EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, initially ±globular, not motile, branched; showing gravitropism; glycolate oxidase +, glycolate metabolism in leaf peroxisomes [glyoxysomes], acquisition of phenylalanine lysase* [PAL], flavonoid synthesis*, microbial terpene synthase-like genes +, triterpenoids produced by CYP716 enzymes, CYP73 and phenylpropanoid metabolism [development of phenolic network], xyloglucans in primary cell wall, side chains charged; plant poikilohydrous [protoplasm dessication tolerant], ectohydrous [free water outside plant physiologically important]; thalloid, leafy, with single-celled apical meristem, tissues little differentiated, rhizoids +, unicellular; chloroplasts several per cell, pyrenoids 0; centrioles/centrosomes in vegetative cells 0, microtubules with γ-tubulin along their lengths [?here], interphase microtubules form hoop-like system; metaphase spindle anastral, predictive preprophase band + [with microtubules and F-actin; where new cell wall will form], phragmoplast + [cell wall deposition centrifugal, from around the anaphase spindle], plasmodesmata +; antheridia and archegonia +, jacketed*, surficial; blepharoplast +, centrioles develop de novo, bicentriole pair coaxial, separate at midpoint, centrioles rotate, associated with basal bodies of cilia, multilayered structure + [4 layers: L1, L4, tubules; L2, L3, short vertical lamellae] (0), spline + [tubules from L1 encircling spermatid], basal body 200-250 nm long, associated with amorphous electron-dense material, microtubules in basal end lacking symmetry, stellate array of filaments in transition zone extended, axonemal cap 0 [microtubules disorganized at apex of cilium]; male gametes [spermatozoids] with a left-handed coil, cilia 2, lateral, asymmetrical; oogamy; sporophyte +*, multicellular, growth 3-dimensional*, cuticle +*, plane of first cell division transverse [with respect to long axis of archegonium/embryo sac], sporangium and upper part of seta developing from epibasal cell [towards the archegonial neck, exoscopic], with at least transient apical cell [?level], initially surrounded by and dependent on gametophyte, placental transfer cells +, in both sporophyte and gametophyte, wall ingrowths develop early; suspensor/foot +, cells at foot tip somewhat haustorial; sporangium +, single, terminal, dehiscence longitudinal; meiosis sporic, monoplastidic, MTOC [= MicroTubule Organizing Centre] associated with plastid, sporocytes 4-lobed, cytokinesis simultaneous, preceding nuclear division, quadripolar microtubule system +; wall development both centripetal and centrifugal, 1000 spores/sporangium, sporopollenin in the spore wall* laid down in association with trilamellar layers [white-line centred lamellae; tripartite lamellae]; plastid transmission maternal; nuclear genome [1C] <1.4 pg, main telomere sequence motif TTTAGGG, KNOX1 and KNOX2 [duplication] and LEAFY genes present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes [precursors for starch synthesis], tufA, minD, minE genes moved to nucleus; mitochondrial trnS(gcu) and trnN(guu) genes +.
Many of the bolded characters in the characterization above are apomorphies of more or less inclusive clades of streptophytes along the lineage leading to the embryophytes, not apomorphies of crown-group embryophytes per se.
All groups below are crown groups, nearly all are extant. Characters mentioned are those of the immediate common ancestor of the group,  contains explanatory material, () features common in clade, exact status unclear.
Sporophyte well developed, branched, branching dichotomous, potentially indeterminate; hydroids +; stomata on stem; sporangia several, terminal; spore walls not multilamellate [?here].
II. TRACHEOPHYTA / VASCULAR PLANTS
Sporophyte long lived, cells polyplastidic, photosynthetic red light response, stomata open in response to blue light; plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; plant endohydrous [physiologically important free water inside plant]; PIN[auxin efflux facilitators]-mediated polar auxin transport; (condensed or nonhydrolyzable tannins/proanthocyanidins +); borate cross-linked rhamnogalactan II, xyloglucans with side chains uncharged [?level], in secondary walls of vascular and mechanical tissue; lignins +; roots +, often ≤1 mm across, root hairs and root cap +; stem apex multicellular [several apical initials, no tunica], with cytohistochemical zonation, plasmodesmata formation based on cell lineage; vascular development acropetal, tracheids +, in both protoxylem and metaxylem, G- and S-types; sieve cells + [nucleus degenerating]; endodermis +; stomata numerous, involved in gas exchange; leaves +, vascularized, spirally arranged, blades with mean venation density ca 1.8 mm/mm2 [to 5 mm/mm2], all epidermal cells with chloroplasts; sporangia in strobili, sporangia adaxial, columella 0; tapetum glandular; sporophyte-gametophyte junction lacking dead gametophytic cells, mucilage, ?position of transfer cells; MTOCs not associated with plastids, basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; archegonia embedded/sunken [only neck protruding]; embryo suspensor +, shoot apex developing away from micropyle/archegonial neck [from hypobasal cell, endoscopic], root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Sporophyte growth ± monopodial, branching spiral; roots endomycorrhizal [with Glomeromycota], lateral roots +, endogenous; G-type tracheids +, with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangium dehiscence by a single longitudinal slit; cells polyplastidic, MTOCs diffuse, perinuclear, migratory; blepharoplasts +, paired, with electron-dense material, centrioles on periphery, male gametes multiciliate; nuclear genome [1C] 7.6-10 pg [mode]; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; mitochondrion with loss of 4 genes, absence of numerous group II introns; LITTLE ZIPPER proteins.
Sporophyte woody; stem branching axillary, buds exogenous; lateral root origin from the pericycle; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].
SEED PLANTS† / SPERMATOPHYTA†
Growth of plant bipolar [plumule/stem and radicle/root independent, roots positively geotropic]; plants heterosporous; megasporangium surrounded by cupule [i.e. = unitegmic ovule, cupule = integument]; pollen lands on ovule; megaspore germination endosporic, female gametophyte initially retained on the plant, free-nuclear/syncytial to start with, walls then coming to surround the individual nuclei, process proceeding centripetally.
EXTANT SEED PLANTS
Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); microbial terpene synthase-like genes 0; primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignin chains started by monolignol dimerization [resinols common], particularly with guaiacyl and p-hydroxyphenyl [G + H] units [sinapyl units uncommon, no Maüle reaction]; roots often ≥1 mm across, stele diarch to pentarch, xylem and phloem originating on alternating radii, cork cambium deep seated, gravitropism response fast; stem apical meristem complex [with quiescent centre, etc.], plasmodesma density in SAM 1.6-6.2[mean]/μm2 [interface-specific plasmodesmatal network]; eustele +, protoxylem endarch, endodermis 0; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; cork cambium superficial; leaf nodes 1:1, a single trace leaving the vascular sympodium; leaf vascular bundles amphicribral; guard cells the only epidermal cells with chloroplasts, stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; branching by axillary buds, exogenous; prophylls two, lateral; leaves with petiole and lamina, development basipetal, lamina simple; sporangia borne on sporophylls; spores not dormant; microsporophylls aggregated in indeterminate cones/strobili; grains monosulcate, aperture in ana- position [distal], primexine + [involved in exine pattern formation with deposition of sporopollenin from tapetum there], exine and intine homogeneous, exine alveolar/honeycomb; ovules with parietal tissue [= crassinucellate], megaspore tetrad linear, functional megaspore single, chalazal, sporopollenin 0; gametophyte ± wholly dependent on sporophyte, development initially endosporic [apical cell 0, rhizoids 0, etc.]; male gametophyte with tube developing from distal end of grain, male gametes two, developing after pollination, with cell walls; embryo cellular ab initio, suspensor short-minute, embryonic axis straight [shoot and root at opposite ends], primary root/radicle produces taproot [= allorhizic], cotyledons 2; embryo ± dormant; chloroplast ycf2 gene in inverted repeat, trans splicing of five mitochondrial group II introns, rpl6 gene absent; ??whole nuclear genome duplication [ζ/zeta duplication event], 2C genome size (0.71-)1.99(-5.49) pg, two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], 5.8S and 5S rDNA in separate clusters.
IID. ANGIOSPERMAE / MAGNOLIOPHYTA
Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANA grade?], lignin also with syringyl units common [G + S lignin, positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], hemicelluloses as xyloglucans; root cap meristem closed (open); pith relatively inconspicuous, lateral roots initiated immediately to the side of [when diarch] or opposite xylem poles; epidermis probably originating from inner layer of root cap, trichoblasts [differentiated root hair-forming cells] 0, hypodermis suberised and with Casparian strip [= exodermis]; shoot apex with tunica-corpus construction, tunica 2-layered; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, multiseriate rays +, wood parenchyma +; sieve tubes enucleate, sieve plates with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, not occluding pores of plate, companion cell and sieve tube from same mother cell; ?phloem loading/sugar transport; nodes 1:?; dark reversal Pfr → Pr; protoplasm dessication tolerant [plant poikilohydric]; stomata randomly oriented, brachyparacytic [ends of subsidiary cells ± level with ends of guard cells], outer stomatal ledges producing vestibule, reduction in stomatal conductance with increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, secondary veins pinnate, fine venation hierarchical-reticulate, (1.7-)4.1(-5.7) mm/mm2, vein endings free; flowers perfect, pedicellate, ± haplomorphic, protogynous; parts free, numbers variable, development centripetal; P = T, petal-like, each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], each theca dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, endothecium +, cells elongated at right angles to long axis of anther; tapetal cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine restricted to the apertural regions, thin, compact, intine in apertural areas thick, orbicules +, pollenkitt +; nectary 0; carpels present, superior, free, several, spiral, ascidiate [postgenital occlusion by secretion], stylulus at most short [shorter than ovary], hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry; suprastylar extragynoecial compitum +; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across, nucellar cap?; megasporocyte single, hypodermal, functional megaspore lacking cuticle; female gametophyte lacking chlorophyll, four-celled [one module, egg and polar nuclei sisters]; ovule not increasing in size between pollination and fertilization; pollen grains bicellular at dispersal, germinating in less than 3 hours, siphonogamy, pollen tube unbranched, growing towards the ovule, between cells, growth rate (ca 10-)80-20,000 µm h-1, tube apex of pectins, wall with callose, lumen with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametophytes tricellular, gametes 2, lacking cell walls, ciliae 0, double fertilization +, ovules aborting unless fertilized; fruit indehiscent, P deciduous; mature seed much larger than fertilized ovule, small [<5 mm long], dry [no sarcotesta], exotestal; endosperm +, ?diploid [one polar nucleus + male gamete], cellular, development heteropolar [first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous, embryo short [<¼ length of seed]; plastid and mitochondrial transmission maternal; Arabidopsis-type telomeres [(TTTAGGG)n]; nuclear genome [2C] (0.57-)1.45(-3.71) [1 pg = 109 base pairs], ??whole nuclear genome duplication [ε/epsilon event]; ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, palaeo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]]; chloroplast IR expansions, chlB, -L, -N, trnP-GGG genes 0.
[NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]]: wood fibres +; axial parenchyma diffuse or diffuse-in-aggregates; pollen monosulcate [anasulcate], tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.
[AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: phloem loading passive, via symplast, plasmodesmata numerous; vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood + [reaction wood: with gelatinous fibres, G-fibres, on adaxial side of branch/stem junction]; anther wall with outer secondary parietal cell layer dividing; tectum reticulate; nucellar cap + [character lost where in eudicots?]; 12BP [4 amino acids] deletion in P1 gene.
[[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]] / MESANGIOSPERMAE: benzylisoquinoline alkaloids +; sesquiterpene synthase subfamily a [TPS-a] [?level], polyacetate derived anthraquinones + [?level]; outer epidermal walls of root elongation zone with cellulose fibrils oriented transverse to root axis; P more or less whorled, 3-merous [?here]; pollen tube growth intra-gynoecial; extragynoecial compitum 0; carpels plicate [?here]; embryo sac monosporic [spore chalazal], 8-celled, bipolar [Polygonum type], antipodal cells persisting; endosperm triploid.
[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (veins in lamina often 7-17 mm/mm2 or more [mean for eudicots 8.0]); (stamens opposite [two whorls of] P); (pollen tube growth fast).
[CERATOPHYLLALES + EUDICOTS]: ethereal oils 0 [or next node up]; fruit dry [very labile].
EUDICOTS: (Myricetin +), asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; (vessel elements with simple perforation plates in primary xylem); nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; protandry common; K/outer P members with three traces, ("C" +, with a single trace); A ?, filaments fairly slender, anthers basifixed; microsporogenesis simultaneous, pollen tricolpate, apertures in pairs at six points of the young tetrad [Fischer's rule], cleavage centripetal, wall with endexine; G with complete postgenital fusion, stylulus/style solid [?here], short [<2 x length of ovary]; seed coat?; palaeotetraploidy event.
[PROTEALES [TROCHODENDRALES [BUXALES + CORE EUDICOTS]]]: (axial/receptacular nectary +).
[TROCHODENDRALES [BUXALES + CORE EUDICOTS]]: benzylisoquinoline alkaloids 0; euAP3 + TM6 genes [duplication of paleoAP3 gene: B class], mitochondrial rps2 gene lost.
[BUXALES + CORE EUDICOTS]: mitochondrial rps11 gene lost.
CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one position]; micropyle?; γ genome duplication [allopolyploidy, 4x x 2x], x = 3 x 7 = 21, 2C genome size (0.79-)1.05(-1.41) pg, PI-dB motif +; small deletion in the 18S ribosomal DNA common.
[ROSIDS ET AL. + ASTERIDS ET AL.] / PENTAPETALAE / [SANTALALES, CARYOPHYLLALES, SAXIFRAGALES, DILLENIALES, VITALES, ROSIDAE, [BERBERIDOPSIDALES + ASTERIDAE]: root apical meristem closed; (cyanogenesis also via [iso]leucine, valine and phenylalanine pathways); flowers rather stereotyped: 5-merous, parts whorled; P = K + C, K enclosing the flower in bud, with three or more traces, odd K adaxial, C with single trace; A = 2x K/C, in two whorls, alternating, (many, but then usually fasciculate and/or centrifugal); pollen tricolporate; G [(3, 4) 5], when 5 opposite K, whorled, placentation axile, style +, stigma not decurrent, compitum + [one position]; endosperm nuclear/coenocytic; fruit dry, dehiscent, loculicidal [when a capsule]; floral nectaries with CRABSCLAW expression, RNase-based gametophytic incompatibility system present.
Phylogeny. Prior to the seventh version of this site asterids were part of a major polytomy that included rosids, Berberidopsidales, Santalales, and Caryophyllales, but then the order of branching below the asterids seemed to be stabilizing, perhaps with a clade [Berberidopsidales [Santalales [Caryophyllales + Asterids]]] while rosid relationships seemed to be [Saxifragales [Vitales + Rosids]]]. However, recent work suggests a polytomy is indeed probably the best way to visualize relationships around here at present. So for further discussion of relationships at the base of asterids and rosids, see the Pentapetalae
[BERBERIDOPSIDALES + ASTERIDAE]]: ?
