EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, not motile, initially ±globular; showing gravitropism; acquisition of phenylalanine lysase [PAL], phenylpropanoid metabolism [lignans +, flavonoids + (absorbtion of UV radiation)], xyloglucans in primary cell wall, side chains charged; plant poikilohydrous [protoplasm dessication tolerant], ectohydrous [free water outside plant physiologically important]; thalloid, leafy, with single-celled apical meristem, tissues little differentiated, rhizoids +, unicellular; chloroplasts several per cell, pyrenoids 0; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles/centrosomes in vegetative cells 0, microtubules with γ-tubulin along its length [?here], interphase microtubules form hoop-like system; metaphase spindle anastral, predictive preprophase band of microtubules [where cell plate will join parental cell wall], phragmoplast + [cell wall deposition spreading from around the spindle fibres], plasmodesmata +; antheridia and archegonia jacketed, surficial; blepharoplast +, centrioles develop de novo, bicentriole pair coaxial, separate at midpoint, centrioles rotate, associated with basal bodies of cilia, multilayered structure + [4 layers: L1, L4, tubules; L2, L3, short vertical lamellae] (0), spline + [tubules from L1 encircling spermatid], basal body 200-250 nm long, associated with amorphous electron-dense material, microtubules in basal end lacking symmetry, stellate array of filaments in transition zone extended, axonemal cap 0 [microtubules disorganized at apex of cilium]; male gametes [spermatozoids] with a left-handed coil, cilia 2, lateral; oogamy; sporophyte multicellular, cuticle +, plane of first cell division transverse [with respect to long axis of archegonium/embryo sac], sporangium and upper part of seta developing from epibasal cell [towards the archegonial neck, exoscopic], with at least transient apical cell [?level], initially surrounded by and dependent on gametophyte, placental transfer cells +, in both sporophyte and gametophyte, wall ingrowths develop early; suspensor/foot +, cells at foot tip somewhat haustorial; sporangium +, single, terminal, dehiscence longitudinal; meiosis sporic, monoplastidic, MTOC [MTOC = microtubule organizing centre] associated with plastid, sporocytes 4-lobed, cytokinesis simultaneous, preceding nuclear division, quadripolar microtubule system +; wall development both centripetal and centrifugal, sporopollenin + laid down in association with trilamellar layers [white-line centred lamellae; tripartite lamellae], >1000 spores/sporangium; nuclear genome size <1.4 pg, main telomere sequence motif TTTAGGG, LEAFY and KNOX1 and KNOX2 genes present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes, precursor for starch synthesis in plastid.
Many of the bolded characters in the characterization above are apomorphies of subsets of streptophytes along the lineage leading to the embryophytes, not apomorphies of crown-group embryophytes per se.
All groups below are crown groups, nearly all are extant. Characters mentioned are those of the immediate common ancestor of the group,  contains explanatory material, () features common in clade, exact status unclear.
Abscisic acid, L- and D-methionine distinguished metabolically; sporophyte with polar transport of auxins, class 1 KNOX genes expressed in sporangium alone; sporangium wall 4≤ cells across [≡ eusporangium], tapetum +, secreting sporopollenin, which obscures outer white-line centred lamellae, columella +, developing from endothecial cells; stomata +, on sporangium, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and of rhizoids/root hairs; spores trilete; shoot meristem patterning gene families expressed; MIKC, MI*K*C* genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns, mitochondrial trnS(gcu) and trnN(guu) genes 0.
[Anthocerophyta + Polysporangiophyta]: gametophyte leafless; archegonia embedded/sunken [on;y neck protruding]; sporophyte long-lived, chlorophyllous; cell walls with xylans.
Sporophyte well developed, branched, branching apical, dichotomous, potentially indeterminate; hydroids +; stomata on stem; sporangia several, terminal; spore walls not multilamellate [?here].
Vascular tissue + [tracheids, walls with bars of secondary thickening].
EXTANT TRACHEOPHYTA / VASCULAR PLANTS
Sporophyte with photosynthetic red light response; (condensed or nonhydrolyzable tannins/proanthocyanidins +); plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; plant endohydrous [physiologically important free water inside plant]; (condensed or nonhydrolyzable tannins/proanthocyanidins +); xyloglucans with side chains uncharged [?level], in secondary walls of vascular and mechanical tissue; lignins +; stem apex multicellular, with cytohistochemical zonation, plasmodesmata formation based on cell lineage; tracheids +, in both protoxylem and metaxylem, G- and S-types; sieve cells + [nucleus degenerating]; endodermis +; leaves/sporophylls spirally arranged, blades with mean venation density ca 1.8 mm/mm2 [to 5 mm/mm2], all epidermal cells with chloroplasts; sporangia adaxial, columella 0; tapetum glandular; ?position of transfer cells; MTOCs not associated with plastids, basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; suspensor +, shoot apex developing away from micropyle/archegonial neck [from hypobasal cell, endoscopic], root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Sporophyte endomycorrhizal [with Glomeromycota]; growth ± monopodial, branching spiral; roots +, endogenous, positively geotropic, root hairs and root cap +, protoxylem exarch, lateral roots +, endogenous; G-type tracheids +, with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangium dehiscence by a single longitudinal slit; cells polyplastidic, MTOCs diffuse, perinuclear, migratory; blepharoplasts +, paired, with electron-dense material, centrioles on periphery, male gametes multiciliate; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; LITTLE ZIPPER proteins.
Sporophyte woody; stem branching lateral, meristems axillary; lateral root origin from the pericycle; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].
Plants heterosporous; megasporangium surrounded by cupule [i.e. = unitegmic ovule, cupule = integument]; pollen lands on ovule; megaspore germination endosporic [female gametophyte initially retained on the plant].
EXTANT SEED PLANTS / SPERMATOPHYTA
Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignin chains started by monolignol dimerization [resinols common], particularly with guaiacyl and p-hydroxyphenyl [G + H] units [sinapyl units uncommon, no Maüle reaction]; root stele diarch to pentarch, xylem and phloem originating on alternating radii, cork cambium deep seated; stem apical meristem complex [with quiescent centre, etc.], plasmodesma density in SAM 1.6-6.2[mean]/μm2 [interface-specific plasmodesmatal network]; eustele +, protoxylem endarch, endodermis 0; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; cork cambium superficial; leaf nodes 1:1, a single trace leaving the vascular sympodium; leaf vascular bundles amphicribral; guard cells the only epidermal cells with chloroplasts, stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; axillary buds +, exogenous; prophylls two, lateral; leaves with petiole and lamina, development basipetal, lamina simple; sporangia borne on sporophylls; spores not dormant; microsporophylls aggregated in indeterminate cones/strobili; grains monosulcate, aperture in ana- position [distal], primexine + [involved in exine pattern formation with deposition of sporopollenin from tapetum there], exine and intine homogeneous, exine alveolar/honeycomb; ovules with parietal tissue [= crassinucellate], megaspore tetrad linear, functional megaspore single, chalazal, sporopollenin 0; gametophyte ± wholly dependent on sporophyte, development initially endosporic [apical cell 0, rhizoids 0, etc.]; male gametophyte with tube developing from distal end of grain, male gametes two, developing after pollination, with cell walls; female gametophyte initially syncytial, walls then surrounding individual nuclei; embryo cellular ab initio, suspensor short-minute, embryonic axis straight [shoot and root at opposite ends; plant allorhizic], cotyledons 2; embryo ± dormant; ycf2 gene in inverted repeat, mitochondrial trans- nad2i542g2 and coxIIi3 introns present; whole nuclear genome duplication [ζ - zeta - duplication], two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], 5.8S and 5S rDNA in separate clusters.
ANGIOSPERMAE / MAGNOLIOPHYTA
Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANA grade?], lignin also with syringyl units common [G + S lignin, positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], hemicelluloses as xyloglucans; root apical meristem intermediate-open, pith relatively inconspicuous, lateral roots initiated immediately to the side of [when diarch] or opposite xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0, hypodermis suberised and with Casparian strip [= exodermis]; shoot apex with tunica-corpus construction, tunica 2-layered; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, not occluding pores of plate, companion cell and sieve tube from same mother cell; ?phloem loading/sugar transport; nodes 1:?; dark reversal Pfr → Pr; protoplasm dessication tolerant [plant poikilohydric]; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance with increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, secondary veins pinnate, fine venation hierarchical-reticulate, (1.7-)4.1(-5.7) mm/mm2, vein endings free; flowers perfect, pedicellate, ± haplomorphic, protogynous; parts free, numbers variable, development centripetal; P +, ?insertion, members each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], each theca dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, endothecium +, cells elongated at right angles to long axis of anther; tapetal cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine lamellate only in the apertural regions, thin, compact, intine in apertural areas thick, pollenkitt +; nectary 0; carpels present, superior, free, several, ascidiate [postgenital occlusion by secretion], stylulus at most short [shorter than ovary], hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry; suprastylar extragynoecial compitum +; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across, nucellar cap?; megasporocyte single, hypodermal, functional megaspore lacking cuticle; female gametophyte lacking chlorophyll, not photosynthesising, four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; ovule not increasing in size between pollination and fertilization; pollen grains land on stigma, bicellular at dispersal, mature male gametophyte tricellular, germinating in less than 3 hours, pollen tube elongated, unbranched, growing between cells, growth rate (20-)80-20,000 µm/hour, apex of pectins, wall with callose, lumen with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametes lacking cell walls, ciliae 0, siphonogamy; double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; mature seed much larger than fertilized ovule, small , dry [no sarcotesta], exotestal; endosperm +, cellular, development heteropolar [first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous, embryo short [<¼ length of seed]; plastid and mitochondrial transmission maternal; Arabidopsis-type telomeres [(TTTAGGG)n]; nuclear genome very small [1C = <1.4 pg, mean 1C = 18.1 pg, 1 pg = 109 base pairs], whole nuclear genome duplication [ε/epsilon event]; ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, palaeo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]]; chloroplast chlB, -L, -N, trnP-GGG genes 0.
[NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]]: wood fibres +; axial parenchyma diffuse or diffuse-in-aggregates; pollen monosulcate [anasulcate], tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.
[AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: phloem loading passive, via symplast, plasmodesmata numerous; vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood + [reaction wood: with gelatinous fibres, g-fibres, on adaxial side of branch/stem junction]; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; nucellar cap + [character lost where in eudicots?]; 12BP [4 amino acids] deletion in P1 gene.
[[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]] / MESANGIOSPERMAE: benzylisoquinoline alkaloids +; sesquiterpene synthase subfamily a [TPS-a] [?level], polyacetate derived anthraquinones + [?level]; outer epidermal walls of root elongation zone with cellulose fibrils oriented transverse to root axis; P more or less whorled, 3-merous [?here]; pollen tube growth intra-gynoecial; extragynoecial compitum 0; carpels plicate [?here]; embryo sac bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid.
[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (extra-floral nectaries +); (veins in lamina often 7-17 mm/mm2 or more [mean for eudicots 8.0]); (stamens opposite [two whorls of] P); (pollen tube growth fast).
[CERATOPHYLLALES + EUDICOTS]: ethereal oils 0.
EUDICOTS: (Myricetin, delphinidin +), asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; (vessel elements with simple perforation plates in primary xylem); nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; protandry common; K/outer P members with three traces, ("C" +, with a single trace); A ?, filaments fairly slender, anthers basifixed; microsporogenesis simultaneous, pollen tricolpate, apertures in pairs at six points of the young tetrad [Fischer's rule], cleavage centripetal, wall with endexine; G with complete postgenital fusion, stylulus/style solid [?here]; seed coat?
[PROTEALES [TROCHODENDRALES [BUXALES + CORE EUDICOTS]]]: (axial/receptacular nectary +).
[TROCHODENDRALES [BUXALES + CORE EUDICOTS]]: benzylisoquinoline alkaloids 0; euAP3 + TM6 genes [duplication of paleoAP3 gene: B class], mitochondrial rps2 gene lost.
[BUXALES + CORE EUDICOTS]: ?
CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one position]; micropyle?; γ whole nuclear genome duplication [palaeohexaploidy, gamma triplication], PI-dB motif +, small deletion in the 18S ribosomal DNA common.
[ROSIDS ET AL. + ASTERIDS ET AL.] / PENTAPETALAE: root apical meristem closed; (cyanogenesis also via [iso]leucine, valine and phenylalanine pathways); flowers rather stereotyped: 5-merous, parts whorled; P = calyx + corolla, 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, internal/adaxial to the corolla whorl, alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G , G  also common, when [G 2], carpels superposed, placentation axile, style +, stigma not decurrent; compitum +; endosperm nuclear; fruit dry, dehiscent, loculicidal [when a capsule]; RNase-based gametophytic incompatibility system present; floral nectaries with CRABSCLAW expression; (monosymmetric flowers with adaxial/dorsal CYC expression).
[DILLENIALES [SAXIFRAGALES [VITALES + ROSIDS s. str.]]]: stipules + [usually apparently inserted on the stem].
[SAXIFRAGALES [VITALES + ROSIDS]] / ROSANAE Takhtajan / SUPERROSIDAE: ??
[VITALES + ROSIDS] / ROSIDAE: anthers articulated [± dorsifixed, transition to filament narrow, connective thin].
ROSIDS: (mucilage cells with thickened inner periclinal walls and distinct cytoplasm); if nectary +, usu. receptacular; embryo long; chloroplast infA gene defunct, mitochondrial coxII.i3 intron 0.
ROSID I / FABIDAE / [ZYGOPHYLLALES [the COM clade + the nitrogen-fixing clade]]: endosperm scanty.
[the COM clade + the nitrogen-fixing clade]: ?
[FABALES [ROSALES [CUCURBITALES + FAGALES]]] / the nitrogen-fixing clade / fabids: (N-fixing by associated root-dwelling bacteria); tension wood +; seed exotestal.
[ROSALES [CUCURBITALES + FAGALES]]: ovules 1-2/carpel, apical.
Age. This node is estimated to be (110-)105(-100) or (94-)89(-84) m.y.o. (Hengcheng Wang et al. 2009); a very different age of around 429-199 m.y. is suggested by Jeong et al. (1999), while ages of around 92.2-78.9 m.y. are offered by Naumann et al. (2013), of (110-)97(-92) m.y.a. by Bell et al. (2010: c.f. topology), of ca 126 m.y. by Z. Wu et al. (2014), of around 107.4 m.y. by Hohmann et al. (2015), and about 106.4 m.y. by Tank et al. (2015: Table S1).
Evolution. Divergence & Distribution. It is difficult to optimize ovule number in this part of the tree; see also Taylor et al. (2012) for possible apomorphies.
Ecology & Physiology. Nitrogen fixing in this clade usually involves symbioses with the actinomycete Frankia, and this is discussed further on the Fabales page.
Bacterial/Fungal Associations. Rose (1980) noted that vesicular-arbuscular mycorrhizae co-occured on all plants with actinorrhizal Frankia nitrogen fixation that she studied - seven families, 7+ origins of the associations, and in four there were also/only associations with ectomycorrhizal fungi.
