Plant a shrub or tree; true roots +, origin endogeneous, root cap +, apex multicellular; endodermis +; shoot apical meristem multicellular; lateral meristems +, cork cambium producing cork abaxially, vascular cambium producing phloem abaxially and xylem adaxially; lamina with mean venation density 1.8 mm/mm2 (to 5 mm/mm2).
EXTANT SEED PLANTS/SPERMATOPHYTA
Plant woody, evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins derived from (some) sinapyl and particularly coniferyl alcohols, thus containing p-hydroxyphenyl and guaiacyl lignin units, so no Maüle reaction; root xylem exarch, cork cambium deep seated; arbuscular mycorrhizae +; shoot apical meristem interface specific plasmodesmatal network; stem with vascular tissue around central pith [eustele], vascular bundles with interfascicular tissue, ectophloic, endodermis 0, xylem endarch; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; stem cork cambium superficial; branches exogenous; leaves with single trace from vascular sympodium ["nodes 1:1"]; vascular bundles collateral [stem: phloem external; leaf: phloem abaxial]; stomata morphology?, pore opening controlled by abscisic acid; leaves with petiole and lamina, spiral, development basipetal, blade simple; axillary buds +, not associated with all leaves; prophylls two, lateral; plant heterosporous, sporangia borne on sporophylls; microsporophylls aggregated in indeterminate cones/strobili; true pollen +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, parietal tissue 2+ cells across, megaspore tetrad tetrahedral, only one megaspore develops, megasporangium indehiscent; male gametophyte development first endo- then exosporic, tube developing from distal end of grain, to ca 2 mm from receptive surface to egg, gametes two, developing after pollination, with cell walls, flagellae numerous; ovules increasing considerably in size between pollination and fertilization, female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large" [ca 8 mm3], but not much bigger than ovule, with morphological dormancy; embryo cellular ab initio, endoscopic, plane of first cleavage of zygote transverse, suspensor +, short-minute, embryo straight, shoot and root at opposite ends [allorrhizic], white, cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], nrDNA with 5.8S and 5S rDNA in separate clusters; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.
Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, non-hydrolysable tannins, quercetin and/or kaempferol +, apigenin and/or luteolin scattered, [cyanogenesis in ANITA grade?], S [syringyl] lignin units common, positive Maüle reaction [syringyl:guaiacyl ratio more than 2-2.5:1], and hemicelluloses as xyloglucans; root apical meristem intermediate-open; root vascular tissue oligarch [di- to pentarch], lateral roots arise opposite or immediately to the side of [when diarch] xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0, exodermis +; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, associated gelatinous fibres [g-fibres] with innermost layer of secondary cell wall rich in cellulose and poor in lignin; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, cytoplasm not occluding pores of sieve plate, companion cell and sieve tube from same mother cell; sugar transport in phloem passive; nodes unilacunar [1:?]; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, secondary veins pinnate, overall growth ± diffuse, venation hierarchical, fine venation reticulate, veins (1.7-)4.1(-5.7) mm/mm2, endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, ± haplomorphic, parts spiral [esp. the A], free, numbers unstable, development in general centripetal; P not sharply differentiated, with a single trace, outer members not enclosing the rest of the bud, often smaller than inner members; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], ± embedded in the filament, with at least outer secondary parietal cells dividing, each theca dehiscing longitudinally, endothecium +, endothecial cells elongated at right angles to long axis of anther; tapetum glandular, cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellar, endexine thin, compact, lamellate only in the apertural regions; nectary 0; G superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry [not secretory]; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across [crassinucellate], nucellar cap?; megasporocyte single, hypodermal, megaspore tetrad linear, functional megaspore chalazal, lacking sporopollenin and cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; ovule not increasing in size between pollination and fertilization; pollen binucleate at dispersal, male gametophyte trinucleate, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing between cells, growth rate 20-20,000 µm/hour, outer wall pectic, inner wall callose, with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametes lacking cell walls, flagellae 0, double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; seed exotestal, becoming much larger than ovule at time of fertilization; endosperm diploid, cellular [micropylar and chalazal domains develop differently, first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous; embryogenesis cellular; germination hypogeal, seedlings/young plants sympodial; Arabidopsis-type telomeres [(TTTAGGG)n]; 2C genome size 1-8.2 pg [1 pg = 109 base pairs], whole genome duplication, ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, paleo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]].
[NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]]: vessels +, elements with elongated scalariform perforation plates; wood fibres +; axial parenchyma diffuse or diffuse-in-aggregates; pollen monosulcate [anasulcate], tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.
[AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood 0; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; carpels plicate; nucellar cap + [character lost where in eudicots?]; 12BP [4 amino acids] deletion in P1 gene.
[[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]] / MESANGIOSPERMAE: benzylisoquinoline alkaloids +; polyacetate derived anthraquinones + [?level]; outer epidermal walls of root elongation zone with cellulose fibrils oriented transverse to root axis; P more or less whorled, 3-merous [possible positiion]; embryo sac bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid; ?germination.
[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (veins in lamina often 7-17mm/mm2 or more [mean for eudicots 8.0]); (stamens opposite [two whorls of] P); (pollen tube growth fast).
[CERATOPHYLLALES + EUDICOTS]: ethereal oils 0.
EUDICOTS: myricetin, delphinidin scattered, asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; K/outer P members with three traces, "C" with a single trace; A few, (polyandry widespread, initial primordia 5, 10, or ring, ± centrifugal), filaments fairly slender, anthers basifixed; microsporogenesis simultaneous, pollen tricolpate, apertures in pairs at six points of the young tetrad [Fischer's rule], cleavage centripetal, wall with endexine; G with complete postgenital fusion, stylulus/style solid [?here]; seed coat?
[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 place]; micropyle?; 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, the calyx enclosing the flower in bud, sepals with three or more traces, petals with a single trace; stamens = 2x K/C, in two whorls developing internally/adaxially to the corolla whorl and successively alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G , G  also common, when [G 2], carpels superposed, compitum +, placentation axile, style +, stigma not decurrent; endosperm nuclear; fruit dry, dehiscent, loculicidal [when a capsule]; RNase-based gametophytic incompatibility system present; floral nectaries with CRABSCLAW expression.
[SANTALALES [BERBERIDOPSIDALES [CARYOPHYLLALES + ASTERIDS]]] / ASTERIDS ET AL. / SUPERASTERIDS : ?
[BERBERIDOPSIDALES [CARYOPHYLLALES + ASTERIDS]]: ?
[CARYOPHYLLALES + ASTERIDS]: seed exotestal; embryo long.
ASTERIDS / Sympetalae redux? / ASTERIDAE / ASTERANAE Takhtajan: nicotinic acid metabolised to its arabinosides; (iridoids +); tension wood decidedly uncommon; C enclosing A and G in bud, (connate, if evident only early in development and then petals often appearing to be free); anthers dorsifixed?; (nectary gynoecial); style +, long; ovules unitegmic, integument thick, endothelium +, nucellar epidermis does not persist; exotestal cells lignified, esp. on anticlinal and/or inner periclinal walls; endosperm cellular.
[ERICALES [ASTERID I + ASTERID II]]: (ovules lacking parietal tissue) [tenuinucellate].
[ASTERID I + ASTERID II] / CORE ASTERIDS: ellagic acid 0, non-hydrolysable tannins not common; sugar transport in phloem active; inflorescence basically cymose; A = and opposite sepals or P, (numerous, usu. associated with increased numbers of C or G); (pollen with orbicules); style short[?]; duplication of the PI gene.
ASTERID II / CAMPANULIDAE: myricetin 0; vessel elements with scalariform perforation plates; flowers rather small; endosperm copious, embryo short/very short.
