EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, initially ±globular, not motile, branched; showing gravitropism; glycolate oxidase +, glycolate metabolism in leaf peroxisomes [glyoxysomes], acquisition of phenylalanine lysase* [PAL], flavonoid synthesis*, microbial terpene synthase-like genes +, triterpenoids produced by CYP716 enzymes, CYP73 and phenylpropanoid metabolism [development of phenolic network], 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; centrioles/centrosomes in vegetative cells 0, microtubules with γ-tubulin along their lengths [?here], interphase microtubules form hoop-like system; metaphase spindle anastral, predictive preprophase band + [with microtubules and F-actin; where new cell wall will form], phragmoplast + [cell wall deposition centrifugal, from around the anaphase spindle], 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, asymmetrical; oogamy; sporophyte +*, multicellular, growth 3-dimensional*, 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 [= MicroTubule Organizing Centre] associated with plastid, sporocytes 4-lobed, cytokinesis simultaneous, preceding nuclear division, quadripolar microtubule system +; wall development both centripetal and centrifugal, 1000 spores/sporangium, sporopollenin in the spore wall* laid down in association with trilamellar layers [white-line centred lamellae; tripartite lamellae]; plastid transmission maternal; nuclear genome [1C] <1.4 pg, main telomere sequence motif TTTAGGG, KNOX1 and KNOX2 [duplication] and LEAFY genes present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes [precursors for starch synthesis], tufA, minD, minE genes moved to nucleus; mitochondrial trnS(gcu) and trnN(guu) genes +.
Many of the bolded characters in the characterization above are apomorphies of more or less inclusive clades 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.
Sporophyte well developed, branched, branching dichotomous, potentially indeterminate; hydroids +; stomata on stem; sporangia several, terminal; spore walls not multilamellate [?here].
II. TRACHEOPHYTA / VASCULAR PLANTS
Sporophyte long lived, cells polyplastidic, 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]; PIN[auxin efflux facilitators]-mediated polar auxin transport; (condensed or nonhydrolyzable tannins/proanthocyanidins +); borate cross-linked rhamnogalactan II, xyloglucans with side chains uncharged [?level], in secondary walls of vascular and mechanical tissue; lignins +; roots +, often ≤1 mm across, root hairs and root cap +; stem apex multicellular [several apical initials, no tunica], with cytohistochemical zonation, plasmodesmata formation based on cell lineage; vascular development acropetal, tracheids +, in both protoxylem and metaxylem, G- and S-types; sieve cells + [nucleus degenerating]; endodermis +; stomata numerous, involved in gas exchange; leaves +, vascularized, spirally arranged, blades with mean venation density ca 1.8 mm/mm2 [to 5 mm/mm2], all epidermal cells with chloroplasts; sporangia in strobili, sporangia adaxial, columella 0; tapetum glandular; sporophyte-gametophyte junction lacking dead gametophytic cells, mucilage, ?position of transfer cells; MTOCs not associated with plastids, basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; archegonia embedded/sunken [only neck protruding]; embryo 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 growth ± monopodial, branching spiral; roots endomycorrhizal [with Glomeromycota], 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; nuclear genome [1C] 7.6-10 pg [mode]; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; mitochondrion with loss of 4 genes, absence of numerous group II introns; LITTLE ZIPPER proteins.
Sporophyte woody; stem branching axillary, buds exogenous; lateral root origin from the pericycle; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].
SEED PLANTS† / SPERMATOPHYTA†
Growth of plant bipolar [plumule/stem and radicle/root independent, roots positively geotropic]; 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, free-nuclear/syncytial to start with, walls then coming to surround the individual nuclei, process proceeding centripetally.
EXTANT SEED PLANTS
Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); microbial terpene synthase-like genes 0; 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]; roots often ≥1 mm across, stele diarch to pentarch, xylem and phloem originating on alternating radii, cork cambium deep seated, gravitropism response fast; 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.; branching by 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; embryo cellular ab initio, suspensor short-minute, embryonic axis straight [shoot and root at opposite ends], primary root/radicle produces taproot [= allorhizic], cotyledons 2; embryo ± dormant; chloroplast ycf2 gene in inverted repeat, trans splicing of five mitochondrial group II introns, rpl6 gene absent; ??whole nuclear genome duplication [ζ/zeta duplication event], 2C genome size (0.71-)1.99(-5.49) pg, two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], 5.8S and 5S rDNA in separate clusters.
IID. 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 cap meristem closed (open); pith relatively inconspicuous, lateral roots initiated immediately to the side of [when diarch] or opposite xylem poles; epidermis probably originating 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, multiseriate rays +, wood parenchyma +; sieve tubes enucleate, sieve plates 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 randomly oriented, brachyparacytic [ends of subsidiary cells ± level with ends of guard cells], 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 = T, petal-like, 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 restricted to the apertural regions, thin, compact, intine in apertural areas thick, orbicules +, pollenkitt +; nectary 0; carpels present, superior, free, several, spiral, 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, four-celled [one module, egg and polar nuclei sisters]; ovule not increasing in size between pollination and fertilization; pollen grains bicellular at dispersal, germinating in less than 3 hours, siphonogamy, pollen tube unbranched, growing towards the ovule, between cells, growth rate (ca 10-)80-20,000 µm h-1, tube 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 gametophytes tricellular, gametes 2, lacking cell walls, ciliae 0, double fertilization +, ovules aborting unless fertilized; fruit indehiscent, P deciduous; mature seed much larger than fertilized ovule, small [<5 mm long], dry [no sarcotesta], exotestal; endosperm +, ?diploid [one polar nucleus + male gamete], 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 [2C] (0.57-)1.45(-3.71) [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]; anther wall with outer secondary parietal cell layer dividing; tectum reticulate; 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 monosporic [spore chalazal], 8-celled, bipolar [Polygonum type], antipodal cells persisting; endosperm triploid.
[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (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 [or next node up]; fruit dry [very labile].
EUDICOTS: (Myricetin +), 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], short [<2 x length of ovary]; seed coat?; palaeotetraploidy event.
[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]: mitochondrial rps11 gene lost.
CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one position]; micropyle?; γ genome duplication [allopolyploidy, 4x x 2x], x = 3 x 7 = 21, 2C genome size (0.79-)1.05(-1.41) pg, 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 = K + C, K enclosing the flower in bud, with three or more traces, C with single trace; A = 2x K/C, in two whorls, internal/adaxial to C, alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G [(3, 4) 5], whorled, placentation axile, style +, stigma not decurrent, compitum + [another position]; endosperm nuclear/coenocytic; fruit dry, dehiscent, loculicidal [when a capsule]; floral nectaries with CRABSCLAW expression.
[SANTALALES [BERBERIDOPSIDALES [CARYOPHYLLALES + ASTERIDAE]]] / ASTERIDS ET AL. / SUPERASTERIDS : ?
[BERBERIDOPSIDALES [CARYOPHYLLALES + ASTERIDAE]]: ?
[CARYOPHYLLALES + ASTERIDAE]: seed exotestal; embryo long.