Phylogeny. For relationships, see above.
ROSALES Perleb Main Tree.
(Frankia infection +, by intercellular penetration); (isoflavonoids, dihydroflavonols +); mucilage cells +; roots diarch [lateral roots 4-ranked]; prismatic crystals in ray cells [not Barbeyaceae, Elaeagnaceae]; (sieve tube with non-dispersive protein bodies), (sieve tube plastids lacking starch - Rhamnaceae, Dirachmaceae?]); inflorescence cymose; hypanthium +, nectariferous, K valvate, C clawed; stigma dry; ovule 1/carpel, epitropous, micropyle endostomal; K and/or hypanthium persistent in fruit; (polyembryony +). - 9 families, 261 genera, 7725 species.
Age. Wikström et al. (2001) dated crown Rosales at (79-)76(-73) m.y., while other estimates are rather older: (96-)93, 88(-85) m.y. (two penalized likelihood dates), Bayesian relaxed clock estimates to 103 m.y. (Hengcheng Wang et al. 2009), ca 94 m.y. (Magallón & Castillo 2009), (104-)85, 82(-73) m.y. (Bell et al. 2010) and ca 97 m.y. (Z. Wu et al. 2014). However, the estimate in Xue et al. (2012) is only 40.8 or 31.9 m.y., that in Hohmann et al. (2015) is ca 87.7 m.y., in Tank et al. (2015: Table S2) is ca 89.4 m.y., in H.-L. Li et al. (2015) is (112.6-)106.5, 106.1(-100.2) m.y., while that in Jeong et al. (1999) is 367-170 m.y., so take your pick.
Note: Boldface denotes possible apomorphies, (....) denotes a feature common in the clade, exact status uncertain, [....] includes explanatory material. Note that the particular node to which many characters, particularly the more cryptic ones, should be assigned is unclear. This is partly because homoplasy is very common, in addition, basic information for all too many characters is very incomplete, frequently coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there are the not-so-trivial issues of how character states are delimited and ancestral states are reconstructed (see above).
Evolution. Divergence & Distribution. Rosales contain ca 1.9% of eudicot diversity (Magallón et al. 1999).
Ronse De Craene (2003, see also 2010) suggested that loss of petals might characterise Rosales, with apparent "petals" occupying the position of stamens and their evolution allowing e.g. Rosaceae to diversify. However, if Rosales are sister to Fabales, as Ronse de Craene (2003) thought, they are not a notably diverse group in terms of species numbers, the more so since almost 4,000 species of Rosales - about half - are in the Ulmaceae-Urticaceae group, which lack petals of any sort. The Ulmaceae-Urticaceae group forms a well-supported clade, and the wind pollination that is so common there cannot be considered basic to Rosales as a whole (c.f. Ronse de Craene 2010). Even with the relationships [Rosales [Cucurbitales + Fagales]] (see above) it seems that no argument connecting petals in Rosales with diversity can be made (see also Ronse de Craene & Brockington 2013).
A granular exine infratectum may be a synapomorphy for the clade (see also Doyle 2009); here it is placed as a synapomorphy for the [Ulmaceae [Cannabaceae [Moraceae + Urticaceae]]] clade, but it is found elsewhere in the order, too.
Plant-Animal Interactions. Quite a number of butterfly larvae - especially caterpillars of "basal" groups and Lycaeninae - feed here (Fiedler 1995; Janz & Nylin 1998).
Bacterial/Fungal Associations. Some taxa in at least Rosaceae, Rhamnaceae, Elaeagnaceae and Ulmaceae are ectomycorrhizal (see Malloch et al. 1980; S. E. Smith and Read 1997). For a summary of what is known about nitrogen fixation in this clade, see Santi et al. (2013).
Genes & Genomes. The position of the duplication that resulted in two copies of the granule bound starch synthase I gene is unclear; two copies are found in all Rosceae, but also in Frangula (Rhamnaceae) (Evans & Campbell 2002).
Chemistry, Morphology, etc. Roots are commonly diarch in Rosaceae, but are also tetrarch, etc.; sampling elsewhere is poor, although less so in Ulmaceae and relatives, and diarch roots are found throughout the order. Tracheary members in Rosaceae commonly have pseudotori (thickenings in pit membranes associated with plasmodesmata), while true tori occur in Rosaceae (Cercocarpus) and also Cannabaceae and Ulmaceae (Jansen et al. 2007; Coleman et al. 2004; Dute 2015), although these tori are formed in two different ways (Dute et al. 2010a) and the torus is only weakly lignified. Sieve tube plastids lacking both starch and protein inclusions are rare outside Rosales, although they have been found in some parasites as well as Crassulaceae and Malpighiaceae (Behnke 1991a). For polyembryony, sporadic here, see G. Dahlgren (1991).
Kubitzki (2004) provides a summary of the order; there is much useful information in Thulin et al. (1998).
Phylogeny. In early molecular studies Rosaceae appeared as sister to the rest of the order (strong support: Savolainen et al. 2000a; Wang et al. 2009), while Ulmaceae and relatives (the old Urticales) and Rhamnaceae and relatives formed two clades (also Thulin et al. 1998; Savolainen et al. 2000b; Richardson et al. 2000b; Sytsma et al. 2002: position of Rosaceae, etc., uncertain; Wang et al. 2009; Soltis et al. 2011), as in the tree below. The position of Elaeagnaceae was sometimes rather labile (Richardson et al. 2000b: successive approximation weighting), even being embedded in Rhamnaceae in a rbcL analysis, and there was quite strong support for a clade [Barbeyaceae + Dirachmaceae]. The tree found by S.-D. Zhang et al. (2011) is based on an analysis of twelve genes (10 plastid genes) from 25 taxa of Rosales, and the major relationships within the order are very well supported, although somewhat less so in the subclade that includes Rhamnaceae; their relationships are followed here. H.-L. Li et al. (2015) found weak support for a [Elaeagnaceae + Dirachmaceae] clade.
There is also the issue of the placement of the holoparasitic Cynomoriaceae. Z.-H. Zhang et al. (2009; see also Moore et al. 2011) placed Cynomoriaceae in Rosales and sister to Rosaceae based on analyses of chloroplast inverted repeat sequences; support was strong, but Moraceae were the only other family in the order examined. Cynomoriaceae certainly were to be excluded from Saxifragales (good sampling) where they had sometimes been included, albeit with modest support (see Saxifragales page for further details). S.-D. Zhang et al. (2011) did not include Cynomoriaceae in their study.
Previous Relationships. In the past, Urticales (Urticaceae, Moraceae, etc.) were kept well separate from Rosaceae, largely because their very reduced and usually wind-pollinated flowers suggested relationships to the old Amentiferae.
Includes Barbeyaceae, Cannabaceae, Dirachmaceae, Elaeagnaceae, Moraceae, Rhamnaceae, Rosaceae, Ulmaceae, Urticaceae.
Synonymy: Rhamnineae Shipunov - Amygdalales Link, Artocarpales Martius, Barbeyales Takhtajan & Reveal, Cannabales Döll, Dryadales Link, Elaeagnales Berchtold & J. Presl, Ficales Dumortier, Frangulales Wirtgen, Morales Martius, Rhamnales Link, Sanguisorbales Link, Spiraeales Link, Ulmales Link, Urticales Berchtold & J. Presl - Barbeyanae Reveal & Doweld, Rhamnanae Reveal, Rosanae Takhtajan, Urticanae Reveal - Frangulopsida Endlicher, Rhamnopsida Brongniart, Rosopsida Batsch Urticopsida Bartling - Rosidae Takhtajan
ROSACEAE Jussieu, nom. cons. Back to Rosales
Triterpenes +, alkaloids 0; cork deep seated; (vessel elements with scalariform perforation plates); (true) and fibre tracheids +; sieve tubes with non-dispersive protein bodies; petiole vasculature of arcuate or annular bundles, or annular; leaves spiral (opposite), lamina vernation usu. conduplicate, (secondary veins palmate), stipules often petiolar; inflorescences racemose; flowers protogynous or condition ± undecided; (C 0); A (1-)15-many [ca 20 common - 10 + 5 + 5, centripetal, in groups], (latrorse); (pollen porate); G free, stigmas punctate to expanded, or decurrent down stylulus; extragynoecial compitum 0; ovules with parietal tissue 2-4 cells across, nucellar cap ca 4 cells across; megaspore mother cells several; fruit aggregate of achenes; exotestal cells periclinally elongated, radial walls thickened, or palisade or tabular, walls with spiral or reticulate thickenings, outer wall often becoming mucilaginous, endotegmic cells slightly thickened, or seed coat undistinguished; chalazal endosperm haustorium +; x = 9; genome size [2C] (0.2-)0.42-3.0 pg, duplication of GBSSI [granule bound starch synthase I] gene.
90[list]/2520. World-wide, but esp. N. hemisphere, often not deserts or tropical rainforest (map: from Vester 1940 [overly optimistic - or inc. Chrysobalanaceae?]; Hultén 1971; Trop. Afr. Fl. Pl. Ecol. Distr. 2. 2006; FloraBase i.2013; Australia's Virtual Herbarium i.2013). [Photos - Collection, Collection.]
Age. Crown-group Rosaceae are dated to (92.8-)88.3(-84.2) m.y.a. (Chin et al. 2014) or around 61.2 m.y. (Hohmann et al. 2015).
Turonian fossils some 90 m.y. old are assignable to Rosaceae (Crepet et al. 2004 for references).
1. Rosoideae Arnott
Herbs to shrubs; 2-pyrone-4,6dicarboxylic acid, ellagic acid +; rays often narrow; cuticle waxes as narrow ribbons and triangular rodlets; leaves usu. compound; (epicalyx +), carpels many; fruits usu. achenes or drupelets; ovule (straight), unitegmic; x = 7; plant with phragmidiaceous rusts.
Especially temperate (to Arctic) areas.
Age. Crown-group Rosoideae (note sampling) are dated to (83.2-)71.1(-64.3) m.y.a. (Chin et al. 2014).
1A. Filipendula - Plant herbaceous; receptacle enlarged; ovules 2/carpel, superposed. - 1/10. Eurasia.
Synonymy: Ulmariaceae Gray
Rosodeae T. Eriksson, Smedmark, & M. S. Kerr [= all other Rosoideae]: ?
Prickly scrambling shrub; receptacle enlarged; ovules 2/carpel, collateral, integument ca 6 cells across; fruit an aggregate of drupelets. - 1/±250-800<. ± Worldwide, esp. N. Temperate.
Synonymy: Chamaemoraceae Lilja
1C. Colurieae Rydberg
Ovule apotropous [Geum]; seed coat vascularized [Waldsteinia].
3/42: Geum (40). Temperate, inc. montane tropics, Chile.
[Sanguisorbeae [Roseae + Potentilleae]]: ?
1D. Sanguisorbeae Candolle
G 1-5; integument 6-8 cells across; phragmidiaceous rusts 0.
Within Sanguisorbeae are two subtribes. Agrimoniinae J. Presl - 5/20: Agrimonia (15). N. Temperate, Africa. Sanguisorbineae Torrey & A. Gray - 7/360: Cliffortia (115), Acaena (100). ± Worldwide, few Indo-Malesia, tropical America.
Synonymy: Agrimoniaceae Gray[?], Fragariaceae Nestler, Poteriaceae Rafinesque, Sanguisorbaceae Berchtold & J. Presl
[Roseae + Potentilleae]: ?
Prickly arching shrub; hypanthium fleshy, urn-shaped, carpellary vascular supply recurrent; integument ca 8 cells across. - 1/100-150. N. temperate; 1/3 spp. in Europe.
1F. Potentilleae Sweet
(Epicalyx +); receptacle enlarged; integument ca 4 cells across. Potentillineae: style often lateral/gynobasic. 5-6/540: Potentilla + Argentina et al. N. temperate to Arctic (montane tropics to S. temperate). [Fragariinae + Alchemillinae]: anther thecae more or less confluent; parietal tissue ca 2 cells across, nucellar cap ca 7 cells across. Fragariinae Torrey & A. Gray: (leaves simple); (G 1); phragmidiaceous rusts 0 (Fragaria +). 10/60. Alchemillinae 3/960-1100: Alchemilla (1000+). N. temperate, esp. Europe, tropical mountains (S. temperate).
Synonymy: Alchemillaceae Martinov, Potentillaceae Berchtold & J. Presl, Tormentillaceae Martynov
[Dryadoideae + Amygdaloideae]: sugar alcohol sorbitol + [transport carbohydrate], cyanogenic glycosides +.
2. Dryadoideae Juel
Association with N-fixing Frankia, (ectomycorrhizal); dhurrin as the cyanogenic glycoside; (torus-margo pits + - Cercocarpus); leaves usu. simple; G 1-many; ovules straight (anatropous, apotropous - Dryas), (with chalazal projection - Cercocarpus); fruits achenes with hairy styles.
4/19: Cercocarpus (8). W. North America, Dryas circumboreal.
Age. Crown-group Dryadoideae are dated to (83.2-)63.1(-44.7) m.y.a. (Chin et al. 2014).
Synonymy: Cercocarpaceae J. Agardh, Dryadaceae Gray
3. Amygdaloideae Arnott
Plant woody, (ectomycorrhizal); flavones +, ellagic acid 0; cuticle waxes as tubules or platelets; leaves simple (compound); G <5, opposite petals or sepals, 2 ovules/carpel, papillate funicular obturator +, stigma usu. wet; fruit a follicle.
Age. Crown-group Amygdaloideae are (91.8-)87.0(-82.8) m.y.a. (Chin et al. 2014), and somewhere around about here (51-)47-46(-42) m.y. (Wikström et al. 2001), (59-)44, 40(-27) m.y. (Bell et al. 2010).
3A. Lyonothamnus A. Gray
Cyanogenic glycosides 0; leaves opposite, compound, stipules deciduous; G seminferior, placentation apical; ovules 4-6/carpel.
1/1: Lyonothamnus floribundus. California Islands, off S. California.
3B. Niellieae Maximowicz
Cyanogenic glycosides?; leaf teeth colleter-like; ovule 1/carpel, apical, apotropous (-5, pleurotropous); fruitlets hard, shiny, indehiscent; n = 9.
2/24: Niellia (14). E. and W. North America, northeast Asia.
Synonymy: Neilliaceae Miquel
[Prunus + The Rest]: ovules 2/carpel, collateral.
Age. Crown-group Prunus + The Rest are dated to 36.1-34.3 m.y. (Naumann et al. (2013: too young), (72.4-)67.8(-63.7) m.y.a. (Chin et al. 2014) and about 49.6 m.y. (Hohmann et al. 2015).
