EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, not motile, initially ±globular; showing gravitropism; acquisition of phenylalanine lysase [PAL], microbial terpene synthase-like genes +, triterpenoids produced by CYP716 enzymes, 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; glycolate metabolism in leaf peroxisomes [glyoxysomes]; 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; oogamy; sporophyte multicellular, cuticle +, plane of first cell division transverse [with respect to long axis of archegonium/embryo sac], sporangium and upper part of seta developing from epibasal cell [towards the archegonial neck, exoscopic], with at least transient apical cell [?level], initially surrounded by and dependent on gametophyte, placental transfer cells +, in both sporophyte and gametophyte, wall ingrowths develop early; suspensor/foot +, cells at foot tip somewhat haustorial; sporangium +, single, terminal, dehiscence longitudinal; meiosis sporic, monoplastidic, MTOC [MTOC = microtubule organizing centre] associated with plastid, sporocytes 4-lobed, cytokinesis simultaneous, preceding nuclear division, quadripolar microtubule system +; wall development both centripetal and centrifugal, 1000 spores/sporangium, sporopollenin in the spore wall laid down in association with trilamellar layers [white-line centred lamellae; tripartite lamellae]; nuclear genome size [1C] <1.4 pg, main telomere sequence motif TTTAGGG, LEAFY and KNOX1 and KNOX2 genes present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes [precursors for starch synthesis], tufA gene moved to nucleus; mitochondrial trnS(gcu) and trnN(guu) genes +.
Many of the bolded characters in the characterization above are apomorphies of subsets of streptophytes along the lineage leading to the embryophytes, not apomorphies of crown-group embryophytes per se.
All groups below are crown groups, nearly all are extant. Characters mentioned are those of the immediate common ancestor of the group,  contains explanatory material, () features common in clade, exact status unclear.
Abscisic acid, L- and D-methionine distinguished metabolically; pro- and metaphase spindles acentric; class 1 KNOX genes expressed in sporangium alone; sporangium wall 4≤ cells across [≡ eusporangium], tapetum +, secreting sporopollenin, which obscures outer white-line centred lamellae, columella +, developing from endothecial cells; stomata +, on sporangium, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and of rhizoids/root hairs; spores trilete; shoot meristem patterning gene families expressed; MIKC, MI*K*C* genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns, mitochondrial trnS(gcu) and trnN(guu) genes 0.
[Anthocerophyta + Polysporangiophyta]: gametophyte leafless; archegonia embedded/sunken [only neck protruding]; sporophyte long-lived, chlorophyllous; cell walls with xylans.
Sporophyte well developed, branched, branching apical, dichotomous, potentially indeterminate; hydroids +; stomata on stem; sporangia several, terminal; spore walls not multilamellate [?here].
Vascular tissue + [tracheids, walls with bars of secondary thickening]; stomata involved in gas exchange.
EXTANT TRACHEOPHYTA / VASCULAR PLANTS
Sporophyte with 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]; sporophyte with polar auxin transport, PIN [auxin efflux facilitator] involved; (condensed or nonhydrolyzable tannins/proanthocyanidins +); xyloglucans with side chains uncharged [?level], in secondary walls of vascular and mechanical tissue; lignins +; roots +, root hairs and root cap +; stem apex multicellular, 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 +; leaves/sporophylls spirally arranged, blades with mean venation density ca 1.8 mm/mm2 [to 5 mm/mm2], all epidermal cells with chloroplasts; sporangia adaxial, columella 0; tapetum glandular; ?position of transfer cells; MTOCs not associated with plastids, basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; suspensor +, shoot apex developing away from micropyle/archegonial neck [from hypobasal cell, endoscopic], root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Sporophyte 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; 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 lateral, meristems axillary; lateral root origin from the pericycle; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].
Growth of plant bipolar [roots with positive geotropic response]; plants heterosporous; megasporangium surrounded by cupule [i.e. = unitegmic ovule, cupule = integument]; pollen lands on ovule; megaspore germination endosporic [female gametophyte initially retained on the plant].
EXTANT SEED PLANTS / SPERMATOPHYTA
Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); 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]; root stele diarch to pentarch, xylem and phloem originating on alternating radii, cork cambium deep seated; stem apical meristem complex [with quiescent centre, etc.], plasmodesma density in SAM 1.6-6.2[mean]/μm2 [interface-specific plasmodesmatal network]; eustele +, protoxylem endarch, endodermis 0; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; cork cambium superficial; leaf nodes 1:1, a single trace leaving the vascular sympodium; leaf vascular bundles amphicribral; guard cells the only epidermal cells with chloroplasts, stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; axillary buds +, exogenous; prophylls two, lateral; leaves with petiole and lamina, development basipetal, lamina simple; sporangia borne on sporophylls; spores not dormant; microsporophylls aggregated in indeterminate cones/strobili; grains monosulcate, aperture in ana- position [distal], primexine + [involved in exine pattern formation with deposition of sporopollenin from tapetum there], exine and intine homogeneous, exine alveolar/honeycomb; ovules with parietal tissue [= crassinucellate], megaspore tetrad linear, functional megaspore single, chalazal, sporopollenin 0; gametophyte ± wholly dependent on sporophyte, development initially endosporic [apical cell 0, rhizoids 0, etc.]; male gametophyte with tube developing from distal end of grain, male gametes two, developing after pollination, with cell walls; female gametophyte initially syncytial, walls then surrounding individual nuclei; embryo cellular ab initio, suspensor short-minute, embryonic axis straight [shoot and root at opposite ends; plant allorhizic], cotyledons 2; embryo ± dormant; chloroplast ycf2 gene in inverted repeat, trans splicing of five mitochondrial group II introns, rpl6 gene absent; whole nuclear genome duplication [ζ - zeta - duplication], two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], 5.8S and 5S rDNA in separate clusters.
ANGIOSPERMAE / MAGNOLIOPHYTA
Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANA grade?], lignin also with syringyl units common [G + S lignin, positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], hemicelluloses as xyloglucans; root cap meristem closed (open); pith relatively inconspicuous, lateral roots initiated immediately to the side of [when diarch] or opposite xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0, hypodermis suberised and with Casparian strip [= exodermis]; shoot apex with tunica-corpus construction, tunica 2-layered; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, not occluding pores of plate, companion cell and sieve tube from same mother cell; ?phloem loading/sugar transport; nodes 1:?; dark reversal Pfr → Pr; protoplasm dessication tolerant [plant poikilohydric]; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance with increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, secondary veins pinnate, fine venation hierarchical-reticulate, (1.7-)4.1(-5.7) mm/mm2, vein endings free; flowers perfect, pedicellate, ± haplomorphic, protogynous; parts free, numbers variable, development centripetal; P +, ?insertion, members each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], each theca dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, endothecium +, cells elongated at right angles to long axis of anther; tapetal cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine lamellate only in the apertural regions, thin, compact, intine in apertural areas thick, pollenkitt +; nectary 0; carpels present, superior, free, several, ascidiate [postgenital occlusion by secretion], stylulus at most short [shorter than ovary], hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry; suprastylar extragynoecial compitum +; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across, nucellar cap?; megasporocyte single, hypodermal, functional megaspore lacking cuticle; female gametophyte lacking chlorophyll [no photosynthesis], four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; ovule not increasing in size between pollination and fertilization; pollen grains land on stigma, bicellular at dispersal, mature male gametophyte tricellular, germinating in less than 3 hours, pollen tube elongated, unbranched, growing towards the ovule, between cells, growth rate (20-)80-20,000 µm/hour, apex of pectins, wall with callose, lumen with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametes lacking cell walls, ciliae 0, siphonogamy; double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; mature seed much larger than fertilized ovule, small [<5 mm long], dry [no sarcotesta], exotestal; endosperm +, cellular, development heteropolar [first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous, embryo short [<¼ length of seed]; plastid and mitochondrial transmission maternal; Arabidopsis-type telomeres [(TTTAGGG)n]; nuclear genome size [1C] <1.4 pg [mean 1C = 18.1 pg, 1 pg = 109 base pairs], whole nuclear genome duplication [ε/epsilon event]; ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, palaeo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]]; chloroplast chlB, -L, -N, trnP-GGG genes 0.
[NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]]: wood fibres +; axial parenchyma diffuse or diffuse-in-aggregates; pollen monosulcate [anasulcate], tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.
[AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: phloem loading passive, via symplast, plasmodesmata numerous; vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood + [reaction wood: with gelatinous fibres, G-fibres, on adaxial side of branch/stem junction]; 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 bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid.
[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (extra-floral nectaries +); (veins in lamina often 7-17 mm/mm2 or more [mean for eudicots 8.0]); (stamens opposite [two whorls of] P); (pollen tube growth fast).
[CERATOPHYLLALES + EUDICOTS]: ethereal oils 0.
EUDICOTS: (Myricetin, delphinidin +), asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; (vessel elements with simple perforation plates in primary xylem); nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; protandry common; K/outer P members with three traces, ("C" +, with a single trace); A ?, filaments fairly slender, anthers basifixed; microsporogenesis simultaneous, pollen tricolpate, apertures in pairs at six points of the young tetrad [Fischer's rule], cleavage centripetal, wall with endexine; G with complete postgenital fusion, stylulus/style solid [?here]; seed coat?
[PROTEALES [TROCHODENDRALES [BUXALES + CORE EUDICOTS]]]: (axial/receptacular nectary +).
[TROCHODENDRALES [BUXALES + CORE EUDICOTS]]: benzylisoquinoline alkaloids 0; euAP3 + TM6 genes [duplication of paleoAP3 gene: B class], mitochondrial rps2 gene lost.
[BUXALES + CORE EUDICOTS]: mitochondrial rps11 gene lost.
CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one position]; micropyle?; γ whole nuclear genome duplication [palaeohexaploidy, gamma triplication], x = 21, PI-dB motif +; small deletion in the 18S ribosomal DNA common.
[ROSIDS ET AL. + ASTERIDS ET AL.] / PENTAPETALAE: root apical meristem closed; (cyanogenesis also via [iso]leucine, valine and phenylalanine pathways); flowers rather stereotyped: 5-merous, parts whorled; P = calyx + corolla, the calyx enclosing the flower in bud, sepals with three or more traces, petals with a single trace; stamens = 2x K/C, in two whorls, internal/adaxial to the corolla whorl, alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G , (G [3, 4]), whorled, placentation axile, style +, stigma not decurrent; compitum +; endosperm nuclear; fruit dry, dehiscent, loculicidal [when a capsule]; RNase-based gametophytic incompatibility system present; floral nectaries with CRABSCLAW expression; (monosymmetric flowers with adaxial/dorsal CYC expression).
