al. 2001).
3. Disanthoideae Harms
Plant deciduous; flowers paired; nectary at base of C; anthers with slits; G superior, styluli short, stout; n = 8.
1/1: Disanthus cercidifolius. E. China, Japan.
Synonymy: Disanthaceae Nakai
4. Hamamelidoideae Burnett
Plant evergreen or deciduous; (stomata anomocytic); (buds naked), (perula 1), prophyll 1 (2), basal, then an internode; lamina with pinnate/craspedodromous venation, vernation conduplicate-plicate; inflorescence racemose, spicate, (with 3-flowered lateral cymes); (K [5-9]); (C not circinate), (0); A 4-23, centripetal or centrifugal, anthers with 1 or 2 pairs of valves, or slits; tapetal cells multinucleate; G superior to inferior; (styluli long); ovules 1/carpel (-3, 2 sterile), (apotropous), parietal tissue 8-10 cells across, (nucellar cap ca 2 cells across); fruit with ballistic dispersal of seeds; (endosperm cellular - Parrotiopsis); n = 12.
23/78. Tropical to temperate, esp. East Asia to Australia, not South America.
Age. Allonia decandra, a fossil probably to be placed in crown-group Loropetalineae (Hamamalidoideae), was collected from ca 83 m.y.o. rocks of the Cretaceous-Campanian in the eastern U.S.A., it has twice as many stamens as petals and a lobed disc adaxial to them (Magallón-Puebla et al. 1996: Friis et al. 2011); the seeds are rather angled, so there may have been more than one per loculus.
Synonymy: Fothergillaceae Nuttall, Parrotiaceae Horaninow
Evolution. Divergence & Distribution. For the early Caenozoic fossil history of what are now East Asian endemic members of the family, see Manchester et al. (2009), for other literature on fossils, see Friis et al. (2011).
For the evolution of the flower in Hamamelidoideae, see Magallón (2007; fossils included, optimisation on to more than one topology).
Pollination Biology. There is considerable variation in floral morphology. Corylopsis has rather ordinary-looking flowers with obovate petals, although this morphology is probably derived. In Parrotiopsis there are showy inflorescence bracts, and these are bright red in Rhodoleia, and there the whole inflorescence is very like the flower of, say, Calycanthaceae. Petals may be lost, as in Fothergilla where the inflorescence is made conspicuous by the plump and showy white filaments (see Endress 1978 for a discussion of the floral morphology of those Hamamelidaceae without a perianth). Nectar is a common reward here, but the nectaries are very variable in morphology (Endress 1993 and references). Eustigma has quite long white styluli and massive, purplish stigmas that are the most conspicuous parts of the flower.
Fertilization in Hamamelidaceae is often much delayed.
Plant-Animal Interactions. For the phylogeny of hormoraphidine aphids, notable gallers on Hamamelidoideae with ca 13 genera of aphids known from Distylium alone, see J. Chen et al. (2014).
Chemistry, Morphology, etc. What is going on with the growth of Exbucklandia? There is variation in the direction of initiation of the stamens in multistaminate androecia (Endress 1976); it can be centripetal (Matudaea) or centrifugal (Fothergilla). Exbucklandia is reported to have a remarkably long outer integument, although it is developed only on one side of the micropyle (Kaul & Kapil 1974).
Much additional information can be found in Endress's early work (1967a [general, comparison with Betulaceae, Corylopsis is the link], 1970 [inflorescence], 1971 [inflorescence, flower], 1976, [floral development], 1993 [general]). For petiole anatomy, see Skvortsova (1960), for embryology, see Kapil and Kaul (1974: Parrotiopsis); for seed anatomy, see Mohana Rao (1974), Z.-Y. Zhang and Wen (1996), and Benedict et al. (2008: also fruits and fossils), and Magállon et al. (2001 and references) and Zhao and Li (2008) for fossils.
Phylogeny. A clade including Exbucklandioideae and Mytilarioideae was apparent only in the analysis of ITS data and good sampling (75% bootstrap, better if gaps scored as a fifth character state: Li et al. 1999b; c.f. Shi et al. 1998); the genera included have in the past been placed in three subfamilies. With rbcL data, Mytilaria alone was rather weakly supported as sister to [Disanthoideae + Hamamelidoideae] (Li et al. 1999a). However, a later two-gene analysis resulted in strong support for the clades represented by the four subfamilies above and their relationships (Li 2008) as did the study by Z.-D. Chen et al. (2016).
Within Hamamelidoideae [Corylopsideae (monotypic) + Loropetaleae (weak support)] were sister to the rest, but tribal interrelationships had for the most part only weak support (Li & Bogle 2001; Li 2008). See Xie et al. (2010) for the phylogeny and biogeography of Hamamelis, which, despite having similar petals to those of Loropetalum, is not immediately related.
Classification. For a classification of Hamamelidoideae, see Li and Bogle (2001).
[Cercidiphyllaceae + Daphniphyllaceae]: plant dioecious; flowers small, C 0; staminate flowers: , filemants at most barely longer than anthers; carpellate flowers: ovary superior; endosperm cellular.
Age. The age of this node is ca 91.8 m.y. (Tank et al. 2015: Table S2).
Chemistry, Morphology, etc. The filaments are at most only slightly longer than the anthers, quite common in wind-pollinated flowers.
CERCIDIPHYLLACEAE Engler, nom. cons. Back to Saxifragales
Deciduous trees, with short shoots; chalcones, dihydrochalcones +; cork in outer cortex; primary stem with continuous cylinder; prophyll adaxial; leaves usu. opposite, lamina vernation involute, (margins entire), stipule adaxial-petiolar; inflorescence capitate; P 0, floral apex?; staminate "flower": A 16-34 [= several flowers], anthers long; pollen tricolpate; carpellate flower: G free, single, suture appearing to be abaxial, ["1-8", = as many flowers, each subtended by a bract], styluli long, stigmas decurrent their entire length; ovules many/carpel, outer integument 4-5 cells across, inner integument 2-3 cells across; fruit a follicle; chalazal appendage with hair-pin loop vascular bundle; testa undistinguished, exotestal cells enlarged, slightly thickened, tegmen tanniniferous; endosperm slight, suspensor single-celled, cell notably enlarged; n = 19.
1[list]/2. China and Japan (map: from Heywood 1978; Fu & Hong 2000). [Photos - Collection.]
Evolution. Divergence & Distribution. For the early Caenozoic fossil history of Cercidiphyllum, see Manchester et al. (2009) and Friis et al. (2011). Qi et al. (2012) found substantial genome structure in populations of Cercidiphyllum, which is by no means a relict.
Palaeocene fossils (Joffrea) have 2-carpellate flowers borne on an elongated axis with the adaxial sutures of the carpels facing each other (Crane & Stockey 1985, 1986; see also Friis et al. 2011). Staminate flowers of fossils may have five stamens and a pentamerous perianth (Kvacek 2008).
Chemistry, Morphology, etc. Takhtajan (1997) described the venation of leaves on the long shoots as being pinnate, but the main secondary veins all arise within 5(-10) mm of the base.
Krassilov and Lowen (2007) thought that the flower of Cercidiphyllum was unlike that of other Saxifragales (see also Maskova 2010). The "flowers" of today's species can be interpreted as pseudanthia. Each carpel represents a carpellate flower, indeed, the carpels are sometimes slightly separated from one another on the stout green axis, that of the "pedicel"=inflorescence. Both individual carpels and groups of stamens are subtended by bracts and are more or less decussately arranged. Yan et al. (2007) suggest that the bract is "really" a tepal because it is developmentally so different from the vegetative leaves, although it may have teeth or be almost bilobed. However, it is most likely that the structure is a bract, and that the suture of the carpel is adaxial with respect to the floral axis that originally bore it. Soltis et al. (2005: fig. 6:11) suggest perhaps inadvertently that the gynoecium is partly inferior.