3C. Amygdaleae Jussieu
(Plant ectomycorrhizal); cork superficial; true tracheids 0; lamina vernation laterally or vertically conduplicate, extrafloral nectaries +, on petiole, towards base of the margin, or abaxial lamina, leaf teeth colleter-like; G 1, stigma bilobed; outer integument 6-8 cells across, inner integument 3-6 cells across, nucellar cap 2-3 cells across, (cotyledon 1, ca 12 cells across), parietal tissue ca 8 cells across, obturator from ovary wall; fruit a drupelet; seed coat mostly pachychalazal; n = 8.
1/200. Temperate and tropical montane.
Age. The beginning of diversification within Prunus has been dated to (67.4-)62.4, 60.7(-55) m.y.a. (Chin et al. 2014); there are well-preserved ca 49.5 m.y.o. fossil flowers of Prunus from Washington State (Benedict et al. 2011).
Synonymy: Amygdalaceae Marquand, Prunaceae Martinov
Kerriodae D. Potter, S. H. Oh, & K. R. Robertson [= Osmaronieae + Kerrieae]: phragmidiaceous rusts 0; non-cyanogenic nitrile glucosides +.
3D. Osmaronieae Rydberg
Cork superficial; pith chambered; stipules deciduous; styles lateral; obturator from ovary wall; fruit a drupe, or septicidal capsule, the carpels also opening adaxially [Exochorda]; seed coat vascularized [Exochorda, Oemleria]; n = 8.
3/9: also Prinsepia. Central to East Asia, W. North America.
Age. Well-preserved fossil flowers of Osmaronia from ca 49.5 m.y.o. are known frrom northeastern Washington State, U.S.A. (Benedict et al. 2011).
3E. Kerrieae Focke
Wart-like projections on lamina; G 1-5; ovule ?obturator; fruit an aggregate, nut-like units, (achenes: Neviusia); n = ?
4/4. East Asia, W. North America, Alabama.
Synonymy: Coleogynaceae J. Agardh, Rhodotypaceae J. Agardh
3F. Sorbarieae Rydberg
Leaves compound (simple: Adenostoma); (G 1, Adenostoma), placentation apical; (fruit an achene: Adenostoma).
4/8: Spiraeanthus (4). Central to East Asia, W. North America
3G. Spiraeeae Candolle
Vestured pits +; nodes 1:1 [?all]; stipules 0; ovules 6-8/carpel, unitegmic; (fruit an achene - Holodiscus).
Age. The age of this clade is estimated to be around (62.9-)59.2(-56.0) m.y. (Chin et al. 2014).
8/106: Spiraea (80-100). N. temperate, to Columbia, (S. and) E. Africa, West Malesia.
Synonymy: Spiraeaceae Bertuch
Pyrodeae C. S. Campbell, R. C. Evans, D. R. Morgan, & T. A. Dickinson
Flavone C-glycosides +; cork superficial [?Gillenia]; rays often narrow; colleters + [probably elsewhere]; G ± connate, adnate to base of hypanthium, opposite sepals or odd member abaxial, gynoecial ring primordium +; ovules two/carpel, ± apotropous, (micropyle bistomal), funicular obturator +; exotesta ± thickened, often mucilaginous, mesotesta thick, sclerotic; Gymnosporangium rust common.
Age. The crown-group age of this clade can be dated to (67.1-)60.6(-55) m.y.a. (Chin et al. 2014).
1/2. E. North America.
N = 17; four copies of GBSSI gene. 33/ca 1000.
3I. [Kageneckia + Lindleya]
(Plant dioecious); 4-many pleurotropous ovules/carpel; (ovules with with chalazal projection - Kageneckia); Gymnosporangium rust 0.
2/5. Mexico, Peru, Chile. [Kageneckia Flower, Fruit.]
Synonymy: Lindleyaceae J. Agardh
Tannin-containing cells pervasive; fruit septicidal, carpels opening adaxially (and partially abaxially as well); ovules with with chalazal projection; n = 15.
1/3. S.W. North America.
3K. Malinae Reveal
(Plant ectomycorrhizal); crystals in axial parenchyma; (leaves compound), stipules deciduous; G at least half inferior, (carpels laterally free); outer integument 5-14 cells across, inner integument 3-6 cells across, nucellar cap ca 4 cells across; hypanthium fleshy in fruit ["pome"], (endocarp +).
30/1000: Sorbus (260), Crataegus (260, inc. Mespilus), Cotoneaster (260), Pyrus (75), Malus (55). Largely north Temperate.[Photo - Flower]
Synonymy: Cydoniaceae Schnizlein, Malaceae Small, nom. cons., Mespilaceae Schultz-Schultzenstein, Pyraceae Vest, Sorbaceae Brenner
Floral formula: * ⚥ K 5; C 5; A (10-)15<; N; G (1-)10< / [3-5].
Evolution. Divergence & Distribution. Rosaceae are perhaps one of the more diverse clades in the angiosperms (Magallón & Sanderson 2001: but c.f. dates and species numbers). Prunus endocarps have been found in the early Eocene of China ca 55 m.y.a., and there was considerable diversification of the family in the Eocene (Wehr & Hopkins 1994; DeVore & Pigg 2007; Benedict et al. 2011; Q.-Y. Li et al. 2011 and references).
The inferior-ovaried Pyrinae may represent a rapid but ancient radiation (Campbell et al. 2007). Stem group Pyrinae have been dated to (64-)58, 53(-43) m.y., with subsequent divergence in the Eocene and Oligocene, a substantial amount of movement around the northern hemisphere, probably via the Beringian land bridge, and much heterogeneity in clade size that is independent of age (Lo & Donoghue 2012). Aldasoro et al. (2005) also suggest biogeographic relationships in this group. There are about 34 species of Lachemilla (= Alchemilla) growing in the páramo (Gehrke et al. 2008; Sklenár et al. 2011).
Optimisation of characters on the tree presents problems. Potter et al. (2007) used DELTRAN, and so being host to Gymnosporangium rusts is not an apomorphy of Pyrodeae; using ACCTRAN (as here) it is. They reasonably divided up the presence of sorbitol (see e.g. Waalart 1980; Rennie & Turgeon 2009) into two states; it might be present in only small amounts (Dryadoideae), or it was more abundant (Amygdaloideae); presence of at least some sorbitol is used here to characterize the larger clade.
Ecology & Physiology. Some, but not all, Dryadoideae, are N-fixers, but the widespread Dryas integrifolia appears to be unable to fix nitrogen (Markham 2009). Nodules and association with Frankia have also been reported from other Rosaceae, e.g. from Rubus ellipticus (Markham 2009). Species of the N-fixing Cowania (Dryadoideae) and the non N-fixing Fallugia (Rosoideae-Colurieae) can form successful grafts; when Fallugia is the stock the combination will not fix nitrogen (Kyle et al. 1986).
Dryas is ectomycorrhizal, and is one of the eight major biomass accumulators in tundra vegetation. Four others are also ectomycorrhizal, and the apparently endomycorrhizal Rubus is also on this list (Chapin & Körner 1995; Gardes & Dahlberg 1996).
Potentilla arguta has glandular hairs and may be protocarnivorous, being able to digest proteins (?source of enzymes) and take up at least some of the products (Spomer 1999); the ability of plants with such hairs to digest at least some proteins is quite widespread.
Pollination Biology. There is a period of about 19 days between pollination and fertilization in Prunus persica (Herrera & Arbeloa 1989).
For apomixis, unequal partitioning of the chromosomes at meiosis, and hybridization, see below.
Plant-Animal Interactions. Galls caused by cecidomyid midges are quite common in North American Rosaceae (Gagné 1989). Cynipid gall wasps of the tribe Diplolepidini are notably common on Rosa, Diplolepis rosae forming the well-known robin's pincushion or bedeguar gall (Csoka et al. 2005; Redfern 2011).
There are prominent basal nectary glands on the lamina of fossils identified as Prunus from the Okanogan Highlands formation of western North America ca 49.5 m.y.o. (DeVore & Pigg 2007; Benedict et al. 2011), apparently the earliest example of foliar extrafloral nectaries.
Bacterial/Fungal Associations. At least some Dryadoideae and Amygdaloideae are ectomycorrhizal. For ectomycorrhizae on Dryas, sometimes very diverse, see Gardes and Dahlberg (1996) and Timling and Taylor (2012). Geopora (Pezizales, an ascomycete) is the fungus involved in the mycorrhizae of Cercocarpus (Amygdaloideae), and it also forms associations with Quercus (Fagaceae) and Arctostaphylos (Ericaceae), the result being a complex mycorrhizal network. Ascomycetes are associated with other ectomycorrhizal members of the family, which include Purshia (McDonald et al. 2010). Rose (1980) recorded vesicular-arbuscular mycorrhizae on Purshia and Cercocarpus.
Savile (1979b; see also Jackson 2004b: possible codivergence) discusses the distribution of phragmidiaceous rusts within Rosaceae-Rosoideae; they are found on no other Rosaceae, and only rarely on plants from other families. Most of these rusts are autoecious, that is, their entire life cycle occurs on the one species. Gymnosporangium rusts, found scattered on Amygdaloideae-Pyrodeae, are heteroecious. Here the telial stage (the teliospore is a thick-walled resting spore that germinates to produce basidiospores) is common on some Cupressaceae, the aecial stage, which produces thinner-walled binucleate aeciospores, is found on Pyrodeae (Lo & Donoghue 2012 for "gains" and "losses" of infestation). Fruits of Amygdaloideae can be seriously damaged by Monilinia (polyphyletic - ascomycete-Sclerotiniaceae), also found on Ericaceae (Holst-Jensen et al. 1997). Interestingly, Rosaceae rarely produce phytoalexins, protective compounds induced by e.g. fungal infection (Harborne 1999).
Genes & Genomes. The basic chromosome number of the family may be x = 7 (Shulaev et al. 2010). It has long been suspected that Pyreae were of wide hybrid origin, as their chromosome number might imply (n = 9 [Rosoideae] x n = 7 [Spiraeaoideae] → n = 16 [some Maloideae]) (Evans et al. 1998). However, Evans and Campbell (2002) suggest that polyploidisation with subsequent aneuploidy (9 x 2 → 18, 18 - 1 → 17) within the diploid Gillenia clade (herbaceous, with compound leaves) or something similar is more likely. Gillenia is sister to Pyreae (Potter et al. 2002; Evans & Dickinson 2002) and is host to the same rusts that are found on other Pyrodeae, but it has only two copies of GBSSI, as is the condition in the rest of the family. Genome sizes in the family are rather low, although higher than in most other members of the family in Pyreae (Dickson et al. 1992). There may have been a genome duplication in Malus and Pyrus somewhere around (21.3-)19.9, 18.3(-16.4 m.y.a., although the oldest fossils assigned to these genera are about 2½ times as old (Vanneste et al. 20104a).
Hybridization and polyploidy are common in Rosaceae, and there is "intergeneric" hybridisation in Rosoideae (Smedmark et al. 2003). For the relationship between polyploidy and diversification - perhaps direct - see Vamosi and Dickinson (2006). Here, as elsewhere in angiosperms, this relationship is probably not because speciation is faster in polyploids (the reverse may be more likely), rather, it is more likely to be the result of a ratchet mechanism since polyploidy is irreversible (Scarpino et al. 2014). Allopolyploidy in Fragariinae and its taxonomic implications were studied by Lundberg et al. (2009). Within Fragaria itself, the only taxon known to have one of the parental genomes of the South American F. magellanica grows in eastern Japan (Rousseau-Gueutin et al. 2009). Within Crataegus clades are linked with geography, but parents of genomes may have very disparate geographic origins (Lo et al. 2009). Deep hybridization within Prunus has been invoked to explain contrasting phylogenies obtained when using nuclear and plastid data, and it also fits with chromosome numbers (Chin et al. 2014).
Further complicating the issue is the fact that apomixis is also common, as in taxa like Rubus (e.g. Sochor et al. 2015), Potentilla and Alchemilla (Rosoideae: e.g. Dobeš et al. 2015) and Amelanchia, Sorbus, Cotoneaster and Crataegus (Amygdaloideae-Pyrodeae) (Dickinson et al. 2007; see also Asker & Jerling 1992; Hörandl et al. 2007; Talent & Dickinson 2007; etc.). Hybridisation occurs in Crataegus, and the hybrids are triploid and apomictic. There were ca 17 North American species of Crataegus in 1896, while 30 years later there were over 1000 species, and at least some were triploid apomictic hybrids; C. S. Sargent described over 700 of these. In general, the evolution of apomixis seems to have preceded hybridisation (Dickinson et al. 2007). In pentaploid Rosa unequal division occurs at meoisis, and as a result megaspores have 4/5th of the genome and microspores 1/5th (Wissemann & Ritz 2007 and references). There are ca 755 species of European brambles, of which 6 are diploid (two of these may be extinct), although there are four more diploids in surrounding areas, as well as others in North America, etc. (Sochor et al. 2015). In Amelanchier the diploid taxa behave as species according to several definitions of the term; polyploid apomicts are as it were superposed on top of them and break down the relative simplicity of the diploid's variation patterns (Burgess et al. 2015).
Chemistry, Morphology, etc. For general chemistry, see Hegnauer (1973, 1990), and for 2-pyrone-4,6dicarboxylic acid distribution, see Wilkes and Glasl (2001). Okuda et al. (1992) discuss tannin distribution in the family; chlorogenic acid was found in nearly all taxa examined. For non-cyanogenic glucosides, apparently restricted to Kerriodae, see Lechtenberg et al. (1996).
A polyderm is common, although perhaps not occurring in Pyreae (Mylius 1913). 1:1 nodes occur in Spiraea, a genus that also lacks stipules, although normally Rosaceae have stipulate leaves and 3:3 nodes (see e.g. Sinnott & Bailey 1914). There are extensive data on cuticle waxes in the family (Fehrenbach & Barthlott 1988), but they are recorded only as summaries in the context of conventional subfamilies; Barthlott (pers. comm.) kindly provided a more detailed breakdown. Chin et al. (2013) surveyed nectaries and nectary-like structures on the leaves of Prunus and optimized them on a phylogenetic tree. Interestingly, leaf teeth in several species of the genus, as well as in Niellia and Physocarpus, are colleter-like both in terms of their structure and what they secrete (mucilage); other species of Amygdaloideae, at least, should be surveyed for such teeth.
The epicalyx that occurs in some Rosaceae seems to represent stipules associated with the calyx members. For hypanthium development, see Rauh and Reznik (1951). Ronse de Craene (2007) wondered whether the petals were modified staminodes. There are often five traces to each carpel. Even in taxa with inferior ovaries, there is great variation in whether or not the carpels are connate, or what parts are connate, and in whether or not the carpels are adnate to the axial tissue enveloping the carpels/hypanthium. Thus Cotoneaster has an inferior ovary in which the carpels are more or less separate from each other although adnate to the hypanthium, c.f. also Pyracantha. The odd genus Dichotomanthes, also included in Pyreae, has a single carpel that is superior in position (Rohrer et al. 1994); this must represent a reversal. In general, the style of a separate carpel is somewhat off-centre, and a gynobasic style is but an extreme form of this asymmetry. The single, basal ovule of Chamaebatia (Dryadoideae) lacks an obturator (Evans & Dickinson 2002), while ovules of Rhodotypos have a protruding nucellus (c.f. Rhamnaceae). Within Prunus there may be one or two integuments, in the latter case, these may be free only above the micropyle (Lora et al. 2015). The lignified exotesta common in the family can be found even in the seeds of the drupaceous Prunus.