[BERBERIDOPSIDALES [SANTALALES [CARYOPHYLLALES + ASTERIDS]]] / ASTERIDS ET AL. / SUPERASTERIDS : ?
[SANTALALES [CARYOPHYLLALES + ASTERIDS]]: ?
[CARYOPHYLLALES + ASTERIDS]: seed exotestal; embryo long.
ASTERIDS / 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, endothelium +, nucellar epidermis does not persist; exotestal [!: even when a single integument] cells lignified, esp. on anticlinal and/or inner periclinal walls; endosperm cellular.
[ERICALES [ASTERID I + ASTERID II]]: (ovules lacking parietal tissue) [tenuinucellate].
[ASTERID I + ASTERID II] / CORE ASTERIDS / EUASTERIDS: plants woody, evergreen; ellagic acid 0, non-hydrolysable tannins not common; vessel elements long, with scalariform perforation plates; nodes 3:3; sugar transport in phloem active; inflorescence usu. basically cymose; flowers rather small [<8 mm across]; C free or basally connate, valvate, petals often with median adaxial ridge and inflexed apex; A = and opposite sepals or P, (numerous [usu. associated with increased numbers of C or G]), free to basally adnate to C; G #?; ovules 2/carpel, apical, pendulous; fruit a drupe, drupe ± flattened, surface ornamented; seed single; duplication of the PI gene.
ASTERID I / LAMIIDAE: ?
[METTENIUSALES [GARRYALES [GENTIANALES, VAHLIALES, SOLANALES, BORAGINALES, LAMIALES]]]: ?
[GARRYALES [GENTIANALES, VAHLIALES, SOLANALES, BORAGINALES, LAMIALES]]: G , superposed; loss of introns 18-23 in RPB2 gene d copy [?level].
[GENTIANALES, VAHLIALES, SOLANALES, BORAGINALES, LAMIALES]: (herbaceous habit widespread); (8-ring deoxyflavonols +); vessel elements with simple perforation plates; nodes 1:1; C forming a distinct tube, initiation late [sampling!]; A epipetalous; (vascularized) nectary at base of G; style long; several ovules/carpel; fruit a septicidal capsule, K persistent.
Evolution: Divergence & Distribution. For the complex patterns of variation in a number of characters in this part of the tree, see the Gentianales page.
Phylogeny. For the relationships of Solanales, see discussion under Gentianales.
SOLANALES Berchtold & J. Presl Main Tree
O-methyl flavonols (flavones) +, myricetin 0; inflorescence terminal; K connate; anther sacs with placentoids; pollen tube usu. with callose; endosperm development?, chalazal endosperm haustorium +. - 5 families, 165 genera, 4,125 species.
Age. Crown-group Solanales may date from (82-)78, 76(-72) m.y. (Wikström et al. 2001) or (102-)90(-75) m.y.o. (Wikström et al. 2015); Bremer et al. (2004) date them to ca 100 m.y., Tank and Olmstead (2017) at (110.1-)93.6(-78.9) m.y., and Lemaire et al. (2011b) to (93-)71(-50) m.y., Nylinder et al. (2012: suppl.) suggest ages of around 87.7 and 85.4 m.y.a., Magallón et al. (2015) ages of around 79.2 m.y.a., Magallón and Castillo (2009) ca 73 m.y., and Bell et al. (2010) suggest ages of (85-)76, 71(-62) m.y. ago.
Note: Boldface denotes possible apomorphies, (....) denotes a feature common in the clade, exact status uncertain, [....] includes explanatory material. Note that the particular node to which many characters, particularly the more cryptic ones, should be assigned is unclear. This is partly because homoplasy is very common, in addition, basic information for all too many characters is very incomplete, frequently coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there are the not-so-trivial issues of how character states are delimited and ancestral states are reconstructed (see above).
Phylogeny. Within Solanales, Montiniaceae were found to be sister to [Solanaceae + Convolvulaceae] (B. Bremer 1996, see also Soltis & Soltis 1997). D. Soltis et al. (2000) found strong support for the association of Montinia and Hydrolea; Sphenoclea was not included. With the inclusion of the latter and broader sampling (all three genera) in Montiniaceae, B. Bremer et al. (2002) found strong support for the association of Sphenoclea and Hydrolea, but only just above 50% for the association of Montiniaceae with that pair; support was stronger in Soltis et al. (2011); see also Refulio-Rodriguez and Olmstead (2014). The topology of the tree here follows that of these latter papers.
Includes Convolvulaceae, Hydroleaceae, Montiniaceae, Solanaceae, Sphenocleaceae.
Synonymy: Cestrales Martius, Convolvulales Berchtold & J. Presl, Cuscutales Martius, Hydroleales Martius, Nolanales Lindley, Sphenocleales Doweld
[Montiniaceae [Sphenocleaceae + Hydroleaceae]]: route I secoiridoids +; petiole bundle(s) arcuate; stigma ± capitate.
Age. The age of this node is estimated to be (71-)66, 65(-60) m.y. (Wikström et al. 2001), (94-)78(-58) m.y. (Wikström et al. 2015),(79-)65, 61(-47) m.y. (Bell et al. 2010), ca 72 m.y. (Magallón et al. 2015), ca 92 m.y. (Bremer et al. (2004), (102.2-)83.2(-60.8) m.y. (Tank & Olmstead pers. comm.), or ca 63.2 m.y. (Tank et al. 2015).
Evolution: Divergence & Distribution. Not a very diverse clade (Tank et al. 2015).
The character "pits vestured" may be best placed at this node.
MONTINIACEAE Nakai Back to Solanales
Shrubs, trees (lianes); plants with a peppery smell; iridioids +, tannin slight; cambium storied or not; pits vestured; young stem with a vascular cylinder (separate bundles); (medullary bundles +); pericyclic fibres 0; crystal sand, acicular crystals and styloids usu. all +; nodes 1:1-11; petiole arc of (rounded) bundles (+ additional strands); axillary tuft of usu. uniseriate hairs at nodes; (stomata anisocytic - some Grevea); leaves also opposite; bracteoles 0; inflorescence cymose, (carpellate flowers single, terminal), bracteoles 0; flowers imperfect, small; C free [absolutely so - Montinia], (valvate); nectary +, vascularized; staminate flowers: 3-4(-5)-merous; A free, anthers basifixed, or dorsifixed, becoming extrorse, filaments short; pollen grains (large), reticulate, with supratectal granules; pistillode minute; carpellate flowers: 4-merous; (C 0 - Kaliphora), staminodes + (0); ovary (semi)inferior, placentation intrusive parietal-subaxile, style short, stout, hollow, stigma with 2 large lobes (style branched, stigma commissural, not capitate - Kaliphora); ovules 1-12/carpel, (campylotropous, apotropous - Kaliphora), integument ca 7 cells across, parietal tissue ca 1 cell across, suprachalazal tissue slight [Montinia]; fruit a capsule; seeds winged, exotesta lignified, periclinal walls thickened, (adjacent wall of mesotesta also thickened [Montinia)]; or fruit ?drupe, placentae at least initially fleshy; testa thin-walled, ± pulpy when wetted, exotesta not persistent [Grevea]; or drupe 2-seeded [Kaliphora]; endosperm +/0, ?development, hemicellulosic, walls thick, layered, cotyledons accumbent, foliaceous; cotyledonary petioles connate [Montinia]; n = 16 [Kaliphora], 34 [Montinia].
3 [list]/5. Africa and Madagascar (map: from Milne-Redhead & Metcalfe 1955; Verdcourt 1975; Bosser 1990; Brummit 2007 [C. and W. Africa]). [Photos - Kaliphora, Montinia Fruits © Serban Procheŝ.]
Age. The age of crown-group Montiniaceae is around 42 m.y. (Bremer et al. (2004), (60-)40(-23) m.y. (Wikström et al. 2015) or (63.6-)38(-14.3) m.y. (Tank & Olmstead pers. comm.).
Chemistry, Morphology, etc. Pericyclic fibres are poorly developed in Kaliphora, ?others; Grevea has vascular bundles in the pith. The axillary tufts of hairs are least well developed in Kaliphora. Kaliphora is anisophyllous, and the leaves are subopposite; successive leaves may be borne on the same side of the stem. The pollen (Hideux & Ferguson 1976) is rather like that of some Araliaceae.
See Milne-Redhead and Metcalfe (1955) and Ronse de Craene (2016), both general, Hegnauer (1973, 1990, as Saxifragaceae) for chemistry, Dahlgren et al. (1977) for germination and iridoids, Ramamonjiarisoa (1980), Carlquist (1989), and Wangerin (1906), Gregory (1998) for vegetative anatomy, Ronse Decraene (1992) and Ronse Decraene et al. (2000a) for details of floral morphology, Ferguson (1977: Kaliphora) for pollen, Mauritzon (1933: Montinia) for embryology, and Krach (1976, 1977) and Takhtajan and Trifonova (1999) for testa anatomy.
Phylogeny. Relationships are [Kaliphora [Grevea + Montinia]]; support is strong (B. Bremer et al. 2002), although the group is very heterogeneous.
Previous Relationships. Montiniaceae have been hard to place, and have generally ended up somewhere around Saxifragaceae s.l.. Thus Cronquist (1981) included them in his heterogeneous Grossulariaceae, while Takhtajan (1997) placed Montiniaceae and Kaliphoraceae next to each other in his Hydrangeales.
Synonymy: Kaliphoraceae Takhtajan
[Sphenocleaceae + Hydroleaceae]: A adnate to C; placentae swollen; ovules many/carpel; endosperm at most scanty, with multicellular micropylar haustoria.
Age. The age for this node is estimated to be around (91-)64.5(-37.9) m.y. (Tank & Olmstead pers. comm.), 56.5 m.y. (Magallón et al. 2015) or 54.6 m.y. (Tank et al. 2015: Table S1).
SPHENOCLEACEAE Baskerville Back to Solanales
Herbs, rather fleshy, annual; fructose with isokestose linkages, cyclic thiosulphinates [zeylanoxides] +, secoiridoids, alkaloids 0; cork ?mid-cortical; cortical air spaces +; stomata tetracytic; inflorescences spicate; K imbricate, C quincuncial, tube formation early, lateral veins connate and commissural; tapetal cells binucleate; pollen grains tricellular; nectary 0; G ± inferior, placentae massive, style short, stigma subcapitate, wet; integument "massive", hypostase 0; synergids elongated, antipodal cells degenerate; fruit capsular, capsule circumscissile; seeds tiny (ca 0.5 mm long); exotestal cells polygonal, inner walls thickened and with radial spine-like processes; endosperm slight, walls thick; n = 12, 16, 20, etc.