ASTERIDAE / ASTERANAE Takhtajan: nicotinic acid metabolised to its arabinosides; (iridoids +); tension wood decidedly uncommon; C enclosing A and G in bud, (connate [sometimes evident only early in development, petals then appearing to be free]); anthers dorsifixed?; if nectary +, gynoecial; G , style single, long; ovules unitegmic, integument thick [5-8 cells across], endothelium +, nucellar epidermis does not persist; exotestal [!: even when a single integument] cells lignified, esp. on anticlinal and/or inner periclinal walls; endosperm cellular.
[ERICALES [LAMIIDAE/ASTERID I + CAMPANULIDAE/ASTERID II]]: ovules lacking parietal tissue [= tenuinucellate] (present).
[LAMIIDAE/ASTERID I + CAMPANULIDAE/ASTERID II] / CORE ASTERIDS / EUASTERIDS / GENTIANIDAE: plants woody, evergreen; ellagic acid 0, non-hydrolysable tannins not common; vessel elements long, with scalariform perforation plates; sugar transport in phloem active; inflorescence usu. basically cymose; flowers rather small [<8 mm across]; C free or basally connate, valvate, often with median adaxial ridge and inflexed apex ["hooded"]; A = and opposite sepals or P, free to basally adnate to C; G [#?]; ovules 2/carpel, apical, pendulous; fruit a drupe, [stone ± flattened, surface ornamented]; seed single; duplication of the PI gene.
ASTERID II / CAMPANULIDAE: myricetin 0; style shorter than the ovary; endosperm copious, embryo short/very short.
[[ESCALLONIALES + ASTERALES] [BRUNIALES [APIALES [PARACRYPHIALES + DIPSACALES]]]] / APIIDAE: iridoids +; C forming a distinct tube, tube initiation early; A epipetalous; ovary inferior, [2-3], style long[?].
[BRUNIALES [APIALES [PARACRYPHIALES + DIPSACALES]]]: ?
[APIALES [PARACRYPHIALES + DIPSACALES]] / DIPSAPIIDAE: nodes 3:3.
[PARACRYPHIALES + DIPSACALES] / DIPSIDAE: true tracheids +; lamina margin serrate; inflorescence terminal.
Phylogeny. For the relationships of Dipsacales, see the asterid II/gentianid clade.
DIPSACALES Berchtold & J. Presl - Main Tree.
Route I secoiridoids +; vessel elements with scalariform perforation plates; petiole bundles arcuate; colleters 0; buds perulate; leaves opposite, margins gland-toothed, bases ± confluent, (amplexicaul); inflorescence with terminal flowers, branches cymose; pollen grains tricellular; G , at least partly inferior; ovules apotropous; fruit indehiscent, wall with fibrous layers perpendicular to each other and thick walled sclereids, containing crystals, K persistent; testa vascularized, exotestal cells enlarged, cuboid/rectangular, variously thickened and lignified, seed coat 1-21 μm across; endosperm without haustoria, cells thin-walled, not differentiated. - 2 families, 46 genera, 1,090 species.
Note: In all node characterizations, boldface denotes a possible apomorphy, (....) denotes a feature the exact status of which in the clade is uncertain, [....] includes explanatory material; other text lists features found pretty much throughout the clade. Note that the precise 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).
Age. The first split within crown-group Dipsacales may have occurred in the mid-Cretaceous, some 111-102 Ma, the oldest of the estimates (Bell & Donoghue 2005a and references; H.-X. Wang et al. 2019 estimate ca 103 Ma, but from the tree their in Fig. 6 it would have to be 110 Ma or a little more). The age has also been estimated at (90-)62(-32) Ma in Lemaire et al. (2011b), who also unaccountably note "more recent stem node ages" of 31 Ma for Dipsacales, which in the context of their tree would be the age of the [Apiales [Paracryphiales + Dipsacales]] clade, and which they dated at (105-)84(-58) Ma. K. Bremer et al. (2004a) date the beginning of diversification here at 101 Ma, Wikström et al. (2001) at (87-)82, 78(-73) Ma, Beaulieu et al. (2013a: 95% HPD) at (94-)80(-87) Ma, Magallón et al. (2015) at around 70.9 Ma, Bell et al. (2010) at (74-)60, 57(-46) Ma, and N. Zhang et al. (2012), (82-)68(-45) My; ca 77.5 Ma is the age in Nicolas and Plunkett (2014; ?sampling), around 75.6-62.0 Ma (Nylinder et al. 2012: suppl.), (94-)80(-65) Ma in Wikström et al. (2015) and ca 90.8 Ma in Tank et al. (2015: Table S2).
Evolution: Divergence & Distribution. The diversification rate may have increased in Dipsacales at around (81.8-)75.8(-70.9) Ma (Magallón et al. 2018). The origin of Dipsacales was probably in the northern hemisphere (Beaulieu et al. 2013a). Major diversification within both Dipsacoideae and Valerianoideae - and hence a major part number-wise of diversification of the whole clade - is relatively recent, occurring within perhaps ca 10 Ma (Bell & Donoghue 2005a); diversification in Dipsacales as a whole has often seemed to increase as plants moved into new geographical areas, especially if these were mountainous (Moore & Donoghue 2007).
For a very detailed discussion of morphological evolution here, see Donoghue et al. (2003); Jacobs et al. (2010b) discussed the evolution of characters of fruit anatomy, and Beaulieu and O'Meara (2016) looked at links between fruit type and diversification - the story is more complicated than in Beaulieu and Dononghue (2013) .Xu et al. (2011) optimised some pollen characters on the tree. Howarth and Donoghue (2004, esp. 2005, 2008, 2009) and Howarth et al. (2011) noted intriguing correlations between gene duplications with possible neofunctionalisation of e.g. Cycloidea-like genes and changes in floral form in the order, with concomitant restriction of expression of some genes in the petaline whorl and resultant changes in the symmetry of the flowers. Nevertheless, direct connections to diversification rates remain to be established.
Genes & Genomes. For cytological variation, see Benko-Iseppon and Morowaetz (2000a); the two families are rather different. There is considerable variation in the presence of the mitochondrial coxII.i3 intron. Rates of molecular evolution vary considerably in Dipsacales, and this is usually associated with changes in the life style, woody plants usually having lower rates of change than herbaceous (Smith & Donoghue 2008).
Chemistry, Morphology, etc.. Anthocyanin variation does not allow a sharp distinction between Caprifoliaceae and Viburnaceae (Jordheim et al. 2006).
Involute vernation of the lamina is commoner in Viburnaceae than in Caprifoliaceae (Cullen 1978). For the morphology of the stipule-like structures and amplexicaul leaves in Caprifoliaceae and Viburnaceae see Weberling (1957); amplexicaul leaves, perhaps most common in the inflorescence, are scattered throughout the order. Split-lateral bundles and a girdling vascular trace occur in taxa with perfoliate leaves (e.g. Colomb 1887) as well as in the Morinoideae-Dipsacoideae area (see below). Glands at the base of the leaf in Sambucus and Viburnum may be vascularized (see also Colomb 1887).