Some general information is taken from Decaisne (1874), Robertson (1974), Kalkman (2004), Judd et al. (2002), and especially Potter et al. (2007). There is information on cork initiation and bark anatomy in Lotova and Timonin (e.g. 1998, 1999, 2002) and Weiss (1890), on wood anatomy in S.-Y. Zhang (1992), on petiole vasculature in Morvillez (1917), on carpel orientation and general morphology in Focke (1888), Schäppi (1951: peltate and plicate carpels), Schäppi and Steindl (1950), Sterling (1969 and references), Kania (1973: also androecium) and Weberling (1989), androecial diversity is discussed in Murbeck (1941: also vasculature, Neurada etc. "basal") and Lindenhofer and Weber (2000 and references), pollen morphology in Sanguisorbeae in Chung et al. (2010), carpel development in van Heel (1981, 1983), ovule morphology in Péchoutre (1902: quite comprehensive, also seeds), Juel (1918: see comments on Péchoutre; orientation of carpels) and Schäppi and Steindl (1950: Rosoideae), exotesta in Frohne and Jensen (1992), and floral development in Evans and Dickinson (1999a, 1999b, 2005); for information on Vauquelinia, see Hess and Henrickson (1987), for that on Geum, see Kajewski (1957: classic cytological work) and Smedmark and Eriksson (2006: development of stylar hook).
Phylogeny. Rosoideae and a number of clades within it, Amygdaloideae, Amygdaloideae minus Lyonothamnus, [Pyrodeae + Sorbarieae] and Pyrodeae are all well-supported, but little can yet be said of other larger patterns of relationship (e.g. Morgan et al. 1994; Potter et al. 2002; Potter 2003; Potter et al. 2007a). The position of Dryadoideae is uncertain, other than being a rather "basal" branch in the tree (Potter et al. 2002: Evans et al. 2002), hence perhaps its lack of obturators. Potter (2003: several genes) found that Dryadoideae were fairly well supported as sister to remaining Rosaceae, but their position was not secure in Potter et al. (2007a), although a sister group relationship with Spiraeaoideae (= Amgydaloideae) was perhaps most likely, while Chin et al. (2014) and H.-L. Li et al. (2015) suggested that Dryadoideae and Rosoideae formed a clade (crown-group age in the latter: (96.1-)87.6, 86.1(-63.3) m.y.).
Eriksson et al. (2003) provide a phylogeny of Rosoideae: Alchemilla, Fragaria, and other genera form a well-supported clade outside Potentilla and relatives (see also Dobeš & Paule 2010). Filipendula is sister to other Rosoideae. Within Potentilleae, Potentilla is sister to the rest (see Eriksson et al. 2003), or, more precisely, Potentilla (including a few genera) is sister to a small clade including Argentina (Potentilla sect. Anserina), the two forming a clade sister to the other Potentilleae (all relationships with strong support: Dobeš & Paule 2010); see Eriksson et al. (2015) for the polyphyly (five separate clades!) of the small genus Sibbaldia. Fragariinae are sister to Alchemillinae; for relationships within Alchemilla s.l., which have a strong geographic signal, see Gehrke et al. (2008). The current infrageneric classification of Rubus does not reflect relationships there (Alice & Campbell 1999). For Rosa, see Bruneau et al. (2007), Wissemann and Cox (2007) and Koopman et al. (2008); relationships here are not easy to disentangle. There is still rather little support in the quite comprehensive analysis of Fougère-Danezan et al. (2015), again, hybridization complicates the issue.
Within Amygdaloideae, Exochorda forms a small clade along with Oemleria and Prinsepia (Evans & Dickinson 1999a for information); they have been placed near Prunus (Potter et al. 2002, see also Lee & Wen 2001) to which they do show some morphological similarity. Amygdaleae are circumscribed narrowly here (one genus, Prunus, from which there have previously been segregates), following Potter et al. (2002, 2007a). For phylogenies of Prunus, see Lee and Wen (2001), Wen et al. (2008: some conflict between ITS and ndhF), Yazbek and Oh (2013: subgenus Amygdalus) and Chin et al. (2014: two main clades, one with racemose inflorescences). The distribution and nature of calcium oxalate crystals correlate quite well with relationships (see Lersten & Horner 2000). Maddenia (dioecious, apetalous) is also to be included in Prunus (Potter et al. 2007a).
Aldasoro et al. (2005) suggest morphological relationships in the inferior-ovaried Pyrinae. Generic limits there have been difficult, since there is little molecular divergence between many of them but considerable divergence within them (Dickinson et al. 2007; Q.-Y. Li et al. 2012: little support for most of the relationships discussed). Recent work including over 330 species and large amounts of data has provided substantial resolution of relationships in Pyrinae, although support along the backbone could still be improved (Lo & Donoghue 2012). Lo et al. (2007), and Zarrei et al. (2014, 2015) focussed on Crataegus s.l. where hybridization greatly confuses the issue, while F. Li et al. (2014) looked at relationships within Cotoneaster, where nuclear and chloroplast genes tended to suggest different relationships, again perhaps because of past hybridization. Interestingly, Cotoneaster forms grafts with Crataegus. See also Chin et al. (2014) for relationships in Amygdaloideae.
Classification. Fruit types are certainly not as good indicators of relationships within Rosaceae as was for a long time thought, but chemistry, chromosomes, and fungi all support the realignments suggested by molecular data (especially Morgan et al. 1994), as does developmental work by Evans and Dickinson (1999a, b, 2002). Thus the old Spiraeoideae (= Amygdaloideae; changed iii.2014), characterised by follicular fruit, are strongly paraphyletic, and include both Prunoideae/Amygdaloideae and Maloideae; Prunoideae were characterized by drupaceous fruits, and Maloideae by their pomes (a pretty useless term). In the past Spiraeoideae had been considered a very natural group (e.g. Kalkman 1988), however, tribes in it may represent clades (especially Evans et al. 2002; Potter et al. 2007a). The classification here follows that of Potter et al. (2007a).
Generic limits in Pyrinae may reflect the European origin of taxonomy and the fact that the group is common in Europe (e.g. Walters 1961). However, there is now support for many of the main clades there and one can now aspire to a stable taxonomy; Sorbus and some other genera have turned out to be polyphyletic (Lo & Donoghue 2012), although it does not make deciding on generic limits any easier (Gehrke in Kadereit et al. 2016). Generic limits in Potentilleae are becoming clearer (Dobes & Paule 2010, but see Soják 2008 for an alternative); Alchemilla is to include Aphanes and Lachemilla (Gehrke et al. (2008).
Previous Relationships. Rosaceae as circumscribed above are holding together very well despite their morphological heterogeneity, but there have been departures. Chrysobalanaceae, often associated with Rosaceae in the past, are well embedded within Malpighiales, Quillaja rather unexpectedly is an isolated clade within Fabales, while Guamatela is correspondingly isolated in Crossosomatales (Oh & Potter 2006).
Botanical Trivia. Trees of Polylepis tarapacana grow at some 5,100 m in Bolivia, the highest known altitude for all trees (Hoch & Körner 2005).
[[Rhamnaceae [Elaeagnaceae [Barbeyaceae + Dirachmaceae]]] [Ulmaceae [Cannabaceae [Moraceae + Urticaceae]]]]: styles branched; ovules apotropous, trans-spliced intron in nad1 gene [cis-spicing elsewhere].
Age. The age for this node is some (70-)67, 65(-62) m.y. (Wikström et al. 2001), (86-)76, 73(-65) m.y. (Bell et al. 2010), ca 68.4 m.y. (Naumann et al. 2013), or ca 78.1 m.y. (Tank et al. 2015: Table S2).
Evolution. Genes & Genomes. For nad1 intron splicing, see Qiu et al. (1998).
[Rhamnaceae [Elaeagnaceae [Barbeyaceae + Dirachmaceae]]]: petiole bundle arcuate; stamens = and opposite C/alternate with P; capsule septicidal; ovule basal, parietal tissue 5-6 cells across; coat multiplicative, exotesta palisade, thick-walled; cotyledons large.
Age. Estimates of the age of this node are (67-)64-62(-59) m.y.a. (Wikström et al. 2001), or (81-)71, 69(-60) m.y. (Bell et al. 2010).
Evolution. Divergence & Distribution. Note that most of the apomorphies mentioned above are those of the [Dirachmaceae + Rhamnaceae + Elaeagnaceae] clade for the pre vi.2011 version of the site; they must now reverse - or be uncertain - in the poorly-known Barbeyaceae if it is embedded in that group... Dense, curly hairs on the abaxial surface of the leaf blade could be an apomorphy here (Sytsma et al. 2002), but Qiu et al. (1998) put this feature at a higher node. For changes in infratectum morphology on the tree, see also Doyle (2009).
Chemistry, Morphology, etc. The wood anatomy of Dirachmaceae is particularly similar to that of Rhamnaceae (Baas et al. 2001).
A granular layer below the tectum is more or less developed in both Rhamnaceae and Dirachmaceae. The flattened seed with an antiraphal vascular bundle of Dirachmaceae is similar to seeds in Rhamnaceae (Boesewinkel & Bouman 1997); the distribution of testal and tegmic epidermal cells with sinuous anticlinal walls could be interesting.
Phylogeny. This grouping is suggested by C. S. Campbell (pers. comm. 2003), Sytsma et al. (2002: support weak) and especially S.-D. Zhang et al. (2011). Rhamnaceae, Barbeyaceae and Dirachmaceae may form a clade (Richardson et al. 2000a). However, this was not confirmed by Zhang et al. (2011), but the maximum parsimony bootstrap values for the relationships there are not strong, nor is the maximum likelihood support for [Elaeagnaceae [Barbeyaceae + Dirachmaceae]], although posterior probabilities are all 1.0.
RHAMNACEAE Jussieu, nom. cons. Back to Rosales
Shrubs to trees; chelidonic acid +; saponins, biflavonyls, benzylisoquinoline alkaloids +, myricetin, ellagic acid 0; (vessel elements with scalariform perforation plates); libriform fibres +; lysigenous mucilage cavities +; leaves opposite or spiral, lamina vernation conduplicate(-plicate) or involute, (margins entire), (stipules 0), colleters +; (plant dioecious); flowers small, 4-5(-6)-merous; K (connate), with a longitudinal median ridge adaxially, C cucullate, enfolding A (0); tapetal cells multinucleate; exine infratectum granulate-intermediate, (nectary as disc; on ovary); G [2-3(-5)], ± inferior, opposite sepals or odd member adaxial, style + or styles separate, with canals as many as carpels (one; 0), stigma papillate; ovules (2; median), (apotropous), (bistomal), outer integument 4-10 cells across, inner integument 3-4 cells across, parietal tissue 4-7 cells across, nucellar cap to 6 cells across, nucellus ± protruding through micropyle, hypostase +, funicular obturator +; often several megaspore mother cells, (embryo sac bisporic, 8-nucleate - Allium type), antipodals degenerate; K often deciduous; seeds often laterally flattened, (arillate); testa with median integumentary antiraphe bundle +/0, (mesotesta with a few sclerotic cells), endotegmen of cuboid cells, with scalariform thickenings (slightly lignified); endosperm +/0, (starchy), (perisperm +?), polyembryony common, embryo chlorophyllous.
52[list]/925 - three groups below. World-wide, especially tropics and warm temperate regions (map: see van Steenis & van Balgooy 1966; Meusel et al. 1978; Frankenberg & Klaus 1980; Richardson et al. 2003; Australia's Virtual Herbarium xii.2012; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010: C. Asia?). [Photo - Flower, Dry fruit, Fleshy fruit.]
Age. Bell et al. (2010) estimated crown Rhamnaceae to be (73-)62, 59(-46) m.y. old, Bell et al. (2010) suggested an age of arounf 73-46 m.y.a., while at 100.6-84.1 m.y. the age in Onstein et al. (2015) is most compatible with the fossil record.
Fossils from the Cretaceous-Cenomanian, some 94 m.y.a., have been identified as Rhamnaceae (Crepet et al. 2004 for references). Calvillo-Canadell and Cevallos-Ferriz (2007) described Mexican fossils in Rhamnaceae from the late Campanian (ca 73 m.y.) onwards; those from the late Campanian itself have tiny spathulate petals ca 0.7 mm long. Apparent rhamnaceous fossils with puzzling fruits and leaves from the Cretaceous-Maastrichtian of Colombia dated to some 68 m.y.a. are in serious conflict with dates of diversification within the family if assigned to tribes, but not if they are placed incertae sedis (Correa et al. 2010). See also Friis et al. (2011) for early fossils.
1. Rhamnoideae Eaton
Ovary inferior; fruit a drupe or samara; n = 6, 10, 12.
Rhamnus (125). Tropical, north temperate.
Synonymy: Frangulaceae de Candolle
Lamina with secondary venation palmate; fruit a drupe; n = ?
3/4. Cuba, north South America, Madagascar.
3. Ziziphoideae Luersson
(Herbs), (lianes), (leaves much reduced and whole plant thorny); (roots with N-fixing Frankia); (indumentum stellate); (axillary buds superposed); (lamina with secondary venation palmate); stipules also petiolar [Colletia]; (hypanthium long and tubular); nectary position variable; G semi-inferior to inferior (superior); (embryo sac bisporic, eight celled [Allium type]); fruit a drupe, (winged), also partly loculicidal capsule; (seed arillate); n = 6, 8, 11.
Phylica (150), Ziziphus (100-170), Ceanothus (55), Gouania (50). Pantropical, warm temperate.
Synonymy: Gouaniaceae Rafinesque, Phylicaceae J. Agardh, Ziziphaceae Adanson
Floral formula: * ⚥ K 5; C 5; A 5 opp. C; N; G  / .
The capsules are rather similar to those of Euphorbiaceae, Phyllanthaceae and Picrodendraceae where the capsule also falls to bits as it dehisces. There, too, the fruit wall often separates into two layers; the inner layer, woody, twists as dehiscence occurs so helping to eject the seed. However, since the seeds are basal in Rhamnaceae there is no columella as is so typical of these other families, and the latter lack a hypanthium. Phyllanthaceae and Picrodendraceae have two seeds per carpel.
Evolution. Divergence & Distribution. Crown Rhamneae are some (31.2-)28.5, 27.6(-24.9) m.y. old and Paliureae (34.7-)31.6, 30.6(-27.5) m.y. (Richardson et al. 2004). Richardson et al. (2004, see also Richardson et al. 2001a) discuss the evolution and historical biogeography of the family in detail, noting i.a. the rapid diversification of the speciose Phylica within the last ca 8 m.y.. However, how the genus gets around is unclear; 8,000 km separates P. arborea on Gough and Amsterdam islands (Richardson et al. 2003). Estimates of the age of crown Phylicieae range from 41.7-22.7 to 36.5-10.3 m.y.o. (Richardson et al. 2004; Onstein et al. 2015).