1 [list]/2. Old World tropics (map: from Brummit 2007; but c.f. Australia's Virtual Herbarium v.2013; esp. Carter et al. 2014). [Photo - Habit © B. Hammel]
Evolution. Ecology & Physiology. The cyclic thioslphinates, and perhaps also the secoiridoids, seem to be responsible for the potent allelopathic efect of Spencolea zeylanica, both on rice and othe plants (Hirai et al. 2000 and references.
Chemistry, Morphology, etc. Corolla tube formation is of the early type, and the corolla lobes are characteristically incurved; the lateral veins of adjacent lobes are fused producing commissural veins. The anticlinal walls of the testa are shown as being massively thickened in Takhtajan (2010).
Some information is taken from Subramanyam (1950b), Monod (1980), Carter et al. (2014) and Lammers (2016), all general, Erbar (1995: floral morphology), and Kausik and Subramanyam (1946) and Tobe and Morin (1996), both embryology.
Previous Relationships. Sphenocleaceae, along with Hydrolea, another genus of uncertain position, were placed near Boraginaceae by Cosner et al. (1994). However, in morphological studies (e.g. Gustafsson & Bremer 1995) Sphenocleaceae are placed well within Asterales; they have often been associated with Campanulaceae (e.g. they are placed in Campanulales by Takhtajan 1997: p. 408 - "it definitely belongs", see also Cronquist 1981), although they lack latex.
HYDROLEACEAE Edwards Back to Solanales
(Annual) herbs to shrubby; mycorrhizae 0; chemistry?; cork?; (vessel elements with scalariform perforation plates); pits vestured; cortex aerenchymatous; stomata usu. anomocytic; thorns +/0, axillary-sublateral; lamina margin toothed to entire; flowers 4-5-merous, medium sized [ca 1.5 cm across]; K basally connate, C connate, tube formation late; A versatile, filament base abruptly broadened/lobed; nectary 0/+; G diagonal, [2(-4)], placentae bilobed or not, styles separate, ± spreading, stigma slightly funneliform or capitate; ovules mostly pleurotropous, funicular bundle absent, integument 6-8 cells across; antipodals degenerating early; fruit a septi-(+ loculi-)cidal capsule, (irregularly dehiscent); seeds longitudinally ridged and ruminate, exotestal cells thin-walled, endotestal cells tanniniferous, with a cuticle; n = (9) 10 (12).
1 [list]/12. Tropical, warm temperate (map: from Davenport 1988; FloraBase 2007). [Photo - Hydrolea Flower © B. Kenney]
Evolution. Bacterial/Fungal Associations. Hydrolea appears to lack mycorrhizae.
Chemistry, Morphology, etc. The axillary inflorescences may be cymose. Davenport (1988) suggested that there is no nectary disc. The two carpels are shown as being oblique by Schnizlein (1843-1870: fam. 147), and this was confirmed by Erbar et al. (2005), even for Hydrolea palustris, which has flowers with the median sepal abaxial. Indeed, Erbar et al. (2005) noted that there the first sepal arose in the adaxial-lateral position, the second was abaxial, an unusual sequence - other species in the genus need study. Di Fulvio (1997) notes that the four ventral bundles of the two carpels are all connate in the center of the ovary - c.f. Hydrophyllaceae/Nameae where there are often two or four such bundles, rarely a single bundle (di Fulvio 1997). There are no nuclear inclusions (di Fulvio 1991).
For general information, see Bittrich and Amaral (2016) and Davenport (1988: monograph), for wood anatomy, see Carlquist and Eckhart (1984), for pollen, see Constance and Chuang (1982), and for embryology Svensson (1925) and di Fulvio (1989b, 1990).
Previous Relationships. Hydrolea has usually been included in Hydrophyllaceae (e.g. Cronquist 1981; Takhtajan 1997). Not only molecular differences but also axile versus parietal placentation and embryological differences (see di Fulvio de Basso 1990) separate the two.
Synonymy: Sagoneaceae Martynov
[Convolvulaceae + Solanaceae]: coumarins, caffeic acid esters, tropane [polyhydroxynortropanes], acyl pyrrolidine, etc., ornithine-derived alkaloids [inc. hygrines], sesquiterpenoid phytalexins, flavonol and flavone glycosides, acylated anthocyanins +, condensed tannins, iridoids 0; (interxylary phloem +), internal phloem + [intraxylary phloem; bicollateral vascular bundles]; leaves with conduplicate vernation; flowers with oblique symmetry, large [>1.5 cm across/long]; C-tube formation late, C contorted-plicate or induplicate-valvate; tapetal cells multinucleate; placentae massive; ovules many/carpel, integument (5-)9-20(-40) cells across, (endothelium ?0); testa often multiplicative; young seeds starchy, endosperm haustoria 0, cotyledons incumbent.
Age. The two families may have diverged (91-)86(-81) m.y.a. (Bremer et al. 2004), (96.9-)80.4(-60.9) m.y.a. (Tank & Olmstead pers. comm.), (71-)66, 65(-61) m.y.a. (Wikström et al. 2001), (89-)70(-49) m.y.a. (Wikström et al. 2015), ca 66.6 m.y.a. (Magallón et al. 2015), (69.7-)62.1(-54.4) m.y.a. (Paape et al. 2008), (74-)62, 59(-49) m.y.a. (Bell et al. 2010), around 64.3 m.y.a. (Naumann et al. 2013), (57.2-)52(-46.8) m.y.a. (Magallón et al. 1999), ca 55 or (53.5-)49(-46) m.y.a. (Särkinen et al. 2013, see also Dupin et al. 2017), ca 57.3 m.y. (Nylinder et al. 2012: suppl.), or ca 56.2 m.y.a. (Tank et al. 2015: Table S2) - or a mere ca 39.9 or 37.5 m.y.a. (Xue et al. 2012). An age of over 150 m.y. is suggested by Eserman et al. (2013), and although the range bars are huge, they do not overlap with any of the other dates just mentioned except those in Bremer et al. (2004).
Evolution: Divergence & Distribution. Flowers with an oblique plane of symmetry may be an apomorphy at this level, or even higher, although J. Zhang and Zhang (2016) suggested that zygomorphy, at least, in Humbertia developed differently than that in Solanaceae.
Plant-Animal Interactions. Chrysomelidae-Cassidinae+Hispinae and -Criocerinae beetle larvae like members of this clade, especially Convolvulaceae (Schmitt 1988; Jolivet 1988; Buzzi 1994; Vencl & Morton 1999).
Chemistry, Morphology, etc. Pyrrolizidine, tropane and pyrrolidine alkaloids are all synthesised from an ornithine precursor (Hegnauer 1973; Dahlgren 1988). Gemeinholzer and Wink (2001) discuss the sporadic distribution of tropane alkaloids in Solanaceae; they are known from Schizanthus and other clades; see Schimming et al. (1998) for the distribution of polyhydroxynortropanes (in most Convolvulaceae, not in Cuscuteae, unknown in Humbertia, scattered in Solanaceae. Eich (2008) provided an extensive summary of the distribution of secondary metabolites in these two families placed in the context of phylogeny, while Kaltenegger et al. (2013) discuss the evolution of pyrrolizinie alkaloids in particular, which, even where they occur in Convolvulaceae, are sporadically distributed.
For inter-/intraxylary pohloem, see Carlquist (2013). The corolla lobes have a thicker central area that is distinct from the margins because of the contorted-plicate or induplicate-valvate aestivation of the corolla; c.f. the "winged" corolla scattered in Asterales. For nectaries, see Erbar (2014). Corner (1976) did not mention an endothelium for Convolvulaceae, but c.f. Kaur (1969) and Kaur and Singh (1970).
CONVOLVULACEAE Jussieu, nom. cons. Back to Solanales
Plant laticiferous, resin glycosides [?level]; stomata usu. paracytic; lamina margins entire; K quincuncial, large, free; anther placentoid 0; pollen tectum imperforate; nectary vascularized, receptacular [?level]; stigma dry; ovules apotropous; K ± dry, scarious in fruit; seeds 4/fruit, hilum <10% of the seed; exotesta with papillae or hairs, usu. little thickened, outer hypodermis of small cells, little thickened, inner hypodermis of 1+ palisade layers, thickened; chloroplast rpl2 intron 0.
59 [list]/1,880 (1,660)- six clades below. World wide.
Age. Crown-group diversification may have begun around 68 m.y.a. (Dillon et al. 2009) or (73.8-)56.5(-39.9) m.y.a (Olmstead & Tank 2017).
1. Humbertioideae Roberty
Large tree; chemistry?; vascular bundles collateral; petiole bundle annular; latex cells in the flowers alone; flowers single, axillary, strongly obliquely monosymmetric rotated 1200 to axis; A adnate to base of C, connective tissue lignified, filaments bent in bud; ?pollen; style ?hollow, stigma clavate; ?ovule morphology; fruit a drupe; hilum crescentic; endosperm copious, cotyledons flat; seedling?; n = ?.
1/1: Humbertia madagascariensis. Madagascar.
Synonymy: Humbertiaceae Pichon, nom. cons.
[Eryciboideae, Cardiochlamyeae [Cuscutoideae [Convolvuloideae, Dichondroideae]]]: plant vine or liane, climbing by twining [sinstrorse]; fibriform vessels +; successive cambia +, (included phloem); latex canals +, usu. articulated; ovules (1-)2(-4)/carpel, erect; fruit a loculicidal capsule; exotestal cells bulging; cotyledons often complexly folded or coiled.
2. Eryciboideae (Endlicher) Roberty
Liane; inflorescence ?racemose, branched (± fasciculate); corolla lobes with thin margins forming two lobes; pollen 3-colpate, smooth; ovary 1-locular, style 0, stigma conical-radiate; fruit a berry, 1-seeded; exotestal cells fleshy; mesotestal cells little elongated and thickened; germination cryprocotylar; n = ?
1/70. Southeast Asia, Indo-Malesia to Australia (Map: from Hoogland 1953a; Flora China 16. 20; Australia's Virtual Herbarium xii.2012).
Synonymy: Erycibaceae Meisner
[Cardiochlamyeae [Cuscutoideae [Convolvuloideae + Dichondroideae]]] [if a clade]: lamina with ± palmate venation, (base cordate).
3. Cardiochlamydeae Stefanovic & Austin
Hairs T-shaped; inflorescence racemose; bracts foliaceous, sessile; pollen 3-colpate, (pantoporate - Cardiochlamys; style single, stigma capitate (slightly two-lobed); fruit ?type, (indehiscent, 1-seeded [= utricle]), K accrescent, forming a wing; seedling with ovate cotyledon; n = ?
5/24. Madagascar, Southeast Asia, West Malesia (Map: from Staples 2006).