For variation in nodal anatomy between leaves on long and short shoots, see Howard (1979), and for general information, see Endress (1993) and Crane and Du Val (2013).
DAPHNIPHYLLACEAE Müller Argoviensis, nom. cons. Back to Saxifragales
Evergreen trees or shrubs; plants Al-accumulators, route I iridoids, triterpene [squalene] alkaloids +, myricetin, hydrolysable tannins 0; pits bordered; true tracheids +; pith at least sometimes septate; pericyclic fibres 0; stomata paracytic (laterocytic, anomocytic); plant glabrous; leaves ± pseudoverticillate, spiral, lamina vernation ± flat, margins entire, secondary veins pinnate, stipules 0; flowers pedicellate; P +, uniseriate, ± sepal-like, 2-6 (0); staminate flowers: A 5-12(-24), anthers with slits, basal pit indictinct, filaments with 3 traces, (staminodes +); pistillode 0; carpellate flowers: P free or connate, or 0; staminodes 0/+; G [2(-4)], placentation apical-axile to parietal, styluli short, recurved, stigmas rather massive, with multicellular protrusions but no papillae; ovules (1)2/carpel, ± apical, pendulous, micropyle exostomal/zig-zag?, outer integument 3-6 cells across, inner integument 4-5 cells across, hypostase +; fruit a 1-seeded drupe; seeds not winged, seed coat persistent but thin-walled and crushed, or endotegmen tanniniferous, walls thickened; perisperm slight, embryo short, cotyledons same width as radicle, (polyembryony +); n = 16.
1[list]/10. East Asia to Malesia (map: from Huang 1997). [Photo - Fruit]
Evolution. Divergence & Distribution. Daphniphyllum pollen is reported from middle Miocene deposits in Austria ca 14 m.y.o. (Grísson et al. 2015b).
Plant-Animal Interactions. Some epiplemine Uraniidae (moths) have caterpillars that eat Daphniphyllaceae - and assorted asterids - probably because of the iridoids they have in common (Lees & Smith 1991).
Chemistry, Morphology, etc. The flowers may be secondarily superior (D. Soltis et al. 2003b). Bhatnagar and Kapil (1982) described the endotegmic cells as being thickened and variously cutinised or sclerotic.
For general information, see Z.-Y. Zhang and Lu (1989) and especially Kubitzki (2006b), for information on stomata, etc, see Tang et al. (2009); for a monograph, see Huang (1965).
Previous Relationships. Daphniphyllaceae have been difficult to place, sometimes being associated with Euphorbiaceae, etc., or placed in a separate order in the Hamamelidae (Cronquist 1981). Balanopaceae (see Malpighiales) were included in a bigeneric Daphniphyllanae by Takhtajan (1997).
[[Crassulaceae [Aphanopetalaceae [Tetracarpaeaceae [Penthoraceae + Haloragaceae]]]] [Iteaceae [Grossulariaceae + Saxifragaceae]]]: vessel elements with simple perforation plates; petiole bundle(s) arcuate; cuticle waxes not tubular; venation ± pinnate; ovules apotropous [all?]; K persistent, withered.
Age. The crown-group age of this clade is some (96-)91, 78(-73) m.y. (Wikström et al. 2001, 2004), (88-)80, 77(-69) m.y. (Bell et al. 2010), or (114-)96.8(-90.1) m.y. (L.-Y. Chen et al. 2014a).
Chemistry, Morphology, etc. Mauritzon (1933) provides information on the ovules and endosperm development for many taxa in this clade.
[Crassulaceae [Aphanopetalaceae [Tetracarpaeaceae [Haloragaceae + Penthoraceae]]]]: stem with endodermis, lamina venation pinnate, stipules 0; inflorescence cymose; flowers 4-merous; A 2X K/C, obdiplostemonous; G opposite C; endosperm cellular.
Age. The crown-group age of this clade is around (88-)80, 77(-69) m.y. (Bell et al. 2010), (82-)77, 69(-64) m.y.a. (Wikstöm et al. 2001), (109.7-)94(-85.6) m.y. (L.-Y. Chen et al. 2014a), or ca 89.6 m.y. (Tank et al. 2015: Table S2).
Chemistry, Morphology, etc. For obdiplostemony and associated features, see Ronse De Craene and Bull-Hereñu (2016) and references.
CRASSULACEAE Jaume Saint-Hilaire, nom. cons. Back to Saxifragales
Succulent herbs to soft-stemmed shrubs; mycorrhizae 0; crassulacean acid metabolism common; flavones, acylated flavonol glycosides, sugar reserve as sedoheptulose, non-hydrolysable tannins +, hydrolyzable tannins 0; red pigment common, even in roots; (cork cortical); young stem with separate bundles; (medullary bundles +); sieve tube plastids lacking starch grains and protein inclusions; xylem rayless; nodes also 1:1-3, 3:3, etc.; cuticle waxes very variable; stomata usu. anisocytic; leaves succulent, lamina vernation flat to curved, margins entire, hydathodes +; inflorescence cymose; anthers median sagittate, latrorse; nectaries ± finger-like, at bases of carpels [outgrowths of carpels]; G ± free, opposite petals, with 5 vascular bundles, (placentation parietal), stigmas punctate to moderately capitate, (wet); ovules 1-many/carpel, micropyle bi- (exo-, endo-)stomal, outer integument ca 2 cells across, inner integument 2-3 cells across, nucellar cap ca 4 cells across, nucellar epidermal cells enlarged, apical cells ?tanniniferous, appearing subpalisade [for all, or Crassuloideae?], (conducting strand +); (megaspore mother cells several); fruit a follicle; exotestal cells with outer wall ± thickened, inner pigmented layer +; endosperm cellular and variants, (nuclear), chalazal haustorium +, embryo long, suspensor uniseriate, basal cell with mycelium-like haustorial branches; x = 8; germination epigeal and phanerocotylar.
34[list]/1400 - three subfamilies below. Cosmopolitan, esp. the Cape region and Mexico, but few in S. South America and the Antipodes, not in Polynesia, frequently in drier regions. (map: see Hultén 1958; Bywater & Wickens 1983; Jürgens 1995; Thiede 1994, 1995; Fl. China 8. 2001; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photo - Flower.]
Age. Diversification in this clade began (44-)41, 39(-36) m.y.a. (Wikstöm et al. 2001), while Bell et al. estimate an age of (63-)50, 47(-36) m.y. ago; around 45 m.y.a. is the estimate in J.-Q. Zhang et al. (2014b).
1. Crassuloideae Burnett
Leaves opposite, lamina with several marginal hydathodes only; flowers 3-9-merous; stamens = and opposite K, slightly introrse at anthesis; (G 3 - odd carpel abaxial - Tillaea); parietal tissue 1(-2) cells across, soon disappearing; follicles releasing seeds through apical pore; testa cells with sinuous anticlinal walls, unipapillate; first division of micropylar endosperm cell in horizontal plane; n = 7, 8.
2/196: Crassula (195). Esp. Southern Africa to S.W. Arabia, "Tillaea" more or less world-wide, the only representative of the family in the Antipodes.
Age. Around 33 m.y. is the estimate of the age of this clade in J.-Q. Zhang et al. (2014b: sampling).
Synonymy: Tillaeaceae Martynov
[Kalanchoöideae + Sempervivoideae]: leaves spiral, lamina with single (sub)apical hydathode; A obdiplostemonous, introrse only in early bud; (placentae lobed); parietal tissue 1-4 cells across; seeds costate; first division of micropylar endosperm cell in vertical plane.
Evolution. Divergence & Distribution. The crown-group age of this clade is estimated at (49-)35, 33(-23) m.y. (Bell et al. 2010) and around 45 m.y.a. in J.-Q. Zhang et al. (2014b).