Millan and Crepet (2014) discuss a Solanaceous fossil from the Eocene that can in fact confidently be assigned to Rhamnaceae; see Friis et al. (2011) for other Caenozoic fossils.
Ecology & Physiology. There seem to have been three origins of the climbing habit in the family (Richardson et al. 2000a), and in two of these the plants have winged fruits. Quite a few species are xeromorphic, and Rhamnaceae are also quite conspicuous in Mediterranean ecosystems. Onstein et al. (2015) estimate that about 112 species in five groups are found there, Phylicieae in the Cape, Ceanothus in California, Pomaderreae in western Australian, Colletieae in Chile, and Rhamneae in the Mediterranean, with another 187 species found in those raeas and also elsehwere. Colonization of those areas and diversification in them was, they thought, not simultaneous, and Rhamnaceae were in all these the areas well before the onset of the winter rainfall regime and diversification rates seem unaffected by the timing of this onset; in the Cape and Western Australia there seem to have been very low extinction rates (Onstein et al. 2015).
Origins of N-fixing in Rhamnaceae are quite young compared to estimates in other families - late Eocene to Oligocene are the dates suggested (H.-L. Li et al. 2015: support for sister-group relationships low). Most diversification within Ceanothus has been within the last ca 6 m.y., well before the origin of the Mediterranean-type vegetation the genus now favours (Burge et al. 2011; Onstein et al. 2015).
Pollination Biology & Seed Dispersal. The nectary position is particlarly variable in Colletieae, members of which have a long hypanthial tube, sometimes with a ligule; the nectary can be on the inside of the tube or on the underside of the ligule (Medan & Aagesen 1995).
Perhaps a third of the family, all in the ziziphoid group, has myrmecochorous seeds (Lengyel et al. 2010).
Bacterial/Fungal Associations. The North American Ceanothus has N-fixing actinomycetes, as do many Colletieae; N-fixing genera may form a monophyletic group, although there is no strong evidence for this yet (Richardson et al. 2000b). The roots of Ceanothus also form VAM associations (Rose 1980).
Ectomycorrhizae have been reported from Rhamnus and Pomaderris (Malloch et al. 1980; Tedersoo et al. 2008), while Rose (1980) recorded vesicular-arbuscular mycorrhizae on the N-fixing Ceanothus.
For the complex ansmycin maytasinoids found in Colubrina and - the precursors, at least - probably synthesized by a bacterium, see references in Cassady et al. (2004).
Genes & Genomes. cox1 introns are common in Rhamnaceae (Sanchez-Puerta et al. 2008).
Chemistry, Morphology, etc. The lamina of New World species of Gouania have glands at the base while that of Karwinskia has pellucid dots.
For pollen tube growth in the hollow styles of Colletieae, which is sometimes through the cells, see Gotelli et al. (2012); hollow styles have been reported elsewhere (Medan 1985: list; Medan & Hilger 1992: Colubrina) and may be an apomorphy for all or part of the family, but they may also be single, or even absent. Is there some kind of chalazal haustorium (see Srinivasachar 1940)? The outer epidermis of the outer integument of the ovule can have rather large cells (Juel 1929).
General information is taken from Brizicky (1964) and Medan and Schirarend (2004); Hegnauer (1973, 1990) summarized chemistry, Cremers (1973, 1974) growth of lianescent taxa, Nair and Sarma (1961) floral anatomy, Medan (1985, 1988) discussed gynoecial development, Medan and Aagesen (1995), Vikhireva (1952: not read) and Medan and Hilger (1992) comparative floral and fruit morphology, and Juel (1929) and Arora (1953) ovules.
Phylogeny. There are three main clades in the family. Richardson et al. (2000b) found weak support for the basic relationships [rhamnoids [ziziphoids + ampeloziziphoids]], and relationships between the major clades in the ziziphoid group in particular were poorly understood. Basic relationships were better supported in Hauenschild et al. (2016a), and although there was some resolution of relationships in the rhamnoid and ziziphoid groups,, the former had one major polytomy and the latter two.
For relationships in Pomaderreae, see Kellermann et al. (2005) and Kellermann and Udovicic (2008), for the phylogeny and morphology of Colletieae, see Aagesen (1999: 63 characters, morphological analyses) and Aagesen et al. (2005), and for Rhamnus and relatives, see Hauenschild et al. (2016b). Ziziphus is wildly para/polyphyletic, species occurring in all three main groups (Islam & Simmons 2006; Hauenschild et al. 2016a).
Classification. For a phylogeny-based classification of the family, see Richardson et al. (2000a). The rhamnoids include three tribes, [Ventilagineae [Maesopsideae + Rhamneae]]. The ziziphoids are made up of five tribes, Phyliceae, Pomaderrieae, Gouanieae, Colletieae, and Paliureae, as well as unplaced genera like Ceanothus and Alphitonia, and include most of the rest of the family. The ampeloziziphoids include three tribes, three genera, and four species (Richardson et al. 2000b). Hauenschild et al. (2016a) adopt the same classification.
[Elaeagnaceae [Barbeyaceae + Dirachmaceae]]: ?
Age. Bell et al. (2010) estimated this node to be (77-)65, 62(-51) m.y. old.
ELAEAGNACEAE Jussieu, nom. cons. Back to Rosales
Trees or shrubs; roots with N-fixing Frankia; dihydroflavonols?, 0-methyl flavonoids, ellagic acid +, myricetin 0; cambium storied; phloem stratified; true and fibre tracheids +, pits vestured [not all], fibre pits bordered; wood with broad rays; sieve tubes with non-dispersive protein bodies, plastids lacking starch grains; nodes 1:1; petiole bundles arcuate or annular; no mucilage cells in leaves; hairs lepidote or stellate; leaves spiral or opposite, lamina vernation conduplicate-flat, margins entire, stipules 0; (plant dioecious - Hippophae); inflorescence a raceme, or flowers axillary; flowers (2-)4(-6)-merous; hypanthium long to short; P +, uniseriate, ± petal-like; A also 2 x P, borne in throat of tube; pollen 3-nucleate; G 1, stylulus long, stigma decurrent or capitate; compitum necessarily 0; ovule orientation?, micropyle?, outer integument 5-16 cells across, inner integument 3-4 cells across, funicular obturator +; megaspore mother cells several; hypanthium accrescent, fleshy, closely investing fruit; pericarp thin [Hippophae]; testa very thick, exotesta with sinuous anticlinal walls at least in part, (not palisade), mesotesta ± thick-walled; endosperm with chalazal haustorium, wall formation delayed, (starchy), cotyledons usu. unequal; n = 6, 10, 11, 13, 14.
3[list]/45: Elaeagnus (20-45). North Temperate, warm tropical; Malesia and Australia - also quite widely cultivated and/or escaped (map: from Meusel et al. 1978; Hultén & Fries 1986; Australia's Virtual Herbarium ix.2014). [Photos - Collection, Shepherdia Fruit © R. Kowal.]
Age. Bell et al. (2010) estimated that the age of the clade [Shepherdia + Elaeagnus] was (30-)20(-10) m. years.
Floral formula: * ⚥ P (5); A 5 alt. P, 10; N; G 1.
Ecology & Physiology. All genera are associated with N-fixing Frankia, and cluster roots have been reported from Hippophae (Shane & Lambers 2005); carboxylate exudation may help in phosphorus acquisition (Lambers et al. 2012b). The maximum age for the aquisition of this feature is (101.8-)91.1, 82.8(-64.5) m.y. (H.-L. Li et al. 2015: support for sister-group relationship to Barbeya low)
Bacterial/Fungal Associations. VAM and ECM associations have been reported from Elaeagnaceae (e.g. Rose 1980). For the host preferences of rusts, see Savile (1979).
Chemistry, Morphology, etc. The androecium is obdiplostemonous according to Huber (1963). When stamens are equal in number to the perianth, they alternate with the lobes; this is consistent with an interpretation of P = K, with antepetalous stamens... Seed anatomy is rather like that of Rhamnaceae (Corner 1976).
For general information, see Bartish and Swenson (2004), for wood anatomy, see Jansen et al. (2000b) and for fruit and seed anatomy of Hippophae, see Harrison & Beveridge (2002).
Previous Relationships. Elaeagnaceae have been difficult to place. They were included in Proteales by Cronquist (1981) because of superficial floral similarities, and in Elaeagnales-Rhamnanae, next to Proteanae, in Rosidae, by Takhtajan (1997).
Synonymy: Hippophaeaceae G. Meyer
[Barbeyaceae + Dirachmaceae]: connective produced; ovule with outer integument 3-5 cells across, parietal tissue 5-6 cells across.
Chemistry, Morphology, etc. In both families the embryo sac is quite deep seated, and in Dirachma socotrana in particular, the nucellar tissue at the chalazal end of the seed is very well developed.
BARBEYACEAE Rendle, nom. cons. Back to Rosales
Trees; ellagic acid +; libriform fibres +; nodes 1:1; no mucilage cells in leaves; stomata laterocytic; hairs unicellular, spirally twisted; leaves opposite, lamina vernation supervolute-curved, margins entire, stipules 0; plant dioecious; inflorescence fasciculate, bracts and bracteoles 0; hypanthium 0; P +, uniseriate, sepal-like, 3-4; A (6-)9-12; pollen exine infratectum granulate-intermediate; nectary 0; G 1-2(-3), ± separate, styluli long, stigma long-clavate, decurrent, ?type; ovule subapical, micropyle long-endostomal, inner integument 5-6 cells across, nucellar cap ca 5 cells across, hypostase +; fruit a nutlet, P accrescent, wing-like; seed coat undistinguished, exotesta perforated, not palisade, anticlinal walls sinuous, endotegmen tanniniferous, anticlinal walls sinuous; n = ?
1[list]/1: Barbeya oleoides. N.E. Africa, Arabia (map: from Aubréville 1974; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010).
Floral formula: * [♂] [♀] P 3-4; A 9-12. /// P 3-4; G 1-2<.
Chemistry, Morphology, etc. The sieve tubes have compound perforations, unlike Ulmaceae and its immediate relatives and other Rosales. The perforated seed coat is rather like that common in the Ulmaceae group (Bouman & Boesewinkel 1997).
Additional information is taken from Dickison and Sweitzer (1970: morphology), Tobe and Takahashi (1990: hairs and pollen), Friis (1993: general), and Bouman and Boesewinkel (1997: ovule and seed); Hegnauer (1990) has a little information on chemistry.
Previous Relationships. The monotypic Barbeyales were placed in Hamamelididae-Urticales by Cronquist (1981) and in Hamamelididae-Barbeyanae by Takhtajan (1997).
DIRACHMACEAE Hutchinson Back to Rosales
Shrub; stalked glands +/0; chemistry?; phloem stratified; nodes ?lacunar; leaves spiral, stipules subulate, persistent; flowers single, terminal; flowers 5-8-merous; epicalyx of 4-8 lobes (in middle of pedicel); K basally connate, C contorted, vasculature fan-shaped; nectaries on base of C, or on subbasal appendages, lacking stomata; anthers extrorse, long, opening from apex; G , deeply longitudinally ridged, opposite the K, style +, stigma clavate or punctate, elongated; ?ovule orientation, micropyle zig-zag, inner integument ca 2 cells across, nucellar cap 0, hypostase ?+; fruit beaked, segments opening from the base, wooly inside, columella +, K deciduous above the "hypanthium"; seeds laterally flattened, tegmen multiplicative?, median integumentary antiraphe bundle +, exotesta with anticlinal walls thickened, endotegmen tanniniferous; endosperm slight, embryo color?; n = ?
1/2. Socotra, Somalia (map: from Link 1991b).
Floral formula: * ⚥ K (5-8); C 5-8; N; A 5-8 opp. C; G .
Chemistry, Morphology, etc. The single flowers may represent a reduced, cymose inflorescence (Ronse De Craene & Miller 2004). A "hypanthium" is described as involving either the sepals and petals and also the petals and stamens (Ronse De Craene & Miller 2004); there does not seem to be a conventional hypanthium. Petal initiation is later than that of the stamens, as is common is rosids, and until quite late in development they are very much shorter than the stamens. There is a lot of starch in the pollen grains (Boesewinkel & Bouman 1997). The presence of an antiraphal vascular bundle means that the outer integument is very thick (6-9 cells or more) when viewed in the abaxial median plane; integument measurements are taken from the sides of the ovule (see Boesewinkel & Bouman 1997). There is a structure on the seed described as a small, funicular aril, perhaps similar to that found in some Rhamnaceae (Ronse De Craene & Miller 2004).
For additional information, see Link (1991b [c.f. 1990], 1994), Boesewinkel and Bouman (1997: ovule and seed), Baas et al. (2001: wood anatomy), Ronse De Craene and Miller (2004: floral morphology), and Bayer (2004: general).
Previous Relationships. The exotestal seeds with straight embryos suggest that Dirachma is not close to Geraniaceae (Geraniales), with which Dirachma had been linked, as by Cronquist (1981) - see e.g. Boesewinkel (1985) and Boesewinkel and Bouman (1997). Takhtajan (1997) included Dirachmaceae in his Malvales because of its similarity in gross morphology.
[Ulmaceae [Cannabaceae [Moraceae + Urticaceae]]]: flavonols and their glycosides, myricetin [some Ulmaceae, Cannabaceae] +, ellagic acid 0; plant with ± watery exudate; hairs unicellular and multicellular-glandular; cambium ± storied; libriform fibres +; phloem stratified; sieve tubes with non-dispersive protein bodies (some Cannabaceae - 0), (plastids lacking starch grains); cystoliths [globose; usu. CaCO3] common, epidermal and hair cell wall silicification and calcification common; at least one prominent prophyllar bud; lamina with secondary veins proceeding straight to non-glandular teeth and higher-order veins convergent on those teeth [urticoid], stipules cauline; flowers small [7> mm across], usu. protogynous; hypanthium?, P +, uniseriate, sepal-like, imbricate; stamens equal and opposite P; pollen porate, exine infratectum granular, intine thickening at the apertures [= oncus]; nectary 0; G , abaxial only fertile, stigmas sessile, spreading, receptive area extending down adaxial surface and ± confluent; ovule single, apical, pendulous; fruit a drupe; testa perforated [rare in Ulmaceae]; endosperm scanty, polyembryony common; x = 14, centromeres both median and subterminal.
Age. This node may be (61-)57-55(-51) m.y.o. (Wikström et al. 2001), (76-)66, 64(-55) m.y.o. (Bell et al. 2010) or ca 70.9 m.y. (Tank et al. 2015: Table S2).
