LIGNOPHYTA

True roots +; lateral meristems: cork cambium producing cork abaxially, vascular cambium producing phloem abaxially and xylem adaxially.

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, (lignins derived from p-coumaryl alcohol, i.e. S [syringyl] lignin units); true roots present, apex multicellular, xylem exarch, and branching endogenous; arbuscular mycorrhizae +; shoot apical meristem multicellular, interface specific plasmodesmatal network; stem with ectophloic eustele, endodermis 0, xylem endarch, branching exogenous; vascular tissue in t.s. discontinuous by interfascicular regions; vascular cambium + [xylem ("wood") differentiating internally, phloem externally]; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, plastids with starch grains; phloem fibres +; stem cork cambium superficial, root cork cambium deep seated; leaves with single trace from sympodium ["nodes 1:1"]; stomata ?; leaf vascular bundles collateral; leaves megaphyllous [determinancy evolved first, then ad/abaxial symmetry], spiral, simple, lamina with vein density up to 5 mm/mm² [mean for all non-angiosperms 1.8]; axillary buds associated with at most some leaves; prophylls [including bracteoles] two, lateral; plant heterosporous, sporangia eusporangiate, on sporophylls, sporophylls aggregated in indeterminate cones/strobili; true pollen [microspores, i.e. no distal pore for release of gametes] +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, crassinucellate, 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, with many flagellae; female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large", first cell wall of zygote transverse, embryo straight, endoscopic [suspensor +], short-minute, with morphological dormancy, white, cotyledons 2; plastid transmission maternal; two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], nrDNA with 5.8S and 5S rDNA in separate clusters; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.

MAGNOLIOPHYTA

Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, non-hydrolysable tannins, quercetin and/or kaempferol +, apigenin and/or luteolin scattered, [cyanogenesis in ANITA grade?], S [syringyl] lignin units common, positive Maüle reaction [syringyl:guaiacyl ratio more than 2-2.5:1], and hemicelluloses as xyloglucans; root apical meristem intermediate-open; root vascular tissue oligarch [di- to pentarch], lateral roots arise opposite or immediately to the side of [when diarch] xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, with gelatinous fibres; 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 cells from same mother cell that gave rise to the sieve tube; sugar transport in phloem passive; nodes unilacunar [1:?]; stomata with ends of guard cells level with pore, paracytic, outer stomatal ledges producing vestibule; leaves petiolate, lamina [formed from the primordial leaf apex], development of venation acropetal, 2ndary veins pinnate, fine venation reticulate, veins (1.7-)4.1(-5.7) mm/mm², endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, polysymmetric, 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 by action of hypodermal endothecium, endothecial cells elongated at right angles to long axis of anther; tapetum glandular, 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 free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, dry [not secretory]; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across [crassinucellate], nucellar cap?; megasporocyte single, hypodermal, megaspore tetrad linear, functional megaspore chalazal, lacking sporopollenin and cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; P deciduous in fruit; seed exotestal; pollen binucleate at dispersal, trinucleate eventually, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing at 80-600 µm/hour, with pectic outer wall, callose inner wall and callose plugs, growing between cells, penetration of ovules via micropyle [porogamous] within ca 18 hours, distance to first ovule 1.1.-2.1 mm, tube moves between nucellar cells; double fertilisation +, endosperm diploid, cellular [micropylar and chalazal domains develop diffently, 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 cellular ab initio, minute; germination hypogeal, seedlings/young plants sympodial; Arabidopsis-type telomeres [(TTTAGGG)_n]; whole genome duplication, ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, paleo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]].

Evolution. Possible apomorphies for flowering plants are in bold. Note that the actual level to which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is because some taxa basal to the [magnoliid + monocot + eudicot] group have been surprisingly little studied, there is considerable homoplasy as well as variation within and between families of the ANITA grade in particular for several of these characters, and also because details of relationships among gymnosperms will affect the level at which some of these characters are pegged. For example, if reticulate-perforate pollen is optimized to the next node on the tree (see Friis et al. 2009 for a discussion), it effectively makes the pollen morphology of the common ancestor of all angiosperms ambiguous... For other features such as details of sugar transport in the phloem, their placement on the tree is frankly speculative. Finally, for features such as parietal tissue/a nucellus only one (Nymphaeales) to three cells thick above the embryo sac and a stylar canal lacking an epidermal layer, although plesiomorphous for basal grade angiosperms (Williams 2009), I am unsure where on the tree a thicker nucellus and a stylar epidermal layer are acquired.

NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: vessels +, elements with elongated scalariform perforation plates; wood fibres +; axial parenchyma diffuse or diffuse-in-aggregates; tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.

ERICALES + ASTERID I + II: ovules tenuinucellate.

[ASTERID I + II] / CORE ASTERIDS: ellagic acid 0, non-hydrolysable tannins not common; sugar transport in phloem active; inflorescence basically cymose; C forming a distinct tube; A epipetalous, = and opposite sepals or P, polyandry associated with increased numbers of C or G, very uncommon; (pollen with orbicules); duplication of the PI gene.

ASTERID II / CAMPANULIDAE: myricetin 0; vessel elements with scalariform perforation plates; flowers rather small; style short; endosperm copious, embryo short/very short.

ASTERALES [ESCALLONIALES [BRUNIALES [APIALES [PARACRYPHIALES + DIPSACALES]]]] / APIIDAE: iridoids +; C tube initiation early; G [2-3], inferior.

ESCALLONIALES [BRUNIALES [APIALES [PARACRYPHIALES + DIPSACALES]]]: ?

[BRUNIALES [APIALES [PARACRYPHIALES + DIPSACALES]]]: ?

[APIALES [PARACRYPHIALES + DIPSACALES]] / DIPSAPIIDAE: ?

[PARACRYPHIALES + DIPSACALES] / DIPSIDAE: nodes 3:3; true tracheids +; lamina serrate; inflorescence terminal.

DIPSACALES Berchtold & J. Presl  Main Tree, Synapomorphies.

Route I secoiridoids +; cork cambium deep-seated; pericyclic fibres 0; petiole bundles arcuate; buds with scales; leaves opposite, bases ± confluent, margins gland-toothed; inflorescence cymose; pollen grains trinucleate; nectary of unicellular hairs, on corolla; G [3], ± inferior; K persistent in fruit; endocarp with two layers of cells of differing kinds, fibrous layers perpendicular to each other, endocarp sclereids thick walled, containing crystals; seed coat 1-21 µm thick, testa vascularized, exotestal cells enlarged, cuboid/rectangular, variously thickened and lignified; endosperm cells thin-walled, not differentiated. - 2 or 7 families, 45 genera, 1090 species.

Evolution. Divergence & Distribution. The first split within crown Dipsacales may have occurred in the mid-Cretaceous, some 111-93 million years before present, 20-30 million years older than some estimates (Bell & Donoghue 2005a and references). Magallón and Castillo (2009) offer estimates of ca 92.8 and 93.1 million years for relaxed and constrained penalized likelihood datings respectively for the stem group, the crown group dating to 58.9 and 59.1 million years (relaxed and constrained again) - but note topology, Paracryphiales are way basal.

However, major diversification within Dipsacaceae and Valerianaceae - and hence a major part of the diversification of the whole order - is relatively recent, occurring within perhaps ca 10 million years (Bell & Donoghue 2005a). For a very detailed discussion of morphological evolution, see Donoghue et al. (2003); Jacobs et al. (2010b) discuss the evolution of characters of fruit anatomy. Howarth and Donoghue (2004, esp. 2005, 2008, 2009) and Howarth et al. (2011) note 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, indeed, diversification in Dipsacales has often seemed to increase as plants moved into new geographical areas, especially if these were mountainous (Moore & Donoghue 2007). The whole clade [Paracryphiales + Dipsacales] is not notably species-rich when compared with its sister taxon, Apiales (ca 1130 versus ca 5490 spp.), although Dipsacales are far more diverse than Paracryphiales - the latter include a mere 36 or so species. Duplication has also occured within Adoxaceae, e.g. in Viburnum plicatum (Howarth et al. 2011), with its monosymmetric marginal flowers that serve as "petals" for the inflorescence.

Genes & Genomes. 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 is more common in Adoxaceae than in Caprifoliaceae (Cullen 1978). Weberling (1957) discussed the morphology of the stipule-like structures and amplexicaul leaves in Caprifoliaceae and Adoxaceae; amplexicaul leaves in particular occur in several families in the order. Split-lateral bundles and a girdling vascular trace occur in taxa with perfoliate leaves (e.g. Colomb 1887) as well as occuring in the Morinaceae-Dipsacaceae area (see below). Glands at the base of the leaf in Sambucus and Viburnum may be vascularized (see also Colomb 1887).