[ASTERALES [ESCALLONIALES [BRUNIALES [APIALES [PARACRYPHIALES + DIPSACALES]]]]] / APIIDAE: iridoids +; C forming a distinct tube, tube initiation early; A epipetalous; G inferior, [2-3], style long[?].
[ESCALLONIALES [BRUNIALES [APIALES [PARACRYPHIALES + DIPSACALES]]]]: ?
[BRUNIALES [APIALES [PARACRYPHIALES + DIPSACALES]]]: ?
[APIALES [PARACRYPHIALES + DIPSACALES]] / DIPSAPIIDAE: nodes 3:3.
[PARACRYPHIALES + DIPSACALES] / DIPSIDAE: true tracheids +; lamina serrate; inflorescence terminal.
DIPSACALES Berchtold & J. Presl Main Tree, Synapomorphies.
Route I secoiridoids +; vessel elements with scalariform perforation plates; petiole bundles arcuate; colleters 0; buds with scales; leaves opposite, margins gland-toothed, bases ± confluent, (leaves amplexicaul); inflorescence cymose; pollen grains trinucleate; G , at least partly inferior; ovules apotropous, with parietal tissue ca 1 cell across; fruit indehiscent, K persistent, endocarp with fibrous layers perpendicular to each other and thick walled sclereids, containing crystals; seed coat 1-21 µm thick, testa vascularized, exotestal cells enlarged, cuboid/rectangular, variously thickened and lignified; endosperm without haustoria, cells thin-walled, not differentiated. - 2 families, 46 genera, 1090 species.
Note: Possible apomorphies are now being added throughout the site; they are in bold. However, the actual level at which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is because there is very considerable homoplasy for many characters, with with variation within and between clades. Furthermore, basic information for all too many characters is very incomplete, often coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there is the not-so-trivial issue of how ancestral states are reconstructed...
Evolution. Divergence & Distribution. The first split within crown Dipsacales may have occurred in the mid-Cretaceous, some 111-93 m.y.a., 20-30 m.y. older than some estimates (Bell & Donoghue 2005a and references). Magallón and Castillo (2009: note topology, Paracryphiales are way basal) offer an estimate of ca 59 m.y.; it is (90-)62(-32) m.y. in Lemaire et al. (2011b), who also unaccountably note "more recent stem node ages" of 31 m.y. 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) m.y... Beaulieu et al. (2013: 95% HPD) date the beginning of diversification here at (94-)80(-87) m.y., N. Zhang et al. (2012), (82-)68(-45) m.y..
The origin of Dipsacales was probably in the northern hemisphere (Beaulieu et al. 2013). Major diversification within both Dipsacoideae and Valerianoideae - and hence a major part number-wise of the whole clade - is relatively recent, occurring within perhaps ca 10 m.y. (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, see Donoghue et al. (2003); Jacobs et al. (2010b) discussed the evolution of characters of fruit anatomy, while 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. CYC-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 Adoxaceae (Jordheim et al. 2006).
Involute vernation of the lamina is more common in Adoxaceae than in Caprifoliaceae (Cullen 1978). For the morphology of the stipule-like structures and amplexicaul leaves in Caprifoliaceae and Adoxaceae 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. The morphology of the basic nectary type for the order is unclear, although Wagenitz and Laing (1984) suggest that most Caprifoliaceae s.l. lack terminal flowers. 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). For variation in floral anatomy, which clearly separates two groups of genera in the old Caprifoliaceae, see Wilkinson (1949 and references), interestingly, taxa in both families which have one or more locules infertile and the fertile locule(s) have but a single ovule, the reduced loculi may have two or more ovules.
Phylogeny. The order has strong support in D. Soltis et al. (2000: see also Wagenitz 1997; 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) and Moore and Donoghue (2007). 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. Takhtajan (1997) included Dipsacales, Adoxales and Viburnales in his Dipsacanae, while Cronquist 1981) recognised four families in his Dipsacales, again, the same circumscription as that adopted here.