ASTERIDAE / ASTERANAE Takhtajan: nicotinic acid metabolised to its arabinosides; (iridoids +); tension wood decidedly uncommon; C enclosing A and G in bud, (connate [sometimes evident only early in development, petals then appearing to be free]); anthers dorsifixed?; if nectary +, gynoecial; G , style single, long; ovules unitegmic, integument thick [5-8 cells across], endothelium +, nucellar epidermis does not persist; exotestal [!: even when a single integument] cells lignified, esp. on anticlinal and/or inner periclinal walls; endosperm cellular.
[ONCOTHECALES [LAMIIDAE/ASTERID I + CAMPANULIDAE/ASTERID II]] / CORE ASTERIDS / EUASTERIDS / GENTIANIDAE: plants woody, evergreen; ellagic acid 0, non-hydrolysable tannins not common; vessel elements long, with scalariform perforation plates; sugar transport in phloem active; inflorescence usu. basically cymose; flowers rather small [<8 mm across]; C free or basally connate, valvate, often with median adaxial ridge and inflexed apex ["hooded"]; A = and opposite K/P, free to basally adnate to C; G [#?]; ovules 2/carpel, apical, pendulous; fruit a drupe, [stone ± flattened, surface ornamented]; seed single; duplication of the PI gene.
ASTERID II / CAMPANULIDAE: myricetin 0; style shorter than the ovary; endosperm copious, embryo short/very short.
[BRUNIALES [ASTERALES [APIALES, DESFONTAINIALES, DIPSACALES, ESCALLONIALES, PARACRYPHIALES]]] / APIIDAE: tube initiation early; G inferior, , style long.
[ASTERALES [APIALES, DESFONTAINIALES, DIPSACALES, ESCALLONIALES, PARACRYPHIALES]] / CORE CAMPANULIDS: C forming distinct tube; A epipetalous.
[APIALES, DESFONTAINIALES, DIPSACALES, ESCALLONIALES, PARACRYPHIALES]: ?If the next is a clade...
[APIALES [PARACRYPHIALES + DIPSACALES]] / DIPSAPIIDAE: nodes 3:3.
Age. The age of this node is estimated at (105-)84(-58) Ma (Lemaire et al. 2011b); K. Bremer et al. (2004) suggested an age of ca 113 Ma, Foster et al. (2016a: q.v. for details) an age of about 95 Ma, Magallón and Castillo (2009: c.f. position of Paracryphiales) an age of ca 92 Ma, Magallón et al. (2015) an age of around 85.6 Ma, Naumann et al. (2013) an age of around 75.2 Ma, and Beaulieu et al. (2013a: 95% HPD) an age of (101-)91(-79) My; around 92 or 86.4 Ma are ages in Nylinder et al. (2012: suppl.), ca 124 Ma in Nicolas and Plunkett (2014), (106.5-)93(-79.7) Ma in Tank and Olmstead (2017), and (107-)96(-84) Ma in Wikström et al. (2015).
Divergence & Distribution. Initial diversification of this clade probably occurred in the southern hemisphere, but clades in it like Apiaceae "coincide" with more recent movements to the north (Beaulieu et al. 2013a).
Phylogeny. For the relationships of Apiales, see the asterid II/gentianid clade.
APIALES Nakai - Main Tree.
Woody; route II decarboxylated iridoids +; vessel elements with scalariform perforation plates, solitary, pits [both vessels and fibres] distinctly bordered, axial parenchyma diffuse-in-aggregate; nodes 3:3 [?level]; stomata anomocytic; lamina venation pinnate, (margins toothed or lobed); inflorescence terminal, branched ["paniculate"]; plant dioecious; pedicels articulated; plant ± dioecious; flowers small, [<1.5 cm across], K small, C apparently free; A free; G , one carpel alone fertile [?Pennantia], placentation apical; ovules 1-2/carpel, apical, pendulous, apotropous, nucellus type?, funicular obturator +; fruit a drupe, seed single; endosperm nuclear; x = ?6; mitochondrial rpl2 gene lost. - 7 families, 494 genera, 5,489 species.
Includes Apiaceae, Araliaceae, Griseliniaceae, Myodocarpaceae, Pennantiaceae, Pittosporaceae, Torricelliaceae.
Note: In all node characterizations, boldface denotes a possible apomorphy, (....) denotes a feature the exact status of which in the clade is uncertain, [....] includes explanatory material; other text lists features found pretty much throughout the clade. Note that the precise node to which many characters, particularly the more cryptic ones, should be assigned is unclear. This is partly because homoplasy is very common, in addition, basic information for all too many characters is very incomplete, frequently coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there are the not-so-trivial issues of how character states are delimited and ancestral states are reconstructed (see above).
Age. The age of crown-group Apiales is estimated to be (130-)117(-103.7) Ma (Nicolas & Plunkett 2014), ca 91.4 Ma (Tank et al. 2015: Table S2), ca 80.8 Ma (Magallón et al. 2015) or (100.9-)86.7(-73.3) Ma (Maurin 2020).
For the fossil record of the order, see Martínez-Millán (2010) and Nicolas and Plunkett (2014).
Evolution: Divergence & Distribution. Apiales contain ca 2.4% eudicot diversity (Magallón et al. 1999). Although Magallón and Sanderson (2001) estimated that diversification in Apiales had increased, as Nicolas and Plunkett (2014) correctly point out, the bulk of the diversity in Apiales is in Apiaceae.
Nicolas and Plunkett (2014: conclusions not affected by the position of Pennantiaceae) suggest that Pennantiaceae, Torricelliaceae, Griseliniaceae, and a clade representing the rest of the order are ancient (Cretaceous) and possibly of East Gondwanan origin, although East Asia is also involved. They thought that vicariance might be involved in some of the distributions, e.g. of the three genera of Torricelliaceae, etc..
Kårehed (2003: see also Chandler & Plunkett 2004; Bittrich & Kadereit 2018) provides a good summary of what is known of the main clades in Apiales (and where they have been placed in the past) However, thinking about morphological evolution is particularly difficult in Apiales because of our incomplete knowledge of and the extensive variation in the characters of interest. The basal pectinations are genera that have transseptal bundles in common, as well as some rays over 10 cells wide and with square or upright cells (Noshiro & Baas 1998; Baas et al. 2000). Pennantia, with a superior ovary, may also be placed here (see below). Unfortunately, corolla initiation, pollen cell number, and many other characters are unknown for these taxa, although some information for the ex-Cornalean genera can be found in Patel (1973), Philipson (1967), and Philipson and Stone (1980). Pennantia has similar (plesiomorphic) wood anatomy, rather like Griseliniaceae but unlike that of other other Apiales (Lens et al 2008a); this suite of characters is scored as having two origins in Apiales... Dioecy may be the ancestral condition for the order (Schlessmann 2010, q.v. for other characters; c.f. Schlessman et al. 2001), and if so, perfect flowers/monoecy have re-evolved, and they overwhelmingly predominate in the clade (Käfer et al. 2014, 2017). Griseliniaceae and Torricelliaceae both have the iridoid griselinoside, transseptal bundles in the ovary, and the abaxial carpel alone is fertile, the single ovule being apotropous. There is other interesting variation. Thus Pittosporaceae and Araliaceae have early corolla tube formation while the petals in at least some Apiaceae are separate even at their initiation (Erbar & Leins 2004c); these observations need to be extended.
Pennantia has a superior ovary (and sometimes a thick, disciform, sessile stigma), and how its gynoecium is interpreted (summarized in Kårehed 2003a) has many implications for character evolution. Here the gynoecium is interpreted as being tricarpelate, although it appears to be single ("pseudomonomerous"), and the carpel that is fertile is abaxial (see also Chandler & Plunkett 2004; Plunkett et al. 2004c for carpel number). Erbar and Leins (1988a, 1996a, 2004c) suggested that the nectary "disc" of Apiaceae and Araliaceae is a carpellary flank nectary displaced by intercalary growth, and that the axile placentation and inferior ovary of these two families is easily related to the parietal placentation and superior ovary of Pittosporaceae which are florally apparently very dissimilar to all other members of the order (see below). The ovary of Pittosporaceae has a short basal zone with separate loculi, the ovules being borne above this zone - essentially the same position in which the ovules of Apiaceae and Araliaceae are found. However, gynoecial development, etc., in the whole Apiales badly needs reinvestigation, since apart from Pennantiaceae (perhaps sister to the rest of the order, but perhaps wrongly placed here), nearly all Apiales have inferior ovaries. Interestingly, clades with with superior and inferior ovaries interdigitate in most other campanulid orders. Further complicating the issue, relationships around Apiales are not very well supported (C. Zhang et al. 2020).
Genes & Genomes. Yi et al. (2004) suggest that the basic chromosome number in Apiales is x = 6 (see also Raven 1975), although the order then would have all polyploid/dysploid members, with several independent origins of polyploidy. The Dc-β genome duplication event probably occurred around here was probably an allotetraploidy and has been dated to 87-77 Ma (J. Wang et al. 2020; see/c.f. also Iorizzo et al. 2016).
Chemistry, Morphology, etc.. For wood anatomy, see Lens et al. (2008a).
Nuraliev et al. (2019) discuss the diversity of floral symmetry in the order; the orientation of the carpels in the basal clades with 3-carpelate gynoecia is unclear (Sokoloff et al. 2018). For nectary morphology, see Erbar and Leins (2010). Endress (2003c) summarizes the rather sparse literature on nucellus development in the clade.
Phylogeny. In earlier studies a grouping [Griselinia [Aralidium + Torricellia]] was rather weakly supported (Backlund & Bremer 1997; see also Chandler & Plunkett 2002). Plunkett (2001) and Lundberg (2001c) both suggested that Torricelliaceae and Griseliniaceae were successive clades near the base of Apiales (Kårehed 2002a: four genes, all genera sampled, strong Bayesian support), and this topology is followed here (see also Soltis et al. 2011; Tank & Donoghue 2010); the relationship is reversed in Chandler and Plunkett (2004), but with a p.p. of 0.93.
The ex-icacinaceous Pennantia is sister to all other Apiales, at least in chloroplast phylogenies (e.g. Kårehed 2003; Lens et al. 2008a: strong support; H.-T. Li et al. 2019: plastome analyses). However, nuclear markers place it elsewhere in the campanulids, perhaps sister to Dipsacales (e.g. Chandler & Plunkett 2004), so its position must be confirmed, but the monophyly of the rest of the order seems not to be in doubt.
Pittosporaceae were found to be sister to the old Apiaceae and Araliaceae (e.g. Kårehed 2002c; Andersson et al. 2006: strong support, Myodocarpaceae not included), a position that was strongly supported by Tank and Donoghue (2010). However, earlier studies might find Pittosporaceae to be embedded in the clade, some Bayesian analyses giving strong posterior probabilities for a relationship between Myodocarpaceae and Pittosporaceae (Chandler & Plunkett 2004), or they provided only weak support for a sister group position (Nicolas & Plunkett 2009). Overall, the relationships [Pittosporaceae [Araliaceae [Myodocarpaceae + Apiaceae]]] for the core Apiales seem most likely (Tank et al. 2007; Tank & Donoghue 2010; Soltis et al. 2011; Nicolas & Plunkett 2014).
There are some similarities between the [Pittosporaceae [Araliaceae [Myodocarpaceae + Apiaceae]]] clade and Asterales like Campanulaceae and Asteraceae (e.g. Erbar & Leins 2004; Leins & Erbar 2004b), thus 1-benzyltetrahydroisoquinoline alkaloids are found in both (Kubitzki et al. 2011). However, given the rather strongly supported set of relationships at the base of Apiales, the other clades that are in this part of the campanulids, and relationships within Asterales (Campanulaceae and Asteraceae are not immediately related), most of these similarities are parallelisms.
Synonymy: Apiineae Plunkett & Lowry, Aralidiinae Thorne & Reveal - Ammiales Small, Araliales Berchtold & J. Presl, Aralidiales Reveal, Griseliniales Reveal & Doweld, Hederales Link, Pennantiales Doweld, Pittosporales Link, Torricelliales Reveal & Doweld
PENNANTIACEAE J. Agardh - Back to Apiales
Trees or shrubs; iridoids ?; vessel elements 1080-1500(-2250) µm long, with ? perforation plates, fibers 1790-2270(-2900) µm long; nodes 3:3; petiole bundle annular (with a medullary bundle) and with solid annular wing bundles; stomata paracytic; lamina ptyxis curved to conduplicate, (margins entire); K ± free, minute, C valvate, connate or not, apex inflexed; nectary 0; staminate flowers: A (epipetalous), variously bent, anthers dorsifixed; pistillode +; carpelate flowers: staminodes +/0; G , also , (longitudinally ridged), 1-locular, styles short, stigmas punctate, or stigma sessile, broad; ovule 1/carpel, at most thinly crassinucellate, integument vascularized; fruit a drupe, endocarp sclereids isodiametric, fibrous lining of loculus well developed; seed coat thin; endosperm development?, embryo short/minute [to 1/3 the seed length]; n = 25, x = 25.
1 [list]/4. N.E. Australia, Three Kings Island, Norfolk Island, New Zealand (map: from van Balgooy 1966; Fl. Austral. 4. 1984). [Photo - Habit.]
Age. Crown-group Pennantiaceae are around 6.6 Ma (Nicolas & Plunkett 2014) or (19.5-)9.5(-2.6) Ma (Maurin et al. 2020).
Chemistry, Morphology, etc.. Collenchyma is only poorly developed, and a pericyclic sheath is present; pits in general are bordered.
For the morphology of the stigma, see Kårehed (2002b). For information, which should be confirmed, on ovule morphology, see Mauritzon (1936c).
For other information, see Gardner and de Lange (2002), Sleumer (1942) and Potgeiter (2018), all general, also Bailey and Howard (1941a-d), Heintzelmann and Howard (1948), van Staveren and Baas (1973) and Baas (1973, 1974), all anatomy, Lobreau-Callen (1980: pollen), Miers (1852: ovule orientation) and Manchester et al. (2017: fruit).
Phylogeny. Pennantia cunninghamii is sister to the rest of the genus(Maurin 2020, see also Keeling et al. 2007).
Previous Relationships. Pennantia until a few years ago was in Icacinaceae. now in several separate orders in the lamiids, i.e. as Icacinaceae s. str. (Icacinales), Cardiopteridales, as well as perhaps in the campanulids as Metteniusales, and as sister to all other core asterids as Oncothecales; Pennantia is the only genus that seems to have wandered away from these orders.
[Torricelliaceae [Griseliniaceae [Pittosporaceae [Araliaceae [Myodocarpaceae + Apiaceae]]]]]: polyacteylenes +; young stems with peripheral collechyma; pericyclic fibres 0 or few; nodes 5(+):5(+); leaf base broad [encircling 2/3 the stem or more]; C apparently free, imbricate; gynoecial nectary +; style branches/stigmas recurved; nectary on top of ovary.