Troll and Weberling (1966) and Weberling (1961, 1989) described the inflorescence structure of the woody Dipsacales in particular in considerable detail; inflorescence structure is notably complex in Caprifoliaceae, although Wagenitz and Laing (1984) suggest that most Caprifoliaceae s.l. lack terminal flowers. The morphology of the basic nectary type for the order is unclear. In Viburnum it is a disc-like structure on top of the inferior ovary, in Adoxa it consists of multicellular hairs on the corolla, and in Caprifoliaceae, unicellular hairs (Wagenitz & Laing 1984, Takhtajan 1997; Leins & Erbar 2010; Erbar 2014). For variation in floral anatomy, which clearly separates two groups of genera in the old Caprifoliaceae, see Wilkinson (1949 and references). Interestingly, some taxa in both families may have one or more ovary loculi infertile, the fertile loculus/i having but a single ovule, however, the reduced loculi may have two to six or so ovules. Particularly when there are only three carpels, their orientation is unclear (Sokoloff et al. 2018). For more on the inferior/superior ovary distinction in the asterid II clade, see e.g. the Asterales page.
Phylogeny. For the relationships of Dipsacales, see the asterid IIclade.
The order has strong support in D. Soltis et al. (2000: see also Wagenitz 1997; K. Bremer et al. 2001; c.f. A.P.G. 1998). The phylogeny here is based especially on work by Donoghue et al. (2001b, 2003), W.-H. Zhang et al. (2003), Davis et al. (2001), Bell (2003), Moore and Donoghue (2007) and C.-L. Xiang et al. (2019: plastome analyses). There are some (not major) disagreements with the phylogeny in Pyck and Smets (2001), while Judd et al. (1994) provide an early morphological analysis which gives a similar topology.
Previous Relationships. This grouping has often been recognised. Takhtajan (1997) included Dipsacales, Adoxales and Viburnales in his Dipsacanae, while Cronquist 1981) recognised four families in his Dipsacales.
Thanks. I am very grateful to Volker Bittrich for catching a number of mistakes on this page.
Includes Caprifoliaceae, Viburnaceae
Synonymy: Dipsacineae Shipunov - Adoxales Nakai, Caprifoliales Berchtold & J. Presl, Lonicerales T. Leibe, Sambucales Berchtold & J. Presl, Valerianales Berchtold & J. Presl, Viburnales Dumortier
VIBURNACEAE Rafinesque, nom. cons. - Back to Dipsacales
0-methylated flavonols only +; true tracheids?; pericyclic sheath poorly developed; (stomata paracytic); (petiole also with adaxial inverted bundles; closed C-shaped and with wing bundles); palisade mesophyll with arm cells; glandular hairs common; (buds not perulate); flowers small [<5 mm across]; K open, usu. very small, sepals with one trace, C rotate; pollen reticulate; G not entirely inferior, lateral and dorsal carpellary bundles free, ventral bundles move from axis to ovary septae, style short, stigma (long-)lobed, dry or wet; ovule 1/carpel, median; fruit drupaceous, stone compressed; seed single, exotestal cells palisade or not, not lignified; chromosomes large, 2.6-10 µm long, centromeres subterminal, interphase nucleus (semi)reticulate, euchromatic granules coarse, chromocentres large, distribution irregular, mitotoic condensing behaviour continuous, telomeric areas in particular of mitotic chromosomes condensed when cold; chloroplast ndhF gene inverted.
5 [list]/200 - two tribes below. North temperate, tropical montane, S.E. Australia, rare in Africa (map: from Hultén 1958, 1971; Meusel & Jäger 1992). 2 groups below. [Photos - Collection]
Age. Crown Viburnaceae are around (67-)60, 57(-50) Ma (Wikström et al. 2001), 85-70.5 Ma (Bell & Donoghue 2005a; see also Lens et al. 2016), or (54-)33, 31(-13) Ma (Bell et al. 2010).
1. Viburneae O. Berg
Shrubs (trees), deciduous or evergreen; hairs stellate and variants; lamina vernation involute or conduplicate (plicate), (aestivation convolute), secondary veins palmate to pinnate, (margin entire); (plant dioecious); G , odd member abaxial, 2 abort, nectary on top of G, epithelial; ovule with parietal tissue ca 1 cell across; (embryo sac bisporic [the chalazal dyad], 8-nucleate [Allium type]); endocarp with layers of fibres oriented parallel to each other, 1+ layers of sclereids; seed coat 21-100 µm across; endosperm ruminate, with crystals, cell walls ± thickened, embryo short; n = 9-11, 16, etc..
1/175. North temperate, tropical montane, but not in Africa. [Photo - Flower.]
Age. Crown-group Viburneae are ca 80 or ca 55 Ma, depending on calibration (Spriggs et al. 2015), some (63-)56(-50) Ma (Lens et al. 2016), or ca 89.3 Ma (H.-X. Wang et al. 2019); see cautionary comments by Beaulieu and O'Meara (2018).
Synonymy: Tinaceae Martynov
2. Adoxeae Dumortier
Shrubs or herbs; (cambium storied - Sambucus); (vessel elements with simple perforation plates); (calcium oxalate crystals 0 - Adoxeae); (nodes 1:1, 5:5), (+ split laterals - Sambucus); leaves compound (deeply lobed), (extrafloral nectaries +), (pseudostipules on leaf base); (flowers 3-4-merous); (lateral flowers of cymule with odd K abaxial); (K 2, 3 develop - Adoxa); anthers extrorse (8, monothecal); nectary on stigma, on C as multicellular hairs, or 0; G 1, [(4), 5], (all fertile), styles separate, stigmas capitate, dry [Ad]; integument ca 4 cells across, (ovules lacking parietal tissue - Adoxa); embryo sac tetrasporic, eight nucleate [Adoxa-type]; endocarp with three layers of cells, 2 layers of fibres, 1 layer of sclereids; (embryo long [Sambucus] or short); n = (8-)9.
4/23. Mainly north temperate, esp. China, also tropical montane (few in Africa), S.E. Australia.
Age. Crown-group Adoxeae are estimated to be around 35.5-32.5 Ma (Bell & Donoghue 2005a) or (66-)58.5(-49) Ma (Lens et al. 2016).
Synonymy: Adoxaceae E. Meyen, nom. cons., Sambucaceae Borkhausen
Evolution: Divergence & Distribution. The evolution and diversification of Viburnum has been much studied over the last twenty years or so. A number of deep branches within Viburnum are occupied by taxa that are currently tropical (ex section Megalotinus - polyphyletic), and the dioecious Malesian V. clemensiae is sister to the rest of the genus (Clement & Donoghue 2011; Clement et al. 2014; Spriggs et al. 2015). There may have been several shifts from evergreen leaves with elliptical blades and entire margins to deciduous leaves with more rounded blades and serrate margins, and there is also very substantial size variation (Schmerler et al. 2012), and leaves with very different morphologies are produced during the course of a single season's growth (preformation vs. neoformation); this heteroblasy can be quite strongly developed. Clement et al. (2014: no out-group) discuss the evolution of these and other such traits, while Spriggs et al. (2017) show that a) there has been quite frequent evolution of wider leaves, whether broadly ovate or trilobed, and b) the evolutionarily novel leaf forms are interpolated at the beginning of the season's growth - i.e. this kind of recurrent ontogeny does not recapitulate phylogeny... Jacobs et al. (2008) discuss variation in endocarp and seed.