[Cuscutoideae [Convolvuloideae + Dichondroideae]]: testa with 2-8 layers of sclereidal cells underneath palisade layer [?here].
Age. The age for this clade is estimated as (57-)34.6(-13.1) m.y. (Naumann et al. 2013).
4. Cuscutoideae Link
Plant parasitic; ectomycorrhizae 0; internal phloem 0; stomata on stem transversely oriented [?all]; leaves reduced to scales; inflorescence monochasial cymes variously grouped; K connate, C imbricate, infrastaminal scales +, scales alternating with C, ± fimbriate [= corona]; anther wall 3 cells across; tapetal cells binucleate, (amoeboid); pollen grains (bi-)tricellular, 3(-12)-colpate, (surface reticulate); styles separate (unequal) to connate or ± 0, (gynobasic), stigma globose to elongated; ovules with integument (?8-)15-17 cells across, usu. unvascularized, parietal tissue none, endothelium 0; megaspore mother cells several, competition between the developing embryo sacs, embryo sac bisporic, spores chalazal, eight-celled [Allium type] (normal); fruit circumscissile; testa multiplicative; embryo spirally coiled, (almost) acotyledonous; radicle absent; n = (4-)7(<), chromosomes 0.4-23 µm long, (holocentric).
1/195. More or less world-wide, ca 3/4 species New World.
Synonymy: Cuscutaceae Dumortier, nom. cons.
[Convolvuloideae + Dichondroideae]: (Plants lianes to 30 m), (shrubs); (cork pericyclic); (fibers or sclereids +); unicellular T-shaped hairs common (hairs stellate); leaves conduplicate, (compound), (margins lobed), (toothed [dentate - Hyalocystis]); inflorescence cymose; pollen pantoporate or 3-polycolpate; G [2(-5)], stigmas capitate, with multicellular papillae or punctate and smooth; integument vascularized, with unbranched bundle, 5-10 cells across, parietal tissue 1-3 cells across, placental obturator common; fruit usu. a variously dehiscent capsule; endosperm nuclear, storing galactomannans [?always], embryo chlorophyllous, curved/folded, cotyledons bifid/bilobed, suspensor haustorium +; n = 7-15+; chloroplast atpB gene with 6-15 bp deletion, ycf15 absent, trnF with 150 bp deletion; incompatibility system sporophytic.
49/1375. World-wide (map: from Meusel et al. 1978; Lebrun 1977; Staples & Brummit 2007). [Photo - Flower, Fruit.]
5. Convolvuloideae Burnett
Homospermidine synthase +, (pyrrolizidine alkaloids +), (ergoline alkaloids + - Convolvuleae); (plant prostrate, mat-forming), (woody); (leaf blade serrate); inflorescence a dichasial cyme; C with interplical veins; (G with false septum - Mina); embryo sac much elongated [Ipomoea]; hilum >10% of the seed, hilum peripheral, hilar pad heart-shaped; (exotestal cells not bulging).
- three tribes below. Ipomoea (605), Convolvulus (215), Argyreia (135), Merremia (105).
Age. The divergence of "Merremieae" and Ipomoeeae has been dated to (70-)55.3(-47.8) m.y. (Eserman et al. 2013), rather old. The clade age in Dillon et al. (2009) that is compared with this age is the crown-group age of the whole family, not just a subclade of it, and that in Wikström et al. (2001) is the age of stem-group Convolvulaceae as a whole.
Synonymy: Evolvulaceae Berchtold & J. Presl, Poranaceae J. Agardh
6. Dichondroideae Roberty
Lamina base cuneate (cordate); cyme monochasial (dichasial), (inflorescence racemose - Calycobolus); styles deeply divided, (unequal), (gynobasic), (single); (hilum >10% of the seed); (exotestal cells fleshy, mesotestal [palisade] cells little elongated and thickened - Maripeae); reversion to a non-edited start codon for the psbL gene.
- four tribes below. Jacquemontia (110), Evolvulus (100), Bonamia (65).
Synonymy: Dichondraceae Dumortier, nom. cons.
Synonymy: Cressaceae Rafinesque
Evolution: Divergence & Distribution. The basal clades in Convolvulaceae are all Old World, including Madagascar but not the African mainland (García et al. 2014). There are some remarkable disjunctions within Cuscuta, including C. kilimanjari, an African member of an otherwise South American clade (García et al. 2014).
As Stefanovic et al. (2003) noted, characters for their /Dicranostyloideae (= Dichondroideae) will depend very much on the position of Jacquemontia, currently unresolved in that clade. Eserman et al. (2013) discuss the evolution of a number of characters in Ipomoeeae.
Ecology & Physiology. Convolvulaceae have about the second highest number of scandent species in the New World (ca 750), Apocynaceae are number 1, Fabaceae are ± = number 2 (Gentry 1991). All told, perhaps 1,500 species are vines or lianas (the parasitic Cuscuta not included). Species of Dichondra and Evolvulus, if not shrubby, are more or less prostrate and with procumbent non-twining stems.
Many Convolvulaceae have alkaloids and are toxic to herbivores. Ergoline alkaloids of Convolvulaceae like Ipomoea and Turbina appear to be synthesized by associated ascomycete clavicipitalean fungi (Eserman et al. 2013), about 20% of Ipomoeeae forming associations with the clavicipitacous asomycete endophyte Periglandula and are ergot alkaloid-positive (Schardl et al. 2013: P. ipomoeae). Concentrations of the alkaloids, at 1,600 to 5,100 µg/g, are up to 1000 times higher than in poöid grasses (Beaulieu et al. 2013). The indolizidine alkaloid swainsonine is synthesised by chaetothryialean ascomycete fungal associates of some Convolvuloideae (Cook et al. 2014). Pyrrolizidine alkaloids (PA), on the other hand, are synthesized by the plant, and homospermidine synthase (HSS) is the first gene in the PA biosynthetic pathway. PA alkaloids may have evolved more than once in the family, but HSS evolved only once (an apomorphy!) in Convolvuloideae (see Stefanovic et al. 2003) following a gene duplication (Reimann et al. 2004; Kaltenegger et al. 2013).
Cuscuta (dodder) is a morphologically distinctive (see also below) stem parasite, although species may have some chlorophyll. Dodder haustoria are often described as being modified roots, although elements of their development are quite different from those of roots (Alakonya et al. 2012); host-parasite phloem connections are marked by a labyrinthine rather transfer cell-like morphology in the Cuscuta phloem (Dörr 1990). The photosynthesis that does occur in dodders is involved in the synthesis of lipids that are i.a. seed reserves used up as the seedling establishes (McNeal et al. 2007; Tesitel 2016), and overall CO2 fixation is at most low (e.g. van der Kooij et al. 2000; see also Funk et al. 2007 for the gradual loss of functionality in the chloroplast genome). For a model of nutrient flow between host and parasite, see Hibberd and Jaeschke (2001); stomata on the flower and/or special protuberances on the stem may increase host transpiration and hence nutient/water flow (Clayson et al. 2014); stomata are also found on extra-floral nectaries (Clayson et al. 2014). Dodders can bridge two hosts, and viruses can be transmitted from one host to another (Hosford 1967). There is also more or less extensive (depending on the host) bidirectional exchange of mRNA between Cuscusta and its hosts, although how this affects the functioning of the partners, whether or not the mRNA is expressed, etc., is unclear (G. Kim et al. 2014). It has recently been found that signals that the host plant - infested with dodder - is experiencing herbivory can cause extensive transcriptomic changes elsewhere in that plant so activating defence responses to the herbivory, but also in other plants to over 1 m away that are connected by the one dodder plant, whether or not those other plants are related to the initial host (Hettenhausen et al. 2017). For details of resistance of other plants to dodders - at least sometimes hypersensitivity is involved - see Hegenauer et al. (2016) and references.
Pollination Biology & Seed Dispersal. The flowers often last for only a single day. S. D. Smith et al. (2010) noted that white corollas were relatively uncommon in Ipomoea subg. Quamoclit because clades in which they evolved speciated relatively less than the others, while McDonald et al. (2011) discuss the numerous origins of self- from cross pollination (and reversals) in Ipomoea.
Convolvulaceae are the only asterid family in which the seeds have physical dormancy. This is caused by the thick, hard seed coat found in nearly all members of the family, indeed, such thick and complex seed coats are unique in the euasterids. Only scarified seeds take up water, but, if unscarified, water initially penetrates the seed only at particular places in the coat; in some temperate species of Cuscuta there is also physiological dormancy. However, in Erycibe and Maripa there is no physical dormancy and the seeds are recalcitrant, being unable to stand either drying or freezing (Jayasuriya et al. 2008b, 2009: what about Humbertia?).
Plant-Animal Interactions. Spermophagus is a bruchid (Chrysomeloidea-Bruchinae) whose larvae eat seeds that has diversified on and is roughly contemporaneous with Old World Convolvulaceae; its primary hosts are Fabaceae (Kergoat et al. 2015: c.f. Malvoideae hosts); other bruchids such as Megacerus are also seed predators (Reyes et al. 2009).
Bacterial/Fungal Associations. The ergoline alkaloids of Convolvulaceae like Ipomoea and Turbina appear to be synthesized by associated ascomycete clavicipitalean fungi and are found in tissues where those fungi also occur (e.g. Ahimsa-Müller et al. 2007; Markert et al. 2008; see also Eserman et al. 2013). About 20% of Ipomoeeae form associations with the endophytic fungus Periglandula and are ergot alkaloid-positive (Schardl et al. 2013: P. ipomoeae), and these fungi at least sometimes grow on the surface of the leaf alone (Beaulieu et al. 2012, 2015). The indolizidine alkaloid swainsonine is synthesised by other ascomycete fungal associates (in Chaetothyriales) of some Convolvuloideae (Cook et al. 2014).
Cuscuta has lost the ability to form endomycorrhizal associations (Delaux et al. 2014).
Genes & Genomes. Cuscuta exaltata and some other species have retained most of the genes associated with photosynthesis, perhaps because of their involvement in lipid synthesis, despite the loss of about half the plastome (McNeal et al. 2007; Barrett et al. 2014). However, gene loss can be quite extensive, many protein-encoding genes being lost in some holoparasitic clades in the genus (Braukmann et al. 2013; see also Krause 2011).
In Cuscuta, the nuclear-encoded SSL gene came from Brassicales (D. Zhang et al. 2014), while the distinctive albumen-1 gene moved from Fabaceae-Faboideae (Y. Zhang et al. 2013). Mitochondrial genes, at least, may move from Cuscuta to its host, an example being in Plantago (Mower et al. 2010). Given the extent of mRNA movment between host and parasite, and the way one parasite individual can bridge different host individuals and even host species, the possibilities are almost endless (G. Kim et al. 2014)!