Age. K. Bremer et al. (2004) dated this node to ca 84 Ma, Tank et al. (2015: Table S2) to ca 82.1 Ma, Tank and Olmstead (2017) to (89.5-)76.1(-63.6) Ma, Magallón et al. (2015) to ca 72.2 Ma, Wikström et al. (2001: note topology) to (74-)69, 63(-58) Ma, Wikström et al. (2015) to (83-)67(-56) Ma, Janssens et al. (2009) to 87±14.1 Ma, Magallón and Castillo (2009) offered an estimate of ca 74.9 Ma, Bell et al. (2010) one of (63-)53, 49(-39) Ma, while Beaulieu et al. (2013a: 95% HPD) thought that it was (95-)84(-71) Ma; (119.8-)106.9(-94) Ma is another estimate (Nicolas & Plunkett 2014) while almost at the other extreme, around 55 or 48 Ma are ages in Nylinder et al. (2012: suppl.). See also Maurin (2020) - (85.5-)73.1(-61.1) Ma.
Chemistry, Morphology, etc.. Polyacetylenes, mainly aliphatic, including the C17 acetylenes, falcarinone, etc., are found in the [Pittosporaceae [Araliaceae [Myodocarpaceae + Apiaceae]]] clade, while the polyacteylenes of Torricellia angulata, quite recently described, are C11 acids that are unique in having a chiral center (Pan et al. 2006); iridoids are found in the same species (Liang et al. 2009).
For the wood anatomy of this clade, see Noshiro and Baas (1998) and Lens et al. (2008a).
TORRICELLIACEAE H. H. Hu - Back to Apiales
Griselinoside/aralidioside [iridoid], (C11 polyacetylenes [acidic] +); vessel elements clustered, septate fibres with minutely bordered pits, exclusively scanty paratracheal parenchyma; crystal sand +; mucilage cells +; glandular hairs +; petiole (with small adaxial flange [ligule]); flowers usu. imperfect; K imbricate or largely connate; staminate flowers: anthers sagittate; pollen (in tetrads), tectum reticulate; carpelate flowers: G [(2-4)]), transseptal bundles +, styluli/style branches distinct; ovule 1/carpel; fruit with two empty and one fertile loculi, sterile loculi with aperture in stone, fertile locule with germination valve, mesoocarp sclereids isodiametric, fibres lining loculus, 1-layer (0); x = 8.
3 [list]/10. Madagascar, South East Asia and W. Malesi. Map: fossils of Torricellia [blue] from Meller (2006).
Age. The age of this node is estimated to be (81-)53(-27) Ma (Lemaire et al. 2011b), ca 57.2 Ma (Nicolas & Plunkett 2014), or a mere (41-)22(-8) Ma (Wikström et al. 2015).
Fossil Pantocarpon fruits known from ca 66 Ma Deccan intertrappean deposits have previously been placed in everything from monocots to Verbenaceae, but Manchester et al. (2020) suggested that they may belong to Torricelliaceae. Like extant Torricelliaceae they have 3-carpellate drupaceous fruits with paired apertures over sterile carpels and valves in the single-seeded fertile carpels, but there are several differences. Pantocarpon has two fertile carpels, extant Torricelliaceae just one, three (versus two) longitudinal ?germination valves in each fertile carpel, notably smaller fruits and a distinctive testa made up of tracheoidal fibres with annular thickenings and of a kind unknown from any other Apiales (Manchester et al. 2020).
1. Aralidium Miquel
Tree, evergreen; alkaloids +; vessel elements with scalariform perforation plates; petiole bundles numerous, scattered; stomata anisocytic; lamina deeply pinnately lobed, petiole base with marginal flange; C imbricate; nectary vascularized; Carpelate flowers: staminodes +; integument "massive", parietal tissue ca 4 cells across, raphe dorsal; seed coat vascularized; endosperm ruminate; n = 20 ±2.
1/1: Aralidium pinnatifidum. Southern Thailand, the Malay Peninsula, Sumatra and Borneo (map: see above).
Synonymy: Aralidiaceae Philipson & B. C. Stone
[Torricellia + Melanophylla]: vessel elements with simple perforation plates; stomata anomocytic; pedicels not articulated.
Age. This clade is estimated to be (61.2-)53.7(-48.0) Ma (Maurin et al. 2020).
2. Torricellia de Candolle
Shrub to tree, deciduous; chemistry largely unknown; lamina (lobed), (margins serrate), venation palmate; K basally connate; staminate flowers: C induplicate-valvate, apex inflexed; pistillode +; carpelate flowers: C 0; staminodes 0; stigmas ± bifid; testa slightly sclerified; embryo thin, curved; n = 12.
1/2. Nepal to western China (map: see above).
3. Melanophylla Baker
Shrub to small tree, deciduous; lamina margin entire; fl0wers perfect; plane of symmetry transverse; K open, basally connate, C contorted [direction variable]; anther connective broad; nectary 0; ?floral vasculature, style stout, short; exotesta scalariform-thickened, unlignified; n = ?
1/7. Madagascar (map: see above). Photo: Melanophylla Habit.
Synonymy: Melanophyllaceae Airy Shaw
Evolution: Divergence & Distribution. For the fossil history of the East Asian endemic Torricellia, see Meller (2006), Manchester et al. (2009, c.f. 2017) and Collinson et al. (2012); the genus was widespread in the northern hemisphere (western North America, Germany) by the late Palaeocene and the first records are dated to 48 Ma (see also Martínez-Millán 2010).
Chemistry, Morphology, etc.. Ellagic acid was mentioned (prior to 10.x.2017) as occurring here; this seems to have been a lapsus calami (it would have been, if I had been using one).
The variabiity of the chirality of corolla aestivation is perhaps more to be expected in a rosid (Karpunina et al. 2019). Manchester et al. (2017) describe the distinctive anatomy of the fruit: In Torricellia and Melanophylla the two sterile loculi are larger than the fertile loculus, while in Aralidium the sterile loculi are quite large at the apex of the fruit but become much smaller at the base where they are entirely surrounded by the fertile loculus.
For general information, see Plunkett et al. (2018c) and Nuraliev (2019), for thata of Aralidium in particular, see Philipson and Stone (1980, and other papers in Taxon 29(4). 1980), for Melanophylla, see Schatz et al. (1998: revision) Sokoloff et al. (2018) and Karpunina et al. (2019), both floral development, Ferguson (1977: pollen) and Trifonova (1998: ovule and seed), and for Torricellia, see Lobreau-Callen (1977: pollen), Philipson (1977: ovule), and Takhtajan (2000: ovule and seed, etc.).
Phylogeny. For the circumscription of this clade, see also Plunkett et al. (2004c); relationships are [Aralidium [Melanophylla + Torricellia]] (see also Soltis et al. 2011).
Previous Relationships. Melanophylla was included in Hydrangeales and Torricellia and Aralidium were placed in separate monogeneric orders, both in Cornidae-Cornanae, by Takhtajan (1997); all have been placed in Cornaceae s.l. in the past.
Synonymy: Aralidiaceae Philipson & B. C. Stone, Melanophyllaceae Airy Shaw
[Griseliniaceae [Pittosporaceae [Araliaceae [Myodocarpaceae + Apiaceae]]]]: C18 petroselinic acid + [in seed: CH3-[CH2]10-CH=CH-[CH2]4-COOH, i.e. cis-6-octadecanoic acid], tannins 0; hairs rarely glandular; lamina vernation conduplicate; ovule with endothelium.
Age. Naumann et al. (2013) suggested an age of a mere 33.9 Ma or so for this node; (115.8-)103.1(-90.2) Ma, three times as old, is the estimate in Nicolas and Plunkett (2014), while Magallón et al. (2015), at around 70.5 Ma, are close to splitting the difference; ca 80.8 Ma is the estimate in Tank et al. (2015: Table S2).
GRISELINIACEAE A. Cunningham - Back to Apiales
Trees or shrubs (climbing, epiphytic); griselinoside [iridoid] +, polyacteylenes?; vessel elements often >1,000 µm long; petiole bundles (incurved) arcuate; mucilage cells +; stomata cyclocytic; hairs unicellular; leaves often two-ranked, lamina margins with distant and strong spines to entire, petiole base (not encircling stem), adaxial flange +; hypaanthium +; K open, small; staminnate flowers: A dorsifixed; pollen tectum striate; pistilode obscure; carpelate flowers: (C 0); staminodes 0 (+); G [(4)], transseptal bundles +, (2 carpels fertile); ovule?, funicular obturator +; fruit ± baccate; testa ?many layered, outer two (and esp. third) layers with thickened walls; embryo long; n = 18, x = ?
1 [list]/6. New Zealand and S. South America. Map: from Dillon and Muñoz-Schick (1993). Photo: Inflorescence, Leaves, Habit, Flower (scroll to end).
Age. Crown-group Griseliniaceae are around 12.1 Ma (Nicolas & Plunkett 2014; see also Dillon 2018).
Evolution: Divergence & Distribution. For the various interpretations of the disjunct austral distribution of the family, see Nicolas and Plunkett (2014) and Dillon (2018). Given the relative youth of the crown group, bird-assisted movement from Australia/New Zealand to South America seems most plausible, however, Wallis and Jorge (2018) emphasizing stem ages (perhaps over 100 My: see above) and categorizing its origin as "archaic", include Griselinia among the very oldest members of the New Zealand biota.
Chemistry, Morphology, etc..For fatty acids in the seeds, see Badami and Patil (1981). The wood has solitary vessels and apotracheal parenchyma (Baas et al. 2000).
For general information, see Philipson (1977), Dillon and Muñoz-Schick (1993) and Dillon (2018), for leaf insertion, c.f. Philipson (1967), and for leaf base, c.f. Takhtajan (1997); Takhtajan (2000) provides details of embryo and testa, for flowers, see Eyde (1964), for pollen, see Ferguson (1977), and for the ovule, see Warming (1913).
Previous Relationships. Eyde (1964) suggested relationships of Griselinia to Garrya (Garryales) and Cornaceae (Cornales); the genus was placed in a monogeneric order in Cornidae-Cornanae by Takhtajan (1997).
[Pittosporaceae [Araliaceae [Myodocarpaceae + Apiaceae]]]: plant often aromatic, ethereal oils, acetate-derived anthroquinones, coumarins mainly aliphatic polyacetylenes + [C17 falcarinone, etc.] +, iridoids 0, flavonols 0; lateral roots originating from either side of the xylem poles [there is a secretory canal at the pole]; vessel elements with simple perforation plates, clustered, septate fibres with minutely bordered pits, exclusively scanty paratracheal parenchyma; schizogenous secretory canals + [in cortex, pericycle, secondary phloem - and then with specialized axial parenchyma surrounding the canals - and in groups with sieve tubes], fibres 0; (nodes 3:3); petiole bundles arcuate or annular; flowers often hermaphroditic, protandrous; C tube formation early; pollen grains tricellular; G , both fertile, stigma wet; embryo (very) small; x = 12; RPB2 duplication.
Age. Suggested ages for this node are (110.2-)97.7(-85.1) Ma (Nicolas & Plunkett 2014), ca 76.4 Ma (Tank et al. 2015: Table S2), ca 63.4 Ma (Magallón et al. 2015), (52-)48, 46(-42) Ma (Wikström et al. 2001), (55-)42, 41(-33) Ma (Bell et al. 2010), (64-)49(-41) Ma (Wikström et al. 2015) and (75.5-)63.4(-52.4) Ma (Maurin 2020).
Evolution: Divergence & Distribution. Diversification rates may have increased both here (70.5-)66.3(- 63.4) Ma and also at the next node up ca 7 Ma later (Magallón et al. 2018).
Australasia seems the most likely place of origin of the whole clade, and of these four families in particular (Nicolas & Plunkett 2014).
There are a number of characters that may delimit clades of various sizes here. These include the presence of sesquiterpene lactones and benzylisoquinoline alkaloids and the presence of crystal sand; see Jay (1969) for suggestions based on plant chemistry that members of this group are related. Lateral roots originate from either side of the xylem poles because a resin canal runs down the stem at the apex of the pole as was noticed some time ago by van Tieghem and Douliot (1888).
Genes & Genomes. There may have been a genome duplication here ca 76.6 Ma (Lanis et al. 2018); for the complex history of the RPB2 gene (DNA-dependent RNA polymerase) duplications, see Nicolas and Plunkett (2013). Chromosome numbers and evolution are discussed by Yi et al. (2004).
Chemistry, Morphology, etc.. Triterpenoid ethereal oils produce the distinctive odour characteristic of many of these plants. Triterpenoid saponins like oleanene are found throughout the group, and also elsewhere (Wang et al. 2012). Stuhlfauth et al. (1985) discuss the distribution of various fatty acids in this clade (and in groups that used to be thought to be related to it).
The vessel:ray pits are bordered (Baas et al. 2000). Leaf teeth have a broad glandular apex with a main and two accessory veins, or one vein proceeds above the tooth; a survey of tooth morphology might be interesting.
Some Pittosporaceae and a few Araliaceae have basally connate petals (Plunkett 2001) and early corolla tube formation while in the corolla of at least some Apiaceae are the petals are separate even at their initiation (Erbar & Leins 2004c). For information on ventral carpel bundles, see Philipson (1970) and Eyde and Tseng (1971); when the united ventral bundles are opposite the carpels, the two bundles come from the same carpel, and when they are in the septal radii, the two bundles come from adjacent carpels. For ovule morphology, see Jurica (1922) and van Tieghem (1898); according to the latter, Apiaceae have a thick integument (e.g. ca 7 cells - Gupta 1970), that of Hedera is very thick, although Philipson (1977) described the integument of Araliaceae as being "thin". Some Pittosporaceae have laterally compressed fruits (M. Liu et al. 2016), so where this character should be placed on the tree is unclear; it is currently at the next node up.
Previous relationships. Pittosporaceae were included in Rosales by Cronquist (1981) and Mabberley (1997). Takhtajan (1997) included Pittosporaceae as a separate order in his Aralianae (but along with Byblidales). However, evidence had been mounting for over 100 years that they were best associated with Apiaceae/Araliaceae (Hegnauer 1969b for a summary of some literature). Thus van Tieghem initially thought Pittosporaceae might be near Violaceae, but later (van Tieghem 1898b) he placed Pittosporaceae, Apiaceae and Araliaceae together in his Ombellinées-Ombellales, the three being united by their secretory canals (see also Evolution above).
PITTOSPORACEAE R. Brown, nom. cons. - Back to Apiales
Trees, shrubs, or twining vines/lianes; furanocoumarins, (hydroxycoumarins), non-hydrolysable tannins +, petroselinic acid 0, C18 [oleic/linoleic], C20, C22 fatty acids abundant; young stem with (± interrupted - Pittosporum) vascular cylinder; cork cambiun (mid cortical); nodes 1:3, 3:3; petiole bundles arcuate; stomata paracytic; hairs uniseriate, terminal cells distinct, vertically or transversely [T-shaped hair] elongated or glandular; lamina vernation supervolute-curved, margins entire, secondary veins pinnate, leaf base narrow to sheathing; (plant dioecious); flowers medium-sized [ca 10 mm long/across], (monosymmetric by the androecium - Cheiranthera); K quite large, free (± connate), C often clawed, often slightly basally connate, 3-5-veined [?basal taxa], imbricate; anthers ± basifixed, placentoid +; tapetal cells multinucleate; (pollen bicellular); nectary on flank of ovary; G superior, [(-5)], placentation parietal (basal/axile)), style undivided, straight, stigma capitate (lobed), wet; ovules many/carpel, anacampylotropous (apotropous), integument 8-20 cells across, (incompletely tenuinucellate), endothelium 0, obturator +, hairy, vascular bundle terminates in upper part of the funicle; fruit a loculicidal (+ septicidal) capsule/berry (woody, K deciduous; seeds with sticky pulp derived from secretions of placental hairs [?level]; testa (multiplicative), 3 or more layers persisting, exotestal cells ± thickened, little differentiated, unlignified; x = 12, nuclear genome [1C] (0.064-)1.322(-27.378) pg.