2. Kalanchoöideae A. Berger
Plant ± woody; bufadienolides + [cardiac glycosides]; crystal sand +; (leaves opposite), (margins with teeth); flowers ?-merous; C connate; A with spherical connective prolongation; (styluli long); (central strand in nucellus); seeds 4-6-costate, with a micropylar corona; x = 9 [n = 9, 17 (18)].
4/200: Kalanchoe (145), Tylecodon (46). Old World, especially the Karroo in southern Africa, but extending to South East Asia and Malesia, not Australasia.
3. Sempervivoideae Arnott
(Pyrrolidine and piperidine alkaloids +), (non-cyanogenic β- and γ-hydroxynitrile glucosides +), (nonhydrolyzable tannins 0 [esp. Sedum acre group]); (leaves opposite); flowers 4-32-merous; (C connate); (stamens = and opposite K); (infra-stylar extra-gynoecial compitum/pollen tube growth - Sedum); nucellus elongated, with central strand; (follicle with abaxial dehiscence - Diamorpha); seeds ³6-costate; suspensor with compound plasmodesmata; n = >5, much variation (up to n = 320 - Sedum suaveolens).
28/1005: Sedum (??420), Echeveria (140), Rhodiola (90), Sempervivum (65), Dudleya (47). Largely N. hemisphere.
Synonymy: Cotyledonaceae Martynov, Rhodiolaceae Martynov, Sedaceae Roussel, Sempervivaceae Jussieu
Evolution. Divergence & Distribution. Aeonium, a largely Macaronesian genus with the most endemic species there, has striking growth forms, some arborescent, each of which seems to have evolved just once (Mes & t'Hart 1996; Jorgensen & Olesen 2001). Diversification in the largely Europaean Jovibarba/Sempervivum clade is a result of vicariance, long-distance dispersal, and edaphic specialization (Klein & Kadereit 2015).
The distinctive wood, which lacks rays and has very short vessel elements with annular and helical thickening, is probably paedomorphic (t'Hart & Koek-Noorman 1989); plant chemistry, in particular the presence of hydrolyzable tannins and the absence of non-hydrolyzable tannins, as in other woody Saxifragales, is consistent with this idea (Thiede & Eggli 2006).
There have been several origins of sympetaly in Sedoideae s.l. ('t Hart et al. 1999; Carrillo-Reyes et al. 2009); both it and epipetaly tend to be weak. The increase in numbers of flower parts in some Sedoideae - some have a multistaminate androecium - is in the context of an increased merousness of the whole flower; the relation between the number of parts of each whorl is like that of other basic core eudicot flowers (see also the euasterid clade), i.e. K = C = G; A = 2x C.
All ca 200 species of the Echeveria group (Sempervivoideae) appear to be interfertile, a remarkable situation apparently without parallel in flowering plants (Uhl 1992). For hybridization in Sempervivum, see Klein and Kadereit (2015).
For suggestions as to the base chromosome numbers of the family and of its major clades, see Mort et al. (2001).
Ecology & Physiology. Members of the family are an important component of the vegetation of the winter rainfall Succulent Karoo of south west Africa (Ogburn & Edwards 2010).
Crassulacean acid metabolism (CAM) is common throughout the family (Winter & Smith 1996a and references; Pilon-Smits et al. 1996). It has also been reported from aquatic species of Crassula (Keeley 1998). For CAM variation within Kalanchoe, see Gehrig et al. (2001), Kluge and Brulfert (1996) and Mioto et al. (2014).
Some species of Kalanchoe produce plantlets in notches at the margin of the leaf blade; these have rather aptly been called foliar embryos (Yarborough 1932). Both embryogenetic and organogenetic pathways have been coopted, and the young plantlets have cotyledon-like first leaves; unlike seeds, plantlets show no dormancy, a gene that induces dormancy in Arabidopsis not being functional (Garcês et al. 2014). Species in which development of plantlets is constitutive, i.e. plantlets are produced without the plant being damaged, do not produce viable seed (Garcês et al. 2007).
Chemistry, Morphology, etc. Anthocyanin is also found in the roots of Saxifragaceae, as well as Melastomataceae, Balsaminaceae, Asteraceae, Droseraceae, and Francoaceae (Krach 1976; Molisch 1928). Sedoheptulose is the most abundant sugar in Crassulaceae; isocitrate is common, unlike in other succulents (Thiede & Eggli 2006).
The extent of rayless wood in the family should be confirmed (Carlquist 2015b). The sieve tube plastids are a distinctive variant, lacking starch, the S0 type (Behnke 1988a). For (mistaken) reports of cortical vascular bundles, see Thiede and Eggli (2006). The leaf blade usually lacks palisade tissue, and there are often stomata on both sides. The stomata may also be heliocytic, with an additional ring of distinct cells outside a basically anisocytic configuration.
There is sometimes only a single vascular trace to the calyx members (t'Hart & Koek-Noorman 1989). Anthers early in development are introrse, but often at maturity the sporangia are equidistant from one another (Wassmer 1955). According to D. Soltis et al. (2003b), the ovary is secondarily superior. Although this seems unlikely, the very base of the ovary is sometimes inferior, and the carpels, apparently free, are slightly connate at the base; a small amount of axial tissue is also apparent in the gynoecial region of some taxa (Wassmer 1955, q.v. for gynoecial details). The nectary is ± receptacular in origin (Erbar 2014 and references). The nucellar epidermal cells tend to be large and more or less radially elongated in Crassuloideae (in particular) and Kalanchoöideae; in some Sedoideae megaspores elongate - sometimes those from the same megaspore mother cell - and grow towards the micropyle, and there and in Kalanchoe two embryo sacs may develop (Mauritzon 1933: much information; Subramanyan 1968). Haustoria from places other than the massive suspensor are reported for Crassulaceae (Mickesell 1990). Distinctive compound plasmodesmata in the suspensor cell walls have been found in some Sempervivoideae, although their distribution within the family is unclear (Kozieradzka-Kiszkurno et al. 2011). The testal cells of Crassula often have a single papilla and sinuous anticlinal walls (e.g. Bywater & Wickens 1983). There is no tegmen. Spongberg (1977) notes that the endosperm is usually scanty, while Mabberley (1997) describes it as being copious; the former is correct.
For general recent accounts of the family, see Eggli (2003: enumeration of all species) and in particular Thiede and Eggli (2006); for chemistry, see Stevens (1995) and Bjarnholt et al. (2008: non-cyanogenic glucosides), for anatomy, see Gregory (1998) and Jensen (1968: nodal anatomy, variable), for floral development, see Nelson (1990), and for embryology, etc., see Rombach (1911), Vignon-Fétré (1968) and Subramanyam (1970).
Phylogeny. The basic phylogenetic structure of the family seems fairly well established (e.g. van Ham 1995; van Ham & 't Hart 1998; Mort et al. 2001, 2010 for a summary; Mayuzumi & Ohba 2004). The rather highly derived Crassuloideae are sister to the rest of the family; Kalanchoe and relatives are sister to the rest of Sedoideae (e.g. Mort et al. 2001; Mort 2002; Thiede & Eggli 2006).
Within Crassuloideae, Tillaea is polyphyletic and embedded within Crassula (Mort et al. 2009; Mort et al. 2010). For the phylogeny of Kalanchoe, see Gehrig et al. (2001) and Kluge and Brulfert (1996).
Sedum appears in five of the seven main clades apparent in phylogenetic analyses of Sempervivoideae (van Ham 1995; van Ham & 't Hart 1998; Mayuzumi & Ohba 2004). Within the Acre clade of Sedum, most New World Sedoideae as well as all the old Echeverioideae in the study formed a single clade, although it was only poorly supported (Carrillo-Reyes et al. 2009). For relationships of the Acre clade and other east Asian Sedoideae, see Mayuzumi and Ohba (2004). The limits of Graptopetalum are unclear, and there was little strong support along the backbone of the tree (Acevedo-Rosas et al. 2004). For relationships within Dudleya, probably monophyletic, see Yost et al. (2014), and for those within Rhodiola, see J.-Q. Zhang et al. (2014a, b). Klein and Kadereit (2015) resolved relationships within the Jovibarba/Sempervivum clade, but chloroplast and nuclear data gave trees with different topologies.