Thanks. I am very grateful to Volker Bittrich for catching a number of mistakes on this page.
Includes Adoxaceae, Caprifoliaceae.
Synonymy: Dipsacineae Shipunov - Adoxales Nakai, Caprifoliales Berchtold & J. Presl, Lonicerales T. Leibe, Sambucales Berchtold & J. Presl, Valerianales Berchtold & J. Presl, Viburnales Dumortier
ADOXACEAE E. Meyen, nom. cons. Back to Dipsacales
0-methylated flavonols only +; true tracheids?; pericyclic sheath poorly developed; (nodes 1:1, 5:5); (stomata paracytic); (petiole also with adaxial inverted bundles; closed C-shaped and with wing bundles); palisade mesophyll with arm cells; glandular hairs common; (bud scales 0); lamina vernation involute or conduplicate (plicate), secondary veins palmate to pinnate, (stipules on leaf base); flowers small [<5 mm across], (4-merous); 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, parietal tissue +, endothelium +; fruit drupaceous, stone compressed; seed single, often ruminate, exotestal cells palisade or not, not lignified; n = (8-)9, chromosomes large, 2.6-10 µm long, centromeres , 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.
5[list]/200. North temperate, tropical montane, S.E. Australia, rare in Africa (map: from Hultén 1958, 1971; Meusel & Jäger 1992). 2 groups below. [Photos - Collection]
Shrubs (trees); hairs stellate and variants; G , odd member abaxial, 2 abort, nectary on top of G, epithelial; endocarp with layers of fibres oriented parallel to each other, 1+ layers of sclereids; seed coat 21-100 µm thick; outer layer of endosperm differentiated, endosperm with crystals, cell walls ± thickened.
1/175. North temperate, tropical montane, but not in Africa. [Photo - Flower.]
Synonymy: Tinaceae Martynov, Viburnaceae Rafinesque
2. Adoxoideae Syme
Shrubs or herbs; (cambium storied - Sambucus); vessel elements with simple perforation plates; (nodes 1:1), (+ split laterals - Sambucus); leaves compound (deeply lobed); anthers extrorse (8, monothecal); nectary on stigma, on C associated with multicellular hairs, or 0; G 1, [(4), 5], opposite petals, [all fertile], styles separate, stigmas capitate; 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 large - Sambucus).
4/23. Mainly north temperate, esp. China, also tropical montane (few in Africa), S.E. Australia.
Synonymy: Sambucaceae Borkhausen
Evolution. Divergence & Distribution. Early divergence within this clade can be dated to ca 91-75 m.y.; crown Adoxaceae are 75-65 m.y. old (Bell & Donoghue 2005a). A number of deep branches within Viburnum are occupied by taxa that are currently tropical in distribution (ex section Megalotinus - polyphyletic); the Malesian V. clemensiae is sister to the rest of the genus (Clement & Donoghue 2011). Indeed, 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 (Schmerler et al. 2012).
The evolution of one-seeded fruits in Viburnum seems to be connected with increased speciation rates there (Moore & Donoghue 2009).
For more details of possible apomorphies within the family, see Donoghue et al. (2001b, 2003) and Jacobs et al. (2010b: fruit and seed characters).
Genes & Genomes. Gene duplication has occurred within Adoxaceae, e.g. in Viburnum plicatum (Howarth et al. 2011), with its 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). A fibrous pericyclic sheath in Viburnum may be absent, and that of Sambucus interrupted; that of Caprifoliaceae is better developed. The cells in the latter are also longer, except those of Linnaea (Cooper 1939). Sambucus has crystal sand.
There is considerable variation in 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, tenuinucellate ovules, weak endothelium, etc. (Erbar 1994). There are five semi-superior carpels with five styles/styluli (Leins 2000) and there are initially five stamen primordia. The leaves at the bases of the rosettes and on the rhizomes are spiral and there are no extrafloral nectaries (c.f. Sambucus). 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). Donoghue et al. (2003) describe the flowers of Sinadoxa as having three corolla lobes and a single carpel. 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).