Spriggs et al. (2015) suggested that diversification in Viburnum has been driven by extrinsic traits such as the occupation of mountainous regions (in South America and the eastern Himalayas) and shifts between cooler and warmer temperate forests rather than by intrinsic traits. They found similar increases in diversification as did Beaulieu and O'Meara (2016) in their rexamination of links between fruit type and diversification. The evolution of one-seeded fruits in Viburnum seems to be connected with increased speciation rates (Moore & Donoghue 2009), while Weber and Agrawal (2014) suggested that the evolution of extra-floral nectaries was associated with an increase in diversification rate.
For more details of possible apomorphies within the family, see Donoghue et al. (2001b, 2003) and Jacobs et al. (2010b: fruit and seed characters). Lens et al. (2016) looked at xylem evolution in the family as a whole with a focus on Viburnum.
Ecology & Physiology. Lens et al. (2016) look at xylem evolution in the family with a focus on Viburnum, which has tracheids. Interestingly, both Sambucus, which has vessels and the xylem of which differs greatly in other respects from that of Viburum, and Viburnum itself have similar climatic niches, at least from present-day distributions; perhaps these differences reflect past climates/events (Lens et al. 2016).
Plant-Animal Interactions. Extrafloral nectaries are notably common in tal; endosperm +, ?diploid, cellular, development (Weber & Keeler 2013).
Genes & Genomes. Cycloidea gene duplication has occurred within Viburnaceae, e.g. in Viburnum plicatum (Howarth et al. 2011), with its large, monosymmetric marginal flowers that serve as "petals" for the inflorescence.
Chemistry, Morphology, etc.. Tannin-secreting tubes in Sambucus are coenocytic and up to 32.8 cm long, they span the length of an entire internode, but do not extend into the nodal region (Zobel 1986). Viburnum may lack a fibrous pericyclic sheath and that of Sambucus is interrupted, however, that of Caprifoliaceae is better developed, and the cells in the latter are also longer, except those of Linnaea (Cooper 1939). Sambucus has crystal sand. In Adoxa the leaves at the bases of the rosettes and on the rhizomes are spiral and there are no extrafloral nectaries (c.f. Sambucus).
There is considerable floral variation in Sambucus and in particular Adoxa and its immediate relatives. Adoxa itself lacks any obvious corolline ring primordium and it has eight stamens with monothecate anthers, nectary on the petal lobes, weak endothelium, etc. (Erbar 1994). There are five semi-superior carpels with five styles/styluli (Leins 2000) and there are initially five stamen primordia. Reports of an amoeboid tapetum are incorrect (e.g. Wangenitz & Laing (1984). In the recently-described Sinadoxa the stamens appear to be divided into two half stamens, each with a separate filament and a monothecal anther; it is molecularly close to Adoxa (Liu et al. 2000). The flowers have three corolla lobes and a single carpel (Donoghue et al. (2003). In another curious genus, Tetradoxa, the half anthers are peltate, there are separate styles (= styluli), the ovary was described as being superior, and the sepals are persistent (Ying et al. 1993). F
The ovules in Sambucus may be attached to the axis below the level of insertion of the sepals (Roels & Smets 1994), although they are also shown as being attached slightly above (Thomé 1889, pl. 555). In both Sambucus and Adoxa there are small groups of meristematic cells above the ovules which may represent aborted ovules (Roels & Smets 1994).
For general information, see Hara (1983: Japanese taxa) and Backlund and Bittrich (2016), for some nodal anatomy, see Neubauer (1977a), arm cells, see Wagenitz and Laing (1984), for sympetaly, see Reidt and Leins (1994), for floral anatomy and morphology, Wilkinson (1949 and references), for nectaries, see Vogel (1997), for some embryology, see Lagerberg (1909: Adoxa), Horne (1914) and Moissl (1941), and for fruits and seeds, see Jacobs et al. (2010b).
Phylogeny. For a phylogeny of Viburnum, see Winkworth and Donoghue (2004, 2005), Schmerler et al. (2012), Clement et al. (2014), Eaton et al. (2017) and C.-L. Xiang et al. (2019: plastome analyses).
CAPRIFOLIACEAE Jussieu, nom. cons. - Back to Dipsacales
Bark papery-flaky; O-methylated flavones, flavonols +; cork cambium deep-seated; wood often fluorescing; (pith diaphragms +); pericyclic fibres moderately developed; inflorescence axis racemose, (branched), with ultimate units cymes; flowers rather weakly monosymmetric [K ± polysymmetric]; K shortly connate, C 2 + 3, tubular, main petal veins laterally connected [transpetalar veins], nectary on C, of unicellular hairs, with irregularly rugose surface; anthers sagittate; tapetum amoeboid; pollen grains spheroid, echinate; ovary inferior, constricted below K, lateral and dorsal carpellary bundles 0, ventral bundles in axis, stigma capitate, wet; embryo small; chromosomes small, 0.6-4.2 µm long, centromeres median or submedian, no C-banding, interphase nucleus semireticulate, euchromatic granules fine, chromocentres small, regular or polarized, mitotic condensing behaviour (continuous to) proximal-early, no condensation of mitotic chromosomes when cold; plastid transmission biparental; duplication of dipsCYC2 and dipsCYC3 genes, horizontal transfer of mitochondrial rps11 gene [?Morinoideae and upwards in the tree].
31 [list: as subfamilies]/890 - 7 groups below. Largely temperate/warm temperate in the northern hemisphere, some montane tropics (exp. Valerianoideae), but neither the Antipodes nor the Pacific.
Age. An estimate of the crown-group age is ca 86-68 Ma (Bell & Donoghue 2005a); K. Bremer et al. (2004a: c.f. topology, Lonicera sister to rest) suggested an age of around 75 Ma, Bell et al. (2010: again, c.f. topology) an age of (40-)37, 36(-35) Ma, Wikström et al. (2015) an age of (76-)62(-49) Ma, while (82.3-)66.1(-50.8) Ma is the estimate in Tank and Olmstead (2017); on the other hand, H.-X. Wang et al. (2019) suggest an age of (119.5-)100.5(-67.4) Ma.
Evolution: Divergence & Distribution. Endress (2011a) suggested that monosymmetric flowers might be a key innovation here, but, as noted above, understanding diversification in Dipsacales is not simple. For some characters in the group, see Weberling (1957), Verlaque (1984).
Genes & Genomes. Biparental plastid transmission is reported for most of the major clades here (Corriveaux & Coleman 1988; Q. Zhang et al. 2003). A more detailed study suggests strongly that the feature is an apomorphy here (Y. Hu et al. 2008).
Chemistry, Morphology, etc.. The glandular leaf teeth have a main vein plus two accessory veins, or one accessory vein proceeding above the tooth.
For paired flowers as inflorescence units, esp. in Linnaeoideae and Zabelia, see Landrein and Prenner (2013). Transpetal veins, branch veins linking adjacent median veins, occur in the upper part of the corolla in at least Diervilla, Kolkwitzia and some Valerianoideae and Dipsacoideae (Gustafsson 1995). The calyx often persists, characteristically remaining small and perched on top of the fruit, which may be narrowed towards the apex.
Some information is taken from Hofmann and Göttmann (1990), Backlund and Pyck (1998: general), Benko-Iseppon and Morawetz (2000a), Backlund and Donoghue (1996), Donoghue et al. (2001b), Bell et al. (2001), Jacobs et al. (2011), and Hofmann and Bittrich (2016), all general, Nilova (2001: bark anatomy), Magócsy-Dietz (1899: pith diaphragms, woody members only) Carlquist (1982) and Ogata (1988, 1991: wood anatomy), and Backlund and Nilsson (1997: pollen).