Weberling (1989) described the inflorescence structure of the woody Dipsacales in particular in considerable detail. The morphology of the basic nectary type for the order is perhaps unclear. In Viburnum (and Sambucus?) it is a disc-like structure on top of the inferior ovary, in Adoxa it is associated with multicellular hairs on the corolla, in Caprifoliaceae, unicellular hairs (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). For optimisation of some pollen characters on the tree, see Xu et al. (2011). There is considerable variation in the presence of the mitochondrial coxII.i3 intron.

Phylogeny. The position of Dipsacales in early phylogenetic analyses was unclear. Downie and Palmer (1992) associate Adoxaceae with Asterales, while they are sister to Apiales in some studies (Backlund & Bremer 1997).

The order has strong support in D. Soltis et al. (2000: see also Wagenitz 1997; Bremer et al. 2001; cf. A.P.G. 1998). The phylogeny of the expanded order is based especially on work by Donoghue et al. (2001b, 2003), 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. Note that the position of Heptacodium was initially somewhat uncertain (Pyck & Smets 2000, 2001), although it is probably to be included in Caprifoliaceae s. str (e.g. Donoghue et al. 2001a, 2003; Soltis et al. 2011 [support weak]). Recently Linnaeaceae have been studied in detail, and Jacobs et al. (2010c) suggest that Zabelia may be in the [Morinaceae [Dipsacaceae + Valerianaceae] clade, although with only moderate support (see also Soltis et al. 2011); pollen morphology is, however, perhaps consistent with this position (Jacobs et al. 2010d). Valerianaceae are sister to the rest of the Caprifoliaceae s. str. part of the clade in some analyses (Soltis et al. 2007a); analyses of mitochondrial data are perhaps particularly challenging (Winkworth et al. 2008b).

Previous Relationships. Takhtajan (1997) included Dipsacales, Adoxales and Viburnales in his Dipsacanae. In earlier versions of this site (pre April 2008), [Columelliaceae + Desfontainiaceae] (= Columelliaceae s.l.) were placed sister to Dipsacales, with which they do show considerable morphological similarity. However, recent work suggests they are to be associated with Bruniaceae and are placed in Bruniales, which are in turn sister to [Apiales [Paracryphiales + Dipsacales]] (Winkworth et al. 2008a; Tank & Donoghue 2010).

Includes Adoxaceae, Caprifoliaceae, Diervillaceae, Dipsacaceae, Linnaeaceae, Morinaceae, Valerianaceae.

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); glandular hairs common; (bud scales 0); leaves involute or conduplicate (plicate), 2ndary veins palmate to pinnate, (stipules on leaf base); (flowers 4-merous); K open, usu. very small, 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.

5[list]/200. North temperate, tropical montane, but not in Africa (map: from Hultén 1958, 1971; Meusel et al. 1992). 2 groups below. [Photos - Collection]

1. Viburnum

Shrubs (trees); hairs stellate and variants; G [3], odd member abaxial, 2 abort, nectary on top, epithelial; parietal tissue ca 1 cell across; endocarp with fibrous layers 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 top of G, on C associated with multicellular hairs, or 0; G 1, [5], opposite petals, [all fertile], style branches separate, stigmas capitate; embryo sac tetrasporic, eight nucleate [Adoxa-type]; endocarp with three layers of cells of differing kinds, 2 fibrous cell layers, 1 sclereid cell layer; (embryo large - Sambucus).

4/23. Mainly north temperate, esp. China, also (sub)tropical montane.

Synonymy: Sambucaceae Borkhausen

• Adoxaceae may be recognised by their opposite, toothed leaves that are compound or simple. The inflorescence is usually flat-topped, cymose, and has numerous small flowers. The flowers are 5- or sometimes 4-merous, the calyx is open during development, the corolla is rotate, the style is at most short, and the fruit is drupaceous. Some Cornaceae look rather similar to Viburnum, but the former often have 4-merous flowers, they lack stellate indumentum, and their lateral veins ascend towards the apex of the blade.

Evolution. Divergence & Distribution. Early divergence within this clade can be dated to ca 91-75 million years before present; crown Adoxaceae are 75-65 million years 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).

The evolution of one-seeded fruits in Viburnum seems to have increased speciation rates there (Moore & Donoghue 2009).

For more details of the possible synapomorphies within the family, see Donoghue et al. (2001b, 2003) and Jacobs et al. (2010b: fruit and seed characters).