Classification. Within Sempervivoideae, generic limits are unclear (an understatement), and many genera, some previously placed in what were considered to be different subfamilies, e.g. Sedoideae and Echeverioideae, hybridise (e.g. Uhl 1976; 't Hart et al. 1999). Thiede and Eggli (2006) provide a guide through the chaos, and although they prefer to retain a paraphyletic Sedum pro tem., this wil have to be dismembered or its circumscription much enlarged - the extremes are a Sedum that is monotypic or that encompasses almost two thirds of the whole family, and Klein (in Kadereit et al. 2016) inclined towards the former solution. For Kalanchoe, see Descoings (2006).
Previous Relationships. Crassulaceae have been linked with Rosaceae and Podostemaceae because of embryological similarities... (Rombach 1911).
[Aphanopetalaceae [Tetracarpaeaceae [Penthoraceae + Haloragaceae]]]: ?nodes 1:1; fruit indehiscent.
Age. The age for this node is estimated to be (92-)82.5(-75.7) m.y. (L.-Y. Chen et al. 2014a) or some 71.3 m.y. (Tank et al. 2015: Table S2).
APHANOPETALACEAE Doweld Back to Saxifragales
Scrambling shrub; chemistry?; vessel elements with scalariform perforation plates; pericyclic fibres 0; petiole with 3 (1) bundles; leaves opposite, margin serrate, teeth with a single vein and a distinct dark apex, or entire, stipules +, blackish [looking like teeth/colleters]; inflorescence axillary, or flowers solitary; hypanthium short; K large, petal-like, C 0/reduced, linear; pollen with rugulate-stellate surface; ?nectary; G seminferior, opposite petals, style single, with four canals, branches short; ovule 1/carpel, apical, pendulous, apotropous, micropyle bistomal, outer integument ca 8 cells across, inner integument ca 2 cells across, parietal tissue ca 4 cells across; archesporium multicellular; fruit a nut, K enlarging; seed 1; seed coat?; endosperm development?, embryo curved, size?; n = ?
1[list]/2. W. and E. Australia (map: from Australia's Virtual Herbarium [outliers omitted] i.2014). [Photo - Flower.]
Age. The two species may have diverged (19.6-)11(-4.7) m.y.a. (L.-Y. Chen et al. 2014a).
Chemistry, Morphology, etc. The ray parenchyma stores starch. Two small bundles soon diverge from the main leaf trace. It is unclear if the stipules "are" stipules or colleters (Kubitzki 2006b).
As in Saxifragaceae and Iteaceae, the vascular trace in the petal plane gives a branch to the lateral sepal position, also carpel wall and lateral carpel traces and a single stamen trace; the trace in the sepal plane supplies the carpel wall and median carpel bundle and provides a stamen bundle.
Some information is taken from Kubitzki (2006b: general), Jensen (1968: vascular system), Dickison (1980b: nodal anatomy), Dickison et al. (1994: anatomy), Bensel and Palser (1975b: floral anatomy), and Mauritzon (1939a: embryology).
Previous Relationships. Aphanopetalum used to be included in Cunoniaceae (Cronquist 1981), latterly as a separate subfamily (Takhtajan 1997).
[Tetracarpaeaceae [Penthoraceae + Haloragaceae]]: nectary 0 [to confirm].
Age. The age of this node is some (72-)61, 58(-46) m.y. (Bell et al. 2010), (62-)58, 53(-49) m.y. (Wikström et al. 2001), or (85.3-)78.1(-72.9) m.y. (L.-Y. Chen et al. 2014a).
Classification. Although combination of these three rather small families was an option in A.P.G. II (2003), there seems to be little or nothing holding them together morphologically (see also Moody & Les 2007) and they are kept separate in A.P.G. III (2009).
TETRACARPAEACEAE Nakai Back to Saxifragales
Evergreen shrub; chemistry?; plant glabrous; leaves spiral, petiole short; inflorescence terminal, racemose; (flowers 5-merous), floral apex convex; C spatulate; A 4-8, anthers with basal pits?, dehiscing by somewhat elongated apical pores, fibrous endothecium 0; G free, 4 (5), opposite petals, style short, stigma not expanded; ovules many/carpel, micropyle exostomal, parietal tissue ca 4 cells across; fruit a follicle; "testa" ca 4 cells across, cells ± elongated longitudinally, cuticle well developed, no mechanical layer; embryo small; n = ?
1[list]/1: Tetracarpaea tasmannica. Australia, Tasmania only. [Photo - Habit.]
Chemistry, Morphology, etc. The lamina teeth are perhaps hydathodal, but there are no water pores. The ovary is apparently secondarily superior (D. Soltis et al. 2003b). It is unclear whether the seed coat is testal or testal + tegmic.
See Kubitzki (2006b: general), Hils et al. (1988) and gronall et al. (1998: as Escalloniaceae), both anatomy, and Mauritzon (1933: ovules) for information.
Previous Relationships. Tetracarpaea used to be included in Grossulariaceae (Cronquist 1981), i.e., it was a woody saxifrage.
[Penthoraceae + Haloragaceae]: ± herbaceous; embryo long.
Age. The age of this node is estimated at (63-)51, 48(-35) m.y. (Bell et al. 2010), (51-)47, 43(-39) m.y. (Wikström et al. 2001), (74.4-)71.3(-70.1) m.y. (L.-Y. Chen et al. 2014a), or around 54.5 m.y. (Tank et al. 2015: Table S2).
PENTHORACEAE Britton, nom. cons. Back to Saxifragales
Rhizomatous herbs; flavonoids +, flavones, myricetin, non-hydrolysable tannins 0; cork ?; young stem with pseudosiphonostele; endodermoid layer?; pericyclic fibers 0; leaves spiral, lamina amphistomatic, vernation supervolute, teeth hydathodal, colleters +; inflorescence terminal, monochasial cyme; flowers 5-7-merous, hypanthium +; C 0(-7); A lacking a basal pit, latrorse; pollen oblate; ?nectary; G [5-8], half inferior, opposite sepals, apical parts free, becoming superior, placentae intrusive, styluli submarginal, stigmas capitate; ovules many/carpel, micropyle?, funicles long; free part of each carpel basally circumscissile in fruit; exotestal cells with outer wall ± thickened, papillate, micropylar operculum endostomal, tegmen otherwise crushed; seeds minute, first endosperm division very asymmetrical, cell at end of suspensor large; n = 8 (9).
1[list]/2. East and South East Asia, E. North America (map: from Hong 1993; Fl. China 8. 2001). [Photo - Penthorum Inflorescence.]
Age. Crown-group Penthoraceae are only 6.5-2.4 m.y.o. (Thiede 2006 for references) or (5.8-)2.9(-1) m.y.a. (L.-Y. Chen et al. 2014a).
Evolution. Divergence & Distribution. The E. North American/East Asian disjunction is dated to a mere 6.5-2.4 m.y.a. (Thiede 2006 for references).
Chemistry, Morphology, etc. Cork in the root is initiated in a superficial position (van Tieghem 1899).
The sepals are unequal in size and the bracts are lateral to the pedicels. There is a much-enlarged but non-dividing micropylar cell in the embryo suspensor - c.f. Haloragaceae and their haustorial suspensor. Danilova (1996) shows the carpels as opposite to the calyx. The first two pairs of seedling leaves are opposite.
See Spongberg (1972: as Saxifragaceae) and Thiede (2006), both general, Haskins and Hayden (1987) and Gornall (1998: as Saxifragaceae), both anatomy, Mauritzon (1933: endosperm), and Nemirovich-Danchenko (1994b: seeds) for information.