The ovules in Sambucus may be attached to the axis below the level of insertion of the sepals, etc (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 some embryology, see Lagerberg (1909: Adoxa) and Moissl (1941), for nectaries in some Adoxaceae, see Vogel (1997), for information about arm cells, see Wagenitz and Laing (1984), for fruits and seeds, see Jacobs et al. (2010b), and for general information about Japanese taxa, see Hara (1983).
Phylogeny. For a phylogeny of Viburnum, see Winkworth and Donoghue (2005), Schmerler et al. (2012), etc., for variation in its endocarp and seed, see Jacobs et al. (2008).
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]; C 2 + 3, tubular, main petal veins laterally connected [transpetalar veins] nectary of unicellular hairs, on C; anthers sagittate; tapetum plasmodial; pollen grains spheroid, echinate; G inferior, lateral and dorsal carpellary bundles 0, ventral bundles in axis, stigma capitate, wet; (testa hypodermis also differentiated, fibrous or not); 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; duplication of dipsCYC2 and dipsCYC3 genes, horizontal transfer of mitochondrial rps11 gene [?Morinoideae and upwards in the tree].
42/890. Largely temperate/warm temperate in the northern hemisphere, some montane tropics (exp. Valerianoideae), neither the Antipodes nor the Pacific.
Evolution. Divergence & Distribution. The crown-group age is ca 81-60 m.y. (Bell & Donoghue 2005a).
Endress (2011a) suggested that monosymmetric flowers might be a key innovation here, but, as noted above, understanding diversification in Dipsacales is not simple.
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. Biparental plastid transmission occurs in some taxa, but sampling is poor.
Some information is taken from Magócsy-Dietz (1899: pith diaphragms, woody members only) Carlquist (1982: wood anatomy), Verlaque (1984: relationships), Ogata (1988, 1991: wood anatomy), Hoffmann and Göttmann (1990: general), Backlund and Donoghue (1996: general), Backlund and Nilsson (1997: pollen), Backlund and Pyck (1998: general), Benko-Iseppon and Morawetz (2000a: general), Nilova (2001: bark anatomy), Donoghue et al. (2001b) and especially Bell et al. (2001) and Jacobs et al. (2011), all general.
Phylogeny. The position of Heptacodium was initially somewhat uncertain (Pyck & Smets 2000, 2001), although there are suggestions that it be included in Caprifolioideae (e.g. Donoghue et al. 2001a, 2003; Soltis et al. 2011 [support weak]; Landrein et al. 2012). However, its flowers have several bracteoles and only one of the three carpels develops, the fruit having a single seed; these are not features characteristic of Caprifolioideae. It may well be a hybrid between members of Caprifolioideae and Linnaeoideae (Z.-Y. Zhang et al. 2002; Landrein & Prenner 2013).
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 was perhaps consistent with this position (Jacobs et al. 2010d). In other analyses Zabelia and Morinoideae formed a clade, although support for this was again 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. Landrein and Prenner (2013) found that Zabelia and Diabelia (Linnaeoideae) had similar "primitive" (their scare quotes) inflorescences.
Soltis et al. (2007a) found that the position of Valerianoideae was unstable in some analyses; analyses of mitochondrial data are perhaps particularly challenging (Winkworth et al. 2008b). Morinoideae migrated basally in an analysis by Beaulieu et al. (2013), but the study was only a 4-gene analysis.
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 also A.P.G. III 2009), since similarities between the families are considerable and differences are mostly slight. There is still (as of iv.2013) instability in the backbone of the tree, furthermore, because of the possible hybrid origin of Heptacodium - Caprifolioideae x Linnaeoideae -it is characterized separately below.