6-9 [list]/200: Pittosporum (140). Old World, especially Australia, tropical and warm temperate, outside the immediate Australian region, mainly Pittosporum (map: from van Steenis & van Balgooy 1966; Good 1974; Coates Palgrave 2002; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photo - Flower.]
Age. The appproximate age for this node ([Sollya + Pittosporum]) is (17-)14, 13(-10) Ma (Wikström et al. 2001), (20-)12, 11(-5) Ma (Bell et al. 2010), or around 19.2 Ma (Nicolas & Plunkett 2014: ?sampling).
Evolution: Divergence & Distribution. Many of the apparently plesiomorphic characters of Pittosporaceae, e.g. superior ovary with several ovules, etc., are likely to be derived (see above.
Chemistry, Morphology, etc.. Glucosinolates are reported from Bursaria spinosa, but this is probably a mistake (Fahey et al. 2001).
In Pittosporum, at least, the flowers are often functionally unisexual. There is a tendency, especially evident in taxa like Cheiranthera, for the flowers to be obliquely monosymmetric, and this is largely because of the position of the stamens and gynoecium. In Pittosporum floribundum, ovules are epi- and apotropous within a single ovary (Narayana & Sundari 1983). Mauritzon (1939a) drew attention to the fact that the funicular bundle appears to expand and end in the upper part of the funicle, rather than in the chalazal region. This may be connected with how the embryo sac curves; I have not looked for this feature in other Apiales. Seedlings of Pittosporum have up to five cotyledons, and seedling leaves may be pinnatifid.
For general information, see Carolin and Bittrich (2018), for seed oils, see Stuhlfauth et al. (1985), for vegetative anatomy, see Wilkinson (1992, 1998), for embryology, see Narayana and Sundari (1983) and references, for endothelium in particular, see Batygina et al. (1985) and for testa anatomy, see Takhtajan (2000).
Phylogeny. See L. W. Cayzer (references in Chandler et al. 2007) for phylogenetic analyses of parts of Pittosporaceae, and these are largely similar to a preliminary molecular study (Chandler et al., in Plunkett et al. 2004c) : [Pittosporum, [Auranticarpa, Bursaria, Rhytidispermum], the rest]. For relationships between species of Pittosporum found in the Pacific, see Gemmill et al. (2002).
Classification. Cayzer (references in Chandler et al. 2007) suggested a number of changes in taxon limits, largely confirmed by Chandler et al. (see Plunkett et al. 2004c). However, generic limits in the Billardiera-Sollya area are still unclear (Chandler et al. 2007), although Cayzer et al. (2004) had redrawn generic boundaries there.
[Araliaceae [Myodocarpaceae + Apiaceae]]: young stem with separate bundles; outer cortical collenchya +, forming a continuous layer; axillary bud vascular tissue derived from several leaf gaps [?level]; leaves compound, lamina margins toothed or otherwise incised; inflorescences terminal, ultimate units umbels; (plants andrmonoecious), (interfloral protogyny); K open, usu. much reduced, C valvate, inflexed, with apical thickening; A inflexed in bud; nectary continuous with ± swollen style base [stylopodium], divided, ventral carpel bundles are fused bundles of adjacent placentae; ovules two/carpel, one descending, the other ascending, aborting, epitropous; fruit dry, schizocarpic, ± laterally flattened, (winged, wings with mesocarp and endocarp, vascular bundles at the margin of wing), caropophore +, undivided, rib oil ducts +, vittae +, branched, calcium oxalate rhomboidal crystals +, endocarp sclerified; exotestal cells (tangentially elongated), tanniniferous [?level]; hemicellulosic seed reserves common; 92 bp deletion in rpl16 gene.
Age. The age of this node is estimated as (48-)38, 35(-25) Ma (Bell et al. 2010), while Wikström et al. (2001) thought that it was (49-)45, 41(-37) Ma and Wikström et al. (2015) (61-)43(-30) My; Xue et al. (2012) put it at (43.6-)41.1(-40.4) Ma, Magallón et al. (2015) at ca 60.2 Ma, Vandelook et al. (2012b) at ca 73.5 Ma, Tank et al. (2015: Table S1, S2) at about 76.5/74.9 Ma and Maurin (2020) at (68.6-)57.4(-47.2) Ma. A much older age of (106.6-)94.6(-82.6) Ma was suggested by Nicolas and Plunkett (2014).
Evolution: Divergence & Distribution. Members of both Araliaceae and Apiaceae in clades that are sister to the rest of those families have simple leaves, as have some Myodocarpaceae (Plunkett 2001) and of course all Pittosporaceae, so compound leaves may have evolved more than once and further up in this clade. Of fatty acids in the seeds, C18 tariric acid is absent although petroselinic acid is common, and there are only small amounts of C20 and C22 fatty acids (Stuhlfauth et al. 1985).
Pollination Biology & Seed Dispersal. For the evolution of andromonoecy in this clade, see Schlessmann et al. (2001; see also Schlessman 2010, 2011). It is rare elsewhere in flowering plants and its evolution here is perhaps connected with dichogamy, successively flowering umbels (all umbelluless of a compound umbel may flower at the same time, or they may flower in waves), and umbels as functional units in pollination. Interfloral dichogamy is common in the clade; perfect flowers in Araliaceae are protandrous, as might be expected, and all flowers of a compound umbel can be at the same stage, indeed, the male and female phases may be synchronized across the whole plant. Nevertheless, about 40% of the records for Apiaceae are for protogyny (Bertin & Newman 1993; Schlessmann 2010).
Plant-Animal Interactions. Ehrlich and Raven (1964) noted that some butterfly larvae that do not seem to like Araliaceae, including Hydrocotyle, are nevertheless found on Apiaceae (?including Saniculoideae). Thus the Papilio machaon group is not found on Araliaceae, probably because that family lacks the furanocoumarins that the caterpillars like (Berenbaum 1983).
Genes & Genomes. For a deletion in the rpl16 gene of the chondrome, see Downie et al. (2000a).
Chemistry, Morphology, etc.. Kleiman and Spencer (1982) surveyed Apiaceae and Araliaceae for the occurrence of petroselinic acid (see also Stuhlfauth et al. 1985). For similarities in wood anatomy between Apiaceae and Araliaceae, see Metcalfe and Chalk (1983); for bark anatomy, see Kotina et al. (2011: crystal types and distributions not integrated into the phylogeny); for wood and stem anatomy, see Rodriguez C. (1957) and Oskolski (2001), for young stem and petiole anatomy, see Mittal (1961), for the sequence of initiation of parts of the flower, see Erbar and Leins (1985: mostly Apiaceae, also Hydrocotyle); and for nectaries, see Erbar and Leins (2010).
Mention of the fruits being dorsi-ventrally or laterally compressed refers to the shape of the contents of individual seeds in transverse section of the mericarp. Individual mericarps can appear to be dorsi-ventrally flattened if they have lateral wings, while two non-flattened mericarps that have not separated can appear to be laterally flattened. For fruit wings and fruit anatomy, see M. Liu et al. (2006); for general fruit anatomy, with complex distribution patterns of characters, see Baumann (1946) and Liu et al. (2016), for the anatomy of the fruit wing, see Magee et al. (2010a). There is variation both in the kinds of calcium oxalate crystals that are found in the fruit wall, i.e., single rhomboidal crystals or druses, and also where they occur, e.g. in the endocarp or mesocarp, or all around the fruit or only in commissural area (Liu et al. 2006; see also Rompel 1895; Burtt 1991a). See Kljuykov et al. (2004) for terms used here, especially in Apiaceae.
Phylogeny. The old woody Araliaceae/herbaceous Apiaceae distinction is no longer tenable, and recent rearrangements have considerable implications for character evolution (c.f. Valcárcel et al. 2014 in part). Myodocarpaceae and some clades in Apiaceae as circumscribed here include genera that used to be in Araliaceae, although the precise relationships of Apiaceae-Myodocarpeae in particular have been uncertain - see Plunkett and Lowry (2001), Lowry et al. (2001), Plunkett (2001) and Chandler and Plunkett (2004) for more information. Some genera in Apiaceae-Mackinlayoideae below used to be in Araliaceae-Mackinlayeae, others in Apiaceae-Hydrocotyloideae. Ex-Araliaceous genera to be included here include Apiopetalum, Mackinlaya, Micropleura and Xanthosia. Melikian and Konstantinova (2006) thought that the gynoecial structure of Actinotus was so different from that of other Apiaceae that the genus deserved to be placed in its own family, which they duly did, however, it is to be included in Mackinlayoideae (Nicolas & Plunkett 2009). There are indeed a number of morphological similarities between the Mackinlaya clade and Apiaceae s. str. and molecular data also link the two (Chandler & Plunkett 2002, 2004), so Mackinlayeae are included in Apiaceae. Nodes along the backbone of this part of the apiaceous tree have rather moderate support (e.g. Nicolas & Plunkett 2009), yet very few genera remain to be sequenced; it will be interesting to see what story nuclear genes will tell.
The old Apiaceae-Hydrocotyloideae (see below), herbaceous and with simple leaves, are hopelessly polyphyletic, and their members now occur in several quite separate clades of which most at least remain in Apiaceae (Nicolas & Plunkett 2009). However, the large genus Hydrocotyle itself is in Araliaceae, a position that makes morphological sense, and although sampling of both it and the related Trachymene must be improved, this is unlikely to affect their position. Arctopus is now in Apiaceae-Saniculoideae; Azorella and a group of genera form a well supported Apiaceae-Azorelloideae, and Centella, Micropleura, Actinotus, etc., are in Apiaceae-Mackinlayoideae, although Centella in particular is superficially very similar to Hydrocotyle (e.g. Downie et al. 1998, Downie et al. 2000; Chandler & Plunkett 2003, 2004; Plunkett et al. 2004; Andersson et al. 2006; esp. Nicolas & Plunkett 2009).
For other work on phylogenetic relationships in the Apiaceae-Araliaceae area, see e.g. Judd et al. (1994), Oskolski et al. (1997), Oskolski & Lowry (2000), Plunkett (1998), Plunkett et al. (1996, 1997a, 1997b), and Kårehed (2002c).
ARALIACEAE Jussieu, nom. cons. - Back to Apiales
Hydroxycoumarins +, furanocoumarins 0; (vessel elements with scalariform perforation plates); fibres septate (not); axial parenchyma paratracheal; rays heterocellular; vascular bundles in pith, usu. inverted; stomata para- or aniso-(anomo-)cytic; stipules +; stigma punctate (dry); (nucellar cap +), (endothelium +), obturator +, as short unicellular funicular hairs; mesocarp thick-walled, lignified; testa ± collapsed, exotestal cell walls a little thickened; x = 8, nuclear genome [1 C] (0.057-)1.25(-27.505) pg.
43 [list: subfamilies]/1450 - three groups below. Largely tropical, few temperate (map: see Meusel et al. 1978; Hultén & Fries 1986; FloraBase 2006; Trop. Afr. Fl. Pl. Ecol. Distr. 6. 2011).
Age. The age of crown Araliaceae is estimated to be (100-)80(-70) Ma (Mitchell et al. 2012); Beaulieu et al. (2013a: 95% HPD) suggested an age of (48-)44(-41) Ma and an age of (83.2-)65(-48.7) Ma has also been mentioned (Nicolas & Plunkett 2014).
1. Hydrocotyloideae Link
± Herbaceous, perennial; nodes 3:3 [Hydrocotyle]; (hairs glandular - Trachymene); lamina orbicular-peltate (± palmately compound), margin crenate, stipules cauline or petiolar; (inflorescences axillary); (K 0 - Hydrocotyle); ovule with "short" funicle, integument ca 5 cells across, parietal tissue 0; carpophore +, undivided/0; n = ³6 [9, esp. 12 - Hydrocotyle, 11 - Trachymene.
4/175: Hydrocotyle (130), Trachymene (45). Tropical, including montane, also warm temperate.
Age. The age of crown Hydrocotyloideae has been estimated at ca 51.4 Ma (Nicolas & Plunkett 2014).
Synonymy: Hydrocotylaceae Berchtold & J. Presl
[Harmsiopanax + Aralioideae]: ?
Age. The age of this clade is around 57.7 Ma (Nicolas & Plunkett 2014) or some 90 Ma (R. Li & Wen 2016; Zuo et al. 2017).
2. Harmsiopanax Harms (if here)
(Plant monocarpic); (spiny); ventral carpel bundles are fused bundles of the one placenta.
3. Aralioideae Eaton
(Herbs), shrubs to trees (climbers by roots/stem twiners/grappling with prickles); nodes >7:>7; (palisade mesophyll with arm cells); (prickles + - origin various); petiole with ectophloic outer ring and usu endophloic inner ring of budles; (hairs stellate, dendroid, lepidote); leaves usu. pinnately to (peltately-)palmately compound, (vernation ± conduplicate-plicate), stipules connate, intrapetiolar, hooded/2, cauline/0; (inflorescences [sub]racemose); pedicels articulated or not; C (± connate to calyptrate), (imbricate - Aralia, Panax, etc.); (A many), (filaments with two traces); tapetal cells 1-nucleate [by fusion]-multinucleate, nectary not divided; G [3<] [(1-5-200+)], when 5, opposite C, when 3, median abaxial, (style with several vascular bundles); integument 10-19 cells across, parietal tissue (0) 1-4 cells across, funicular obturator +/0, hypostase +/0; fruit a drupe, as many pyrenes as carpels, (berry), (dry, schizocarpic), (mesocarp sclereids +), (druses +); testa (multiplicative); (seed ruminate); x = ³11.
41/1,275: Sciodaphyllum* (131, eventually ca ?335), Polyscias (115), Oreopanax (80), Dendropanax (95), Aralia (68), Osmoxylon (60), Didymopanax* (37), Crepinella* (* = ex Schefflera). Largely tropical, few temperate. [Photo - Flowers, Fruits.]
Age. For the clade [Gastonia + Hedera] an age of around 85 Ma or more can be inferred from Valcárcel et al. (2014), while ages of (100-)84(-70) Ma are suggested for the [Schefflera longipedicellata + The Rest] clade (Mitchell et al. 2012), ca 60.2 Ma for the Asian Palmate group, with Oplopanax sister to the rest (R. Li & Wen 2016), and ca 57.5 Ma for the clade [Aralia + Panax] (Li & Wen 2016) - but c.f. some ages for the family as a whole.