Evolution. Divergence & Distribution. The copious information on the four families awaits synthesis; Sytsma et al. (2002) should be consulted for details of character evolution. Sytsma et al. (2002) note that inflexed stamens and their dehiscence, fruit type, and laticifers need detailed study; hypanthium presence and other characters can be added to this list. Two-ranked leaves may be an additional synapomorphy (or pegged at a still higher level), as well as urticoid teeth. For the evolution of fruits in this clade, see Tiffney (1986a).
Ecology & Physiology. 12/42 of the commoner species in west Amazonian rainforests are members of Urticales (Pitman et al. 2001).
Plant-Animal Interactions. Some Nymphalinae-Nymphalini butterflies and other nymphalids like Apaturinae, Libytheinae, Pseudoergolinae, etc., have larvae that eat members of these families (see also under Urticaceae) - but also on the immediately unrelated Euphorbiaceae (Malpighiales: see Ehrlich & Raven 1964); the ancestor of Nymphalinae may have fed on Urticaceae and relatives (Nylin & Wahlberg 2008; Wahlberg et al. 2009; Nylin et al. 2014). Members of the clade shifted to Lamiales some time around the K/T boundary (Nylin & Wahlberg 2008). Caterpillars of Acraea (Acraeinae, also Nymphalidae) are quite common on Urticaceae (including Cecropia), and also on Moraceae, etc.; this particular genus is also commonly found on Passifloraceae and their relatives.
Chemistry, Morphology, etc. Raffinose and stachyose are common oligosaccharides in phloem exudate in Ulmaceae, Moraceae and Cannabaceae sampled (Zimmermann & Ziegler 1975). The group has homogeneous wood anatomy: Rays are relatively broad, pits are simple, intervessel pitting is alternate, fibres are septate, and parenchyma is paratracheal (Baas et al. 2000). For torus-margo pits, see above. Phytoliths are common in this clade (Piperno 2006; see Satake 1931 for spodograms).
Because of the well-developed prophyllar bud(s), the inflorescences are often paired, with a bud between them, and/or the branches may have a bud on one or both sides at the base; Ulmus does not show this arrangement. The "stipular buds" of Cannabis (Miller 1970 and references) are really prophyllar buds.
It is not clear which taxa have a hypanthium; at least some species of Ulmus and Pilea do, but other species of Ulmus, Zelkova and Trema show no obvious signs of one (see also Bechtel 1921). Staedler (1923) discussed the absence of an anther epidermis, although it is present in Ficus (other Rosales?); there is no obvious link with dehiscence mechanism. Starchy pollen is common, but apparently not in Urticaceae. Bechtel (1921) and Eckardt (1937) described gynoecial morphology in considerable detail. Taxa with a perforated testa are quite common, although this feature may have arisen more than once (Kravtsova & Oskolski 2007; Yang et al. 2013).
For further information, see Tippo (1938) and Sweitzer (1971), both anatomy, Giannasi (1978, 1986: chemistry), Terabayashi (1991: vernation), Hennig et al. (1994: cuticle waxes), Tobe and Takaso (1996) and Behnke and Barthlott (1983) both hairs, Takaso and Tobe (1990: testa), Omoron and Terabayashi (1991: gynoecial vascular anatomy), Mohan Ram and Nath (1964: embryology), and Kravtsova and Wilmot-Dear (2013: fruit anatomy).
Phylogeny. The phylogenies suggested by Sytsma et al. (2000) and Song et al. (2001) place Cannabis within Celtidaceae (see also e.g. Ueda et al. 1997b); Cannabaceae is the earliest name for the combined group. They also place Cecropia within Urticaceae, and this set of relationships has been strongly supported by a more comprehensive analysis (Sytsma 2002) and other studies since. See Judd et al. (1994) for a morphological phylogeny and Zavada and Kim (1996) for a molecular phylogeny focussed on the old paraphyletic Ulmaceae s.l.
ULMACEAE Mirbel, nom. cons. Back to Rosales
Trees, (growth symopodial, apex of innovation aborts); (ectomycorrhizae +); lignans +; (wood fluoresces); unicellular hairs smooth; sieve tube plastids often with protein crystalloids; torus-margo pits +; cystoliths usu. pegless; leaves two-ranked, lamina vernation laterally (vertically) conduplicate-plicate, secondary veins going into teeth, stipules extrapetiolar; flowers perfect and mixed; P spiral, (connate); A extrorse, (2 x P); pollen 4-7-porate, exine rugulose; at least one stigma with 3(-5) vascular bundles; ovule (with bistomal micropyle), outer integument 4(-6 - Holoptelea) cells across, inner integument ca 4 cells across; fruit also a (asymmetric) samara; seeds flattened, coat undistinguished, exotestal cells elongated, unthickened; (embryo curved - Zelkova); often terminal/subterminal diffuse-complex centromeres; 69bp ndhF deletion.
6[list]/35: Ulmus (20-30, species limits uncertain). Mostly N. temperate, esp. Asian, few species tropical, not in Australia and the Pacific (map: from Soepadmo 1977; Hultén & Fries 1986; Fl. N. Am. 3. 1997; Todzia 1989, 1992: Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010). [Photos - Collection.]
Age. Ulmus is known as leaves and fruits from Early Eocene deposits of northeastern China some 50 m.y. old (Wang et al. 2010; see also Friis et al. 2011 for Caenozoic fossils); this suggests an appreciably greater age for crown-group Ulmaceae as a whole.
Evolution. Divergence & Distribution. The family has two main clades. One, including Ampelocera, Phyllostylon and Holoptelea, is largely tropical, and the other is north temperate in distribution (Neubig et al. 2012b).
Chemistry, Morphology, etc. There are distinctive fatty acids in the seeds of some Ulmaceae, but not in those of Cannabaceae or Moraceae (Badami & Patil 1981: sampling). Ulmus lacks well-developed prophyllar buds and has one of the two stipules intrapetiolar, they are both intrapetiolar in seedlings of some species, and the leaves may also be opposite, as in seedlings. Hemiptelea has pegged cystoliths. The breeding system in the family is variable, but at least some flowers are perfect. Nawaschin (1895) suggested that chalazogamy occurred in Ulmus. Holoptelea has a thick-walled exotesta.
For gynoecial morphology, see Okamoto et al. (1992), and for a summary of fruit morphology, see Herrera et al. (2014).
Phylogeny. The poorly-known Ampelocera is to be included here (see Ueda et al. 1997b; also Wiegrefe et al. 1998); although its hairs are smooth, its leaves have ascending veins. A clade including Ampelocera, Phyllostylon and Holoptelea is sister to the rest of the family (Neubig et al. 2012b).
[Cannabaceae [Moraceae + Urticaceae]]: C-glycoflavones also +; (sieve tube plastids with starch grains); unicellular hairs usu. micropapillate; secondary veins palmate; stipules cauline-intrapetiolar; flowers imperfect; stigmas with single vascular bundle; fruits not or barely flattened; embryo curved.
Age. The age for this clade has been estimated at (52-)49, 42(-39) m.y. (Wikström et al. 2001: c.f. topology), (65-)56, 54(-45) m.y. (Bell et al. 2010), or around 59.2 m.y. (Tank et al. 2015: Table S2).
Evolution. Seed Dispersal. Members of all three families are quite often dispersed by bats in the New World (Lobova et al. 2009). Trema, Ficus and Cecropia are all important food sources for frugivorous birds (Snow 1981).
CANNABACEAE Martynov, nom. cons. Back to Rosales
Trees or ± herbaceous, erect or twining; (plant ectomycorrhizal); (flavonoids), sesquiterpene lactones +, (flavonols 0); (torus-margo pits + - Celtis), true tracheids +; cystoliths usu. with pegs [distribution?]; leaves (spiral; opposite), lamina vernation (laterally) conduplicate-plicate (conduplicate; supervolute); (strongly palmately lobed or compound, veins proceeding to the apex of lobes - Cannabis, Humulus), secondary veins ascending, stipules connate or not; (P valvate); pollen 3(-2) porate, exine scabrate to verrucate; micropyle bistomal, outer integument 2-4(-8) cells across, inner integument 2-3 cells across, parietal tissue ca 6 cells across, nucellar cap ca 2 cells across; embryo sac haustorium +; fruit a drupe (an achene, samara); exotestal cells tangentially elongated, with arms, unthickened; endosperm +, embryo also coiled; (n = 8-11, 13, 15), centromeres medial/submedial, simple.
11[list]/170: Celtis (ca 100). Worldwide, but not Arctic, distribution of Humulus lupulus in Asia is unclear (map: from Wickens 1976; Soepadmo 1977; Hultén & Fries 1986; Fl. Austral. 3. 1989; Fl. N. Am. III 1997; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010). [Photos - Collection, Celtis Flower.]
Age. The age of the clade excluding the three basal genera mentioned below is (47-)37, 36(-26) m.y. (Bell et al. 2010).
Evolution. Divergence & Distribution. The Caenozoic fossil history of Cannabaceae that are now East Asian endemics is discussed by Manchester et al. (2009); see also the general summary in Friis et al. (2011).
For the optimization of a number of characters on the tree, see Yang et al. (2013).
Seed Dispersal. Fruits of Trema are favoured by frugivorous birds of all sort, both specialists and generalists (Snow 1981).
Plant-Animal Interactions. Caterpillars of most Apaturinae (Nymphalidae) are found on Cannabaceae, although those of Hestinalis eat Urticaceae, Sephisa, Fagaceae, and Apatura, the spectacular purple emperor, has moved on to salicin-containing Salicaceae (Salix and Populus: Ohshima et al. 2010).
Bacterial/Fungal Associations. Parasponia (?= Trema) is the only non-legume nitrogen fixer that is associated with other than actinomycetes, and its rhizobia - a variety of taxa are involved - remain in infection threads like those of some Fabaceae, especially "Caesalpinioideae". Unlike Fabaceae, lipochitooligosaccharide recognition leading to nodule formation as well as arbuscular mycorrhizal symbioses are controlled by the same receptor kinase enzyme; infection of the plant is by entry through cracks in the epidermis. The nodules are modified lateral roots and have central vascular tissue, the bacteria being in the cortex; this is unlike the nodules of Fabaceae but like those found elsewhere in the N-fixing clade that are Frankia-induced (Streng et al. 2011; Behm et al. 2014 for literature).
Gironniera is reported to be ectomycorrhizal (Smits 1994).
Genes & Genomes. Cannabis and Humulus have an X-autosome balance system determining the 'sex' of the plant.
Economic Importance. For the biology of Cannabis sativa, see Small (2015).
Chemistry, Morphology, etc. Only the "basal" Aphananthe and Gironniera have flavonols. Whether the laticifers of Cannabis etc., really are similar to those of Urticaceae and Moraceae must be confirmed; there is no milky exudate and they occur throughout the plant. Given the derived position of Cannabis, they may not be homologous.
Humulus, with its opposite leaves, has split laterals/a commissural vascular bundle (Colomb 1887). The "distinctive" camptodromous (to semicraspedodromus) venation of Celtidaceae s. str. is disturbed by the inclusion of Cannabis, etc., in this clade, however, strictly craspedodromous venation is reported from Palaeocene Celtis itself (Manchester et al. 2002). Lozanella, with its opposite leaves and boxy venation, looks rather like Urticaceae, but it has a bilobed stigma. The anticlinal walls of the testa of Humulus are sinuous and its embryo is green. n = 10 is common in Cannabaceae.
For general information, see Grudzinskaya (1967), Mohan Ram and Nath (1964: Cannabis ovules and seeds), Leins and Orth (1979: Cannabis flowers), Todzia (1993: general, as Ulmaceae), and Kubitzki (1993b: general, as Cannabaceae), for chemistry, see Hegnauer (1973, 1990, as Ulmaceae; also 1964, 1989), and for ftuit anatomy, see Kravtsove and Wilmot-Dear (2013).
Phylogeny. Pteroceltis, Humulus, and Cannabis are close, and they and some other members of this clade have sieve tube plastids with starch grains (Behnke 1989). Studies suggested that Lozanella was sister to Aphananthe or sister to the rest of the family (Wiegrefe et al. 1998; Soltis et al. 2002), but Yang et al. (2013; see also van Velzen et al. 2006) found that Aphananthe was well supported as sister to the rest of the family, with either Lozanella and/or Gironniera sister to the remainder. Trema appears to be paraphyletic, the N-fixing Parasponia being embedded in it (Sytsma et al. 2002; van Velzen et al. 2006; Yang et al. 2013).
Synonymy: Celtidaceae Link, Humulaceae Berchtold & J. Presl, Lupulaceae Link
[Moraceae + Urticaceae]: latex system +; (calcium carbonate crystals); (lamina with pinnate secondary veins); P valvate (imbricate); staminate flowers: stamens incurved in bud [explosively straightening]; pollen 2- or 5-porate; pistillode +; seed coat undistinguished; polyembryony 0.
Age. Zerega et al. (2005) suggested that the age of this node was at least 89 m.y., while around 58.8 or 55.3 m.y. are ages in Tank et al. (2015: Table S1, S2).
Evolution. Divergence & Distribution. There is a group of genera of Moraceae with explosive pollen dispersal, and inflexed stamens may be a synapomorphy for [Moraceae + Urticaceae] (Datwyler & Weiblen 2004), although where stamen dehiscence changes on the tree of the former family depends very much on how it is optimized (Clement & Weiblen 2009). The moraceous genera with such stamens are in the paraphyletic Moreae that was part of a basal polytomy within Moraceae in early reconstructions.
Genes & Genomes. Rates of molecular evolution are likely to have increased at least twice in this clade, e.g. in most Urticaceae and also in Dorstenia, the increase being associated with the adoption of the herbaceous habit (Smith & Donoghue 2008).
Chemistry, Morphology, etc. Scattered in the group are taxa in which the tepals are persistent (e.g. Pilea) or accrescent (e.g. Morus), i.e. the fruits are anthocarps in the strict sense.
Phylogeny. For a morphological phylogeny focussing on Urticaceae s.l., i.e. Moraceae and Urticaceae here, see Kravtsova and Oskolski (2007).
Classification. The two families have much in common, and Corner (1952) even included Moraceae in Urticaceae.
MORACEAE Gaudichaud, nom. cons. Back to Rosales
Largely woody; (isoflavonoids +); (cork in outer cortex); laticifers throughout the plant, latex milky; (stomata aniso- and cyclocytic); leaves spiral, lamina vernation variable, stipule also ensheathing stem, (0 - Fatoua); dioecious; inflorescence congested, ± spicate [staminate] or ± globose [carpellate); flowers 4-merous, (P 0-10); staminate flower: bracts peltate; P free; carpellate flower: P connate; (G inferior), styles 1 or 2, often unequal; ovule (subapical; campylotropous), outer integument 3-4 cells across, inner integument ca 3 cells across, nucellar cap ca 5 cells across [nucellar beak]; fruits an achene, (drupe; P accrescent), receptacle often accrescent; exotesta ± tanniniferous, (several thickened layers - Prainea); (endosperm +); (n = 12 upwards, esp. 13, 14), chromosomes 0.5-2.7 µm long, both terminal and median centromeres.