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 s.l. is better developed. The cells in the latter are also longer, except those of Linnaea (Cooper 1939). Sambucus has crystal sand. There is the same number of stamens as petals (cf. many Dipsacaceae s.l.). The chromosomes are distinctive. They are large (cf. Caprifoliaceae, etc.), continuously condensed from prophase to metaphase, the proximal regions normally condensing first, but when cold, areas of the mitotic chromosomes are not condensed (Benko-Iseppson & Morawetz 2000).

Adoxa is distinctive in lacking any obvious corolline ring primordium and in its eight stamens with monothecate anthers, amoeboid tapetum, nectary on the petal lobes, tenuinucellate ovules, weak endothelium, etc. (Erbar 1994). The leaves at the bases of the rosettes and on the rhizomes are spiral and there are no extrafloral nectaries (cf. Sambucus) In 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 the 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). Adoxa itself has five semi-superior carpels with five styles (Leins 2000) and there are initially five stamen primordia. 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 there are small groups of meristematic cells above the ovules which may represent aborted ovules (Roels & Smets 1994).

For information about fruit and seed, see Jacobs et al. (2010b).

Phylogeny. For a phylogeny of Viburnum, see Winkworth and Donoghue (2005), for variation in its endocarp and seed, see Jacobs et al. (2008).

Diervillaceae [Caprifoliaceae [Linnaeaceae [Morinaceae [Valerianaceae + Dipsacaceae]]]] [= Caprifoliaceae s.l.]: bark papery-flaky; O-methylated flavones, flavonols +; cork cambium deep-seated; wood often fluorescing; (pith diaphragms +); pericyclic fibres moderately developed; flowers rather weakly monosymmetric [K ± polysymmetric], medium-sized; C 2 + 3, tubular; anthers sagittate; tapetum plasmodial; pollen grains spheroid, echinate; lateral and dorsal carpellary bundles 0, ventral bundles in axis, stigma capitate, wet; (testa hypodermis also differentiated, fibrous or not); chromosomes "small"; duplication of dipsCYC2 and dipsCYC3 genes, horizontal transfer of mitochondrial rps11 gene [?Morinaceae and upwards in the tree].

Evolution. Divergence & Distribution. Crown-group divergence within this clade can be dated to ca 81-60 million years before present (Bell & Donoghue 2005a).

Endress (2011a) suggested that the monosymmetric flowers of Dipsacales might be a key innovation for them, but, as noted above, understanding diversification in this clade 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. Transpetal veins, branch veins linking adjacent median veins, occur in the upper part of the corolla in at least Diervilla, Kolkwitzia and some Valerianaceae and Dipsacaceae (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), Wagenitz and Laing (1984: nectaries), Verlaque (1988: 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-Iseppson and Morawetz (2000: general), Nilova (2001: bark anatomy) and Donoghue et al. (2001b) and especially Bell et al. (2001: both general).

Classification. The circumscription, etc., of families follows Backlund and Bremer (1997) and Backlund and Pyck (1998). Note that the small families recently recognised in Dipsacales are a consequence of maintaining the well known Dipsacaceae and Valerianaceae in their old circumscriptions - the small clades resulting from the break-up of the old, broadly-circumscribed Caprifoliaceae remained unaccounted for. The whole lot might usefully be combined in a Caprifoliaceae s.l. (see also A.P.G. II 2003, esp. III 2009), since similarities between the families are considerable and differences are mostly slight. Furthermore, there is persistent instability in the backbone of the tree.

DIERVILLACEAE Pyck   Back to Dipsacales

Shrubs; leaves involute [Weigela]; nectary at base of C; filaments hairy, pollen pororate, membrane granulose; G [2]; ovules many/carpel, ?marginal; fruit b;aked, 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.

Caprifoliaceae [Linnaeaceae [Morinaceae [Valerianaceae + Dipsacaceae]]]: fruit indehiscent.

Chemistry, Morphology, etc. Note that taxa with connate leaf bases, especially of inflorescence bracts, are scattered through this clade.

CAPRIFOLIACEAE Jussieu, nom. cons.   Back to Dipsacales

Shrubs (trees); vessel elements usu. with simple perforation plates; leaves supervolute or conduplicate (involute - Heptacodium), margins entire, 2ndary 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 million years ago, possibly beginning in Asia (Smith 2009).