Leaves and fruits ca 40.4 Ma are attributed to this subfamily (Martínez-Millán 2010).
Synonymy: Hederaceae Giseke, Botryodendraceae J. Agardh
Evolution: Divergence & Distribution. Nicolas and Plunkett (2014) suggest some dates for nodes along the spine of the subfamily.
Major groupings within Aralioideae in particular show some geographical signal (see below), even if they do not map on to previous classifications. Mitchell et al. (2012, other Araliaceae, too; see also Wallis & Jorge 2018) give some dates in the Antipodean Greater Raukaua clade, which seems to be quite an ancient inhabitant of New Zealand, while Valcárcel et al. (2014) offer some dates in the Asian Palmate clade, and they depend on the marker used. Zuo et al. (2017) give ages for clades in Panax and discuss its biogeography.
For shifts in the rate of molecular evolution within Araliaceae that are correlated with changes in habit, see Smith and Donoghue (2008).
Basal Araliaceae may well be bicarpelate (see also Wen et al. 2001) and have simple leaves, as in the herbaceous Hydrocotyloideae; more needs to be known about that subfamily and other relatively small and putatively basal clades to understand evolution in the family as a whole. In terms of diversification, given than Schefflera (in the old sense, see Frodin et al. 2010) contained ca 620 spp, but it is being divided into five or so genera with a total (including undescribed species) of around 1,600 spp, it is difficult to say much.
Ecology & Physiology. For the biomechanics of how Hedera helix attaches to trees and climbs, see Melzer et al. (2012) and Rowe and Speck (2015).
Pollination Biology & Seed Dispersal. Little seems to be known about pollination of the morphologically unspecialized flowers of Araliaceae. Ollerton et al. (2007) noted that flowers of Hedera helix, for example, were visited by a variety of insects, but they were in fact functionally quite specialized, Vespula wasps being the main pollinator. There is commonly quite a range of different visitors to the flowers (Plunkett et al. 2018b).
Although not much in is known about fruit dispersal in the family, in the New World the nutritious fruits are important food sources for frugivorous birds while in northern Europe Hedera fruits are fed to nestling birds that otherwise eat animal material (Snow 1981).
In Osmoxylon (inc. Boerlagiodendron) inflorescence development is somewhat protracted. The first heads to develop heads produce false (= infertile) fruits that attract frugivorous birds that also pollinate the flowers, and these birds later visit the infructescences, eat the true fruits that have been produced, and disperse the seeds (Roitman et al. 1997 for some references). Schlessman (1991) found that smaller plants of Panax trifolius produced staminate flowers, inflorescences with perfect flowers appearing when the plants became larger (see also Arisaema-Araceae). For andromonoecy, see above.
Genes & Genomes. Hydrocotyloideae, almost alone in the family, can be highly polyploid (Pimenov et al. 2003), although tetraploidy elsewhere is not uncommon. For chromosome numbers and chromosome evolution, see Yi et al. (2004); there are suggestions that x = 12 for Araliaceae (Raven 1975; see also K. Kim et al. 2017) - but c.f. Carta et al. (2020).
Chemistry, Morphology, etc.. Hedera may have an interrupted fibrous pericyclic sheath; creeping forms have two-ranked leaves. As to stipules: Fatsia (no stipules) x Hedera (no stipules) = XFatshedera (stipules), but some species of Hedera do have a hollowed leaf base with a flanged margin that encloses the axillary bud. Variation in basic leaf construction is considerable, and leaves may be peltate (Hydrocoyle) to peltately palmate (see Kim et al. 2003), to bundle compound, with leaflets arranged like flowers in an umbel, as in some species of Agalma and Heptapleurum, ex-Schefflera (Grushvitzky & Skvortsova 1970; Plunkett et al. 2020).
Araliaceae show considerable floral variation, and this is reflected in their floral vasculature. The calyx may be entirely absent (e.g. Hydrocotyle: Tseng 1967), not even reduced vascular traces suggesting that it was ever there, the petals may have three traces and may be slightly to completely connate (Osmoxylon has basally connate petals), and the stamens sometimes have two traces (Nuraliev et al. 2010, 2011). Both Aralioideae and Hydrocotyle show early corolla tube initiation (Leins & Erbar 1997; Erbar & Leins 2004). Tetraplasandra gymnocarpa and T. kavaiensis have secondarily more or less completely superior ovaries (Costello & Motley 2000, 2001, 2004 - see photograph on the cover of American J. Bot. 91(6). 2004).
Variation in merosity is particularly striking in Aralioideae, and flowers are up to 12-merous or more there (Viguier 1906). Some species have about as many stamens as carpels; separate members of the calyx cannot be distinguished (the calyx forms a low, entire rim (Nuraliev et al. 2014); the petals may be connate and form a calyptra; and although the symplicate zone of the gynoecium develops first, the carpels are largely synascidiate, and there is a large, flat remnant of the floral axis within the carpel whorl (Sokoloff et al. 2007b). Tupidanthus calyptratus (= Asian Schefflera) has up to 172 stamens and 132 carpels; the carpels are initiated in a single elongated and sometimes contorted whorl looking rather like a brain cactus (fasciation: Oskolski et al. 2005; Nuraliev et al. 2009, 2014; see also Eyde & Tseng 1971). Plerandra has up to 25 or more carpels and to 500 stamens, while in other species there are up to five series of stamens initiated centripetally, the vasculature of members of each whorl being connected radially (very unusual in the gentianids); carpel number is 14 or fewer (Philipson 1970; Oskolski et al. 2010c; Plunkett et al. 2020). A few species of Polyscias subg. Arthrophyllum have unicarpelate gynoecia (and five stamens), but there is no evidence that they represent reduced bi-(or more-)carpelate gynoecia, unlike the single carpels of some Apiaceae-Apioideae (Karpunina et al. 2016), and there is also extensive variation in carpel arrangement (Sokoloff et al. 2017 and references). Nuraliev et al. (2019) outline the variety of symmetry types in the family, largely the result of the variation just mentioned, and these are well illustrated. For further discussion, see the euasterid clade.
For general information, see Philipson (1970) and Plunkett et al. (2018b), for general anatomy, see Viguier (1906) and Mittal (1981), for that of the leaf, see de Villiers et al. (2010), for bark, see Kotina & Oskolski (2010), for wood, see Oskolski (1996) and Kotina et al. 2013 and references, for gynoecial development in Seemannaralia, see Oskolski et al. (2010b), for embryology, see Ducamp (1902), Gopinath (1944) and Mohana Rao (1973b), and for fruit anatomy, see Konstaninova and Suchorukow (2010). For Hydrocotyle, see Leins and Erbar (2010), flowers, Cerceau-Larrival (1980) and Shu and She (2001: Chinese spp.), both pollen, and Håkansson (1923), ovules.
Phylogeny. Relationships between Apiaceae and Araliaceae, in particular the positions of Hydrocotyle, ex-Apiaceae, and Mackinlaya and relatives, ex-Araliaceae, are discussed above. In general, relationships with Araliaceae have presented problems (S. A. Smith et al. 2013).
Hydrocotyloideae (ex Apiaceae) are sister to the rest of the family (Chandler & Plunkett 2004; Plunkett et al. 2004a; Nicolas & Plunkett 2009). The S.W. Australian genera Neosciadium and probably Homalosciadium also belong to Hydrocotyloideae (Andersson et al. 2006). Hydrocotyle has laterally flattened fruits with a sclerified (= woody) endocarp and stipules that are either cauline or are borne on the leaf base - and it also has trilacunar nodes (Sinnott & Bailey 1914). Trachymene, perhaps to include Uldinia, is also in Hydrocotyloideae; morphologically it is rather similar to them, and although there is a carpophore in the fruit, it is undivided. For a phylogeny of Trachymene, see Henwood et al. (2010).
Astrotricha and Osmoxylon may be part of a polytomy at the node immediately above Hydrocotyloideae (see also Lee et al. 2008; Zuo et al. 2017), while the position of Harmsiopanax, which has fruits that are schizocarpic like those of Hydrocotyloideae, is also uncertain (Nicolas & Plunkett 2009).
For more details on the phylogeny of Aralioideae in particular, see Henwood and Hart (2001) and especially Wen et al. (2001), Plunkett et al. (2004a, c), Lowry et al. (2004) and Z.-D. Chen et al. (2016: Chinese taxa). Schefflera, with perhaps 1,600 species under 2/5 of which have been described (Frodin et al. 2010), is in fact highly polyphyletic, and five major clades have become apparent in it - of which Schefflera s. str. is the smallest. These are circumscribed geographically and some also have morphological support. African plus Madagascan taxa form a clade, as do the some 250-300 neotropical species, the Asian species (the last two clades are close on the tree), and two groups of species restricted to the Pacific, the small Schefflera s. str. and the much larger Melanesian clades (Plunkett et al. 2005: general, 2009, 2010, 2020: extensive, inc. summary of some foliar and floral variation; Plunkett & Lowry 2012: Melanesian clade; Fiaschi & Plunkett 2011; Gostel et al. 2009: Africa-Madagascan; R. Li & Wen 2014: Asian; Z.-D. Chen et al. 2016: China). The Neotropical = Sciodaphyllum group has recently been monographed (Lowry et al. 2019a), and Crepinella, most species of which are from the Guyana shield, belongs here (Lowry et al. 2019b). Didymopanax, largely Brazilian, is also part of this complex and has recently been resurrected (Fiaschi et al. 2020), and there is palynological support for this (Fiaschi et al. 2009).
The Schefflera problem aside, there are four major clades in Aralioideae, the largely South East Asian Palmate and Aralia-Panax groups (e.g. R. Li & Wen 2015, Zuo et al. 2017; K. Kim et al. 2017 for relationships), the Pacific and Indian Ocean basin Greater Raukaua group (Mitchell et al. 2012), and the Polyscias-Pseudopanax group (Wen et al. 2001; Mitchell & Wen 2004; Plunkett et al. 2004a; Valcárcel et al. 2014 for a summary). Within the Palmate group, which includes Hedera, relationships are rather poorly resolved, and details depend on the markers used - polyploidy and ancient hybridization may be involved - and the position of Osmoxylon seems particularly uncertain (Yi et al. 2004; Mitchell & Wen 2004; Valcárcel et al. 2014). For relationships in Panax, see Zuo et al. (2017: P. bipinnatifidus to be dismembered?). Lee et al. (2008) focussed on relationships of Malesian Araliaceae; Osmoxylon was isolated. Most (?all) Dendropanax are likely to be monophyletic, with two large clades restricted to the Old and New Worlds (Li & Wen 2013).
Classification. For a now dated checklist of the family, see Frodin and Govaerts (2003). Generic limits in Aralioideae need much attention; see Plunkett et al. (2004a) for genera, but many more changes will be needed. In part the clades into which species of the old Schefflera have been placed map on to earlier infrageneric groupings recognised by David Frodin and have names at the generic level, which are being taken up (Plunkett et al. 2020 gives an outline). Thus the Pacific clade of Schefflera is to be called Plerandra (Lowry et al. 2013, q.v. for infrageneric classification), and for the Afro-Malagasy ex Schefflera, see Lowry et al. (2017: Astropanax, Neocussonia). Polyscias has been substantially enlarged (Lowry & Plunkett 2010, subgenera here, too).
[Myodocarpaceae + Apiaceae]: furanocoumarins +.
Age. Ages for this node of (42-)32, 29(-20) Ma (Bell et al. 2010), (42-)38, 33(-29) Ma (Wikström et al. 2001), ca 58 Ma (Magallón et al. 2015), and much older, (103.2-)91.3(-78.6) Ma (Nicolas & Plunkett 2014), have been suggested. Tank et al. (2015: Table S1, S2) estimated it to be around 59.1 (?mistake) and 59.1 Ma respectively.
MYODOCARPACEAE Doweld - Back to Apiales
Trees; (sclereids in phelloderm); (vessel elements with scalariform perforation plates, numerous thin bars - Delarbrea); fibres non-septate; libriform fibres with very thick walls; axial parenchyma apotracheal (and paratracheal), diffuse-in-aggregates; rays homogeneous; leaves pinnately compound, leaflet margin entire (serrate), venation brochidodromous, base with adaxial or lateral flange; K valvate, C imbricate; G ?arrangement; nucellus?; fruit ventral carpel bundles various, mesocarp sclereids +, druses scattered in mesocarp, secretory vesicles in inner pericarp; x = 12.
2 [list]/17. New Caledonia, E. Malesia, and Queensland, Australia, Map: from van Balgooy (1993). [Photo - Habit.]
Age. Crown-group Myodocarpaceae are estimated to be (47.4-)25.4(-8) Ma (Nicolas & Plunkett 2014).
1. Delarbrea Vieillard
petiole with continuous ring of vascuklar tissue, secondary thickening +; C clawed, lacking inflexed apical thickening; fruits fleshy, endocarp thin, rib oil ducts 0; pyrenes dorsally compressed; testa thick, 2-layered; n =.
1/7. Most New Caledonia, also E. Malesia, and Queensland, Australia
2. Myodocarpus Bunge
petiole with ring and scattered medullary vascular bundles; leeaves (simple); C connate apically, calyptrate; fruit dry, winged basally, mericarps attached basally; n = .
1/10. New Caledonia.
Evolution: Divergence & Distribution. The age of Myodocarpaceae suggests that their presence on New Caledonia is due to long distance dispersal rather than vicariance (Nattier et al. 2017).
For some apomorphies, see Raquet (2004) and M. Liu et al. (2010).
Chemistry, Morphology, etc.. In wood anatomy Myodocarpus is perhaps more like Cornaceae than any other members of the Apiaceae-Araliaceae complex, but in other features it is more like Apiaceae (Rodrigues C. 1957).
Myodocarpus has a number of distinctive features of the flower and in particular its schizocarp (Baumann 1946; Konstantinova & Yembaturova 2010 for morphology, etc.) - the mericarps are beautiful little laterally-flattened samaras that at first sight are similar to those of Serjania (Sapindaceae)!
General information is taken from Plunkett et al. (2004c) and Lowry and Plunkett (2018) and also Lowry (1986: Delarbrea); for wood anatomy, see Oskolski (1996).
Previous Relationships. This group used to be included in Araliaceae as Myodocarpeae.
APIACEAE Lindley, nom. cons. // UMBELLIFERAE Jussieu, nom. cons. et nom. alt. - Back to Apiales
Pyranocoumarins, myricetin, mannitol +, umbelliferose [raffinose (trisaccharide) isomer] the storage carbohydrate; hydroxycoumarins, flavones 0; vessel elements aggregated; axial parenchyma scanty, paratracheal; (vascular bundles in cortex); stomata various; lamina vernation also supervolute; K a ring of teeth, (obsolete), C free [no early C tube formation], vein single, unbranched [?all]; G superposed, stigma usu. capitate; ovule (with -2 lateral layers of nucellar tissue), funicle "short"; fruit ventral carpel bundles two, on opposite sides of the commissural plane, mesocarp lignified, rhomboidal crystals of calcium oxalate in inner mesocarp; exotestal cells thin-walled; endosperm oily, with starch; x = 8, nuclear genome [1 C] (0106-)1.593(-23.888) pg.