39[list]/1125 - six groups below. Mostly tropical to warm temperate (map: from Jalas & Suominen 1976; Wickens 1976; Frankenberg & Klaus 1980; Fl. Austral. 3. 1989; Fl. N. Am. 3. 1997; Wilmott-Dear & Brummit 2007: Asia and South America only approximate).
Age. Zerega et al. (2005) dated crown-group Moraceae to at least 79 m.y. ago.
[Artocarpeae + Moreae]: carpellate flowers: bracts peltate.
1. Artocarpeae Lamarck & de Candolle
(P connate, that of adjacent flowers adnate in the middle portion [completely]); staminate flowers: 2 merous; A 1(-3), filaments straight.
3/67: Artocarpus (61). Largely tropical, Indo-Malesia (Artocarpus) and America. Photo: Fruit].
Synonymy: Dorsteniaceae Chevallier
2. Moreae Dumortier
Staminate flower: (bracts not peltate), (filaments straight).
7/56. Tropical, some temperate.
[Maclureae [Dorstenieae [Ficeae + Castilleae]]]: ?
3. Maclureae Clement & Weiblen
Habit various, axillary thorns +; inflorescence with golden dye; staminate flowers: bracts not peltate, (filaments straight); carpellate flower: (bracts peltate).
1/11. Tropical to Temperate. [Photo - Inflorescence].
[Dorstenieae [Ficeae + Castilleae]]: radial latex tubes +; plant monoecious, inflorescence bisexual; inflorescence axis expanded; pistillode conical.
4. Dorstenieae Dumortier
(Herbs); inflorescence disciform; staminate flowers: (3-merous), (P connate); (filaments straight); carpellate flowers: (2-merous), (embedded in receptacle.
13/145: Dorstenia (105). Pantropical. Photo: Fruit.
Synonymy: Dorsteniaceae Chevallier
[Ficeae + Castilleae]: insect pollination +; staminate flowers: filaments straight; carpellate flowers: bracts not peltate [inc. Maclureae, etc.?]; P free.
5. Ficeae Dumortier
Lianes, stranglers, etc.; (latex 0); (leaves opposite), ensheathing stipules open in leaf axil; inflorescence axis urceolate; flowers 3-merous: staminate flowers: bracts not peltate; A 2; carpellate flowers: style branches unequal or not; fruit a syconium.
1/800. Pantropical. Photo: Fruit.
Age. Estimates of the age of crown-group Ficus range from around 86.7 to (92.6-)69.9(-60) m.y. (L. Xu et al. 2011 and Chantarasuwan et al. 2016 respectively).
Synonymy: Ficaceae Berchtold & J. Presl
6. Castilleae C. C. Berg
(Branches spreading), (cladoptosis +); (cystoliths 0); infloresence involucrate, unisexual, disciform to urceolate; staminate flower: bracts 0, pistillode 0; carpellate flowers: (bracts 0).
11/62. Pantropical, esp. America.
Evolution. Divergence & Distribution. Berg (2005) suggested that diversification in Moraceae occurred on a still physically coherent tropical supercontinent. Zerega et al. (2005) advance a more complex hypothesis to explain the distribution and diversification of the family, while there are various suggestions for the the biogeographical history of Ficus (see Chantarasuwan et al. 2015 for references, also below).
Within Moraceae, there are suggestions for the ages of some clades. Berg and Hijman (1999) suggested that the distribution of Dorstenia, found in both Africa and South America, could be explained by continental drift; Zerega et al. (2005), however, estimated the crown-group age of the genus to be a mere 18.4-3.5 m.y.a. However, in a more complete analysis, Misiewicz and Zerega (2012) dated the crown age at (132.0-)112.3(-84.8) m.y., with the age of the New World crown group, (44.8-)30.3(-16.5) m.y. - and in fact the latter was the age that Zerega et al. (2005) had estimated, given their sampling. The age of crown group Ficus was estimated to be (101-9-)74.9(-60.0) m.y., its origin being Eurasia, while most diversification was in the Caenozoic, dispersal rather than vicariance best explaining details of the current distribution of the genus (Cruaud et al. 2012b). Subgenus Pharmacosycea is restricted to the New World, as is Urostigma section Americana, the latter being sister to the African section Urostigma, while Urostigma-Malvanthera is Australasian (Cruaud et al. 2012b).
Ecology & Physiology. Moraceae, and in particular Ficus, includes a number of (hemi)epiphytes, stranglers and lianes. They are the second to eigth most speciose family in lowland tropical rainforest in both America and Africa, and in Amazonian forests they include a disproportionally large number of the species (11/227) that make up half the stems 10 cm d.b.h. or more in Amazonian forests (Gentry 1988; ter Steege et al. 2013). For interactions between figs and frugivores, see below.
Pollination Biology & Seed Dispersal. The early evolution of the fig/fig wasp association is unclear, but there are remarkable pollination systems in other Moraceae. Ficus is sister to Castilleae. Female inflorescences of Castilleae such as Antiaropsis are urceolate. The pollinators (thrips) breed among the flowers of the male inflorescences, eating pollen, etc., pollination occurs when the pollen-coated thrips visit female inflorescences (Datwyler et al. 2003; Datwyler & Weiblen 2004; esp. Zerega et al. 2004; Clement & Weiblen 2009). Insect pollination here is a reversal from wind pollination. In Artocarpus integer larve of dipteran cecidomyid gall midges (Contarinia) eat fungi growing on the male inflorescences, and pollination occurs when the midges visit female inflorescences, perhaps attracted by scent (Sakai et al. 2000).
Seed dispersal in Moraceae is often by animals, but just what part of the plant contributes to the fleshiness that attracts the disperser varies. In Morus the fruits, achenes, are surrounded by the fleshy perianth and are closely packed on an erect inflorescence axis. In Artocarpus - it includes the bread and jack fruits - the more or less elongated infructesences can weigh up to 50 kg, and the fleshy part comes both from perianth members and the inflorescence axis itself (see Zerega et al. 2010: phylogeny and morphology). Broussonetia papyrifera has heads of bright red, dangling drupes, while Dorstenia, etc., have "dehiscent" drupes; there the stone is shot out of the turgid fruit, the separation following a line of weakness in the mesocarp tissue. In both these cases the developing fruits are initially extruded by the closely-packed perianth members. In Antiaropsis (Castilleae) the inflorescence axis is concave at first, but spreading ("dehiscing") when ripe, when the drupes contrast in colour with the bracts, etc. (e.g. Zerega et al. 2004). In Ficus, of course, the achenial-type fruits are borne on the inside of the fleshy, invaginated axis.
Figs, their agaonid wasp pollinators, and the animals that disperse their fruits.
Basic details of the association between figs and their agaonid chalcid fig-wasp pollinators (Agaonidae) may be summarized as follows. Female wasps are fertilized by flightless males inside the fig, and many females actively pick up pollen from the staminate flowers - at least sometimes aggregated around the ostiole - using their coxal combs and store it in thoracic pockets specia;lized for this purpose before leaving via exit holes in the wall of the fig that are prepared by the males (e.g. Kjellberg et al. 2001; Cook & Rasplus 2003). They then enter a receptive fig via the ostiole, having specialised jaws and a head that is shaped to allow them to get between the bracts surrounding the ostiole, although they often lose their wings and antennae in the process (van Noort & Compton 1996). Carpellate flowers in monoecous figs are layered, i.e., they have styles of different lengths, and the wasps lay eggs in the carpellate flowers with long styles, and these develop into the next generation of wasps (Kerdelhué et al. 2000). They do not lay eggs in ovaries of other flowers, but as they place pollen onto the stigmas of flowers (active pollination) or as pollen on their bodies brush off onto the stigmas, other flowers are pollinated and may develop into fruits. The life cycle in dioecious figs is slightly more complex, even if the layering of the female flowers is less well developed, but it follows the same basic principles; male figs produce at most few fruits but many wasps, while female figs produce lots of fruits but few if any wasps (see Janzen 1979 for a good early account; Kerdelhué et al. 2000; Cook & Segar 2010). In figs with active pollination there are fewer male flowers in the syconium than if there is passive pollination, where the wasp simply becomes coated with pollen before it leaves the fig; whether active or passive pollination is ancestral for Ficus is unknown (Cruaud et al. 2012b). Wasps pollinating dioecious figs have shorter ovipositors than those pollinating monoecious figs since the styles of sterile female flowers in "male" figs all have short styles and produce wasps (Cook & Segar 2010).
The fig/fig wasp association seems to be an excellent example of an obligate one-on-one association between the plant and pollinator (e.g. Herre 1996 and references); there is strict co-evolution, figs and their pollinating agaonid wasps are monophyletic and the two speciate almost in synchrony. However, things are not so simple. Recent work suggests that there may be rather less specificity in the association between fig and wasp than was previously thought (Cook & Rasplus 2003; Machado et al. 2005; Jackson et al. 2008; P. Yang et al. 2012; G. Wang et al. 2016), and there are up to four pollinator species per fig species, as many as one third of all monoecious figs have multiple pollinators, and wasps speciate more than the figs (Cook & Segar 2010). However, there is at least a general association between species of figs and species of wasps, and in groups like section Ficus sect. Galoglychia cospeciation is likely, even in the non-pollinating wasps that are members of the system (Jousselin et al. 2008; Cruaud et al. 2012a, b; c.f. Cook & Segar 2010 in part). Pollinator-sharing between fig species seems to be more common in monoecious neotropical figs than in dioecious palaeotropical figs (Moe et al. 2011, but c.f. G. Wang et al. 2016); it also occurs in some African taxa, where one wasp may reproduce in a number of closely related figs. Lineage duplication, wasp speciation occuring within the one species of fig, also occurs (McLeish & van Noort 2012). Moe and Weiblen (2012) also suggest that in some situations the fig wasp may evolve without there being corresponding change of the host; the wasp is adapting to is pollinator, rather than vice versa or both changing together (Hembry et al. 2014 discuss the fig-fig wasp association from the point of view of the extent to which it represents a coevolutionary situation; see also papers in J. Biogeog. 23(4). 1996, also Plant-Animal Relationships [below] for further details). In dioecious figs, hybridization and gene flow has been reported (Wang et al. 2016). Overall, about 30% of Ficus species are pollinated by more than one species of wasp (this figure is likely to be an underestimate), and L.-Y. Yang et al. (2015) found that in dioecious Ficus, where the figure may be over 40%, the wasps are sister species, and there co-/sympatric speciation is possible, however, in monoecious Ficus around two thirds of the co-pollinators were not sister species. In parallel with this difference, phylogenies of plant and insect in dioecious figs may be largely congruent, less so in monoecious figs (Yang et al. 2015).
Since fig development is often more or less synchronized within trees but asynchronous between trees, and within a single fig staminate flowers mature later than the carpellate flowers, out-crossing is favoured (Ahmed et al. 2009). Indeed, although oviposition by fig wasps may be staggered, adults tend to hatch at the same time (e.g. Kerdelhué et al. 2000; Lopez-Vaamonde et al. 2001; Jousselin et al. 2003; Jackson 2004a; Kjellberg et al. 2005; Rønsted et al. 2005b, 2008a for references). Although agaonid wasps are tiny, they can be carried by air currents for up to 14 km even in the rainforest, and so the breeding units of figs may be an order of magnitude larger - covering some 100 square kilometres or more - than those of other plants there (Herre 1996; Nason et al. 1998). Pollen is transported by wasps for distances over 160 km in riparian populations of the monoecious Ficus sycomorus in the Namib desert (Ahmed et al. 2009). In general pollinators of monoecious figs fly further than those of dioecious figs (Harrison & Rasplus 2006), and monoecious figs tend to be large tress with (very) low population densities while dioecious figs are small trees with higher population densities (L.-Y. Yang et al. 2015). The wasps are attracted to the figs by fragrances secreted by glands on the ostiolar bracts or the outside of the fig, depending on the species (Souza et al. 2015; G. Wang et al. 2016 and references), an there are a variety of other glands in figs, some of which may produce phenolics that may protect the fig against overheating.
Figs are a very important and dependable source of food for frugivores, both birds and mammals, in many places in the tropics (e.g. Shanahan et al. 2001). The diversity of their growth forms means they are encountered throughout the forest. Figs are perhaps surprisingly nutritious (Herre et al. 2008 for references), although there is some argument about this (see Fleming 1986; Shanahan et al. 2001), and there is no comparative study of the nutritional content of Old and New World figs (Snow 1981). In at least some communities figs may be especially important food resources when other plants are not fruiting; whether or not fruits on individual fig trees ripen synchronously, individual species often do not fruit synchronously, so they can be a reliable food resource. "All accounts agree that figs are among the most important foods of specialized frugivores in Africa, southeast Asia, and Australia..." (Snow 1981: p. 9). In the New World, however, specialised frugivores are less prominent on figs. Figs are ecologically important in both the New (e.g. Cocha Cashu, Peru) and Old (e.g. Borneo) Worlds, although perhaps less so in Africa and India, and they have considerable local diversity - for example, there are 77 species in Lambir Hills National Park in Sarawak alone (Shanahan et al. 2001; Harrison & Shanahan 2005). The species richness of Ficus is correlated with that of their avian frugivores, particularly specialised frugivores, and the frugivores also select on particular aspects of the morphology of the fig species (Shanahan et al. 2001; Kissling et al. 2007; Herre et al. 2008: see below). Leighton and Leighton (1983) called the relationship between Ficus and its frugivores a keystone mutualism, since the loss of the figs would deplete the populations of animals that dispersed both Ficus and the fruits of other plants. Similarly, Terborgh (1986: p. 339) observed, "[s]ubtract figs from the ecosystem and one could expect to see it collapse"; in some New World ecosystems figs, less than 1% of the species (12 out of ca 2,000), sustained nearly the entire frugivore community for three months of the year. Janzen (1979) had calculated that seven species of figs on Barro Colorado Island produced 200,000 ± 75,000 figs ha-1/yr - maybe 195 kg dry weight. Kattan and Valenzuela (2013, see also Snow 1981) discuss the arguments pro and con as to whether figs really are keystone species for frugivores.
Figs are commonly dispersed by bats (Muscarella & Fleming 2008) or birds (Snow 1981; see also Fleming 1986). New and Old World bats search for food in different ways and have selected figs with different qualities; overall fig morphology is quite diverse. The fig may be dull coloured and scented; in the New World some 21 species of Artibeus bats (phyllostomids) are the predominant ficivores. The bats are slow feeders and spit out larger seeds, fibre, etc., but they still commonly disperse the tiny fig achenes. Like other bat-dispersed taxa in the New World, including Cecropia (Urticaceae) and Trema (Cannabaceae), particularly in Mexico (Lobova et al. 2009), species of Ficus can be found in early successional communities (Muscarella & Fleming 2008). The altitudinal ranges of the bats and figs are similar (Fleming 1986). Bat-dispersed fruits in the New World often tend to be greenish and odoriferous (Compton 1996 [a whole series of papers]; Korine et al. 2000; Shanahan et al. 2001; Harrison 2005). In the Old World bat-dispersed fruits are often yellow, etc., and are sometimes quite large (Kalko et al. 1996; Harrison & Shanahan 2005; Lomáscolo et al. 2008, 2010); bat-dispersed figs in Malesia, also dull-coloured, may not smell, and pteropodids (fruit bats) are the dispersers there (Hodgkinson et al. 2003). Figs that are eaten by birds are often small and red.