Chemistry, Morphology, etc. There is no stem endodermis. Heptacodium has cork forming in the middle of the cortex and well-developed cortical fibres. Caprifoliaceae also include Triosteum and Symphoricarpus. Triosteum seems to lack dorsal carpellary bundles only and has apotropous ovules (Wilkinson 1949), while the drupes in Symphoricarpus have a thick layer of narrow, vertical fibres on the outside, then a layer of horizontal fibres, and the seed coat itself is crushed.

Phylogeny. For relationships in Caprifoliaceae - [Heptacodium [Triosteum *[Lonicera [Leycesteria + Symphoricarpos]]]] - are relationships suggested by Theis et al. (2008); the node with the asterisk has a poor posterior probability, but a good bootstrap value.

Synonymy: Loniceraceae Vest

Linnaeaceae [Morinaceae [Dipsacaceae + Valerianaceae]]: supernumerary bracts from aborted flowers +; A 4, didynamous; G [3], 2 abort; fruit a cypsela; seed coat flattened, exotesta not lignified.

Evolution. Divergence & Distribution. For fruit characters apomorphic at this level, see Jacobs et al. (2010b).

Chemistry, Morphology, etc. For various interpretations of the supernumerary bracts, bracteoles, epicalyx, and involucel in these families, see Weberling (1992), Roels and Smets (1996), Donoghue et al. (2003, and literature cited) and Pyck and Smets (2004). 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). In the characterisations below, the particular derived condition for each family is described; what synapomorphies might "be" morphologically is unclear (Bell et al. 2001). In general, where there are only two stamens, the adaxial pair persists. Of the three carpels, it is the adaxial lateral carpel that remains fertile (Donoghue et al. 2003).

LINNAEACEAE Backlund   Back to Dipsacales

Shrubs (± herbaceous); vessel elements usu. with simple perforation plates; leaves supervolute(-curved); nectariferous petal abaxial; filaments hairy; (G [4], 2 fertile); ovule ?apotropous; K and/or bracts often modified in fruit; ?embryo length; n = 8, 9.

6 [list]/36. Temperate South East Asia (N. Temperate, inc. Mexico). [Photo - Habit, Photo - Flower]

Evolution. For distinctive Eocene fruits assignable to this group and their implications for biogeography and evolution, see Manchester and Donoghue (1995; see also Manchester et al. 2009 for the fossil distribution of Dipelta).

Phylogeny. Jacobs et al. (2010c, 2011) suggest that not only is the circumscription of Abelia questionable, but also that Zabelia is perhaps a member of the [Morinaceae [Dipsacaceae + Valerianaceae] clade.

Classification. For generic limits, see Landrein (2010).

Morinaceae [Dipsacaceae + Valerianaceae]: perennial rosette herbs with taproot; monoterpenoids, cathecolic tannins, alkaloids +, ellagic acid 0; libriform fibres +; flank-bridge in stem between lateral bundles; bud scales 0; nectary at base of C; filaments glabrous, anthers dorsifixed; pollen "large"; G with sterile loculi much reduced, placentation apical; ovule 1/carpel, endothelium prominent, with crystal layer; chalazal nuclei variously proliferating; exotesta not thickened; endosperm scanty, embryo large; distinctive expansion of the chloroplast inverted repeat.

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 in the middle, so forming the bridging bundle. Bundles innervating the petiole arise from the bridging bundle, except in Morina.

For a comparison of the three families, see Cannon and Cannon (1984), for embryology, see Johri et al. (1991), for pollen sixe, see Xu et al. (2011: Zabelia included), and for relationships suggested by some morphological characters, see Peng et al. (1995).

Phylogeny. For the possible inclusion of Zabelia in this clade, see Jacobs et al. (2010c); it is possible that Linnaeaceae, Zabelia and Morinaceae form a clade, although support for this is very weak (Jacobs et al. 2011).

MORINACEAE Rafinesque   Back to Dipsacales

Ethereal oils +, iridoids 0; nodes 5:5; stems hollow; leaves involute, margins spinose to pinnatifid (entire), 2ndary veins palmate, bases sheathing; inflorescence of sessile cymes [verticels], epicalyx 12-ribbed; flowers strongly monosymmetric; K 4, monosymmetric; A pairs inserted at different heights on the C tube (2, + 2 staminodes); tapetum ?glandular; pollen binucleate, (turret-like triporate), extra thickened layer of pollen wall, exine columellae reduced; embryo with hypostase; embryo sac with chalazal cells producing multicellular structures; integument multiplicative, not vascularized, outer layer only persisting; endosperm ruminate; n = 17, chromosomes 0.7-1.5 µm long; duplication of dipsCYC2 and dipsCYC3 genes.