Shrubs; lamina vernation involute [Weigela]; nectary at base of C; filaments hairy; pollen pororate, membrane granulose; G ; ovules many/carpel, ?marginal; fruit beaked, septicidal down sides; n = 9.
1-2/16. East Asia, S.E. U.S.A. (map: from Li 1952, approximate).[Photo - Flowers © M. Clayton]
Evolution. Divergence & Distribution. For the early Tertiary 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.
Synonymy: Diervillaceae Pyck
[Caprifolioideae [Linnaeoideae [Morinoideae [Valerianoideae + Dipsacoideae]]]]: inflorescence lacking terminal flower.
Shrubs (trees); vessel elements usu. with simple perforation plates; lamina vernation supervolute or conduplicate (involute - Heptacodium), margins entire, secondary veins pinnate to palmate; K small; A (4-)5, filaments glabrous; G [3(-4)], all, 3/4 or 2/4 fertile, odd member adaxial (opposite petals - Leycesteria); ovules 1-8/carpel; fruit baccate [Lonicera] or drupaceous [Symphoricarpus]; n = 9; deletion in the chloroplast gene clpP.
5[list]/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.]
Evolution. Diversification occurred 51-36 m.y.a., possibly beginning in Asia (Smith 2009).
Chemistry, Morphology, etc. There is no stem endodermis.
Triosteum seems to lack dorsal carpellary bundles only and has apotropous ovules (Wilkinson 1949). The drupes of Symphoricarpus have a thick outer layer of narrow, vertical fibres and an layer of horizontal fibres; the seed coat itself is crushed.
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.
Synonymy: Loniceraceae Vest
Cork mid-cortical; fibres in cortex; lamina tripli-nerved; 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 [Morinoideae [Valerianoideae + Dipsacoideae]]]: epicalyx + [from aborted flowers, etc.]; A 4, didynamous; 1 carpel fertile, 2 carpels abort; fertile ovule 1/carpel; fruit a cypsela; seed coat flattened, exotesta not lignified.
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) and Landrein and Prenner (2013). 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.
In general, where there are only two stamens, it is 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).
Shrubs (± herbaceous); vessel elements with scalariform perforation plates; lamina vernation supervolute(-curved); epicalyx with 4 or 6 members, accrescent or not, nectariferous petal abaxial, bulging, (with four lines of compact hairs); filaments hairy; (G , 2 fertile - Dipelta); ovule ?apotropous; K and/or bracts often modified in fruit; ?embryo length; n = 8, 9.
6 [list]/32. Circumboreal (Linnaea), Mexico (Abelia), China to Japan (five genera), Mexico (map: from Hultén & Fries 1986; Meusel & Jäger 1992; note, Zabelia not included). [Photo - Habit, Flower.]
Evolution. Divergence & Distribution. For distinctive late Eocene fruits assignable to this group and their implications for biogeography and evolution, see Manchester and Donoghue (1995). Manchester et al. (2009) discussed the fossil distribution of Dipelta, which is known from Eocene/Oligocene rocks in southern England.
Chemistry, Morphology, etc. For general information, see Hara (1983) and Landrein et al. (2012). For details of inflorescence morphology, see Landrein and Prenner (2013), although they did not interpret the variation that they found in the context of phyloreny.
Phylogeny. For relationships, see Jacobs et al. (2010c, 2011) and Landrein et al. (2012); the basic phylogenetic structure may be [Linnaea [Vesalea + The Rest]].
Classification. For generic limits and groupings, see Landrein (2010) and Landrein et al. (2012).
Synonymy: Linnaeaceae Backlund
[Zabelia, Morinoideae [Valerianoideae + Dipsacoideae]]: vessel elements with simple perforation plates; petioles connate basally/leaves amplexicaul; nectary at base of C.