446 [approx. list]/3,820 - four main groups below. World-wide, esp. N. temperate.
Age. Beaulieu et al. (2013a: 95% HPD) thought that crown-group diversification of Apiaceae began (66-)54(-43) Ma, however, (98.9-)87.4(-76) Ma, much older, is the age in Nicolas and Plunkett (2014), while at (71.2-)65.8(-60.9) Ma, Calviño et al. (2016) are in the middle.
Fruits (Carpites) from the late Cretaceous (Maastrichtian) of Wyoming and Montana, around 69 Ma, have been assigned to Apiaceae (Manchester & O'Leary 2010).
1. Mackinlayoideae Plunkett & Lowry
Herbs (annuals) to shrubs; (centellose [oligosaccharide] - Centella); (cork cambium subepidermal - Centella); (vessel elements with scalariform perforation plates); apotracheal (+ paratracheal) parenchyma; fibres non-septate; leaf ± pedately compound [Mackinlaya], ± palmate, to simple, (stipules +); (pedicel not articulated); (K petal-like); (nectary not divided/on style - Actinotus/spherical-stipitate - Xanthosia); nucellus?; (fruit drupaceous),usu. compressed laterally, carpophore 0; n = 5, 7, 9-12, etc..
10/98: Centella (45-50), Xanthosia (20), Actinotus (18). Southern Hemisphere, scattered, Centella esp. South Africa, C. asiatica pantropical (Map: from Trop. Afr. Fl. Pl. Ecol. Distr. 6. 2011; Australia's Virtual Herbarium i.2013; GBIF i.2013; van Wyk et al. 2013; green = mostly Centella asiatica).
Age. The age of crown-group Mackinlayoideae is estimated to be (83.6-)66.3(-50.2) Ma (Nicolas & Plunkett 2014) or (45.8-)36.8(-26.5) Ma (Calviño et al. 2016: genera examined?).
Synonymy: Actinotaceae Konstantinova & Melikian, Mackinlayaceae Doweld
[Platysace [Azorelloideae [Hermas [Saniculoideae + Apioideae]]]]: plant herbaceous; vessel elements with simple perforation plates; umbels compound; carpophore +, mericarps separating at maturity.
Age. The age of this node is estimated to be (94.8-)83.6(-72.9) Ma (Nicolas & Plunkett 2014).
Herbs to shrubs; (stem photosynthetic); leaves simple, (scale-like), blade linear to orbicular, entire (deeply trifid), base rather narrow; bracteoles usu. 3; K 0; fruit compressed laterally, carpophore entire to bifid; ?ventral carpel bundles; oil ducts in ribs obscure; cotyledons rounded, toothed; n = 8.
1(-2)/26. Australia, most in the southwest, not Tasmania. Map: from FloraBase (consulted viii.2009) and Australia's Virtual Herbarium (i.2013).
Age. Crown-group Platysace is around 18.4 Ma (Nicolas & Plunkett 2014).
[Azorelloideae [Hermas [Saniculoideae + Apioideae]]]: fruits dorsally compressed; mesocarp vittae irregular, anastomosing and/or branching.
Age. The age of this node may be (85.6-)75.8(-65.7) Ma (Nicolas & Plunkett 2014) or (72.6-)63.6(-55.4) Ma (Calviño et al. 2016).
2. Azorelloideae Plunkett & Lowry
Herbs (annuals) to small shrubs, often hummock-forming; ?petroselinic acid; (cork cambium deep-seated - Mulinum); (hairs stellate); leaves simple, trifid to palmately lobed, (± compound), stipules (+); C flat; nucellus "large", relatively persistent; megaspore mother cells 2-4, embryo sac tetrasporic, 16-nucleate [more than one embryo sac "type"]; fruit usu. compressed dorsally, with wings/ribs [made up of the entire fruit wall, including a vascular bundle], lateral ribs/wings largest, carpophore (0), entire (apically cleft, bifid), ventral bundles 0, 1, 2, lateral [commissural], (opposite), (druses +, in outer mesocarp - Azorella); n = 5, 8, x = 8.
17/155: Azorella (58). South American-Australian, Antarctic islands, esp. the Andes; Drusa glandulosa from the Canary Islands and Somalia, Dickinsia from China; probably not native in North America (map: from Mathias & Constance 1965; Martinez 1993; Fl. China 14: 2005; Australia's Virtual Herbarium i.2013). [Photo - Habit.]
Age. The age of this node - [Bowlesia et al. + The Rest] - is around 65.5 Ma (Nicolas & Plunkett 2014) or (68.9-)58.4(-49.3) Ma (Calviño et al. 2016).
[Hermas [Saniculoideae + Apioideae]]: stipules 0.
Age. The age of this node (assuming it exists) is some (80-)70.6(-62) Ma (Nicolas & Plunkett 2014) or (72.2-)63.1(-54.9) Ma (Calviño et al. 2016).
Woody perennials or shrublets; plant densely hairy; leaf blade simple, margin variable; umbels compo, bracts quite large; K large, C-like, persistent, C filiform; fruit compressed dorsally, with 2 ventral bundles, rib oil ducts small, carpophore entire; n = 7.
1/8. South Africa (map: from van Wyk et al. 2013).
[Saniculoideae + Apioideae]: lamina with pinnate venation [?level]; ovules lacking parietal tissue [incompletely so], nucellar cap +, funicle "long"; fruit wings with mesocarp only, vascular bundles at the base, (secondary [i.e. lateral] ribs +), mesocarp cells lignified, endocarp single cell layer thick, parenchymatous, calcium oxalate as druses scattered in mesocarp and around commissure, rhomboidal crystals 0; RPB2 duplication +.
Age. The age of this node has been estimated as ca 64.3 Ma (Vandelook et al. 2012b: "crown group of Apiaceae" (sic)), (74.3-)65.8(-58.2) Ma (Nicolas & Plunkett 2014), (72.2-)63.1(-54.9) Ma (Calviño et al. 2016) and (73.5-)56.6(-45.2) Ma (Wen et al. 2020).
3. Saniculoideae Burnett
Kaurene-type diterpenoids +; (cork cambium outer cortical); umbels simple; development of K, C, and A sequential; (nectary outside A); nectary separated from styles by narrow groove [stylopodium 0]; exocarp often with outgrowths, outer sclereidal fibre-like cells longitudinal, innermost (if present) transverse, ribs with large oil ducts/cavities; cotyledons rounded.
10/335 - three groups below. World-wide.
Age. Crown-group Saniculoideae are estimated to be around 60.7 Ma (Vandelook et al. 2012b: [Molopo [Stego....]]), 53.1 Ma (Nicolas & Plunkett 2014) or (76.1-)58(-46.8) Ma (Calviño et al. 2016).
4a. Phlyctidocarpeae Magee, Calviño, Liu, et al.
Annual herb; leaves tripinnately compound; ?infloresence; bracts foliaceous; fruits compressed dorsally, with stipitate obconical processes, ribs bifurcate, with two vascular bundles, ventral bundles 2, lateral [vallecular and commissural], carpophore 0, vittae vallecular and commissural; n = ?
1/1: Phlyctidocarpa flava. Namibia (map: from van Wyk et al. 2013).
[Steganotaenieae + Saniculeae]: ?
4b. Steganotaenieae C. I. Calviño & S. R. Downie
Subshrubs to trees, (deciduous); phelloderm with chambered crystalliferous cells; dilation of secondary phloem by expansion of axial parenchyma [not ray cells]; leaves at ends of shoots, palmately compound, appearing sfter flowering; fruits dorsally or laterally compressed, heteromericarpic, 2-3 winged [wings exo- and mesocarp alone], rib oil ducts forming cavities, ventral bundles 2, lateral [commissural], carpophores +, bifid, (mesocarp druses 0); n = ?11, 12
2/5. Tropical, S.W. Africa (Map: from van Wyk et al. 2013).
4c. Saniculeae Burnett
Plant ± herbaceous, (annual); rosmarinic acid + [caffeic acid ester], (cardenolides - Eryngium); root lacking hypodermis [?level: Eryngium]; leaves simple, often palmately lobed (palmately compound), lamina often broad, (amphistomatous), teeth with hairy or spiny tips; umbels simple (a capitulum - Eryngium), (compound - Astrantia, Arctopus), with ± petal-like inflorescence bracts (green); (flowers blue); K quite large; carpelate flowers: ± sessile; sessile; fruit barely dorsally or laterally flattened, scaly or spiny, (± smooth), (ribs with two vascular bundles), carpophore 0 (+, entire), or ventral bundles 2, opposite [carinal], (rib secretory ducts/cavities 0), (mesocarp druses 0); n = 5-11 etc. [esp. variable Eryngium], x = ?8.
8/333: Eryngium (250), Sanicula (41), Alepidea (27). World-wide. Map: see Meusel et al. (1978), Hultén & Fries (1986), Trop. Afr. Fl. Pl. Ecol. Distr. 6 (2011), Wörz (2011) Australia's Virtual Herbarium (consulted i.2013) and van Wyk et al. (2013).
Age. The crown-group age of this clade (Arctopus and Sanicula) is (57.8-)41.7(-27.5) Ma or (Astrantia + Sanicula) (40.4-)27.3(-16.3) Ma (Calviño et al. 2016).
Synonymy: Eryngiaceae Berchtold & J. Presl, Saniculaceae Berchtold & J. Presl
4. Apioideae Seemann
Flavones, methylated flavonoids, phenylpropenes +; cortical collenchyma often interrupted; leaves palmately compound; (outer flowers of umbel monosymmetric); tapetum multinucleate; integument 6-8 cells across, hypostase +, (postament +); ventral bundles 2, opposite [carinal], rib oil ducts small/0; seed reserves mannans [?level]; x = 11.
Ca 380/3,200 - six groups below. Worldwide, esp. N. Temperate.
Age. The age of crown-group Apioideae is some (71.6-)63.7(-56.1) Ma (Nicolas & Plunkett 2014) or (76.1-)58.4(-45.9) Ma (Calviño et al. 2016).
5A. Lichtensteinieae Magee, Calviño, Liu, et al.
Annual to perennial herbs to compact shrublets, (basal leaves appearing well before flowering); plant glabrous; K conspicuous or not; fruits dorsiventrally flattened or not, (heteromericarpic), (ventral bundles 0, 1), carpophore +, bifid/short, hygroscopic - Choritaenia/0, (endocarp woody, druses 0 - Choritaenia), rib oil ducts +/0, two vascular strands in each rib, (huge oil ducts/cavities in wings), (surrounded by concentric rings of cells); n = 11.
3/9: Lichtensteinia (7). South Africa, 1 sp. in the Namib desert.
Age. The age of crown-group Lichtensteinieae is about 39.6 Ma (Nicolas & Plunkett 2014).
[Annesorhizeae [Heteromorpheae + Euapioids]]: rib oil ducts 0 (small), carpophore free, bifid [mericarps attached at apex], vittae unbranched, vallecular vittae +; cotyledons (1), various.
Age. The age of this node is (65.3-)58.3(-52.2) Ma (Nicolas & Plunkett 2014) or (71.6-)54.5(-40.6) Ma (Calviño et al. 2016).
5B. Annesorhizeae Magee, Calviño, Liu, et al.
Herbs, roots ± fleshy; (plant woody); (fruits heteromericarpic), commissural vittae +, vascular bundles highly lignified; n = 11, 12.
6/41: Annesorhiza (22), Chamarea (11). Most South Africa, also Southern Europe (1 sp.) and North Africa, Canary Islands and Madeira (1 sp.) Map: from van Wyck et al. (2013).
Age. Crown-group Annesorhizeae are around 37.4 Ma (Nicolas & Plunkett 2014) or (78-)51.2(-42.8) Ma (Calviño et al. 2016).
[Heteromorpheae + Euapioids]: tanniniferous exotestal cells 0.
Age. The age of this node is about 63.4 Ma (Vandelook et al. 2012b) or 58.3 Ma (Nicolas & Plunkett 2014).
5C. Heteromorpheae M. F. Watson & Downie
Plants often shrubby (scrambler); (vessel walls with helical thickenings); fibres septate; (periderm cortical - Anginon), chloroplasts in phelloderm cells [het. pol.]); (secretory canals in single ring in cortex); (leaves undivided); (involucral bracts dentate); (K well developed); fruits (heteromericarpic), not or slightly dorsiventrally or laterally compressed, (vittae branching/anastomosing), carpophore bifid, (two vascular strands in each rib); n = 11, ?12.
12/27: Anginon (12). Africa (esp. the southwest) to the Yemen, Madagascar (Map: from Winter & van Wyk 1996; Allison & van Wyk 1997; Trop. Afr. Fl. Pl. Ecol. Distr. 6. 2011; van Wyk et al. 2013).
Age. Crown Heteromorpheae are around 60.7 Ma (Vandelook et al. 2012b), 35.5 Ma (Nicolas & Plunkett 2014) or ca 30 Ma (Calviño et al. 2016).
Euapioids: druses in fruit wall absent (present, on commissural side only).
Age. The age of this node is about (68-)51.4(-37.2) Ma (Calviño et al. 2016) or (58.7-)49.89-42.7) ma (Wen et al. 2020).
5D. Chamaesieae J. Zhou & F. D. Pu
Perennial herb; leaves pinnate; stylopodium divided, very broad; fruit 9-ribbed.
1/8. Himalayas and west China, high altitudes.
[Bupleureae + The Rest]: ?
Age. The age of this node is estimated to be ca 59.3 Ma (Vandelook et al. 2012b), (51.6-)44.5(-39.1) Ma (Banasiak et al. 2013), ca 51.5 Ma (Nicolas & Plunkett 2014) or (52.4-)44.9(-39.5) Ma (Wen et al. 2020).
5E. Bupleureae Sprengel
(Plant shrubby); vessel walls with helical thickenings; fibres septate; leaves simple, margins entire, (venation parallel); umbels and umbellules (sessile), with well-developed leafy inflorescence/floral bracts [= "bracts" + "bracteoles"]; K and C initiated simultaneously; pollen usu. rhomboidal; fruit not flattened, ?carpophore, vittae branching; cotyledons linear, single veined, glabrous; n = 7, 8.
1/195. Europe and North Africa, to the Canary Islands and East Asia, also N.W. North America and South Africa, both one species (Map: from Meusel et al. 1978; GBIF iv.2010; van Wyk et al. 2013).
Age. Crown-group Bupleureae are ca 37.4 Ma (Vandelook et al. 2012b: ?sampling).
Synonymy: Bupleuraceae Berchtold & J. Presl
Pleurospermeae + the rest
Age. this node is around (47.8-)41.2(-36.6) Ma (Wen et al. 2020). - Physospermopsis + [40.0-)33.19-27.4) Ma.
The Rest: (plant rarely shrub or little-branched small tree); sugar alcohol sorbitol + [?level]; (stipules intrapetiolar, hooded); K, C, A initiated in groups/from common primordia, or K initiated after C; K + [e.g. Hohenackeria] or 0, C (imbricate); fruit not or dorsiventrally flattened, carpophore bifid; (cotyledon 1); x = 11 [?level].