For the rpl2 intron, Downie et al. (1991) and Stefanovic et al. (2002), and for holocentric chromosomes in Cuscuta, see Cuacos et al. (2015) and Escudero et al. (2016) and references.
Chemistry, Morphology, etc. Glycine betaines are rather commonly accumulated in Convolvulaceae (Rhodes & Hanson 1993), perhaps surprising since it is not a family of halophytes; glycosides are known only from Cuscuta and Convolvuloideae. Wood fluorescence occurs, but not often. Humbertia has hard wood with the odor of sandalwood. Successive cambia have been reported from some species of Ipomoea (Terrazas et al. 2011) and Carlquist (2013) noted the occurrence of interxylary phloem in that genus and Turbina. Adventitious roots on the stem may develop in two lines sublateral to and below the petiole. Adventitious shoots develop from the roots of the sweet potato.
The bracts may be adnate to the pedicel and accrescent (wind dispersal: Neuropeltis), or the bracteoles may be much enlarged (e.g. Calystegia). Some Convolvuloideae have flowers with slight oblique disymmetry (Lefort 1951), while the zygomorphy of the flowers of Humbertia is largely positional, indeed, they are drawn as being polysymmetric by Pichon (1947). The sepals of Humbertia have five traces, but in Convolvuloideae there are fewer; secretory cells are apparently restricted to the flower in the former (Deroin 1993). The corolla tube of some Cuscuta and some other members of the family is strictly speaking a corolla-stamen tube, both contributing integrally to the tubular structure (Prenner et al. 2002). The infrastaminal scales found in Cuscuta may protect the nectar or the ovary (Riviere et al. 2013). Nectaries in the family, including those of Humbertia, are discussed by Deroin (1993). Weberling (1989) described the ovary as being fundamentally gynobasic, although with an apical septum. The diversity of style and stigma morphology in Cuscuta alone is as great as that in the rest of the family (e.g. Wright et al. 2011).
The seed coat is perhaps the most complex of that of any other euasterid, being up to about 30 cells thick and consisting of several types of cells, some much thickened and lignified; see Govil (1971), Kaur and Singh (1970, 1987) and Jayasuriya et al. (2008a, esp. 2009, the bulges and bulging cells and cell layers a bit confusing) for details. In Humbertia there is a thick layer of collapsed cells underneath the palisade layer; the testa of the seed examined showed no ligification (Deroin 1993).
There are a few, mostly old records of protein crystalloids in the nucleus (Speta 1977; Thaler 1966).
Cuscuta: For some anatomy, see Solms-Laubach (1867), for stomata, see Poisson (1874), for embryology, see Sastri (1956: embryo sac haustoria), see also Johri and Nand (1935: parietal cells), Tiagi (1951), and Vázquez-Santana et al. (1992), for seeds, etc., see Johri and Tiagi (1952); Sherman et al. (2008) for germination; and Welsh et al. (2010) for pollen. For hybridization, see García et al. (2014 and references). General references include Kuijt (1969), Heide-Jørgensen (2008), the Parasitic Plants website (Nickrent 1998 onwards) and the Digital Atlas of Cuscuta (Costea 2007 onwards).
For general information, see Staples and Brummitt (2007), Hoogland (1953b) and especially Convolvulaceae Unlimited, for chemistry, see Hegnauer (1964, 1989), Eich (2008) and Kaltenegger et al. (2013: homospermidine synthase and pyrrolizidine alkaloids), for successive cambia, etc., see Rajput (2016), etc., Rajput et al. (2008, 2014), for seed reserves, see G. Dahlgren (1991), for ovary morphology, see Deroin (1999b), for floral anatomy, Deroin (2004 and references), for embryology, see Raghava Rao (1940), Kaur (1969), Kaur and Singh (1970) and Yana and Rao (1993), for galactomannans and their like, see Kooiman (1971) and Reid (1985), for seedling morphology, see Austin (1973), and for the chloroplast ycf15 gene, see McNeal et al. (2007). Some information about Humbertia is taken from Pichon (1947) and K. Kubitzki and H. Manitz (pers. comm.), but the genus is poorly known, especially embryologically.
Phylogeny. The distinctive Humbertia is sister to the rest of the family (e.g. Refulio-Rodriguez & Olmstead 2014; García et al. 2014). Within the rest of the family, part of Poraneae (Cardiochlamyeae: Porana itself is polyphyletic), Erycibeae s. str., and a clade made up of all other Convolvuloideae form a basal trichotomy. Erycibe in particular can look very unlike other Convolvulaceae and herbarium specimens are often misidentified. Within the third clade, Ipomoea, Convolvulus, and their relatives form a clade that is sister to a rather unexpected clade made up of Poraneae, Cresseae, Dichondreae (with gynobasic styles), some Erycibeae (Maripeae), etc., as well as Jacquemontia. Several members of this latter clade have styles divided to the base or only an at most shortly connate style with long branches (but Jacquemontia, etc., have a long style), and leaf blades with more or less pinnate venation; Jacquemontia could be sister to the other taxa. Relationships in Z.-D. Chen et al. (2016: Chinese taxa) seem somewhat scrambled, but support is poor; for a morphological phylogeny of the family, see Austin (1998).
Despite the sequencing of over 6800 bp, the position of Cuscutoideae was unclear (Stefanovic & Olmstead 2001, 2004; Stefanovic et al. 2002 and esp. 2003), however, they may be close to a clade containing species with bifid styles (Wight et al. 2011). For relationships within Cuscuta, see e.g. Stefanovic et al. (2007), García and Martín (2007), Stefanovic and Costea (2008) and Braukmann et al. (2013); see Costea et al. (2015) for a summary tree. García et al. (2014) found that the predominantly Asian subgenus Monogynella was sister to the rest of the genus. Species limits in Cuscuta are difficult (Costea & Stefanovic 2009); see also Costea et al. (2011) and references.
Relationships within Convovuloideae are unclear. Merremieae - and Merremia itself - are not monophyletic, Ipomoeae being embedded in the former (Simões et al. 2015). Ipomoea is very much paraphyletic. Within it there is a well-supported spiny pollen clade that comprises some 50% of the larger Ipomoea clade (Manos et al. 2001a). There seem to be two main clades in a largely monophyletic Convolvulus, although C. nodiflorus did not link with the rest (Carine et al. 2004: sampling needs to be extended), however, perhaps mercifully, the latter is a species of Jacquemontia, and in an extensive study Williams et al. (2014) found that Calystegia was well embedded in the Convolvulus clade.
Classification. For the tribes above, some of which may be paraphyletic, see the useful classification in Stefanovic et al. (2003). What to do with Ipomoea - to split, or to lump (then Ipomoea = Ipomoeeae) - is difficult, and none of the options is without its drawbacks (Stefanovic et al. 2003). Simões and Staples (2017) suggest that Merremieae should no longer be recognised (the tribe is paraphyletic - Simões et al. 2015), but provide a reclassification of its members barring a few that it is still premature to place. Costea et al. (2015) provide an infrageneric classification (4 subgenera, 18 sections) for the speciose Cuscuta.
Thanks. To George Staples, for information, corrections, etc.
SOLANACEAE Jussieu, nom. cons. Back to Solanales
Herbs to shrubs, branching sympodial; hygroline alkaloids, oligosaccharides, (myricetin) +; roots diarch [lateral roots 4-ranked]; (hairs branched/stellate); wood commonly fluoresces; pits vestured; crystal sand +, esp. in stem; cystoliths +; stomata various; leaves simple to compound; flowers (4 merous), rotated 36o to axis; K often valvate; anthers often dehiscing by pores, or ± connate and pollen exiting communal apical hole, endothecial thickenings reticulate; often pseudo-4-locular, placentae swollen, stigma capitate or peltate, wet; ovules usu. many/carpel, ?epitropous, often campylotropous; embryo sac with chalazal haustorium; K ± accrescent; exotestal walls thickened usu. on inner periclinal and anticlinal walls, endotesta [= endothelium] ± persistent, walls ± lignified; cotyledons and radicle same width, cotyledons incumbent, oblique, to as little as 1/4 the length of the embryo; chromosomes usu. 1.5-5 µm long, protein bodies in nuclei.
102 [list]/2,460 - 8 clades below, but treatment needs work. World-wide, but overwhelmingly tropical America (map: from van Steenis & van Balgooy 1966; Meusel et al. 1978; van Balgooy 1984; Heywood 2007).
Age. Crown Solanaceae have been dated to (45-)41, 36(-32) m.y. (Wikström et al. 2001); Zamora-Tavares et al. (2016) think that they are as old as (82.4-)61.9(-47.8) m.y., Janssens et al. (2009) date them to 58±9.1 m.y., Paape et al. (2008) to ca 51 m.y., Olmstead and Tank (2017) to (65.3-)42.6(-21) m.y., and Bell et al. (2010) to (49-)38, 37(-29) m.y.a.; still younger estimates are around 35 m.y. (Dillon et al. 2009), and (34.0-)30.4(-26.3) m.y. (Särkinen et al. 2013: c.f. topology, see also Dupin et al. 2017).
Note, however, that most of these ages are questioned by the discovery of ca 52.5 m.y.o. fossils of Physalis from Argentina (Wilf et al. 2017); see also below.
1. Schizanthoideae Hunziker
Annual to biennial herbs; pyrrolidine alkaloids [hygrine, etc.], distinctive tropane alkaloids; cork cambium pericyclic; pericyclic fibres 0; flowers strongly monosymmetric, functional A developing before the C; K ± free, C cochleate, margins laciniate, abaxial pair connate, forming a keel; A 2 [abaxial-lateral], anthers explosive, staminodes 3; ektexine foot layet well developed; fruit a septicidal capsule; endosperm nuclear, copious, embryo curved, cotyledons 1/2> length embryo; n = 10.
1/12. Chile, adjacent Argentina. [Photo - Schizanthus Flower.]
Age. Crown-group Schizanthoideae have been dated to slightly over 5 m.y.o., certainly under 10 m.y.o. (Särkinen et al. 2013).
[Goetzeoideae ... [Schwenkioideae [Petunioideae [Nicotianoideae + Solanoideae]]]: K connate; ektexine foot layet not well developed; G oblique; endosperm helobial, nuclear?, cellular.
2. Goetzeoideae Thorne & Reveal
Trees to shrubs; (flowers single, terminal); pollen tricolpate, exine echinate, tectum perforate; fruit a capsule. seeds to 9/loculus, or 1-7-seeded berry; endosperm at most slight (copious - Tsoala), embryo straight, cotyledons large, fleshy (small - Tsoala); n = 12, 13.
6/8. Most Greater Antilles, but not Jamaica, east Brazil, Madagascar (Tsoala). [Photo - Flower.]