Previous Relationships. Penthorum used to be included in Saxifragaceae (Cronquist 1981).
HALORAGACEAE R. Brown, nom. cons. Back to Saxifragales
Flavones +, flavonols 0; cork ?; often calcium oxalate crystals in hair-like cortical cells; cuticle waxes 0 (parallel platelets); leaves opposite (spiral), (deeply pinnately lobed), lamina vernation conduplicate-flat, colleters +?; inflorescence ± determinate, (branches dichasial), fasciculate, or flowers solitary; flowers small [petals <4 mm long], 4-merous; K valvate, C deciduous; A (= and opposite sepals), anthers much longer than filaments, (apiculate), basal pits?; pollen grains tricellular, 4-6 colpate, tectum distantly verruculate, otherwise smooth and with minute pores; ovary inferior, (sub 1-locular), opposite petals or odd member adaxial, styluli with swollen bases, stigmas (sessile), capitate or not, penicillate, dry; ovule 1/carpel [fertile], apical, pendulous, apo(epi-)tropous, outer integument 2-3 cells across, inner integument ca 2 cells across, parietal tissue 2-3 cells across, nucellar cap +/0, postament +, poorly developed funicular obturator +; embryo sac with antipodal cells persistent; fruit nut-like, 1-4-seeded, indehiscent, (schizocarp), exocarp often ornamented; exotesta (and hypodermal layer) persistent, thin-walled, rest obliterated; endosperm starchy, (nuclear), haustorial suspensor +, (embryo short), cotyledons rather short.
9[list]/145 - two groups below. World-wide, but especially Australia.
Age. Crown-group Haloragaceae are estimated to be (56.3-)47.1(-37.3) m.y.o. (L.-Y. Chen et al. 2014a).
Hernández-Castillo and Cevallos-Ferriz (1999) described Tarahumara sophiae, from Mexico in deposits ca 70 m.y.o., as having four carpels free from one another but adnate to a hypanthial wall, while its fruit is described as being drupe-like, with one seed per carpel. Although perhaps assignable to this part of the tree, its morphology is unlike that of any extant Haloragaceae (see also Friis et al. 2011 for fossils). It is older than most estimates for stem-group Haloragaceae.
1. Glischrocaryon Endlicher
Herbs with woody rootstock to small trees; flowers perfect; whole flower (inflorescence) brightly coloured; (petals to 4 cm long); pollen apertures crassimarginate; fruit winged, 1-seeded; n = 7.
1-2/9. Southern and Western Australia, Northen Territory.
Age. The crown-group age of this clade may be some (14.8-)10.3(-6.4) m.y. (Chen et al. 2014).
2. Halorageae Bartling
Aquatic (ephemeral) herbs to small shrubs; plant monoecious (dioecious), or flowers perfect; C (0), (hooded); pollen 4-6(-20)-aperturate, (porate), apertures tenuimarginate; (ovules 2/carpel); fruit 1-4-seeded, (schizocarp); n = 6, 7 (8).
7/136: Myriophyllum (60), Gonocarpus (41), Haloragis (28). Largely Australian, but Proserpinaca and some Myriophyllum making the distribution more or less cosmopolitan (map: from van Steenis 1962; Hultén 1958, 1971; van der Meijden 1971; Wood 1972; Orchard 1981; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Chen et al. 2014). [Photo - Collection.]
Age. The crown-group age of this clade is estimated to be (50.9-)42(-33.5) m.y. (L.-Y. Chen et al. 2014a).
Synonymy: Cercodiaceae Jussieu, Myriophyllaceae Schultz-Schultzenstein
Evolution. Divergence & Distribution. For the ages of some intercontinental disjunctions within Haloragaceae, see Les et al. (2003).
Proserpinaca fossils are common in Europe and Asia, but the genus is now restricted to the New World, where it is scattered (L.-Y. Chen et al. 2014a: Fig. 1).
The family may have an Australian origin (e.g. Moody & Les 2007), and there has since been substantial dispersal, especially of the aquatic taxa - probably by birds (L.-Y. Chen et al. 2014a, q.v. for more details and dates).
Ecology & Physiology. The aquatic habit has evolved at least twice in the family (L.-Y. Chen et al. 2014a).
Pollination Biology. In some species of Glischrocaryon the whole inflorescence is coloured. However, details of its pollination are unknown; wind pollination is likely in other Haloragaceae.
Chemistry, Morphology, etc. Nodal anatomy was observed in Haloragis erecta and Laurembergia, vernation in the first. Pelargonidin occurs in leaves, as in Saxifragaceae (Doyle & Sogin 1988). Adventitious roots arise between the leaves in Haloragis.
Trihaloragis has flowers in which all whorls are trimerous, very unusual in eudicots; Moody and Les (2007) point out the extensive variation in floral merism in the family. Myriophyllum appears to have endostomal ovules (Batygina et al. 1985), while Bawa (1970) noted that the archesporial cell was hypodermal, i.e. the ovule is tenuinucellate/there is no parietal tissue. Nijalingappa (1975) described the embryo sac of Haloragis micrantha as having a hypostase; there is definitely a postament. Corner (1976) described the endosperm as being starchy.
For general information, see Orchard (1975: Antipodean taxa, inc. much detail about floral anatomy, etc.), Orchard (1990; Australian taxa), and Kubitzki (2006b); for other information, see Orchard and Keighery (1993: Meziella) and Praglowski (1970: pollen).
Phylogeny. See Moody and Les (2001, 2004 and especially 2007, in the latter study nuclear ITS and chloroplast genes in some conflict) for relationships within the family. The [Glischrocaryon + Haloragodendron] clade is sister to other Haloragaceae (see also L.-Y. Chen et al. 2014a), although the reciprocal monophyly of the two genera is not certain. The rest of the family forms a single clade, but relationships within it are uncertain, Meionectes and Proserpinaca in particular not having well-supported positions (Moody & Les 2007); the latter two genera are sister taxa, the combined clade being sister to the remainder (L.-Y. Chen et al. 2014a). The trimerous Trihaloragis is sister to all other members of this clade (Moody & Les 2007). For the phylogeny of Haloraghis (and the disappearance of Meziella) see Moody and Les (2009).
Previous Relationships. The monotypic Haloragales were placed near Saxifragales by Takhtajan (1997) or linked with Gunneraceae and placed next to Myrtales, as by Cronquist (1981). Historically Gunneraceae and Haloragaceae q.v. have often been associated, although their pollen is quite different (e.g. Praglowski 1970), the perianth of Gunneraceae is not differentiated into sepals and petals, etc..
[Iteaceae [Grossulariaceae + Saxifragaceae]]: (vessel elements with scalariform perforation plates); leaves spiral; inflorescence terminal; hypanthium +; stamens = and opposite K; nectary ± gynoecial; ovules many/carpel; fruit a septicidal capsule.
Age. The age of this node may be (86-)81, 73(-68)) m.y. (Wikström et al. 2001: c.f. topology) or ca 84.8 m.y. (Tank et al. 2015: Table S2).
Chemistry, Morphology, etc. Nectaries are common here, and are often associated with the gynoecium, although in Itea and Ribes, for example, they extend to the hypanthium, and in some Saxifragaceae on to the receptacle (Erbar 2014 and references).
ITEACEAE J. Agardh, nom. cons. Back to Saxifragales
C-glycosylflavones +; placentation axile, micropyle?, style well developed; endosperm slight, ?type.
2[list]/21. Rather scattered, warm temperate to tropical.
Age. The age of crown Iteaceae is (51-)46, 39(-34) m.y. (Wikström et al. 2001).