360/3045: Ferula (185), "Pimpinella" (180), Seseli (140), Heracleum (130), Angelica (120), Peucedanum s.l. (110), Lomatium (85), Chaerophyllum (65), Arracacia (55), Ferulago (50), Thapsia (45) (map: from Meusel et al. 1978; Hultén & Fries 1986; Trop. Afr. Fl. Pl. Ecol. Distr. 6. 2011; van Wyk et al. 2013).
Age. This clade may be ca 42.9 Ma (Nicolas & Plunkett 2014).
Synonymy: Ammiaceae Berchtold & J. Presl, Angelicaceae Martynov, Caucaulidaceae Berchtold & J. Presl, Coriandraceae Burnett, Daucaceae Martynov, Ferulaceae Saccardo, Imperatoriaceae Martynov, Lagoeciaceae Berchtold & J. Presl, Pastinacaceae Martynov, Pimpinellaceae Berchtold & J. Presl, Scandicaceae Berchtold & J. Presl, Selinaceae Berchtold & J. Presl, Sileraceae Berchtold & J. Presl, Smyrniaceae Burnett
Evolution: Divergence & Distribution. Manchester and O'Leary (2010) thought that fruits of the Late Cretaceous Carpites ulmiformis, 69-66 Ma, might be of a member of Apiaceae (Dioscoreaceae were less likely); these are not mentioned by Martínez-Millán (2010).
As relationships get sorted out, evolutionary and biogeographic studies become possible, but our understanding of the phylogeny of Apioideae in particular is still (2020) very imperfect. Nicolas and Plunkett (2014, q.v. for details) suggested an Australian origin for Apiaceae, with at least some scenarios suggesting an African origin for Apioideae and Saniculoideae. Calviño et al. (2016) also emphasized a southern connection for early-branching in Apiaceae, movement being largely by long distance dispersal. Indeed, a glance at the maps of the clades from Hermas to core apioids shows a concentration of taxa in southern Africa in particular, the three basal clades of Apioideae and the two basal clades in Saniculoideae being small and made up very largely of southern African genera. 49/50 species of Centella (Mackinlayoideae) are restricted to the Cape Floristic Region, South Africa (Linder 2003). Euapioids, the bulk of the family species-wise and overwhelmingly Eurasian, represent a radiation from this southern African Apiaceae (see also Banasiak et al. 2013; Nicolas & Plunkett 2014; Calviño et al. 2016), and the features of these basal clades will affect character optimisations (Calviño et al. 2006; Magee et al. 2010a for details). The Dc-α; genome duplication event, dated at 52-46 Ma (J. Wang et al. 2020), may be associated with the euapioid node.
A number of taxa in the small clades in basal Apiaceae are woody and have undivided leaves (see the characterisations above). Although these woody Apiaceae are quite common and Myodocarpaceae, sister to Apiaceae, are also woody, the ancestral habit for Apioideae, at least, is likely to be herbaceous (Calviño et al. 2006). Woodiness in Bupleurum is derived and has evolved several times (H.-C. Wang et al. 2013); the genus may have evolved in archipelagic early Caenozoic Europe, with much subsequent diversification in eastern Asia, although anywhere from Europe and North Africa to Eastern Asia may have been involved (Banasiak et al. 2013, q.v. for much more detail). Myrrhidendron, from Central America and Colombia, and a few other euapioids, are also woody. These include Daucus from the Cape Verde islands, Canaries, etc., woodiness having two origins, the plants being monocarpic or polycarpic (Frankiewicz et al. 2020, see also Banasiak et al. 2016). Two more woody genera, Monizia and Melanoselinum, the latter also known from fossils some 1.2 Ma, are endemic to the Madeira Islands and are derived from Daucus (Marques et al. 2020). Beaulieu et al. (2013b; see also Beaulieu & O'Meara 2018) found high rates of transition between the woody and herbaceous habits in Apiaceae.
Around 60 Apioideae have monocotylar seedlings, and there is also a cotyledonary tube (Kljuykov et al. 2020). These features are likely to be adaptations to the geophilous life stye, the adults of all such seedlings having tuber-like structures and growing in areas that have (had) Mediterranean climate - and monocotyly has evolved some seven times or so (Kljuykov et al. 2020).
Spalik et al. (2010) looked at wide disjunctions in Apioideae, providing dates for various nodes. Later Spalik et al. (2014) focused on biogeographic patterns in the largely aquatic Oenantheae where there seems to have been much dispersal from Eurasia to North America. Spalik et al. (2014) found that the Hawaiian "Peucedanum sandwicense" (a split from stem Oenanthe) may have arrived on Hawai'i around 17.2 Ma, so being another example of a clade older than the current islands. Lilaeopsis brasiliensis and L. mauritiana are very close, even though they are separated by the Atlantic Ocean and the African continent (Spalik et al. 2010).
M. Liu et al. (2016) mapped the evolution a number of characters of hair and fruit morphology in the Mackinlayoideae. Wojewódzka et al. (2019), looking at dispersal in Scandiceae where traxa have winged or spiny/hooked mericarps, could not recognize distinct dispersal syndromes and also found that homoplasy of the individual characters they examined was high, and their systematic value was low. Carpophores, chromosome numbers other than 8, and inflorescences that are not condensed (all in African taxa) could be plesiomorphic in Saniculoideae; simple umbels are apomorphic for Saniculeae, etc. (Magee et al. 2010a, q.v. for numerous character optimisations; see also Calviño et al. 2008a; Kadereit et al. 2008).
Ecology & Physiology. Seed dormancy decreases with increasing relative embryo length, and fast-germinating seeds are likely to be found in short-lived plants of open and dry conditions (Vandelook et al. 2012b; see also Kadereit et al. 2017 and references). Vandelook et al. (2012b) noted that these relationships did not hold for seeds incubated at low (50C) temperatures, and species with seeds that did germinate at such temperatures did not show a positive correlation between temperature and germination; they had to cope with winter and so germination in the summer or autumn would not be desirable. For the evolution of anti-freeze proteins in Daucus carota, see references in Sandve et al. (2008).
Apiaceae commonly have hollow stems, and then the nodes may be solid, together a combination that saves on material costs and yet maintains rigidity (Speck et al. 2003), however, little is know about the biomechanics of umbel stems and the distribution of hollow stems in the family.
Pollination Biology & Seed Dispersal. All the flowers in an umbel open more or less simultaneously. In a number of Saniculoideae and a few Hydrocotyloideae in particular the inflorescence bracts function as petals, the rest of the inflorescence being much reduced and the whole looking more or less like a simple flower (Froebe & Ulbrich 1978). In the umbels of a number of Apioideae, the marginal flowers are larger than the others, and their abaxial petals may be larger than the adaxial, so increasing the resemblance of the inflorescence to a polysymmetric flower. The dark flower in the centre of the umbel of taxa like Daucus carota may attract flies that pollinate the flowers (Westmoreland & Muntan 1996).
Although the flowers appear unspecialized, being potentially pollinated by a variety of pollinators, oligolectic pollinators may play a major role in pollination - in the case examined, the bee Andrena ziziae as a pollinator of Thaspium and in particular Zizia in the southeast U.S.A. (Lindsey 1984; Lindsey & Bell 1985). However, as with other such flowers - Asteraceae are a case in point - other bees (and a syrphid fly) were also effective pollinators, and pollinators varied with geography, too. Ollerton et al. (2007) emphasized that some insects like large bees did not visit Apiaceae, so they showed at least a degree of ecological specialization, and Olesen et al. (2007) emphasized that many of the large numbers of flower visitors of temperate Apiaceae visited only species of Apiaceae.
Many Apiaceae have hooks (animals) or wings (wind) on their fruits, and Platysace and some Mackinlayoideae in particular have myrmecochorous fruits (Lengyel et al. 2010). However, Wojewódzka et al. (2019) could not recognize distinct dispersal syndromes in Scandiceae. Dispersal by water has been invoked for some Apiaceae (Calviño et al. 2016 and references).
Plant-Animal Interactions. For general insect-umbellifer relationships, see Berenbaum (1990) and Sperling and Feeny (1995). Microlepidopteran larvae of the Elachistidae-Depressariinae are also common on Apiaceae, which they have colonized twice, although initially they may have been associated with rosids and they have also colonised some Asteraceae (Fetz 1994: host plants; Berenbaum & Zangerl 1998: chemistry of the [co]evolution of resistance; Berenbaum & Passoa 1999: phylogeny). In particular, both this and the next group are most diverse on Apioideae with angular furanocoumarins (the axes of the two elements are not in line), and these are the most toxic form of furanocoumarins (Berenbaum 2001). Furthermore, genera of Apioideae with angular furanocoumarins are more diverse than those with other kinds of fumarocoumarins (Berenbaum 2001), although I do not know how this correlation is holding in the context of new ideas of relationships.
Caterpillars of Papilionidae-Papilioninae-Papilionini butterflies are quite common (ca 13% of all records) on Apiaceae, perhaps shifting here at least twice from Aristolochiaceae via Rutaceae (Dethier 1954; Fordyce 2010; see also Berenbaum et al. 1996; Berenbaum & Feeney 2008; Simonsen et al. 2011; Condamine et al. 2012; Allio et al. 2020/2021). Interestingly, they are found on neither Pittosporaceae nor Araliaceae; Rutaceae (q.v.), on which they are commonly found, also have furanocoumarins (Berenbaum 2001). The caterpillars will not eat Hydrocotyle (here Araliaceae), many of the larvae of Papilio ajax tested absolutely refusing to eat it (see also Dethier 1941; Fraenkel 1959; Ehrlich & Raven 1967). Linear furanocoumarins (the axes of the furan ring and coumarin elements are aligned; the furan ring is a five-membered aromatic ring with four carbons and one oxygen) are often phototoxic but are tolerated by caterpillars that will not eat plants with the non-photoxic linear coumarins (Berenbaum & Feeney 1981). For more on swallowtails and Apiaceae, see papers in Scriber et al. (1995) and elsewhere in this site. For the trenching behaviour of herbivores on Apiaceae, see Dussourd (2016).
Agromyzid dipteran leaf miners have diversified on north temperate Apiaceae; they were previously on Ranunculaceae, also a group with noxious secondary metabolites (Winkler et al. 2009).
Perhaps 600 species of aphids (Aphididae), about 1/8 of the total, are known from Apiaceae, more than from any other angiosperm clade of comparable size (Peccoud et al. 2010).
Bacterial/Fungal Associations. Platysace is reported to be ectomycorrhizal, although this should be confirmed (Brundrett 2017a; Tedersoo & Brundrett 2017).
Vegetative Variation. Seeds with relatively longer embryos may have evolved in open habitats and in plants with an annual life cycle (Vandelook et al. 2012b). There is considerable variation in seedling morphology. A number of taxa have cryptogeal germination during which the plumule is as it were planted under ground; associated with this, monocotyly is also quite common (see Haccius 1952b; Cerceau-Larrival 1962; Haines & Lye 1979). This single cotyledon can look quite unlike any ordinary cotyledon (Cerceau-Larrival 1962; Plunkett et al. 2018a and references).
Variation in leaf morphology, even within Apioideae, is considerable. Thus the small circum-Pacific genus Oreomyrrhis (= Anthriscus) includes species with ordinary-looking highly dissected leaves, leaves with a series of almost tooth-like leaflets on either side of the rachis, linear leaves, sometimes lobed at the apex, although the lobes are not articulated, and small, undivided leaves. In the last case the plant is tussock-forming and almost moss-like, and I have seen specimens identified as Centrolepidaceae (= Restionaceae), a monocot! Species with all these leaf morphologies are found on the mountains of New Guinea. Although Oreomyrrhis is probably monophyletic, it is well embedded in Chaerophyllum, a genus hitherto thought to be fairly well understood (Chung et al. 2005; Chung 2007; Sklenár et al. 2011: pâramo species), again with ordinary-looking leaves. Lilaeopsis occidentalis and Oxypolis greenmanii have linear, terete leaves that are marked by articulations at intervals. These leaves are comparable with the rhachis of compound leaves, hydathodes borne at the articulations representing much reduced and modified pinnae (Kaplan 1970b, c.f. esp. Figs 3E and 6A; see Charlton 1992: L. brasiliensis ± dorsiventral). Such leaves appear to have evolved several times (Feist & Downie 2008; Feist et al. 2012). Bupleurum has undivided leaves, those of B. rotundifolium being almost orbicular, entire, and perfoliate, hence its common name, thorow wax.
Azorelloideae show great variation in both habit and leaf form, as Plunkett and Nicolas (2017) emphasized. Thus the scale-like leaves of genera like Gymnophyton soon wither, and photosynthesis is carried out by the stems and fruits, the latter being bright green until just before they mature. Leaves are commonly more or less orbicular (up to the size of a large rhubarb leaf - Stilbocarpa) and palmately toothed or lobed, rarely very deeply lobed = compound (Domeykoa oppositifolia).
Genes & Genomes. For chromosome numbers in the family, see Bell and Constance (1957) and Pimenov et al. (2003). The Dc-α genome duplication event, probably an allotetraploidy, has been dated to ca 43 Ma (Iorizzo et al. 2016) or to 52-46 Ma (J. Wang et al. 2020). There is also a Dc-β genome triplication event that is dated at ca 70 Ma; this is different from any other Asterales-associated duplication event (Iorizzo et al. 2016), indeed, it has also been assoiated with Apiales as a whole.
For biparental inheritance of the plastid gene in Daucus, see Boblenz et al. (1990).
There has been quite extensive expansion and contraction of the chloroplast inverted repeat in Apioideae, for instance, around Aegopodium and Apium respectively (Plunkett & Downie 2000; Downie & Jansen 2015). For the occurrence of the coxl pseudogene (a mitochondrial gene) in the plastid in Daucus and relatives, see Straub et al. (2013); Downie and Jansen (2015; see also Gandini & Sanchez-Puerta 2017) discuss other examples of this in Apioideae, where it seems to be quite common.
Chemistry, Morphology, etc.. Gums and resins are scattered in the family. In Apiaceae the flavone apigenin is synthesized by an enzyme belonging to the oxoglutarate dependen dioxygenase family, not by a member of the cytochrome P450 family, as is usual in angiosperms (Pichersky & Lewinsohn 2011). For the distinctive rosmarinic acid glucoside found in Saniculoideae-Saniculeae, see Olivier et al. (2008), rosmarinic acid is an ester of caffeic acid and is uncommon elsewhere in Apiales (Petersen et al. 2009). Bowlesia lacks petroselinic acid, but it was apparently the only Azorelloideae studied (Kleiman & Spencer 1982). Oskolski et al. (2010a) describe wood and bark anatomy of Steganotaenieae in particular and Saniculoideae in general. Peripheral collenchyma in the stem is often especially well developed, and petiole anatomy is very variable and complex (e.g. Metcalfe 1950). Taxa such as Foeniculum have stipules of sorts.