Synonymy: Goetzeaceae Miers
Age. A clade including Duckeodendron has been dated to (39-)35, 33(-29) m.y.a. (Wikström et al. 2001).
3. Duckeodendroideae Reveal
Large tree; wood with large, open, radial canals [c.f. Apocynaceae s. str.]; K, C quicuncial; pollen striate; 1 ovule/carpel; fruit a drupe, pericarp complex, seed 1; endosperm slight, embryo U-shaped, cotyledons very small; n = ?
1/1: Duckeodendron cestroides. Amazonian Brazil.
Synonymy: Duckeodendraceae Kuhlmann
4. Browallioideae Kosteletzky / Cestroideae Burnett
(Low concentrations pyrrolidine-type nicotinioids), (steroid alkaloids - Cestrum), (withanolides - Browallia); cork cambium superficial or deep-seated; bordered pits +; pericyclic fibres +; C cochlear; A 4 or 5, often didynamous, staminode +/0; G stipitate; (fruit fleshy); exotestal cells somewhat thickened on all walls - Cestrum; endosperm copious, embryo ± straight, cotyledons ca 1/4 length of embryo; n = (8-)11(-13), (chromosomes 6-14 µm long - Cestreae).
10/210: Cestrum (175). South, Central (and North) America.
4A. Reyesia C. Gay
Annuals to perennial subshrubs; cork cambium pericyclic; flowers single, weakly monosymmetric; A 4 or 2 + 2 adaxial staminodes, abaxial stamens with unequal divergent thecae; style spathulate apically, (hollow), stigma on margin; fruit a capsule; embryo coiled; n = ?
1/4. N. Chile, adjacent Argentina (map: from Hunziker & Subils 1979).
Synonymy: Cestraceae Schlechtendal, Salpiglossidaceae Hutchinson
[Schwenkioideae [Petunioideae [Nicotianoideae + Solanoideae]]] (if this clade exists): endothecial thickenings variable.
Annual herbs; pericycle fibres +; inflorescence a raceme, or with ± cymose branches; flowers monosymmetric; C valvate-conduplicate/induplicate, lobes 3-lobed; A 4, didynamous, or 2 + 3 staminodes; (G with 1 loculus, 1 ovule); endosperm copious to scanty, embryo ± straight, short to long; n = 10, 12.
4/31: Schwenkia (25). South America.
[Petunioideae [Nicotianoideae + Solanoideae]] (if this clade exists): low concentrations pyrrolidine-type nicotinioids; branching particularly distinctive [see below]; seeds flattened laterally [?level]; genome triplication.
Age. This node has been dated to (28-)25, 23(-20) m.y. (Wikström et al. 2001) or ca 28 m.y. (Särkinen et al. 2013). For dates of the genome triplication - anything from 95-39 m.y.a. or so - see Genes and Genomes below.
6. Petunioideae Thorne & Reveal
Herbs to shrubs; (polyhydroxylated nortropane alkaloids [calystegins] + - Brunfelsia); (cork deep-seated); bordered pits +; pericyclic fibres +(0); druses 0(+); (flowers monosymmetric); (K with hypodermal crystals); C cochlear, contorted, reciprocative [anterior C induplicate, covers other 4, conduplicate]; A 4(-5), usu. didynamous; fruit a capsule; embryo straight to slightly curved; n = 7-11.
13/160: Brunfelsia (45), Petunia (35). Central and South America.
[Nicotianoideae + Solanoideae]: stigma wet; (cotyledons accumbent); x = 12.
Age. The age of this clade has been estimated at ca 23.7 m.y. (Wu & Tanksley 2010; Y. Wang et al. 2008), (17-)14, 12(-9) m.y. (Wikström et al. 2001), (25.5-)24.0(-23.0) or ca 29 m.y. (Särkinen et al. 2013), ca 30.2 or 26.2 m.y. (Naumann et al. 2013), and (72.8-)44.7(-23.0) m.y. (Eserman et al. 2013).
7. Nicotianoideae Miers
Mostly (annual) herbs; (polyhydroxylated nortropane alkaloids [calystegins] + - Duboisia), pyrrolidine-type nicotinioids; pericyclic fibres +/0; (K with hypodermal crystals); C valvate-supervolute, contorted, conduplicate; A 4 (staminode +), 5, (didynamous); fruit a capsule, K at most weakly accrescent; endosperm copious, with small oil sector, embryo straight (curved), cotyledons short [at most 1/7 the length of the embryo]; n = 9, 10, 12, etc., 30, 31, etc..
8/125: Nicotiana (95). Mostly Australian, also North and South America, Africa.
Synonymy; Nicotianaceae Martynov
?. Benthamielleae Hunziger - ?where
Herbs to shrubs; C valvate-induplicate or contorted-conduplicate; (fruit partly loculicidal); <7 seeds/capsule; endosperm copious, embryo curved; n = 11./p>
3/15. Argentina, Chile.
?. Solandreae Miers (inc. Juanulloeae) - ?where
Lianes or shrubs, (epiphytic); (lamina margin entire), (venation indistinct); flowers often large; (G semi-inferior), (to 10-locular); n = ?
10/63. Tropical Central and South America, Caribbean, mostly Andean Ecuador and Colombia.
8. Solanoideae Kosteletzky
(Annual) herbs (to small trees); pyrrolidine alkaloids [hygrine, etc.], polyhydroxylated nortropane alkaloids [calystegins], withanolides + [substituted steroidal lactones]; pits not vestured; (interxylary phloem +); (crystal sand +) [level?]; C valvate, cochlear, contorted; A 5 (4), (heteranthy +), base of the filament [stapet] often enlarged, with lobes, etc.; (pollen surface striate - Anthocercis); (G 3, or subdivision of carpels into 1-seeded units, style gynobasic - Nolaneae); integument 7-13 cells across; fruit a berry (drupe), (circumscissile capsule - Hyoscyameae), (schizocarp - Nolaneae), (K very accrescent); (exotestal cells anticlinally elongated); endosperm cellular, ± copious, embryo curved, often coiled, (cotyledon incumbent, oblique); (n = 10-)12(15), chromosomes 1-14 µm long.
62/1,940: Solanum (1250-1700), Lycianthes (200), Lycium (90), Nolana (90), Physalis (90), Deprea (42). World-wide, but esp. South America and others N. temperate. [Photo - Flower, Iochroma Flower, Przewalkskia Fruiting Calyx.]
Age. The age of crown Solanoideae has been estimated to be (23.3-)21.0(-19.0) m.y. (Särkinen et al. 2013).
Fossils perhaps to be assigned to Solanoideae are dated at ca 33.9 m.y. (Martínez-Millán 2010).
Synonymy: Atropaceae Martynov, Browalliaceae Berchtold & J. Presl, Daturaceae Berchtold & J. Presl, Hyoscyamaceae Vest, Lyciaceae Rafinesque, Nolanaceae Berchtold & J. Presl, nom. cons., Sclerophylacaceae Miers
Evolution: Divergence & Distribution. For the identities of some Eocene fossils that are putatively solanaceous, see Millan and Crepet (2014) - none of them belongs. However, Wilf et al. (2015, esp. 2017) describe ca 52.2 m.y.o. fossils from Chubut, Argentina, which they place in crown Physalis; not only is this over twice the age of crown Solanoideae above, but the fossil is in a quite derived clade within the subfamily.
Solanaceae may have had a New World origin, with perhaps 8-9 dispersal events to the Old World (Tu et al. 2010; Dupin et al. 2017) - or, given the early Eocene age of the Patagonian fossil of Physalis, continental drift may have been involved in the early distribution of the family (Wilf et al. 2017). Olmstead (2013) suggested that ten clades were involved, but he could not find any connection between the likelihood of dispersal and disseminule type (dry versus fleshy). The Malagasy endemic Tsoala (Goetzioideae) was found to be sister to Metternichia, from Minas Geraes, Brazil (Särkinen et al. 2013: see add. file 2), and Janssens et al. (2015) suggested that long distance dispersal (America to Madagascar) was involved in setting up this disjuction.
The early-diverging clades in the family are currently temperate and/or Andean-South American in distribution, perhaps reflecting its original climatic preferences (Olmstead 2013: much more on possible niche conservatism here). The family is most diverse in the New World, particularly South America, where it grows in a variety of habitats, including along the foggy west coast, where it is particularly common - with ca 75 endemic species - in Lomas vegetation (Barboza et al. 2016). They are less common elsewhere, particularly in Africa.
Accepting the age estimates of Särkinen et al. 2013), there was a ca 20 m.y. "fuse" between the origination of the family and its crown-group diversification. The [Nicotianoideae + Solanoideae] clade includes ca 85% of the species in the family (Olmstead & Sweere 1994), and Schranz et al. (2012) suggested that there was a lag time between a duplication event that characterized this clade and its subsequent diversification, largely represented by the speciose Solanoideae with its fleshy fruits (see also Vanneste et al. 2014b). Bombarely et al. (2016) suggest that genes involved in pollination systems may have evolved considerably after the genome triplication event, hence contributing to the diversification of the clade with that triplication. Diversification in Solanaceae may be connected with a gene duplication in the family that Soltis et al. (2009) place as an apomorphy of the species-rich Solanoideae, although with hesitation - however, ages for the event vary (see Genes and Genomes below), and it may have nothing particularly to do with Solanaceae at all.
The crown-group age for the ca 1,500 species of Solanum (inc. tomato and eggplant) is a mere 15.5 m.y. or so (add Capsicum - ca 19.6 m.y.: Wu & Tanksley 2010; Y. Wang et al. 2008); Paape et al. (2008: see also estimates for other nodes) gave ages of (20.6-)16.1(-12.2) m.y., while (17.5-)15.5(-13.3) m.y. ((18.7-)17.0(-14.5 m.y.) - Jaltomata sister, (21.0-)19.1(-17.0) m.y. - Capsicum) are estimates in Särkinen et al. (2013, q.v. for much else). Adaptation in Solanum sect. Lycopersicon - the genus has ca 1,200 species - was linked to introgression, recruitment from ancestral variation, and de novo mutations (Pease et al. 2016).
For the evolution of Nolana, a speciose clade of the coastal deserts (lomas) in the Atacama Desert of western South America, see Dillon et al. (2009); the genus was perhaps originally from Peru. Nolana is the most speciose genus in this remarkable Peruvian-Chilean vegetation. Hyperarid deserts, i.e., with ≤5 mm rain/year, have been dated to ca 8 m.y.b.p., and a clade of Nolana invaded them ca 3.8 m.y.a., and another five clades rather later, ca 2 m.y.a. - interestingly, the region has been semiarid, with ≤250 mm rain/year, since the Late Jurassic ca 150 m.y.a. (Guerrero et al. 2013).