Phylogeny. The position of Heptacodium was initially somewhat uncertain (Pyck & Smets 2000, 2001), although there were suggestions that it be included in Caprifolioideae (e.g. Donoghue et al. 2001a, 2003; Soltis et al. 2011 [support weak]; Landrein et al. 2012). Its flowers have several bracteoles and only one of the three carpels develops, the fruit having a single seed - not features characteristic of Caprifolioideae. It may be a hybrid between members of Caprifolioideae and Linnaeoideae (Z.-Y. Zhang et al. 2002; Landrein & Prenner 2013), while C.-L. Xiang et al. (2019) and H.-X. Wang et al. (2019), focussing on plastomes as they did, were unable to clarify the story.
Recently much attention has been paid to the circumscription of Linnaeoideae. Jacobs et al. (2010c) found that Zabelia (ex Abelia) might be in the [Morinoideae [Dipsacoideae + Valerianoideae] clade, although support was only moderate (see also Soltis et al. 2011). Pollen morphology is perhaps consistent with this position (Jacobs et al. 2010d), while Landrein and Prenner (2013) suggested that Zabelia and Diabelia (Linnaeoideae) had similar "primitive" (their scare quotes) inflorescences. In some analyses Zabelia and Morinoideae formed a clade, although support for this was only moderate (Jacobs et al. 2011). Landrein et al. (2012: useful table of characters, topology of some trees difficult to interpret) suggested that Zabelia was sister to the whole [Morinoideae [Valerianoideae + Dipsacoideae]] clade; see also H.-F. Wang et al. (2015), while relationships in Z.-D. Chen et al. (2016: support weak) are [Morinoideae [Zabelia + The Rest]]. Soltis et al. (2007a) found that the position of Valerianoideae was unstable in some analyses; analyses of mitochondrial data being perhaps particularly challenging (Winkworth et al. 2008b). Morinoideae migrated basally in an analysis by Beaulieu et al. (2013a: only 4 genes), and they were sister to Linnaeoideae in Wikström et al. (2015: c.f. taxon sampling). Recently, C.-L. Xiang et al. (2019) carried out analyses of complete plastomes of 32 species in this clade. By and large the relationships that they found are similar to those below, but with two main differences: They recovered a clade [Zabelia + Morinoideae], and it was part of a tritomy that also involved Linnaeoideae and [Dipsacoideae + Valerianoideae]. Finally, in the plastome analysis of H.-X. Wang et al. (2019), strong support was found for the relationships [[Linnaeoideae [Morinoideae + Zabelia]] [Dipsacoideae + Valerianoideae]] - now the nuclear element has to be added.
Classification. The circumscription and number of families in the area of the Caprifoliaceae and Dipsacaceae sensu versions 12 and before (see also A.P.G. II 2003) was the direct result of deciding to maintain the well known Dipsacaceae and Valerianaceae in their old circumscriptions - the small clades resulting from the break-up of the old, broadly-circumscribed and strongly paraphyletic Caprifoliaceae had to be accounted for (Backlund & Bremer 1997; Backlund & Pyck 1998; c.f. Stevens 1998). The whole lot are usefully be combined in a Caprifoliaceae s.l. (see A.P.G. III 2009), since similarities between the families are considerable and differences are mostly slight, however, C.-L. Xiang et al. (2019) elect to recognise families. There is still (as of xi.2019) some uncertainty about the backbone relationships of the tree (see above), furthermore, because of the possible hybrid origin of Heptacodium - Caprifolioideae x Linnaeoideae - it is characterized separately below.
1. Diervilloideae Rafinesque
Deciduous shrubs; (successive periderms +); lamina vernation involute [Weigela]; (K monosymmetric); nectary at base of C; filaments hairy; pollen pororate, membrane granulose; G ; ovules many/carpel, ?marginal; fruit beaked, dehiscing laterally, septicidal; (seeds winged); n = 18.
1-2/16. East Asia, S.E. U.S.A. (map: from Li 1952, approximate).[Photo - Flowers © M. Clayton]
Age. For the early Caenozoic fossil history of Weigela, see Manchester et al. (2009).
Chemistry, Morphology, etc.. The large nectary at the base of the corolla in Diervilla (perhaps including Weigela) is a swelling covered by nectar-secreting hairs similar to those in Lonicera, etc. Only one carpel may be fertile, and in some species there may be an "epicalyx" (see below) immediately below the ovary.
Phylogeny. For relationships in Diervilloideae, see Kim and Kim (1999). Weigela maximowiczii is of uncertain position at the base of the tree, while W. middendorffiana is weakly supported as sister to Diervilla.
Synonymy: Diervillaceae Pyck
[Caprifolioideae [Linnaeoideae [Zabelia, Morinoideae [Valerianoideae + Dipsacoideae]]]]: inflorescence lacking terminal flower.
Age. The age of this node is ca 84-66.5 Ma (Bell & Donoghue 2005a); Wikström et al. (2001: c.f. scrambled topology) suggested an age of (62-)58, 54(-50) Ma, while an age of ca 40.7 Ma is suggested by Naumann et al. (2013).
2. Caprifolioideae Eaton
Evergreen or deciduous hrubs (trees); lamina vernation supervolute or conduplicate, margins entire, secondary veinspinnate to palmate; K small; A (4-)5, filaments glabrous; G [(2-)3-5(-10)], (1 or 2 sterile), (G opposite C - Leycesteria); ovules 1-8/carpel; fruit baccate [Lonicera] or drupaceous [Symphoricarpus]; testa (multiplicative), (± compressed-parenchymatous)/(exotesta thick-walled); n = 9; deletion in the chloroplast gene clpP.
5/220: Lonicera (180). Mostly N. temperate, esp. East Asia and E. North America (map: see Hultén 1971; Hultén & Fries 1986; Meusel et al. 1992). [Photo - Flower.]
Age. The age of crown Caprifolioideae is ca 79-64 Ma (Bell & Donoghue 2005a: note position of Heptacodium). Other estimates of their age are 51-36 Ma (Smith 2009), (66.4-)47.9(-35.9) Ma (Bell & Gonzalez 2019) or almost double, (115.6-)93.9(-76.2) ma (H.-X. Wang et al. 2019).
Evolution: Divergence & Distribution. For additional ages in this clade, see Bell and Gonzalez (2019). Diversification possibly began in Asia (Smith 2009), and Beaulieu and O'Meara (2016: hidden rates shift) suggest there may have been an increase in the diversification rate.
Chemistry, Morphology, etc.. There is no stem endodermis.
Landrein and Prenner (2016) suggest that flowers of Lonicera subgenus Periclymenium have some kind of nectar disc. Triosteum seems to lack dorsal carpellary bundles only and has apotropous ovules (Wilkinson 1949). The ovule of Abelia tyaihyoni has a massive raphal region, a long micropyle, no endothelium, a multiplicative testa and a distinctive embryo sac (Ghimire et al. 2018); not all these features are in the characterization above. The drupes of Symphoricarpus have a thick outer layer of narrow, vertical fibres and a crossing inner layer of horizontal fibres; the seed coat itself is crushed (ref?).
For the morphology of Japanese taxa, see Hara (1983).