[Morinoideae [Valerianoideae + Dipsacoideae]]: perennial rosette herbs with taproot; monoterpenoids, cathecolic tannins, alkaloids +, ellagic acid 0; libriform fibres +; nodes 5:5; vascular flank-bridge in stem between lateral bundles; bud scales 0; filaments glabrous, anthers dorsifixed; pollen "large"; G with sterile loculi much reduced,; ovule apical, endothelium prominent, with crystal layer; chalazal nuclei variously proliferating; exotesta not thickened; endosperm scanty, embryo large; distinctive expansion of the chloroplast inverted repeat.
Evolution. Divergence & Distribution. The inclusion of Zabelia will affect character optimizations. 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 until there is more certainty over its position in the tree, it is characterized separately below, and characters for [Morinoideae [Valerianoideae + Dipsacoideae]] are also listed separately.
Chemistry, Morphology, etc. For 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 a comparison of Morinoideae, Valerianoideae and Dipsacoideae, see Cannon and Cannon (1984). Zabelia and Morinoideae have smooth pollen grains with endocinguli (Jacobs et al. 2011; Landrein et al. 2012).
For embryology, see Johri et al. (1991), for pollen size, see Xu et al. (2011: Zabelia included), and for relationships suggested by some morphological characters, see Peng et al. (1995).
Shrubs; ?chemistry; wood ring porous; lamina entire, petiole bases swollen, enclosing axillary bud; epicalyx with 6 or 14 members, not accrescent; nectary pouched abaxially, with four lines of compact hairs; pollen grains smooth, with endocinguli; ovule?; seed?; n = 9.
1/4: Central Asia (Tian Shan) to the Far East (Map: from Meusel & Jäger 1992; FoC vol. 19. 2011).
Chemistry, Morphology, etc. For general information, see Hara (1983), Landrein et al. (2012) and Landrein and Prenner (2013).
Ethereal oils +, 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, + 2 staminodes); tapetum ?glandular; pollen binucleate, (turret-like triporate), surface smooth, with endocinguli [extra thickened layer of pollen wall], exine columellae reduced, intine-covered tubular extrusions; embryo with hypostase; embryo sac with chalazal cells producing multicellular structures; integument multiplicative, not vascularized, outer layer only persisting; endosperm ruminate; n = 17; duplication of dipsCYC2 and dipsCYC3 genes.
2-3[list]/13. Balkans to China (map: see Cannon & Cannon 1984). [Photo - Morina Inflorescence, Acanthocalyx Inflorescence.]
Chemistry, Morphology, etc. Remarkable intine-covered structures 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).
For tables of differences between Morinoideae and Dipsacoideae, see Vijayaraghavan and Sarveshwari (1968), Cronquist (1981), Cannon and Cannon (1984) and Johri et al. (1992). 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 plasmodial (and that of Dipsacoideae as being glandular).
For embryology, see Vijayaraghavan and Sarveshwari (1968: Morina longifolia only), for pollen, Verlaque (1984, 1986), for a monograph of the subfamily, Cannon and Cannon (1984: as Morinaceae), and for phylogeny and biogeography, see Bell and Donoghue (2003).
Synonymy: Morinaceae Rafinesque
[Valerianoideae + Dipsacoideae]: (annual herbs); saccharose +, quercetin 0; (nodes 5 or more:5 or more); leaves simple to ± pinnate, lamina vernation conduplicate, (margins entire); flowers rather small; 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 green; centromeres metacentric to subtelocentric, no C bands.
(Shrubby); (vessel elements with scalariform perforation plates); 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[list]/290. Eurasia, Africa, esp. Mediterranean region, to Malesia.
5a. Triplostegia de Candolle
Valpotriate-type iridoids +; flowers with bracteoles and double epicalyx; C ± polysymmetric; pollen aperture with a halo, colpus granulose; fruit surrounded by capitate-glandular outer epicalyx, the tips hooked; endosperm slight; n = ?
1/2. Southeast Asia, East Malesia (map: from van Steenis 1951).