1. Pterostemon Schauer
Shrubs; ?chemistry; ?nodes; unicellular hairs with rough walls, glandular hairs =, conical to peltate; stipules cauline, minute; inflorescence a corymbose cyme; bracteoles +, hypanthium short; K valvate, C shortly clawed or not; filaments flattened, toothed, anthers with basal pits?, connective apiculate, staminodes 5, opposite petals; nectary 0; G [5(-6)], largely inferior, orientation?, stigmas (± radiating), capitate, ?type; ovules 4-8/carpel, ascending, apotropous, parietal tissue ca 8 cells across; fruit indehiscent, 1(-2) seeded, C also persistent; seed coat "cartilaginous"; n = ?
1/3. Mexico (map: from N. Smith et al. 2004).
Synonymy: Pterostemonaceae Small, nom. cons.
2. Itea L.
Trees to shrubs; allitol +, flavonols, ellagic acid 0; hairs unicellular only; young stem with separate bundles; pith chambered; lamina vernation conduplicate, margins spiny- or gland-toothed, stipules small, on petiole base or adjacent stem; inflorescence (branched) racemose; flowers rather small; C valvate; anthers lacking basal pits, connective protrusion apical, globular; pollen bilateral, 2-porate, ektexine homogeneous; G  to subinferior, styles postgenitally fused at least at the stigma, stigma punctate-lobed, wet; parietal tissue 3-4(?-7) cells across; exotestal cells with outer walls thickened; (endosperm moderate - Itea rhamnoides), embryo incumbent; n = 11.
1/18. South East Asia to W. Malesia, E. North America, E. and S. Africa (map: from Mai 1985; Aubréville 1974a; Coates Palgrave 2002; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photo - Itea Flower.]
Age. The fossil Divisestylus, from the late Cretaceous some 90 m.y. before present and perhaps part of the Itea clade, has five stamens opposite the sepals and ovaries and stigmas fused, but there are separate styles - just like Itea. However, the pollen is tricolpate and striate, suggesting that the the fossil is stem-group Itea (Hermsen et al. 2003; see also Friis et al. 2011).
Evolution. Divergence & Distribution. The distinctive pollen of Itea is known fossil in Europe in the Eocene and somewhat later in North America (Hermsen et al. 2003); fossils in western North America have been dated to 59-42 m.y., although there is some uncertainty here, or ca 3.7 m.y. in Western Europe (Hermsen 2013).
Chemistry, Morphology, etc. Itea: For the chemistry of Itea, see Bohm et al. (1999). Pterostemon also has flavones, in this being like other Saxifragales. Choristylis (= Itea) lacks axial parenchyma.
The inflorescences of Itea may be terminal on rather short shoots. The ovule of Itea is sometimes described as being unitegmic, with the integument 6-7 cells across, but this appears to be incorrect (Kubitzki 2006b). Although the carpels are free initially, they become connate, even along the style (Ge et al. 2002), so perhaps the styles are more accurately described as being postgenitally connate styluli.
For additional information, see Spongberg (1972), Gornall et al. (1998), and Kubitzki (2006b), all general, Ramamonjiarisoa (1980) and Gornall et al. (1998: as Escalloniaceae), both anatomy, Bensel and Palser (1975b) and Ge et al. (2002), both floral anatomy and development, and Mauritzon (1933: ovules).
Pterostemon: The pericyclic fibres of Pterostemon seem to be weakly developed and the androecium is obdiplostemonous. Similar peltate glandular hairs are known from Grossulariaceae.
For more information, see Goldberg (1986), Wilkinson (1994, 1998) and especially Kubitzki (2006b) and Guzmán et al. (2013), but Pterostemon is not well known.
Classification. Combination of Iteaceae and Pterostemonaceae was optional (as Iteaceae s.l.), see A.P.G. II (2003); this broadened circumscription was formally adopted by A.P.G. III (2009).
[Grossulariaceae + Saxifragaceae]: glandular hairs +; leaf base broad,, ensheathing ca 1/2 stem or more; secondary veins palmate; G ; (postament +); endosperm ± cellular, first division asymmetrical [chalazal chamber small], (micropylar chamber nuclear); germination epigeal, cotyledons expanded.
Age. The age of this node is ca 75.8 m.y. (Tank et al. 2015: Table S2).
Chemistry, Morphology, etc. For endosperm development, see Gaümann (1919) and Dahlgren (1930).
GROSSULARIACEAE de Candolle, nom. cons. Back to Saxifragales
Shrubs; non cyanogenic β- and γ-hydroxynitrile glucosides; cork cambium outer cortical/pericyclic; underground stems with endodermis; pericyclic fibres 0; axial parenchyma 0; petiole bundles ± connate; lamina vernation conduplicate-plicate, margins also lobed, some teeth hydathodal, leaf base with thin margins, (paired prickles at the nodes); inflorescence axillary, leafy below, racemose; pedicels articulated, bracteole single; (flowers 4-merous), hypanthium forming an obvious tube, nectary at base, or hypanthium very short, flowers rotate, nectary on top of G; C small, aestivation open; (A 4, 10), tapetal cells binucleate, (staminodes +); pollen 5-15-porate, with distinctively rugose ectoapertures, tectum complete; ovary inferior, carpels usu. superposed, placentation parietal, style single, long, stigma capitate, wet; ovules with exostomal micropyle, outer integument 3-5 cells across, inner integument ca 2 cells across, parietal tissue ca 3 cells across, nucellar cap 0, postament +, hypostase +; fruit baccate; seeds hard, arillate, exotestal cells palisade, mucilaginous, then a layer 3-6 cells across, endotestal cells crystalliferous, radial and inner walls lignified, ?tegmen cells elongated, tanniniferous; endosperm hemicellulosic, embryo short to long, cotyledons accumbent; n = 8, chromosomes 1.5-2.5 µm long.
1[list]/150: Ribes. Temperate N. hemisphere, also along the Andes (map: from Hultén 1968; Hultén & Fries 1986; Jalas et al. 1999; Fl. China 8. 2001; Malyschev & Peschkova 2004). [Photos - Collection.]
Age. Tylerianthus crossmanensis, ca 90 m.y.o. from the Upper Cretaceous of New Jersey, has been compared with Grossulariaceae, although it does not have a hypanthium (Friis et al. 2011 for references), but see Hydrangeaceae here.
Evolution. Plant-Animal Interactions. The fruits of Ribes are an important food for Andean frugivorous birds. Several species of insects have been recorded as eating species of Ribes (Weigend 2006).
Bacterial/Fungal Associations. A number of fungi, including the ecomonically very important white pine blister rust (the basidiomycete Cronartium ribicola), spend part of their life cycle on the plants of this genus. In some places in North America attempts - largely unsuccessful - have been made to eradicate Ribes so as to disrupt the life cycle of this damaging fungus, Ribes harbouring the telial stage.
Chemistry, Morphology, etc. For non-cyanogenic β- and γ-hydroxynitrile glucosides, which ar found along with cyanogenic α-hydroxynitrile glucosides, see Bjarnholt et al. (2008). Stem collenchyma is well developed.
Nectar glands on the anthers are reported from some species. There is considerable variation in pollen morphology, and Ribes divaricatum has pentacolpo-di-orate pollen (Weigend 2006). The stylar bundles are ventral carpellar (Saxena 1969). Wronska-Pilarek (2001) described a cellulose-pectinous layer surrounding the seed; it was ca 6 cells across and made up of thin-walled, elongated cells, perhaps tegmic/nucellar in origin. Wronska-Pilarek (2001) also thought that the aril sometimes developed from placental tissus.
Additional information is taken from Weigend (2006: general), Stern et al. (1970) and Gregory (1998), both anatomy, Klopfer (1969a, 1973) and Gelius (1967), floral morphology, and Mauritzon (1933) and Shamrov (1998), ovule/embryology.
Phylogeny. Weigend et al. (2002) and Senters and Soltis (2003) suggest phylogenies for Ribes.
Previous Relationships. Grossulariaceae as circumscribed by Cronquist (1981) are very heterogeneous, and include genera now placed in Phyllonomaceae and Escalloniaceae (both campanulids), Montiniaceae, Tribelaceae (both lamiids), Tetracarpaeaceae, Iteaceae (including Pterostemonaceae), and Celastraceae (all rosids).