Vanneste et al. (2015) link the evolution of fruit fleshiness - especially evident in Solanoideae - in the family to the genome triplication event. L. Wang et al. (2015) discuss the development and evolution of fruit morphology in the family.
Ecology & Physiology. Solanaceae are an important component of understory vegetation in l.t.r.f. of the New World.
Pollination Biology & Seed Dispersal. Knapp (2002a, 2010) summarises information on pollinators and basic floral morphology of Solanaceae. J. Zhang and Zhang (2016) discuss the more frequent expression of monosymmetry in the androecium than in the corolla - almost twice as frequent in the former. More or less well developed monosymmetry is quite common and is of the 3:2 sort (see Eichler 1875; Robyns 1931; Cocucci 1989; Knapp 2002a; Ampornpan & Armstrong 2002). In the complex flowers of Schizanthus dehiscence of the two functional anthers is explosive (Cocucci 1989a). For floral evolution in the genus, not very speciose, see Pérez et al. (2006: midpoint rooting). Nierembergia (Petunioideae), with ca 21 species, has oil flowers (Coccucci 1991; Tate et al. 2009 for a phylogeny). It has recently been shown that the Carolina sphinx/tobacco hornworm, Manduca sexta is preferentially attracted to Nicotiana flowers that have a corolla tube the "right" length for its proboscis by volatiles produced by those flowers, but not those by flowers with tubes of different lengths - co-evolution (see Haverkamp et al. 2016), and/but what about other flowers the moth pollinates?
Within Solanoideae, the Andean Iochrominae are notably diverse florally and have a variety of pollinators, and there is significant variation in flower colour in both bee- and bird-pollinated species when in sympatry (Smith & Baum 2006; Muchhala et al. 2014). Zygomorphy and heteranthy, which in this context is really a kind of zygomorphy, have evolved several times in Solanum, also in other Solanoideae like Sclerophylax, etc. (Bohs et al. 2007). In heteranthous flowers some of the anthers are feeding anthers, while others deposit pollen on the pollinator in such a way that pollination can take place (Stern & Bohs 2012). Buzz pollination is common in Solanum (see Teppner 2005: pollination of the tomato; Harter et al. 2002; García et al. 2008), and over a million pollen grains can be produced by a single flower (Anderson & Symon 1988); the corolla is often rotate, the flowers lack nectar and the anthers dehisce by terminal pores, all features of buzz-pollinated flowers. A number of species of Cyphomandra (= S. subgenus Leptostemon) are pollinated by orchid bees that collect fragrances from the connectives, simultaneously pushing against the thin walls of the anthers which behave as little bellows, directing jets of pollen on to the bees (Sazima et al. 1993). A number of Solanoideae have capillary nectary grooves on the bases of the petals along which nectary moves, sometimes to dark spots on the corolla whence it can be removed (Dong et al. 2013). For the evolution of floral scent, see Martins et al. (2007).
The common ancestor of Solanaceae is likely to have had RNase-based gametophytic self incompatibility (SI) (Paape et al. 2008), and self-compatability (SC) has since evolved many times, but never SI from SC; for a detailed study of the frequent loss of gametophytic incompatibility in Solanaceae, see Igic et al. (2006). Overall diversification of SI clades is greater than that of SC clades, yet SC species are frequent perhaps because of the frequency of the SI → SC transition and high speciation within those clades - and high extinction rates (Goldberg & Igic 2012: scoring of dioecious taxa?; Goldberg et al. 2010), although other models fit the data (Bromham et al. 2015b). The evolution of polyploidy and self-compatibility in the family are correlated (Miller at al. 2008; Roberston et al. 2010), interestingly, there was effective dispersal of SI Lycium to Africa, with subsequent restoration of diversity of SI alleles following the dispersal-caused bottleneck (Miller et al. 2008).
How seeds are dispersed very much follows what fruit morphology might suggest (see Knapp 2002b for a summary). In the New World, Solanum in particular, with its relatively nutritious fruits, is an important food source for Sturnira, a phyllostomid bat (Fleming 1986; Lobova et al. 2009 for records). The bats are slow feeders and spit out seeds, fibre, etc.; Solanum, like other bat-dispersed taxa in the New World, tend to be early successional plants (Muscarella & Fleming 2008), and the altitudinal ranges of the bats and plants are similar (Fleming 1986). The berries of Solanum sect. Gonatotrichum are explosive... (Stern & Bohs 2012).
Plant-Animal Interactions. Most Solanaceae synthesize a variety of metabolites including nicotinoids, capsaicinoids, steroidal alkaloids, and withanolides of varying degrees of toxicity that defend the plant against herbivores (Wink 2003). Nevertheless, New World Solanaceae are eaten by larvae of some 360 species of Nymphalidae-Danaeinae-Ithomiini (or Ithomiinae) butterflies alone, and they seem to have switched host plants from Apocynaceae q.v., perhaps Parsonsieae in particular, although they also est a few Gesneriaceae (Ehrlich & Raven 1964; Edgar 1984; Drummond & Brown 1987; Willmott & Freitas 2006). There seem to be no records of caterpillars eating Schizanthoideae, Goetzeoideae and Schwenkioideae, and Solanum is particularly favoured (Garzón-Orduña et al. 2015 and references). Strict co-evolution seems not to be involved, but the diversification rate of the butterflies seems to have temporarily increased with this shift (Fordyce 2010), although this shift occurred within a larger clade of butterflies that utilizes Solanaceae (Hamm & Fordyce 2015). The mimicry rings in which Ithomiini are involved may be associated with particular solanaceous host plants (Willmott & Mallet 2004). Solanum itself is especially important as a food source for ithomiine caterpillars (ca 70% records of neotropical Solanaceae food sources, ca 89% those of all Ithomiini: Willmott & Freitas 2006; see also Brower et al. 2006). Most species of Solanaceae even in more diverse communities are eaten by ithomiine larvae, perhaps suggesting that the host plant niche is almost saturated by the butterfly (Willmott & Elias, in Elias et al. 2009).
However, the timing of this ithomiine radiation is problematic. The move onto Solanaceae has been estimated as happening 46-37 m.y.a. (Nylin et al. 2013 and references), with diversification beginning at middle elevations on the Andes in the middle Miocene some 15 m.y.a.; Solanaceae are common all along the Andes today (Elias et al. 2009). Wahlberg et al. (2009) had suggested that Ithomiini were (40.3-)37.1(-34) m.y. old. Using calibrations derived from the Solanaceae phylogeny of Särkinen et al. (2013), Garzón-Orduña et al. (2015: Nylin et al. not mentioned) estimated that the ages for nodes within Ithomiini in particular were about half the ages of those suggested by Wahlberg et al. (2009). In particular, the age of a major ithomiine clade [Mechanitina—Godyridina, see Garzón-Orduña et al. 2015) for which feeding on Solanum may be basal was estimated at around 30 m.y. by Wahlberg et al. (2009), far older than estimated ages of Solanum, some ages above being (20.6-)16.1, 15.5(-12.2) m. years. These younger ages were not only consistent with host-plant ages (not surprisingly), but they fit scenarios of Andean uplift better. But if there are 52 m.y.o. fossils of crown Physalis from Argentina (Wilf et al. 2015, esp. 2017), what then?
Some ithomiine larvae are distasteful because of the alkaloids, etc., in the leaves they eat (confirm: any sequestration is much less common than was first thought: Drummond 1986), and the noxious solanaceous chemicals also guide oviposition by adults and the feeding preferences of the larvae: "Though the butterflies may be able to recognise their food plants, biologists have greater difficulty in Solanaceae identification" (Brown 1987: p. 373). Ithomiine butterfies are also distasteful because of the 1,2-dehydropyrrolizidine alkaloids that the adults obtain mostly from Apocynaceae, Heliotropaceae and Asteraceae-Asteroideae (especially Eupatorieae), which also may be precursors to the pheromones that they produce. The butterflies are quite palatable immediately after hatching, but that soon changes, and massive amounts (to ca 20% dry weight) of these chemicals may be sequestered (Brown 1987). Interestingly, Ithomiini preferentially visit bait with withered flowers, while Arctiinae moths, who also go after these alkaloids, prefer crushed roots.
Tobacco hornworm caterpillars prefer members of the [Solanoideae + Nicotianoideae] clade as food sources, although they didn't like Nicandra much; they died on Petunia, and didn't grow on Browallia and Brunfelsia. Other plant feeders show similar distinctive patterns (e.g. Fraenkel 1959), thus other sphingids are found here and on Oleaceae (Forbes 1958). Rauscher and Huang (2015) note that a gene duplication of the threonine deaminase in Nicotianoideae and Solanoideae is involved in herbivore defence, sometimes by depleting threonine in the gut of the caterpillar; selection on this gene may have been very prolonged, around 25 m.y. or far more. Phytophagous Chrysomelidae beetles (perhaps especially Criocerinae) are notably more common on New World than Old World Solanaceae, perhaps because the beetles first used the family as a food source in the former area (Jolivet & Hawkeswood 1995; see also Hsiao 1986); Criocerinae may have moved onto Solanaceae from monocots. Chrysomelinae and Megalpodinae are also found on New World Solanaceae (Jolivet 1988). The larvae are covered by faecal shields (Vencl & Morton 1999; see Gómez-Zurita et al. 2007). Finally, in Solanum dulamara nectar exudes from wounds and attracts ants that protect the plant against herbivores; this composition of this exudate, largely sucrose, differs from that of phloem sap which contains other sugars, amino acids, etc., and, like extrafloral nectar itself, wound secretions are induced by jasmonate (Lortzing et al. 2016; also Heil et al. 2015, see also Fagaceae). Solanaceae have multiple lines of defence and are avoided by most insect herbivores (Harborne 1986; Hsiao 1986).
Touch-sensitive trichomes are common in Solanoideae (or perhaps they have simply been most studied here), and glandular hairs are common, as well as many other hair types (see Seithe 1962; Seithe & Sullivan 1990 and references for hair morphology, esp. in Solanoideae). Insect-deterrent secretions are produced when the sensitive hairs are brushed by the insect; the secretions may contain poisonous/deterrent metabolites such as sequiterpenes, or they may rapidly oxidise and become sticky, so trapping and killing small insects, or they hydrolyse, and attract insects that then target caterpillars eating the plant (van Dam & Hare 1998 and references; Kellogg et al. 2002; Weinhold & Baldwin 2011; Bleeker et al. 2011). Mutants of tomatoes lacking the protective metabolites have been found to be susceptible to herbivory in the field (Kang et al. 2010). There is another wrinkle to the possession of dense, glandular trichomes that is common in the family (Glas et al. 2012) - mirid bugs of subtribe Dicyphina in particular are able to walk easily on the plant despite these hairs and may eat the trapped insects (Wheeler & Krimmel 2015); nitrogen may be taken up by the leaf (Spomer 1999).