Synonymy: Triplostegiaceae Airy Shaw
5b. The Rest.
Inflorescence a capitulum, with involucral bracts; epicalyx single, 8-ribbed; (C with 4 lobes); (A 2-3); (pollen 3-porate); G ; ovule with integument 10-15 cells across; fruit with calycine awns or bristles; endosperm +; n = 5, 7-9(-10).
10/290: Scabiosa (80), Cephalaria (65), Knautia (60). Eurasia, Africa, esp. Mediterranean region (Map: see above; red). [Photo - Habit, Inflorescence, Flower.]
Synonymy: Dipsacaceae, Juss., nom. cons., Scabiosaceae Martinov
Evolution. Divergence & Distribution. For large-scale migration within Scabiosa, including north to south movement in Africa, see Carlson et al. (2012).
Seed Dispersal. Caputo et al. (2004) examined the evolution of seed dispersal syndromes. The well-developed epicalyx 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).
Chemistry, Morphology, etc. The cork of Knautia may be superficial (Metcalfe & Chalk 1950).
For embryology, see Kamelina (1983), and for fruit, see Verlaque (1977), for a general study, see Verlaque (1985, 1986).
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; W.-H. Zhang et al. 2001; Bell 2004; Soltis et al. 2011). 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. As they note, [Triplostegia + Valerianoideae] have valpotriate-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) found that Triplostegia might be sister to [Valerianoideae + Dipsacoideae], and used this topology in their character state reconstruction. Where Triplostegia ends up will substantially affect apomorphy positions, and the characters that Triplostegia and Valerianoideae have in common may be either paralellisms, or apomorphies for the larger clade, but with reversals.
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 rest (Avino et al. 2009; Carlson et al. 2009). For other phylogenetic studies, see Caputo et al. (2004) and Carlson et al. (2012: Scabiosa).
Classification. Mayer and Ehrendorfer (2013: much morphology) provide a classification of the subfamily.
Foetid monoterpenoids and sesquiterpenoids, valpotriates +; true tracheids ?; (leaf bases not sheathing); (plant dioecious); flowers small, corolla ± polysymmetric, bracteoles +, epicalyx 0; K small, abaxial C basally spurred (or not); A (1-)3(4-5), (anthers bisporangiate - Valeriana subg. Phyllactis); pollen colpate; (G with sterile loculi well developed); K + (a pappus; reduced); testa 1-layered; (endosperm 0); n = (7-)8(9-12).
17[list]/315: Valeriana (200), Valerianella (80). N. temperate, especially Mediterranean, and Andean South America (half the subfamily) (map: from Hultén 1958; Meusel et al. 1978). [Photo - Habit, Flower, Flower.]
Synonymy: Valerianaceae Batsch
Evolution. Divergence & Distribution. Crown-group Valerianoideae may be 60-55 m.y. old (Bell & Donoghue 2005a), ca 50 m.y. (Moore & Donoghue 2007) and (54-)42(-33) m.y. (Beaulieu et al. (2013: 95% HPD).
There were ca four migrations to South America (20-)15.7(-12) m.y.a. (Bell et al. 2102), but diversification in the Andean paramo, where ca 1/7 of the subfamily grow, happened less than 5 m.y.a. (Bell & Donoghue 2005b). Further diversification - ca 1/6 of the species - occured 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, and dispersal is by a variety of mechanisms.
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 calyx in Patrinia and in particular Nardostachys is well-developed. 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 (Hoffmann & Göttmann 1990).
For ovule morphology (no vascular tissue?), see Guignard (1893), and for general morphology, see Eriksen (1989).
Phylogeny. Patrinia may be sister to the rest of the subfamily (Pyck 2002), Nardostachys sister to the remaining taxa (Bell 2004; Bell & Donoghue 2005b: both with very strong support), or the two together 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); Valerianamay indeed be para- or polyphyletic (Hidalgo et al. 2004). For other phylogenies, see Bell (2004).