Synonymy: Ribesiaceae Marquis
SAXIFRAGACEAE Jussieu, nom. cons. Back to Saxifragales
Herbs, rhizomatous or stoloniferous, mycorrhizae 0 [?how common]; cork also pericyclic; young stem with separate vascular bundles; nodes also 1:1, 1:2 and 3<:3<; petiole bundles also annular (with medullary or adaxial bundles); hairs (uni-)multiseriate with multicellular glandular head; leaves (opposite), lamina vernation variable, (secondary veins pinnate), hydathodes +, (margins entire), colleters +; (C clawed); A 10; tapetal cells (1-)2-4-nucleate; (pollen 2-3- colpate), surface striate, reticulate, or smooth with warts; nectary +, ± annular (0); G superior to inferior, (free), carpels with 5 bundles, apical parts quite often free, orientation variable, placentation parietal to axile, styluli ± long, adaxially channeled, stigma spatulate to capitate, wet or dry; outer and inner integuments ca 2 cells across, parietal tissue 2-6 cells across, nucellar cap +/0, (hypostase +); fruit also a follicle, (splash cups); exotestal cells with outer wall (radial walls) ± thickened, variously ornamented, inner pigmented layer +, (endotegmen crystalliferous); (endosperm helobial), moderate, embryo medium (large), cotyledons incumbent, suspensor massive [Saxifraga s.l.]; radicle with anthocyanin; n = (5-)7(+); chloroplast rpl2 intron 0.
Ca 33[list]/600 - two groups below. Mostly N. temperate and Arctic (S. temperate, some tropical mountains) (map: from Hultén 1958, 1971; Meusel et al. 1965; Fl. China 8. 2001; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photos - Collection]
Age. The age of crown-group Saxifragaceae may be (50-)38(-26) m.y. (Bell et al. 2010), (59-)54, 49(-44) m.y. (Wikström et al. 2001), or (46.1-)38.4(-31) m.y. (Deng et al. 2014).
The Upper Cretaceous Tylerianthus crossmanensis has been compared with Saxifragaceae s. str. (but also including Parnassiaceae, Gandolfo et al. 1998b) - see Hydrangeaceae.
1. Saxifragoideae Beilschmied
(Flowers obliquely monosymmetric); (C 0); (A 5); (pollen grains tricellular), nexine ca 1/2 thickness of sexine; testa smooth to papillate.
1/370-500. Mostly Arctic and northern montane, although Saxifraga magellanica and a few other species grow along the Andes.
Age. The age of crown-group Saxifragoideae is (39.3-)30.8(-23.5 m.y. (Deng et al. 2014).
2. Heucheroideae Burnett
(Leaves palmately or ternately compound), (stipule adaxial ["ligule"], basal or sub-basal on petiole, persistent, or paired, cauline [Astilbe]); flowers (3-10-merous); (hypanthium 0); K 0-10, (with a single trace - Astilbe), C (linear, deeply laciniate, or toothed), (0[Chrysosplenium]-6); (A 3-15); pollen colpate, colporate, or 6-9-porate, exine often reticulate, nexine ca = thickness of sexine; nectary disc-like (0); G [(3-5)], (placentation parietal); (integument single, 4-6 cells across - Darmera); (seed ornamented); testa various, (endotegmen thick-walled - Heuchera, Tolmeia).
Ca 30/220: Micranthes (85), Chrysosplenium (55), Heuchera (43). Mostly N. temperate, also tropical montane and Arctic.
Age. Crown-group Heucheroideae are (37.2-)30(-23.9) m.y.o. (Deng et al. 2014).
Synonymy: Brachycaulaceae Panigrahi & Dikshit, Chrysospleniaceae Berchtold & J. Presl, Pectiantiaceae Rafinesque
Evolution. Divergence & Distribution. Deng et al. (2014: q.v. for dates, etc.) discuss the biogeography of Saxifragaceae. They suggested that Saxifraga bicuspidata, from the Tierra del Fuego area, diverged from the rest of the genus ca 22 m.y.a., while Saxifragodes albowiana, from the same part of the world, was sister to Cascadia nuttallii, from the Pacific Northwest, the two diverging slightly over 20 m.y.a. (Deng et al. 2014: c.f. the topology of Fig. 3, the dated DIVA tree, and Fig. 1; in the former [Saxifragodes + Cascadia] were sister to all other Heucheroideae, in the latter, they were part of the Astilbe et al. clade). Much speciation in Saxifraga section Ciliatae is quite recent and associated with the uplift of the Qinghai-Tibet plateau, with that of the ca 110 species of subsection Hirculoideae occuring in within the last two million years (Gao et al. 2015).
Ecology & Physiology. Despite being quite a small family, Saxifragaceae have about 100 species that are cushion plants adapted to cold and dry environments, often growing at higher altitudes (Boucher et al. 2016b). Indeed, the only other family with a comparable number of cushion species, Caryophyllaceae, has three times as many species overall.
Pollination Biology & Seed Dispersal. The polyphyletic Mitella, along with a few other Saxifragaceae, is very largely pollinated by fungus gnats, and this association has evolved in parallel. Flowers of these species are often more or less broadly saucer-shaped and the petals have very narrow lobes (Okuyama et al. 2008). Cryptic species are being discovered in the fungus gnat-pollinated Mitella sect. Asimitellaria (Okuyama & Kato 2009).
The moth Greya (Prodoxidae), related to Tegeticula of yucca moth fame (see Asparagales-Agavoidoideae), is both a seed predator and pollinator of some Saxifragaceae (Segraves & Thompson 1999); this association is being studied in considerable detail, clarifying the diversification of both plant and pollinating seed parasite (Rich et al. 2008 and references). Other insects can also pollinate the flowers, and their number varies from year to year (Pellmyr & Thompson 1996). There is great - and unusual, at least in taxa with comparable floral biologies - variation in floral scent in Lithophragma, one of the saxifragaceous genera involved (Friberg et al. 2013). It has been suggested that the general lability of ovary position in the family (e.g. Klopfer 1972b) is connected to selection by such pollinators (Soltis & Hufford 2002); protected, i.e. inferior, ovaries will be favoured.
The seeds of a number of forest-dwelling Saxifragaceae are dispersed by rain, whether by a splash-cup mechanism, as in Mitella or Chrysosplenium, or by the seeds being thrown from the fruit as it moves violently after being hit by a drop of water, as in Heuchera.
Bacterial/Fungal Associations. Short-cycle Puccinia rusts (Uredinales, basidiomycetes) are frequently found on Saxifragaceae (Savile 1979a, b).
Genes & Genomes. Introgressive hybridisation in the Heuchera clade is extensive and there are various combinations of chloroplast and nuclear genomes, for example, the chloroplast genome of Tellima is also found in Mitella (e.g. Soltis et al. 1993).
In Saxifraga s. str. the diploid chromosome number varies from 12-ca 200, in Micranthes from 10-120.
Chemistry, Morphology, etc. The distribution of druses and acicular crystals is of systematic interest (Gornall 1987); only Saxifraga s.l. has been studied in detail. Over 50 vascular bundles may enter the petiole base in some taxa. Hydathodes are common.
Saxena (1973) suggested that the androecium of Saxifragaceae was not obdiplostemonous; from Gelius's (1967) description of androecial development, the relationship between the whorls can change during development. The stylar vascular supply is from dorsal and ventral carpellar bundles; the vascularization of the nectary is variable (Saxena 1973). In at least some species of Saxifraga, and in Astilbe and Rodgersia, the two carpels are oblique, but in the latter two this is associated with inverted floral orientation, the odd K being abaxial; many other taxa have superposed carpels (Eichler 1878; Engler 1930a; Eckert 1966). Variation in ovary position within the family is extreme, occurring within genera and even between the different morphs of heterostylous flowers (e.g. Kuzoff et al. 2001; Soltis & Hufford 2002). In Chrysosplenium one carpel is open, the other closed. There is great variation in endosperm development, some taxa apparently having helobial endosperm (Mauritzon 1933).