The usually compact inflorescence units of Saniculoideae may be best interpreted as a group of reduced umbellules (Froebe 1964, 1971), although they are called simple umbels above. There is quite a bit of variation in floral development (Ajani et al. 2016) which has tentatively been incorporated into the character hierarchy above. Centella (Mackinlayoideae) has a few branches from the petal bundle (Gustafsson 1995); petal vasculature may repay attention. For nectaries in other than Apiaceae-Apioideae in particular, see Magin (1983); nectaries are to be found in places other than the base of the style. Spichiger et al. (2002) show the two carpels as being collateral. According to Eyde and Tseng (1971), whether the ventral carpel bundles are fused bundles of adjacent placentae or are from the same placenta varies within Apiaceae but without any particular systematic significance. Van Tieghem (1898) noted that in Apiaceae the ascending ovule aborts and the pendulous ovule persists, however, other reports suggest that both ovules are pendulous (Philipson 1970).
Fruit anatomy and morphology vary greatly (and have been used to separate genera) and have been studied by M. Liu and co-workers and others. Some of this variation shows at least some correlation with clades. For vittae, druses, etc. in the fruits, see M. Liu et al. (2007, 2012b), for fruit anatomy of Azorelloideae, see Liu et al. (2009), and for carpophores, see Liu et al. (2012a) - although Phlyctidocarpa (Saniculoideae) by one definition in this last paper would seem to lack a carpophore (group A), yet it is scored as having a bifid carpophore.
There is much useful information in Chandler and Plunkett (2003, 2004), in all four numbers of Plant Divers. Evol. 128. 2010, inc. Stepanova & Oskolski (2010: Bupleurum) and in Plunkett et al. (2018a); see also Burtt (1991a: southern African genera) and Van Wyk et al. (2013: African taxa) for information about Apiaceae in a biogeographically/phylogenetically critical area. For chemistry, see also Hegnauer (1971) and Olivier and van Wyk (2013: Saniculeae), for stomata, see Guyot 1971 and references - value slight?), for wood anatomy in Mackinlayoideae and Apioideae-Heteromorpheae, see Oskolski and van Wyk (2008, 2010; Long & Oskolski 2018), and in woody Saniculoideae, see Oskolski et al. (2010a), for inflorescences of Saniculoideae and Hydrocotyloideae in particular, see Froebe (1964, 1979), for those of Eryngium, see Harris (1999), for floral development, see Mair (1977), Leins and Erbar (2004b) and especially Erbar and Leins (1985) and Ajani et al. (2016), for pollen of Platysace and Mackinlayoideae, see Cerceau-Larrival (1980), that of European Apiaceae, see Punt (1984), and that of Chinese Apiaceae, see Shu and She (2001), for the nectary, see Erbar (2014), for the distribution of the hypostase, see Gupta (1970), for embryo sac morphology and fruit anatomy, esp. of genera in the old Hydrocotyloideae, see Tseng (1967), and for ovules, etc., see Håkansson (1923).
Phylogeny. Relationships between Apiaceae and Araliaceae, in particular the positions of Hydrocotyle, ex-Apiaceae, and Mackinlaya and relatives, ex-Araliaceae, are discussed above. The Australian Platysace, perhaps to include Homalosciadium, is not a member of Mackinlayoideae, where it had been placed (e.g. Chandler & Plunkett 2004). It is sister to Apioideae in some analyses (Henwood & Hart 2001; Andersson et al. 2006), but a position rather lower in the tree sister to [Azorelloideae [Saniculoideae + Apioideae]] has been strongly supported (Nicolas & Plunkett 2009, 2014), while Soltis et al. (2011: but sampling) found that it was moderately supported as sister to Mackinlaya. The positions of Klotzschia ("distinctive fruits") and Hermas, both of which used to be in Hydrocotyloideae, are unclear (Andersson et al. 2006; Calviño et al. 2006, 2008). Klotzschia, herbs to subshrubs with peltate leaves from Brazil, may go with Azorelloideae, Apioideae, or join the back-bone immediately above Azorelloideae (Nicolas & Plunkett 2014). Hermas, a South African endemic, has some similarities with Saniculoideae, but it is unlikely to be placed within any currently recognized subfamily (Nicolas & Plunkett 2009); there is some support for a position as sister to [Saniculoideae + Apioideae] (e.g. Nicolas & Plunkett 2014; Calviño et al. 2016), and I have tentatively placed it there.
Within Mackinlayoideae, the clade of [Actinotus + Apiopetalum] is quite well supported as sister to the rest of the subfamily (Nicolas & Plunkett 2009; M. Liu et al. 2016).
For the phylogeny of Azorelloideae, which includes about half the genera that used to be in Hydrocotyloideae, see Downie et al. (1998, 2000a, 2001), Mitchell et al. (1999), Plunkett & Lowry (2001), Henwood and Hart (2001: the Bowlesia clade), Chandler and Plunkett (2004), Andersson et al. (2006), Nicolas and Plunkett (2009), Fernández et al. (2017). Stilbocarpa used to be in Araliaceae, but it is probably sister to the Andean Huanaca. Klotzschia may also belong here, but its position is unstable (see above); this genus aside, the South American Diposis is sister to other Azorelloideae (Nicolas & Plunkett 2009). Azorella is para/polyphyletic with respect to Laretia, Mulinum, and three other genera, in particular, the type of Azorella is rather distant from most of the rest of the genus (Nicolas & Plunkett 2012) and there has been extensive hybridization (Fernández et al. 2017); for a comprehensive phylogeny of the whole group, see Plunkett and Nicolas (2017).
The monophyly of Saniculoideae (except Lagoecia and Lichtensteinia, both now in Apioideae) is upheld in all molecular analyses, and some details of relationships within it were suggested by Valiejo-Roman et al. (2002). The African ex-hydrocotyloid Arctopus (see Magin 1980 for floral development) was sometimes sister to other Saniculoideae, the woody Steganotaenia and Polemanniopsis, and perhaps also Lichtensteinia, being part of the same clade (Downie et al. 2001; van Wyck 2001; M. Liu et al. 2003; Plunkett et al. 2004c; Magee et al. 2010a); at least some of the latter genera have a slightly lignified endocarp, apparently alone in both Saniculoideae and Apioideae (M. Liu et al. 2004). Calviño et al. (2006, esp. 2007: good general discussion of variation), however, expressed reservations about this expanded - and characterless - Eryngioideae, but Calviño and Downie (2007, c.f. Magee et al. 2010a) found that the clade could be circumscribed satisfactorily so long as Lichtensteinia moved to Apioideae; they recognised two tribes, both well supported and with unique indels. A clade including Lichtensteinia and Choritaenia were weakly supported as being sister to other Saniculoideae (Nicolas & Plunkett 2009); although this set of relationships has not been upheld, the monotypic African Phlyctidocarpa does seem to be a member of Saniculoideae, although its exact position there is unclear (Magee et al. 2010a, see also Nicolas & Plunkett 2014). The large genus Eryngium has separate New and Old World clades (Calviño et al. 2008b, 2010); a recent morphological analysis suggested that four unrelated species (unrelated in the system later used in the same paper) made up a series of basal pectinations, although there was no strong support for this topology (Wörz 2011).
Relationships at the base of Apioideae are strongly pectinate and are something like [Lichtensteinieae [Annesorhizeae [Heteromorpheae [Chamaesieae [Bupleureae + The Rest]]]]] (Downie & Katz-Downie 1999; Plunkett et al. 2004; Calviño et al. 2006, 2016; Magee et al. 2008, also a revision of Ezosciadium; Magee et al. 2010a; Downie et al. 2010; Nicolas & Plunkett 2014). Apart from the position of Lichtensteinia, in some analyses sister to [Saniculoideae + Apioideae], relationships in Nicolas and Plunkett (2009) are similar; above Bupleurum on the tree was the Mexican Neogoezia. The Annesorhiza clade appeared to be allied with Heteromorpheae, while Bupleurum was strongly supported as sister to the remainder of the subfamily (Calviño et al. 2005, 2006). The position of Chamaesieae with respect to Bupleurum is unclear (J. Zhou et al. 2009), although Calviño et al. (2016) place them as sister to all remaining euapioids, i.e. branching off immediately below Bupleurum in the tree. Similarly, in the single-copy-gene transcriptome analysis of Wen et al. (2020) relationships are [Chamaesium [Bupleurum [Pleurospermeae [Physospermopsis etc. + remaining Apioideae]]]]./p>
Bupleureae: For relationships within Bupleurum, in which the sole South African species is derived and a Mediterranean clade of sometimes shrubby, pinnately-veined taxa is sister to the rest of the genus, see Neves and Watson (2004) and H.-C. Wang et al. (2014). Within the remaining Apioideae, the monotypic Pleurospermopsis, from the eastern Himalayas, and included in an expanded Pleurospermeae (J. Zhou et al. 2009; Calviño et al. 2016), are sister to the remainder. Apioideae also include Lagoecia, with its quite well developed calyx and 1-seeded fruits, which was previously associated with Saniculoideae (Magion 1980). For other relationships within Apioideae, see e.g. Downie et al. (2000a, b, 2001, 2002), Plunkett and Downie (2000: junction of chloroplast inverted repeat/large single copy shifts characterise clades in part of Apioideae), Spalik and Downie (2001a, b), Sun and Downie (2004, 2010a, b: perennial W. North American Apioideae, morphological and molecular analyses), Sun et al. (2004: Cymopterus and Lomatium about as polyphletic as you can get), Hardway et al. (2004), Downie et al. (2008) and Spalik et al. (2009: Sium, 2014), all Oenantheae, J. Zhou et al. (2008: China), Ajani et al. (2008: Iran), Winter et al. (2008: Africa), Degtjareva et al. (2009: Bunium polyphyletic, monocotyledonous species separate), Magee et al. (2009: especially Cape genera), Logacheva et al. (2010: Tordylieae), Yu et al. (2011: Chinese Heracleum, genus polyphyletic), Valiejo-Roman et al. 2012: Pleurospermum - surprise, surprise, polyphyletic), (Liao et al. 2013: Angelica and relatives ), Feist et al. (2013: Tauschia), Degtjareva et al. (2013: Asian geophilous genera), and Terentieva et al. (2015: Coriandreae polyphyletic). 30 species of Arracacia (Selineae - arracacha roots) and 62 species of its immediate relatives were studied by Danderson et al. (2017); 8 main clades were recognised, although some were poorly supported, and species of Arracacia were in six of these, five of its species being unplaced as to clade. Pimpinella is turning out to be very much polyphyletic; Magee et al. (2010b) and Fernández Prieto et al. (2018) discuss relationships here. For relationships in Scandiceae, particularly Ferula, somewhat paraphyletic, and relatives, see Kurzyna-Mlynik et al. (2008) and Panahi et al. (2015, 2018: conflict between nuclear ITS and plastid data). The limits of Daucus and its relatives are discussed by Banasiak et al. (2016). Here Spooner et al. (2020) perhaps not surprisingly found that analyses of taxa within Daucus carota and between it and neighbouring species using chloroplast, mitochondrial and nuclear genes all suggested different relationships, however, this was true even in analyses of different aspects of the nuclear genome - SNPs, all chromosomes, 460726 parsimony informative characters, versus 94 nuclear orthologues, all chromosomes, 21011 characters. Oreomyrrhis is embedded in Chaerophyllum (Chung et al. 2005; Chung 2007) and forms a largely Taiwanese-Australo-Papuan clade along with some species from Central America and two from the U.S.A. (Piwczynski et al. 2015). Sun et al. (2008) and more recently J. Zhou et al. (2020) looked at relationships in Ligusticum, a genus centred on China, the Zhou et al. study including ca 46 of some 60 species placed in the genus in their ITS analysis. They included all Apioideae with ITS sequences, a wise move since species of Ligusticum appeared in six different clades and associated with species from a variety of other genera, themselves sometimes also polyphyletic. Sun et al. (2008) had carried out a morphological phylogenetic analysis of the Chinese species, and there L. scoticum, quite separate in the molecular analyses of Zhou et al. (2020), was embedded in those species...
Classification. The subfamilial classification of Plunkett et al. (2004c, 2018a), Downie et al. (2010) and is largely followed here, but further changes may be needed given the positions taken by some ex-Hydrocotyloideae in the trees recovered by Nicolas and Plunkett (2009, 2014). Downie et al. (2010) placed the 41 major clades they obtained in Apioideae in 30 groups, recognising tribes and subtribes where they exist, and listing included genera; some groups of genera were unnamed. For tribes in Saniculoideae and in the basal pectinations in Apioideae, see Magee et al. (2010a); five of the tribes in the latter were newly described (and all are small) and Marlothielleae and Choritaenieae, both monospecific, are combined with Lichtensteinieae above; the expanded Lichtensteinieae still muster a mere 9 species.
Generic and tribal limits in Apioideae are a notable disaster area, perhaps as bad as in any other major group (e.g. Spalik in Kadereit et al. 2016). The old tribal and generic classification was based primarily on gross fruit morphology; convergence of fruit architecture as adaptations to particular modes of fruit dispersal has resulted in many non-monophyletic groupings (see also Piwczynski et al. 2015; Banasiak et al. 2016; etc.). For genera, old style, see Pimenov and Leonov (1993). Just about all the papers dealing with phylogenetic relationships in Apioideae (see above) have implications for generic limits. For instance, 13/18 genera for which two or more sequences were included in a study by Downie et al. (2000b) were found not to be monophyletic, while Weitzel et al. (2014) included five genera in Thapsia, "the deadly carrot", a genus of under 50 species. Downie et al. (2010) listed 18 genera that were wildly polyphyletic, i.e., had members in two or more of their 41 major clades; Pimpinella was no. 1 in the list, species being known from seven of these clades (see also above; Plunkett et al. 2018a). Ligusticum, with some 60 species and previously in the list of larger genera in Apioideae, now includes just two species (J. Zhou et al. 2020) - c.f. Schefflera in Araliaceae. The problem is further compounded by the disproportionately large number of mono- or di-typic genera, thus around 40% of the 466 genera listed by Plunkett et al. (2018a) are monotypic and over 75% have ten or fewer species (see also Spalik et al. 2001; Valiejo-Roman et al. 2006; Spalik & Downie 2007). It is not that fruit characters, hitherto the major source of generic characters, never correlate with redrawn generic boundaries (c.f. Feist et al. 2012: rhachis-leaved North American taxa; M. Liu et al. 2012), but they often mislead when used by themselves and/or without detailed examination of their anatomy.
The extensive para- and polyphyly of the various genera in the Azorella group (Azorelloideae) seemed best solved by extending the limits of that genus and recognizing 10 setions in it (Plunkett & Nicolas 2017). For a classification of Apieae (and diagrams showing the plasticity of morphological characters used to classify the group), see Jiménez-Mejías and Vargas (2015), for genera in Scandiceae-Daucinae, see Banasiak et al. (2016), and for the beginning of an infrageneric classification of Ferula, see Panahi et al. (2018)..
Thanks. I am particularly indebted to Mark Watson for comments on Apiaceae s.l.; mistakes remain mine.