Lopez-Vaamonde et al. (2009) discuss dating and biogeography of the wasps, suggesting that their ancestors lived in Asia, dispersal rather than Gondwanan break-up being important for their subsequent distribution (see also Cruad et al. 2012b: Xu et al. 2012 suggested a Gondwanan ancestry, but with much subsequent dispersal). Some recent estimates of the age of crown group Ficus, (101.9-)74.9(-60.0) m.y., and that of the fig wasps, (94.9-)75.1(-56.2) m.y., are quite similar (Cruaud et al. 2012b), however, comparing the ages of figs and pollinators at 36 nodes, in only eight of these the estimates of the ages of the figs were older, in the rest, the wasps were older, and the numbers were often quite different.
Numerous species of galling chalcid wasps, parasitoids of both pollinating and galling wasps, and inquilines (species living commensally in figs) are part of the fig-fig wasp ecosystem. There can be up to 40 non-pollinating species of wasps per fig species (Cook & Segar 2010), although the diversity of the fig wasp community is lower in dioecious figs (Kerdelué & Rasplus 1996; see also Cook & Rasplus 2003). The parasitoid wasps that parasitize the fig wasps may be of considerable importance in preserving the relationship between the pollinating wasp and fig (Dunn et al. 2008). The wasps belong to several quite different clades and gall individual flowers (none are parasitoids); they may have have moved on to figs some 50-40 m.y.a., with subsequent dispersal to other groups (Cruaud et al. 2011), and as many as 36 species of chalcids may be found on a single species of fig (Cruaud et al. 2011). The phylogenetic diversity of non-pollinating fig wasps is greater in the Old World than the New World (Cook & Segar 2010). Parasitoid wasps may have very large geographic ranges, even larger than those of pollinating wasps (Sutton et al. 2015; see also above).
Another element in this microcosm are the drosophilid flies that in Africa, at least, have a very close association with figs and oviposit either on the stomium or the exit holes made by the male fig wasps (Harry et al. 1996, 1998). For more information on figs and wasps, as well as gallers and parasitioids, see also Kjellberg et al. (2005), the papers in Symbiosis 45, 1-3 (2008), Silvieus et al. (2008), and especially Herre et al. (2008).
Plant-Animal Interactions. Bombyx mori (the silkworm) caterpillars can eat quite a number of species of Moraceae, but not those of most other members of the Ulmaceae group - although they will grow on Ulmus itself (Fraenkel 1959). Caterpillars of danaine butterflies quite commonly eat Moraceae; both they and their usually preferred Apocynaceae are rich in latex, although Moraceae do not often have cardenolides (Ackery & Vane-Wright 1984).
Chemistry, Morphology, etc. Laticiferous cells elongate and branch and intrude between other cells, the nuclei divide, but cell walls are not formed. Some species of Dorstenia have small, cauline stipules that do not overlap the petiole.
For fig/syconium development, see Rauh and Reznik (1951). Chromosome numbers in Dorstenia are very variable, and ovule morphology and embryology there need examination (Berg & Himan 1999).
Some information is taken from Rohwer (1993a); for embryology, see Johri and Konar (1956: Ficus), for chemistry, see Hegnauer (1969, 1990); for pollen, see Burn and Mayle (2008); chromosomes, see Oginuma and Tobe (1995).
Phylogeny. For the phylogeny of Moraceae, see Datwyler et al. (2003), Datwyler and Weiblen (2004) and especially Clement and Weiblen (2009). Some of the old and paraphyletic Moreae with their incurved stamens are now placed in Maclureae, Castilleae are sister to Ficeae, and relationships between the other tribes are on the whole well supported (Clement & Weiblen 2009). Analyses of morphological characters alone provided little resolution, only Ficeae (one genus!) being well supported, although most Castilleae formed a clade, albeit with very little support (Clement & Weiblen 2009).
Zerega et al. (2010) provided a detailed phylogeny of Artocarpeae, which they recircumscribed. Cruad et al. (2012b) found that relationships along the backbone of Ficus were still rather poorly supported, although section Pharmacosycea was likely to be sister to the rest of the genus (see also Pederneiras et al. 2015: F. crassivenosa sister to the section) and subgenus Pharmacosycea was polyphyletic (Pederneiras et al. 2015). For rleationships in subsection Urostigma, see Chantarasuwan et al. (2015), the strict consensus tree of the analysis of 60+ morphological and anatomical characters is one gigantic polytomy.
Classification. See Clement and Weiblen (2009) for tribes and their delimitation (note the likely position of Treculia); they also discuss one or two problems with generic limits. Pederneiras et al. (2015) discuss the infrageneric classification of Ficus.
Botanical Trivia. The straightening stamens and reflexing tepals of Morus alba are reported to show the fastest movement of any plant parts known, over half the speed of sound (Taylor et al. 2006).
URTICACEAE Jussieu, nom. cons. Back to Rosales
Herbs to shrubs; dihydroflavonols?, (furanocoumarins) +; cork cortical [Urtica]); (wood fluoresces); (wood parenchyma not lignified); laticifers in bark only, latex not milky (milky); petiole bundle(s) annular or arcuate; bundle sheath extensions 0; cystoliths often elongated; stomata often anisocytic (paracytic, etc.); lamina base often asymmetric, vernation laterally or vertically conduplicate, stipule also intrapetiolar or sheathing; P (1-)4, 5(-6), valvate, (connate), staminate flowers: anther endothecium 0; pistillode +; carpellate flower: staminodes +; G 1, stylulus +, or stigma sessile, penicillate; ovule basal, ± straight, both integuments often 2 cells across, (protruding into the stylar canal; inner integument obturator, of several 1-celled thick projections in t.s.), parietal tissue 4-6 cells across, nucellar cap 2-4 cells across; fruit often a nut or achene; seed coat perforated, ± crushed, but various testal/tegmic layers persisting; chalazal endosperm haustorium +, (endosperm +; starchy), embryo straight; n = 7-14 [x = 14 is unlikely to be basal], 0.9-1.6 µm long, protein bodies in nuclei.
54[list]/2625 - five groups below. World-wide, but mainly tropical (map: from Frankenberg & Klaus 1980; Hultén & Fries 1986; Fl. Austral. 3. 1989; Fl. N. Am. 3. 1997: ??Arabia, Central Asia). [Photo - Shoot, Flower, Fruit.]
[Cecropieae + Boehmerieae]: ?
1. Cecropieae Gaudichaud
Trees to shrubs (lianas); (stilt roots +); bundle sheath extensions +; stomata anomocytic; hairs arachnoid, unicellular; cystoliths 0; leaves spiral, lamina palmately compound or -lobed (venation pinnate - some Coussapoa), stipules sheathing [open on side of stem opposite leaf]; plant dioecious, inflorescences terminal, ([elongated-]capitate); staminate flowers: filaments straight; (cotyledons thick, radicle short - Pouruma, Myrianthus)
5/177: Cecropia (80), Coussapoa (50). African and esp. New World tropics (Map: red, see Bonsen & ter Welle 1963; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010).
Synonymy: Cecropiaceae C. C. Berg
2. Boehmerieae Gaudichaud
(stipules 0 - Soleirolia).
3. [Leucosyke + Maoutia]: ?
[Elatostemateae + Urticeae: plant herbaceous; leaves 2-ranked, stipule 1; achenes asymmetrical.
4. Elatostemateae Gaudichaud
(leaves opposite), stipules (2), interpetiolar; P 2, 3; (achenes symmetrical).
Pilea (500-600), Elatostema (300).
5. Urticeae Lamarck & de Candolle
(Shrubs, trees); plant stinging (not); (leaves spiral, opposite), stipule 1, intrapetiolar, (stipules 2, interpetiolar); P 4 (1); (filaments not explosive - Poikilospermum), (achenes symmetrical).
Evolution. Divergence & Distribution. Urtica, although only of moderate size, is widely distributed and has many island endemics. Surprisingly, the small annual U. lobulata, from South Africa is sister to the shrubby New Zealand U. ferox, the clade they form being associated with clades that are basically Eurasian in distribution (Grosse-Veldmann et al. 2016b).
For the evolution of characters in Urticeae and Elatostemateae, see C. Kim et al. (2015a).
Ecology & Physiology. Cecropia is a fast-growing pioneer tree of the Neotropics that dominates the succession after clearing in South America, but the forest soon changes composition - c.f. situations where Vismia (Hypericaceae) is common (Mesquita et al. 2001).
Pollination Biology & Seed Dispersal. Explosive dispersal of the pollen as the filaments abruptly straightens is common in Urticaceae. The name "artillery plant", used for cultivated species of Pilea, refers to the little puffs of pollen visible when the inflorescence is jogged.
In Pilea the achenes are similarly dispersed by the abrupt straightening of the fleshy, inflexed filaments of the staminodes. The phyllostomid bat Artibeus eats Cecropia in Mexico in particular (Lobova et al. 2009 for records). Frugivorous birds of all kinds also favour the genus (Snow 1981; see also Charles-Dominique 1986 and other papers in Estrada & Fleming 1986) which is a prominent component of secondary vegetation in the New World (also Musanga in Africa). Myxospermy occurs here and elsewhere in the family (Western 2012).
Plant-Animal Interactions. It has been suggested that caterpillars of Nymphalini butterflies have a plesiomorphic association with Urticaceae as food plants (Janz et al. 2001); caterpillars in a clade of Nymphalidae-Heliconiinae-Acraeini utilise members of this family, probably switching from host plants in the Passifloraceae area (Silva-Brandão et al. 2008; see also Nylin & Wahlberg 2008; Wahlberg et al. 2009; Nylin et al. 2014).
The Neotropical Cecropia is associated with Azteca and some other ants that live in the stems and eat glycogen-rich food bodies (Müllerian bodies) produced by the plant at the abaxial base of the petiole (for a phylogeny of Cecropia, see Treiber et al. 2016). The age of this aasociation is unclear (c.f. the topology in Chomicki & Renner 2015: fig. S3). Glycogen is uncommon in plants, and Bischof et al. (2013) describe how it is synthesized. Beetles also eat these food bodies, as well as ant eggs, etc. (Jolivet 1991; Longino 1991; Yu & Davidson 1997). The association between plant and ant can break down, especially on islands and at high altitudes (Janzen 1973); Musanga, e.g. M. cecropioides, from Africa, also lacks ants but is otherwise very similar to Cecropia, and may be derived from within Cecropia (its sister species there, perhaps C. sciadophylla, is not myrmecophilous - Treiber et al. 2016). Species of Macaranga (Euphorbiaceae) are ecological analogues of Cecropia in Malesian forests, and in both bacteria living off colony debris are eaten by rhabditid nematodes that may in turn be eaten by ants (Maschwitz et al. 2016).
The parasitoid chalcoid wasps Aximopsis parasitize only Azteca queens, laying its eggs through the entrance hole to the colony soon after the queen has closed it (Gates & Pérez-Lachaud 2012 and references).
Chemistry, Morphology, etc. Groups of cells in the vascular tissue may be unlignified and the pericyclic sheath may also be late in lignifying; the presence of unlignified apotracheal parenchyma was used to divide the family (minus Cecropiaceae) into two main groups (Bonson & ter Welle 1984); Cecropia et al. have lignified parenchya (Bonson & ter Welle 1983). The different leaf types of anisophyllous Pellionia are very differently vascularized and have different nodal anatomies (Dengler & Donnelly 1987). Variation in stipule position and morphology around Urtica is considerable (Deng et al. 2013); no mention of prophylls...
Carpellate inflorescences of Zhengyia are borne towards the apex of the whole inflorescence, staminate inflorescences are basal (Deng et al. 2013). Boehmeria has a fleshy perianth. For the absence of an endothecium, see Staedtler (1923); this character needs more extensive sampling. The gynoecium is basically bicarpellate, but one carpel is highly reduced (Eckardt 1937). Shamrov (2004) shows the inner integument of Leucosyke becoming much elaborated and functioning as an obturator. The seeds of Dendrocnide may lack holes in the exotesta, and the whole seed coat is relatively well developed, while Kravtsova (2006) found ingrowths in cell walls of both the pericarp and seed coat, observations that should be extended.
See also Bigalke (1933: cystoliths and hairs), Fagerlind (1944a: Elatostema - embryology, apomixis, quite a lot of variation in ovule), Miller (1971: general), Hegnauer (1973, 1990: chemistry), Berg (1978), Kubitzki (1993b: general), Friis (1993: general) and Kravtsova (2003: seed coat anatomy, 2009: also fruit wall anatomy) for additional information.
Phylogeny. Urticaceae minus Cecropiaceae are paraphyletic (e.g. Sytsma et al. 2000, 2002 - three genes; Monro 2006 - two genes). Datwyler & Weiblen (2004 - one gene) and Zerega et al. (2005) found strong support for Poikilospermum (map above - green) as sister to the rest of the family - [Poikilospermum [Cecropiaceae s. str. [rest of Urticaceae]]]. However, Chomicki and Renner (2015: fig. S3) grouped Poikilospermum with Cecropia et al., but this is probably a sampling issue. In an extensive seven-gene/three compartment study, Cecropieae, only moderately supported, were sister to [Leucosyke + Maoutia], while Poikilospermum was part of a well supported clade that includes Urticeae, etc. (Wu et al. 2013). All told, four main clades were evident and provide a basis for thinking about diversification in the family. Hadiah et al. (2008) had found similar relationships, Poikilospermum being associated with Urtica, etc. (see also C. Kim et al. 2015a).
For a preliminary phylogenetic study of Elatostema, see Hadiah et al. (2003); Procris might have to be included (see also Hadiah et al. 2008). However, in a more comprehensive analysis Tseng et al. (2012) found Pellionia to be embedded in Elatostema, with Procris sister to Elatostema s.l.. See Monro (2006) for suggestions as to how to proceed with the phylogenetic analysis of the large genus Pilea. Deng et al. (2013) and in particular C. Kim et al. (2015a) discuss relationships around Urtica; Laportea and Urera are not monophyletic, and Hesperocnide (California, Hawaii!) is embedded in Urtica. For a comprehensive phylogeny of Urtica, which has important implications for species limits there, see Grosse-Veldmann et al. (2016b).
Classification. The four main clades recovered in the phylogeny of Wu et al. (2013) are recognised as tribes above, except that [Leucosyke + Maoutia], sister to Cecropieae, are separated from that tribe. Boehmerieae make up most of clade I, Forsskaoleeae and Parietarieae are sister taxa and in turn are sister to the other Boehmerieae.