Phylogeny. Relationships in Caprifolioideae - [Heptacodium [Triosteum *[Lonicera [Leycesteria + Symphoricarpos]]]] - are suggested by Theis et al. (2008); the node with the asterisk has a poor posterior probability, but a good bootstrap value. Bell and Gonzalez (2019) looked at relationships in Symphoricarpus where the Asian S. sinensis was sister to the rest of the genus (North American); C.-L. Xiang et al. (2019) found that the genus was poly/paraphyletic.
Synonymy: Loniceraceae Vest
Deciduous shrub; cork mid-cortical; vessel elements with simple perforation plates; fibres in cortex; lamina tripli-nerved, vernation involute; inflorescences with flowers in whorls of 6; 2 carpels abort, 1 fertile; fertile ovule 1/carpel; fruit a cypsela; n = 14, centromeres submedian and (sub)terminal.
1/1: Heptacodium miconioides. E. China, uncommon (Map: FoC vol. 19. 2011).
Chemistry, Morphology, etc.. For cytology, etc., see Z.-Y. Zhang et al. (2001).
[Linnaeoideae [Zabelia, Morinoideae [Valerianoideae + Dipsacoideae]]]: epicalyx + [from aborted flowers, etc.]; A 4, didynamous staminode 0; 1 carpel fertile, 2 carpels abort; ovule single (-7 in sterile loculi); fruit a cypsela; seed coat flattened, exotesta not lignified.
Age. Magallón and Castillo (2009: note topology) offer an estimate of ca 59 Ma for the age of this node, Bell and Donoghue 2005) an age of 71.5-49.5 Ma, and H.-X. Wang et al. (2019) an age of (99.2-)78.9(-60) Ma.
Evolution: Divergence & Distribution. For fruit characters perhaps apomorphic at this level, see Jacobs et al. (2010b, 2011).
Chemistry, Morphology, etc.. The morphological nature of structures variously described as supernumerary bracts, bracteoles, epicalyx, and involucel that are associated with flowers in this clade has occasioned much and complex discussion - see Troll and Weberling (1966), Weberling (1992), Roels and Smets (1996), Donoghue et al. (2003), Pyck and Smets (2004), Landrein et al. (2012), Landrein and Prenner (2013) and H.-F. Wang et al. (2015) . The epicalyx is sometimes described as consisting of four fused bracts and having nothing to do with bracteoles (Hofmann & Göttmann 1990; Mayer 1998); the individual flower that it surrounds may then be the terminal flower of a partial thyrsoid inflorescence (esp. Roels & Smets 1996; see also Landrein et al. 2012, Landrein & Prenner 2013). But perhaps some of the bracts presumed to signify "things" like aborted flowers, missing inflorescence branches, etc, may simply be developmentally duplicated structures... In the characterisations below, the particular condition of the epicalyx for each subfamily is described in general terms; what the epicalyx might "be" morphologically is a separate issue.
Landrein and Prenner (2016) describe the floral nectaries of this group in detail. Where there are only two stamens, it is usually the adaxial pair that persists. Of the three carpels, it is an adaxial lateral carpel that remains fertile (Donoghue et al. 2003). If the flower has four carpels, two are fertile (Landrein et al. 2012).
3. Linnaeoideae Rafinesque
Deciduous (evergreen) shrubs (prostrate), (plant ± herbaceous); (stomata paracytic - Abelia); lamina vernation supervolute(-curved); epicalyx with 4 or 6 members, accrescent or not; (K foliaceous), nectariferous petal abaxial, bulging, (nectary as 1-3 lines of compact hairs between abaxial filaments); filaments hairy; (pollen 3-4-colpate, surface spiny - Abelia); (G , 2 fertile - Dipelta), stigma dry; ovule ?apotropous, (obturator + - Abelia); embryo sac (bisporic [the chalazal dyad], 8-nucleate [Allium type] - Abelia); K and/or bracts often modified, enlarged, in fruit; fruits dorsiventrally compressed; ?embryo length [small - Abelia]; n = 8, 9.
6/32. Circumboreal (Linnaea), Mexico (Abelia), China to Japan (five genera), Mexico (map [Zabelia not included]: from Hultén & Fries 1986; Meusel & Jäger 1992; Villareal-Quintanilla 2013; see also H.-F. Wang et al. 2015). [Photo - Habit, Flower.]
Age. The crown-group age of Linnaeoideae has been estimated at 48.5-37.5 Ma (Bell & Donoghue 2005a), (60.2-)50.9(-42.8) Ma (H.-F. Wang et al. 2015) or (65.3-)52.2(-40.6) ma (H.-X. Wang et al. 2019).
Evolution: Divergence & Distribution. For distinctive late Eocene fruits (Diplodipelta, ca 37 My) assignable to Linnaeoideae and their implications for biogeography and evolution, see Manchester and Donoghue (1995); the genus may be sister to Dipelta. H.-F. Wang et al. (2015) offer a somewhat different interpretation, suggesting similarities between the fossil and Diabelia or perhaps Kolkwitzia, but both are also Linnaeoideae. Manchester et al. (2009) discussed the fossil distribution of Dipelta, which is known from Eocene/Oligocene rocks in southern England.
H.-F. Wang et al. (2015, q.v. for dates) discussed the biogeography and evolution of the subfamily in detail.
Pollination Biology & Seed Dispersal. Wind-dispersed fruits predominate in the subfamily (H.-F. Wang et al. 2015).
Chemistry, Morphology, etc.. For details of inflorescence morphology, see Landrein and Prenner (2013), although they did not interpret the variation that they found in the context of phylogeny.
For general information, see Hara (1983), Landrein et al. (2012) and Hofmann and Bittrich (2016), all general, also Villarreal-Quintanilla et al. (2014: Abelia).
Phylogeny. For relationships, see Jacobs et al. (2010c, 2011), Landrein et al. (2012) and C.-L. Xiang et al. (2019); the basic phylogenetic structure may be [Linnaea [Vesalea + The Rest]], but H.-F. Wang et al. (2015) found quite good support for the relationships [[Linnaea + Vesalea] The Rest].
Classification. For generic limits and groupings, see Landrein (2010) and Landrein et al. (2012) and for characterisations of the genera, see H.-F. Wang et al. (2015).
Synonymy: Linnaeaceae Backlund
[[Zabelia + Morinoideae] [Valerianoideae + Dipsacoideae]]: vessel elements with simple perforation plates; petioles connate basally/leaves amplexicaul; nectary at base of C.
Evolution: Divergence & Distribution. The placement of Zabelia will affect character optimizations; below there is the option of following C.-L. Xiang et al. (2019). I have suggested some characters the whole group has in common; given that the petioles of Zabelia are basally connate, I would not be surprised to find that its nodal vascular architecture was like that of other members of this group. However, Zabelia is poorly known, and I have listed characters for both [Zabelia + Morinoideae] and [Morinoideae [Valerianoideae + Dipsacoideae]] separately.
For relationships suggested by some morphological characters, see Peng et al. (1995). For a comparison of Morinoideae, Valerianoideae and Dipsacoideae, see Cannon and Cannon (1984), and for tables of differences between Morinoideae and Dipsacoideae, see Vijayaraghavan and Sarveshwari (1968), Cronquist (1981), Cannon and Cannon (1984) and Johri et al. (1992).