2-3[list]/13. Balkans to China (map: see Cannon & Cannon 1984). [Photo - Morina Inflorescence, Acanthocalyx Inflorescence.]

• Morinaceae are robust, perennial herbs. They may be recognised by their opposite leaves with connate bases and often spiny margins and inflorescences consisting of whorls of flowers, each flower having a 12-ribbed epicalyx. The flowers are sympetalous and strongly monosymmetric.

Chemistry, Morphology, etc. The calyx is distinctly monosymmetric. Remarkable intine-covered structures like pollen tubes are produced in all taxa before pollen germination (Blackmore & Cannon 1983); cf. also Dpisacaceae, sometimes (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 Morinaceae and Dipsacaceae, 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 Dipsacaceae as being glandular).

For embryology, see also Vijayaraghavan and Sarveshwari (1968: Morina longifolia only), for a monograph of the family, see Cannon and Cannon (1984), and for its phylogeny and biogeography, see Bell and Donoghue (2003).

Dipsacaceae + Valerianaceae: (annual herbs); saccharose +, quercetin 0; vessel elements with simple (scalariform) perforations; (nodes 5 or more:5 or more); leaves simple to ± pinnate, 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.

DIPSACACEAE Jussieu, nom. cons.   Back to Dipsacales

(Shrubby); 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.

1. Triplostegia

Valpotriate-type iridoids +; flowers with bracteoles and double epicalyx; C ± polysymmetrical; pollen aperture with a halo, colpus granulose; G [3]; fruit surrounded by capitate-glandular outer epicalyx, the tips hooked; endosperm slight; n = ?

1/2. Southeast Asia, East Malesia (map: from van Steenis 1951).

2. The Rest.

Inflorescence a capitulum, with an involucre; epicalyx single, 8-ribbed; (C with 4 lobes), (A 2-3); (pollen 3-porate); G [2]; ovule with integument 10-15 cells across; fruit with calycine awns or bristles; endosperm +; n = 5, 7-9(-10), chromosomes 1-5 µm long.

10/290: Scabiosa (80), Cephalaria (65), Knautia (60). Eurasia, Africa, esp. Mediterranean region (Map: see above; red). [Photo - Habit, Inflorescence, Flower.]

• Dipsacaceae are herbs with opposite leaves, usually capitate, involucrate inflorescences and more or less monosymmetric flowers each with a well-developed epicalyx. The dry fruit has a single seed.

Evolution. 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 family, 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 Dipsacaceae (e.g. 100% support in a 30 taxon-5 gene analysis - Davis et al. 2001; see also Bell & Donoghue 2000; 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 Valerianaceae. As they note, [Triplostegia + Valerianaceae] 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. Clearly, where Triplostegia ends up can substantially affect apomorphy positions, and the characters that Triplostegia and Valerianoideae have in common may be either apomorophies for the immediate clade, or for a larger clade.

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 of the family (Avino et al. 2009; Carlson et al. 2009). For other phylogenetic studies, see Caputo et al. (2004).

Synonymy: Scabiosaceae Martinov, Triplostegiaceae Airy Shaw

VALERIANACEAE Batsch   Back to Dipsacales

Foetid monoterpenoids and sesquiterpenoids, valpotriates +; true tracheids ?; leaf bases often sheathing; (plant dioecious), flowers small, (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), chromosomes 0.7-4 µm long.

17[list]/315: Valeriana (200: perhaps para- or polyphyletic - Hidalgo et al. 2004), Valerianella (80). N. temperate, especially Mediterranean, and Andean South America (half the family) (map: from Hultén 1958; Meusel et al. 1978). [Photo - Habit, Flower, Flower.]

• Valerianaceae are often foetid herbs with opposite, sometimes connate leaves and rather small flowers. The inflorescence is cymose and bracteolate. The sympetalous corolla is often spurred but other than that may be only weakly monosymmetric; the calyx often develops greatly in fruit.

Evolution. Divergence & Distribution. Crown-group Valerianaceae may be 60-55 million years old (Bell & Donoghue 2005a), but diversification in the Andean paramo - ca 1/7 of the family - happened less than 5 million years ago (Bell & Donoghue 2005b).

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 in the family. 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 family (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 Valerianaceae (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). For other phylogenies of the family, see Bell (2004) and Hidalgo et al. (2004).