For general information, see Morf (1950) and Spongberg (1972); McGregor (2008) provides a well-illustrated summary of the ornamentally important Micranthes and Saxifraga. Some details of vegetative anatomy are taken from Thouvenin (1890) and Gornall (1998), of venation from Z. Zhang et al. (2015b: focus on Saxifraga), of floral anatomy from Bensel and Palser (1975b), of floral morphology from Klopfer (e.g. 1968, 1970a, b, 1973), Klopfer and Ziesing (1971) and Ronse Decraene et al. (1998c: Chrysosplenium), of pollen from Z. Zhang et al. (2015a: mostly Saxifraga), of embryology from Pace (1912), Mauritzon (1933: much detail), Vignon-Fétré (1968) and Gornall (1989), and of seed morphology from Kaplan (1981: also pollen, etc., Saxifraga s.l.) and Knapp (1998). Given the history of the circumscription of Saxifragaceae, early references to it may contain information about several other families, too.
Phylogeny. There are two major clades in Saxifragaceae. One includes Saxifraga s. str., largely arctic-alpine in distribution; for relationships, see Gao et al. (2015) and especially Tkach et al. (2015b, q.v. for references to papers dealing with individual sections of the genus). Section Irregulares is sister to the rest of Saxifraga, and interestingly it may have scapose inflorescences (Tkach et al. 2015b)! Heucheroideae include the rest; Micranthes, which used to be part of Saxifraga, is well embedded in this clade and is not at all close to Saxifraga. The inflorescence of Saxifraga s. str. often has cauline bracts, however, that of Darmera is scapose, and there are pollen and testa surface differences between the two.
Most of the morphological variation in the family is in the predominantly temperate Heucheroideae (Soltis et al. 2001; Xiang et al. 2012; Prieto et al. 2013). Relationships in Heucheroideae are quite well resolved, with a topology of [Astilbe et al. [Heuchera et al. [Darmera et al. [Chrysosplenium et al. + Micranthes]]]] (Deng et al. 2014: Bayesian p.ps all 1.0 or close). Relationships in Tkach et al. (2015b) were somewhat different in detail, although these were not the focus of that paper, in particular, Cascadia and Saxifragodes, separately or together, were on long branches somewhere near the base of Heucheroideae. For relationships within Darmera, see Tkach et al. (2015a: quite well resolved), and in the Heuchera area, see Folk and Freudenstein (2014); Mitella (see also Okuyama 2016) is polyphyletic.
Classification. Generic limits in the Heuchera clade are unclear (Soltis et al. 1996 and refs.; Okuyama et al. 2008).
Previous Relationships. In the past, genera "intermediate" between what was thought to be a very variable Saxifragaceae and other families tended to be included in Saxifragaceae. It hs long been recognized that this was because the inclusion of more odd genera in Saxifragaceae would have little effect on the family description since there was already so much variation included in it (Pace 1912). However, if placed in the more homogeneous Crassulaceae, for example, such genera would greatly affect the description of that family and hence make it less discrete (e.g. Penthorum). Many tenuinucellate and unitegmic genera that used to be included in Saxifragaceae or Grossulariaceae have turned out to be entirely unrelated to each other. There was clearly a division between Saxifragaceae s. str. + Grossulariaceae s. str., with petals that remain very small for quite some time during development, and Hydrangeaceae (also classically placed in this area), with their relatively faster-developing petals, as is common in the asterids (Gelius 1967), and that flags a major separation. Of Saxifragaceae in the old sense, Parnassia is in Celastraceae-Celastrales (a conclusion in agreement with data from floral anatomy - e.g. Bensel & Palser 1975a, d), Francoaceae are in Geraniales, Vahlia is unplaced in the lamiids, but is perhaps to be included in Solanales, and so on. However, the unitegmic Darmera is properly to be retained in Saxifragaceae (e.g. Gornall 1989).
Age. An age of (117-)100.2(-76) m.y. was suggested for the clade [Cynomoriaceae [Paeoniaceae + Altingiaceae]] in Naumann et al. (2013).
CYNOMORIACEAE Lindley, nom. cons. Back to Saxifragales
Echlorophyllous, root parasite; vessel elements?; vascular bundles in the stem scattered; cork?; stomata ?0; plant glabrous; leaves spiral; plant polygamomonoecious; inflorescence clavate-capitate, indeterminate, branches cymose; inflorescence bracts peltate, floral bracts recaulescent; flowers minute; P +, uniseriate, (0-)4-5(-8), basally connate or not; staminate flowers: A 1, introrse; pollen colporate; concave-cristate stylodium +; carpellate flowers: staminodia 0; G 1, inferior, style long, channeled, with 2 vascular bundles, stigma not expanded, papillate; ovule 1/carpel, apical, pendulous, straight/semianatropous, unitegmic, integument 5-8 cells across, parietal tissue 1-3 cells across; fruit an achene; testa ca 7 cells across, persistent, exotesta slightly developed, walls little thickened; endosperm cellular, copious, thick-walled, embryo short, undifferentiated; n = 12, size strongly bimodal.
1[list]/2. Mediterranean to C. Asia (map: from Jalas & Suominen 1976; Jäger et al. 1985; Flora of China 13, 2007 [approx.]; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010). [Photo - Habit © D. L. Nickrent.]
Evolution. Ecology. In the Mediterranean area the hosts of Cynomoriaceae are often members of Cistaceae or Amaranthaceae, elsewhere Cynomorium parasitizes Amaranthaceae, Tamaricaceae, Nitrariaceae, etc. (Jäger at al. 1985).
Chemistry, Morphology, etc. The root has root hairs. The stem seems to develop inside a cavity in the tuber-like haustorial structure attached to the host (Solms-Laubach 1867). Weddell (1860) specifically noted that he did not find stomata on foliar organs.
Perfect flowers are also known. There are a number of questions about the floral morphology of Cynomorium, but very few new data have appeared in the last 150 years. The perianth is less well developed in pistillate than in staminate flowers, and there is debate as to its morphological nature - is it perianth, or (partly) bracteate, and if the latter, what is the structure of the inflorescence? The distinctive concave-cristate stylodium lacks vascularization; it may be nectariferous. The pistillode in staminate flowers may be appear to be superior or inferior and the gynoecium in carpellate flowers has been drawn as being semi-superior (Hooker 1856; Li 2008). The style in pistillate flowers is channelled its entire length and has two vascular bundles, a rather odd combination; Hooker (1856) suggested that there are two carpels. It is unclear whether the ovule has parietal tissue, or whether the cells above the embryo sac represent a nucellar cap; the former is more likely.
For general information, see the Parasitic Plants website (Nickrent 1998 onwards) and also Heide-Jørgensen (2008), for morphology, see Weddell (1860), for some chemistry, see references in Z.-H. Zhang et al. (2009), for pollen nucleus number, see Hansen (1986), for ovule, etc., see Juel (1902: ?nucellar cap), for ovule and seed, see Teryokhin et al. (1975), and for details of seed anatomy, see Takhtajan (2000).
For details of seed anatomy, see Takhtajan (2000), for morphology, see Weddell (1860), for ovule, etc., see Juel (1902) and Teryokhin et al. (1975), for some chemistry, see references in Z.-H. Zhang et al. (2009), and for general information, see the Parasitic Plants website (Nickrent 1998 onwards) and also Heide-Jørgensen (2008).
Previous relationships. Cynomoriaceae have usually been included in Balanophoraceae or Balanophoranae (e.g. Cronquist 1968; Takhtajan 1997), or their position has seemed to be completely uncertain (see above).