Chemistry, Morphology, etc.. For nodal flank-bridges, see Neubauer (1979); it is as if two bundles on each side form split laterals, and one branch from each bundle fuses, so forming the bridging bundle. Bundles innervating the petiole arise from the bridging bundle, except in Morina.
For pollen size, see Xu et al. (2011), for endocinguli, see Jacobs et al. (2011) and Landrein et al. (2012).
[Zabelia + Morinoideae]: pollen grains smooth, with endocinguli [extra thickened layer of pollen wall].
Age. This clade is (80.6-)48.2(-24.4) Ma (H.-X. Wang et al. 2019).
4. Zabelia Makino
Shrubs; ?chemistry; wood ring-porous, aggregate rays +; twigs with six longitudinal grooves; lamina margin entire to dentate, petiole bases swollen, enclosing axillary bud; epicalyx with 6 or 14 members, not accrescent; nectary pouched abaxially, with four lines of compact hairs, bottom half of hairs smooth; stigma mucilaginous; ovule?; seed?; embryo small; n = 9 [most polyploid].
1/4-6: Central Asia (Afganistan, Tian Shan) to the Far East (Japan) (Map: from Meusel & Jäger 1992; FoC vol. 19. 2011).
Chemistry, Morphology, etc.. For general information, see Hara (1983), Landrein et al. (2012), Landrein and Prenner (2013) and Hofmann and Bittrich (2016).
[Morinoideae [Valerianoideae + Dipsacoideae]]: perennial rosette herbs with taproot; monoterpenoids, cathecolic tannins, alkaloids +; stele with vascular bundles separate [?here]; libriform fibres +; nodes 5:5; vascular flank-bridge in stem between lateral bundles; buds not perulate; filaments glabrous, anthers dorsifixed; pollen "large"; G with sterile loculi much reduced; ovule apical, integument massive, endothelium prominent, with crystal layer; chalazal nuclei variously proliferating; exotesta not thickened; endosperm copious, embryo large; distinctive expansion of the chloroplast inverted repeat.
Age. The age of this node is around 69-48 Ma (Bell & Donoghue 2005a: Zabelia not included).
Phylogeny. For relationships suggested by some morphological characters, see Peng et al. (1995).
For embryology, see Johri et al. (1991), for a general comparison, see Hofmann and Göttmann (1990).
Iridoids 0; stems hollow; lamina vernation involute, margins spinose to pinnatifid (entire), secondary veins palmate; inflorescence of sessile cymes [verticels], epicalyx 12-ribbed; flowers strongly monosymmetric; K 4, monosymmetric; A pairs inserted at different heights on the C tube (A 2, adaxial, + 2 staminodes); pollen binucleate, (turret-like triporate), exine columellae reduced, intine-covered tubular extrusions; ovule with integument 14-18 cells across, hypostase +; embryo sac with chalazal cells producing multicellular structures; integument multiplicative, not vascularized, outer layer only persisting; endosperm ruminate; n = 17, small [0.7-1.5 μm long]; duplication of dipsCYC2 and dipsCYC3 genes.
2-3/13. Balkans to China (map: see Cannon & Cannon 1984). [Photo - Morina Inflorescence, Acanthocalyx Inflorescence.]
Age. Crown-group Morinoideae are estimated to be around 46-31 Ma (Bell & Donoghue 2005a).
Evolution: Divergence & Distribution. Bell and Donoghue (2003) discuss biogeographic relationships within the clade.
Chemistry, Morphology, etc.. Remarkable intine-covered structures that look like pollen tubes are produced in all taxa before pollen germination (Blackmore & Cannon 1983), and sometimes also in also Dipsacoideae (Hesse et al. 2009b). The integument is 14-18 cells across when the embryo sac is mature, becoming ca 25 cells across later (Vijayaraghavan & Sarveshwari 1968).
There seems to be total confusion as to the nature of the tapetum of Morina: Vijayaraghavan and Sarveshwari (1968) describe it as being polyploid, multinuclear and secretory, Kamelina (1983) as cellular, binuclear and glandular, and Johri et al. (1992) as being amoeboid (and that of Dipsacoideae as being glandular).
For embryology, see Vijayaraghavan and Sarveshwari (1968: Morina longifolia only), for pollen, Verlaque (1983), and for general information, Cannon and Cannon (1984: monograph) and Hofmann and Bittrich (2016).
Phylogeny. Acanthocalyx is sister to the rest of the family, Morina may be paraphyletic (Bell & Donoghue 2003).
Synonymy: Morinaceae Rafinesque
[Dipsacoideae + Valerianoideae]: saccharose +, quercetin 0; stem with endodermis; (nodes 5 or more:5 or more); leaves simple to ± pinnate, lamina vernation conduplicate, (margins entire); flowers rather small; transpetalar vein single, strong; A ± equal in length; tapetal cells 4 or more nucleate [?level]; pollen with prominent and branched exine columellae; stigma dry; embryo sac with 2-4-nucleate chalazal cells; embryo chlorophyllous; centromeres metacentric to subtelocentric, no C bands.
Age. The age of this node is estimated to be ca 62.5-44.5 Ma (Bell & Donoghue 2005a), (41-)31(-22) Ma (Wikström et al. 2015), or (92.4-)70.2(-51.2) Ma (H.-X. Wang et al. 2019).
6. Dipsacoideae Eaton
Starch almost 0; (stomata anisocytic); lateral abaxial C lobes overlapping adaxial lobes; ovule apotropous, micropyle very long, hypostase +; chalazal nuclei polyploid; stigma entire or 2-lobed.
11/290. Eurasia, Africa, esp. Mediterranean region, to Malesia.
Age. Crown-group Dipsacoideae can be dated to ca 52.5-39.5 Ma (Bell & Donoghue 2005a) or ca 57 Ma (H.-X. Wang et al. 2019).
6a. Triplostegieae Höck
Perennial herb; valepotriate-type iridoids +; fusiform tap root, rhizomes +; glandular hairs +; outer epicalyx 4-lobed, inner epicalyx 8-ribbed; C ± polysymmetric, (4-)5-lobed; pollen aperture with a halo, colpus granulose, surface spiny; stigma capitate; capitate-glandular outer epicalyx persistent, the tips hooked; "achenes 8-ribbed"; endosperm slight; n = 9.
1/?1: Triplostegia grandiflora. Southeast Asia, Celebes, Papua New Guinea (map: from Niu et al. 2019).
Synonymy: Triplostegiaceae Airy Shaw
6b. Dipsaceae Reichenbach
Perennial (annual) herbs, (shrubby); (vessel elements with scalariform perforation plates); (cork cambium subepidermal - Knautia); inflorescence a capitulum, (ray flowers +), involucral bracts + (0); epicalyx single, 8-ribbed; C (with 4 lobes), (± polysymmetric); A (2-3); (pollen 3-porate); G , ?1 aborts; ovule with integument 10-15 cells across; fruit with calycine awns or bristles (K caducous); endosperm +; n = 5, 7-9(-10).
10/290: Cephalaria (80), Knautia (60), Lomelosia (>50), Scabiosa (>30). Eurasia, Africa, esp. Mediterranean region. [Photo - Habit, Inflorescence, Flower.]
Synonymy: Dipsacaceae, Juss., nom. cons., Scabiosaceae Martinov
Evolution: Divergence & Distribution. Beaulieu and O'Meara (2016: hidden rates shift) suggest that there may have been an increase in the rate of diversification of this clade (excluding Triplostegia).
For large-scale migration within Scabiosa, including north to south movement in Africa, see Carlson et al. (2012).
As Pyck and Smets (2004) note, the clade [Triplostegia + Valerianoideae] has valepotriate-type iridoids, a pollen aperture with a halo, a granulose colpus, and also endosperm reduction in common, and possibly even epicalyx/bracteole similarities. Avino et al. (2009) thought that Triplostegia was sister to [Valerianoideae + Dipsacoideae], and used this topology in their character state reconstruction. Indeed, where Triplostegia ends up will substantially affect apomorphy positions, and the characters that Triplostegia and Valerianoideae have in common may be either parallelisms, or apomorphies for a larger clade, but with reversals.
Seed Dispersal. Caputo et al. (2004a) examined the evolution of seed dispersal syndromes. The well-developed epicalyx (for details, see also Mayer 2016) suggests that the fruits are often wind-dispersed, but myrmecochory may occur in almost half of the subfamily, especially in the large genera Knautia and Scabiosa (Lengyel et al. 2009, 2010).
Genes & Genomes. Genome size increased towarsd the periphery of the range of Knautia, although why was unclear; the distribution of polyploidy, etc., was also studied (Frajman et al. 2015).
Chemistry, Morphology, etc.. The cork of Knautia may be superficial (Metcalfe & Chalk 1950).
Centranthus has monosymmetrical 1:4 flowers - very unusual given that the basic floral development in Dipsacales is that common in eudicots - it can also be thought of as being obliquely symmetrical - or asymmetrical (see Donoghue & Ree 2000).
For embryology, see Kamelina (1983), and for fruit, see Verlaque (1977), for general information, see Verlaque (1984, 1985, 1986: Scabiosa), Niu et al. (2019: Triplostegia) and especially Mayer (2016).
Phylogeny. Triplostegia, which has a double epicalyx and valepotriates, seems best assigned to Dipsacoideae (e.g. 100% support in a 30 taxon-5 gene analysis - Davis et al. 2001; see also Bell & Donoghue 2000, 2005a; W.-H. Zhang et al. 2001; Bell 2004; Soltis et al. 2011; C.-L. Xiang et al. 2019). However, Pyck and Smets (2004) showed that although a two-gene analysis places Triplostegia in this position, morphological data alone and when combined with the molecular data place it sister to Valerianoideae.
The position of Triplostegia aside, Pterocephalodes, a recent segregate from Pterocephalus (Mayer & Ehrendorfer 2000), and Bassecoia together form a clade that is sister to the remainder of the family (Avino et al. 2009; Carlson et al. 2009). For other phylogenetic studies, see Caputo et al. (2004a) and Carlson et al. (2012: Scabiosa); Resetnik et al. (2014) look at relationships between diploid species of Knautia.
Classification. Mayer and Ehrendorfer (2013: much morphology) and Mayer (2016) provide a very detailed classification of the subfamily (as Dipsacaceae).
7. Valerianoideae Rafinesque
(Annual herbs); foetid monoterpenoids and sesquiterpenoids, valepotriate-type iridoids + (0 - Patrinieae); root (swollen), (peridem superficial - Valeriana, pericyclic - Centranthus, etc.); (vessel elemenst with scaliform perforation plates), (tracheids + - Patrinia); stem often hollow; leaves (bijugate, 2-ranked)), (bases not sheathing); (plant dioecious); flowers small, corolla ± polysymmetric, bracteoles +, epicalyx 0; K (0), abaxial C basally spurred or not; A (1-)3(4-5), (anthers bisporangiate, bithecate - South American Valeriana subg. Phyllactic); pollen colp(oroid)ate, nexine adjacent to colpus disrupted; G (lacking sterile loculi); K usu. accrescent; testa 1-layered; endosperm 0 (?+ - Patrinia); n = (7-)8(9-13).
5/375: Valeriana (270), Valerianella (65). N. temperate, especially Mediterranean, and Andean South America (half the subfamily) (map: from Hultén 1958; Meusel et al. 1978). [Photo - Habit, Flower, Flower.]
Age. Crown-group Valerianoideae may be 56-34.5 Ma (Bell & Donoghue 2005a), ca 50 Ma (Moore & Donoghue 2007) or (54-)42(-33) Ma (Beaulieu et al. (2013a: 95% HPD).
Synonymy: Valerianaceae Batsch
Evolution: Divergence & Distribution. Beaulieu and O'Meara (2016: hidden rates shift) thought that the rate of diversification may have increased here in the clade above Valeriana celtica (see below). There were around four migrations of Valerianoideae to South America about (20-)15.7(-12) Ma (Bell et al. 2012a), and diversification in the Andean paramo, where ca 1/7 of the subfamily grow, happened less than 5 Ma (Bell & Donoghue 2005b). Further diversification - ca 1/6 of the species - occurred south of 33oS (Kutschker & Morone 2012).
Seed Dispersal. For fruit and seed evolution, see Jacobs et al. (2010a: Nardostachys not included); the fruits are very variable in their morphology. A pappus is common, but a variety of different structures assist in wind dispersal, there can be hooks, elaiosomes, or the fruit may even be explosive (Erikson 1989; Weberling & Bittrich 2016).
Chemistry, Morphology, etc.. Valepotriates are triesters of route I secoiridoids; for their distribution - they are also found in Nardostachys and Triplostegia - see Backlund and Moritz (1998). The anatomy of some of the high-Andean Valerianoideae will repay further investigation (e.g. see Weberling & Uhlarz); they may have unilacunar nodes and distinctive secondary vascular tissue, lack girdling bundles, etc..
The sequence of appearance of parts in the flower of Valeriana officinalis is A, C, K, G (Sattler 1973). The calyx in Patrinia and Nardostachys is polysymmetric and persistent but not much accrescent. Evident sterile loculi, a well developed calyx, an androecium with either four or five stamens, presence of endosperm, etc., are likely to be plesiomorphic here. The corolla tube of Centranthus is divided vertically into two by a septum. The extra "bracteole" of Patrinia may be an interpolated structure that develops into a fruit wing (Hofmann & Göttmann 1990).
For general information, see Eriksen (1989) and Weberling and Bittrich (2016), for anatomy, see Vidal (1903), and for ovule morphology (no vascular tissue?), see Guignard (1893).
Phylogeny. Patrinia may be sister to the rest of the subfamily (Pyck 2002), with Nardostachys sister to the remaining taxa (Bell 2004; Bell & Donoghue 2005a, b: both with very strong support), or the two together may form a well-supported clade sister to other Valerianoideae (Hidalgo et al. 2004); the former topology is more likely. Valeriana celtica, Valerianella and Centranthus may be successively sister to Valeriana (Bell & Donoghue 2005b, for which see for further details); Valeriana may be para- or polyphyletic (Hidalgo et al. 2004). For other phylogenies, see Bell (2004) and Bell et al. (2015).
Classification. The limits of Valeriana are unclear (Hidalgo et al. 2004; discussion in Eriksen 1989: infrageneric classification; Weberling & Bittrich 2016).