Bacterial/Fungal Associations. The distinctively pungent capsaicanoids of chilis (Capsicum spp.) are involved in the protection of the fruit against the fruit-destroying Fusarium fungus (Tewksbury et al. 2008). Capsaicins can be synthesized by the ascomycetous endophytic fungus Alternaria (Devari et al. 2014).
Genes & Genomes. A genome duplication event in Solanaceae has been dated to ca 50-52 m.y.a. (Schlueter et al. 2004) or (64.8-)63.7, 59.6(-57.5) m.y.a. (Vanneste et al. 2014b). A genome triplication (?the same) has been dated at (90.4-)71(-51.6) m.y. (Tomato Genome Consortium 2012) or at least 30 m.y.a. (Bombarely et al. 2016). And another duplication event at 23-18 m.y. (Blanc & Wolfe 2004). Thus F. Wu et al. (2006) dismissed the possibility that there had been a genome duplication either on the branch leading to or within Solanaceae (see also Robertson et al. 2010), although they also allowed the possibility of a duplication well before the the divergence of Solanales and Gentianales - perhaps the γ whole nuclear genome duplication/gamma triplication of the core eudicots (see also Bombarely et al. 2016)?
Interestingly, Petunia and Hyoscyamus, Petunioideae and Solanoideae respectively, can be intergrafted (Taiz & Zeiger 2006).
F. Wu and Tanksley (2010) reconstructed the ancestral genome of the [Nicotianoideae + Solanoideae] clade and the various changes that have occurred in the genomes of Nicotiana, tomato, pepper, etc.. Cybrids, cytoplasmic hybrids containing genome(s) of both species, have been formed between Nicotiana tabacum and Hyoscyamus niger, Nicotianoideae x Solanoideae (Sanchez-Puerta et al. 2014), the two diverging (90.4-)71-12(-9) m.y.a. (see above)! Within Nicotiana, there has been reticulate evolution both at the diploid and polyploid level, as was evident in an attempt to understand the origin of allopolyploid species of the section Suaveolentes (Kelly et al. 2012); for hybridization in the genus, see Soltis et al. (2016b and references). See also Knapp et al. (2004b).
One or more functional genes from Agrobacterium rhizogenes are found in many, but not all, species of Nicotiana and may have coevolved with the plant genome (Intrieri & Buiatti 2002); horizontal gene transfer is relatively quite common in Solanaceae (Talianova & Janousek 2011). It has also occurred quite extensively and recently in the mitochondrial Cox-1 intron both within the family and from outside (Sanchez-Puerta et al. 2011).
Arabidopsis-type telomeres are absent from some Browallioideae (Sýkorová et al. 2003a). Cestreae in particular, which lack these telomeres, have chromosomes that at 7.21-11.51 µm long are considerably larger than those of the rest of the family, which are much smaller, e.g. 1.5-3.52 µm long in Nicotianoideae (Acosta et al. 2006; Tate et al. 2009). The genome of Solanum-Cyphomandra, at 2C = 49.6 pg DNA, is the most massive of any woody angiosperm (Schneider et al. 2015).
Economic Importance. Chillies (Capsicum annuum) were domesticated in Mexico, quite possibly in a number of places (Aguilar-Meléndez et al. 2009); other species of the genus are also economically important (Perry et al. 2007 and references). For information on potatoes, see Spooner et al. (2014). For the domestication of the tomato, see Bai and Lindhout (2007) and for its phylogeny, see Pease et al. (2016) - much reticulation, none of the 2,743 100 kb segments of the transcriptome gave the species tree...
Chemistry, Morphology, etc. Lycium is recorded as accumulating glycine betaines, and some members at least are halophytic (Levin & Miller 2005). For alkaloids in Datureae, see Doncheva et al. (2006), and for withanolides, see Burton and Oberti (2000), Chen et al. (2011) and Pigatto et al. (2014). Schizanthoideae have distinctive tropane alkaloids (Hunziker 2001).
Unusual stomata with degenerate guard cells have often been reported in the family (Cammerloher 1920; D'Arcy & Keating 1973).
Leaves in the fertile part of the stem of Solanaceae, perhaps especially in Solanoideae, are often geminate and/or branching is not simply axillary; Petunia can have ordinary-looking cymose inflorescences, but Schwenkia, Schizanthus and many other taxa have more or less recaulescent bracts, only one branch of the cymose inflorescence is developed at each node, or the two branches develop in different ways, etc.. This makes interpretation of the construction of the plant difficult (see especially Danert 1958, 1967; Child & Lester 1991 for a brief summary; Bell & Dines 1995 and Lippman et al. 2008, branching of inflorescence). Castel et al. (2010) suggest similarities between inflorescences of at least members of Petunioideae and Solanoideae; they note that the absence of bracts here may be only apparent. The growth pattern of Nolanaceae (= Nolaneae) is very like that of other Solanoideae (see also Eichler 1874). Goetzea has an odd growth pattern; its leaves are rather xeromorphic.
For floral development, see Ampornpan (1992), for some floral anatomy, see Armstrong (1986). Knapp (2010) surveyed the considerable floral diversity in Solanaceae. The calyx and corolla are often open in development (Baehni 1946). Heterotopy of a foliar gene may be involved in the development of the notably inflated calyx surrounding the fruit in Physalis (He & Saedler 2007; c.f. Hu & Saedler 2007); inflated calyces occur in some nine genera, although details of the pattern of their acquisition - and perhaps also loss - are unclear. In floral development, petal and stamen primordia together are lifted by zonal growth and the carpel primordia develop on a flat apex; in this respect there are some similarities between Solanaceae, Scrophulariaceae and Gesneriaceae, few with Montiniaceae (Huber 1980: 66-69; Ronse Decraene et al. 2000). For floral development in Datureae, see Yang et al. (2002). The flowers of Nolana have two long and two short stamens. There is considerable variation in corolla aestivation in the family (Ampornpan 1992). The patterns of endothecial thickenings in the family are very diverse (Carrizo García 2002), and quite large and complex stigmas are common (Cocucci 1991, 1995).
The two carpels so common in Solanaceae (but Nicandra has 3-5) are often in the plane determined by the first sepal initiated; this is one of the abaxial pair but is somewhat off the median (= bract-determined) plane. Indeed, the basic plane of symmetry in flowers like Salpiglossis and Schizanthus is oblique/inverted, and the abaxial (and also two adaxial) stamens are sterile (see also Ampornpan & Armstrong 2002 for flowers of Salpiglossis, G median, odd K and staminode abaxial). The complex flower of Schizanthus is described as having oblique rather than inverted symmetry (Cocucci 1989b: functionally equivalent), but c.f. Ampornpan 1992: p. 87, "Schizanthus bipinnatus showed no indication of any oblique orientation of either type" - i.e. when the abaxial sepal is slightly oblque to the subtending bract and/or flowers are displaced by growth of axillary buds and Walters 1969: p. 17 " the gynoecium was "oriented obliquely to the symmetry of the corolla"). For CYC gene expression here, see Preston et al. (2011b). Nolaneae, often separated from Solanaceae because of their distinctive gynoecium, have five carpels borne opposite the petals, but their number secondarily increases; stamen and petal number are unaffected.
Androgenesis, an uncommon condition in which the male gamete in maternal cytoplasm produces an embryo, has been recorded for at least Petunia, Nicotiana, and Capsicum, in Petunioideae, Nicotianoideae and Solanoideae respectively (Chat et al. 2003 for references).
For generic descriptions and much else, see Hunziker (2001) and Barboza et al. (2016); Goodspeed (1954) remains the classic account of Nicotiana. For general chemistry, see Hegnauer (1973, 1990, also 1966, 1990 as Nolanaceae) and Eich (2008), for the evolution of secondary metabolites, see Wink (2003 and references), and for calystegines (tropane alkaloids), see Dräger (2004), and for wood anatomy, see Carlquist (1987a, 1988a) and Jansen and Smets (2001: vestured pits - do Petunioideae and Nicotianoideae have them?).
For floral vascularization, see Liscovsky et al. (2009 and references), for floral development, see Sattler (1977), for floral and inflorescence morphology, see Huber (1980), for nectaries, see Vogel (1998b), for pollen morphology of zygomorphic taxa, see Stafford and Knapp (2006: not integrated with phylogeny), of Hyoscyameae, see Z.-Y. Zhang et al. (2009), and of Nolana and relatives, Gavrilova (2014), for embryology, see di Fulvio (1969: Nolana), for fruit anatomy, see Pabon Mora and Litt (2007), for seed coat morphology and development, see Souèges (1907: he described the chalazal end of the embryo sac as herniating), for seed coat and embryo, see Wojciechowska (1972: European/cultivated taxa), and for chromosome numbers in Solanoideae, see Robertson et al. (2010) and Chiarini et al. (2010) and in Cestrum et al., see Las Penas et al. (2006). For details of the distinctive Sclerophylax, see di Fulvio (1961).
Phylogeny. Relationships along the spine of Solanaceae are poorly known; for early studies, see Olmstead & Palmer (1992) and Fay et al. (1998b). The grouping [Petunioideae [Solanoideae + Nicotianoideae]] is well supported in Olmstead et al. (1999), although less so in Olmstead and Santiago-Valentin (2003); see also Särkinen et al. (2013). However, in the summary tree of Olmstead and Bohs (2007), immediately below the clade [Solanoideae + Nicotianoideae] was a polytomy including Petunioideae, Cestroideae and Schwenkioideae (see Dillon et al. 2009 for another topology). Relationships between these latter clades had only weak support; Schwenkia might be sister to the rest of the family (Olmstead et al. 1999). However, using the nuclear gene SAMT (salicylic acid methyl transferase), Martins and Barkman (2005) found Schizanthus in this position, and with rather strong support (see also Olmstead & Sweere 1994), with Schwenkia weakly linked with Cestroideae (see also Olmstead & Bohs 2007), yet Schizanthus has also been strongly associated with Nicandra (Zamora-Tavares et al. 2016: ?sampling). A Goetzioideae clade has included Duckeodendron as sister to the rest, but with only moderate support (Santiago-Valentin & Olmstead 2001, 2003); here Duckeodendron is left unaffiliated. Wu et al. (2006) found a strongly supported grouping of [Solanoideae [Petunioideae + Nicotianoideae]], and although in this case no other clades of the family were included, the sequences analyzed came from ten orthologous loci each on a different chromosome. The two-gene tree in a study by Olmstead et al. (2008) is rather like that of Martins and Barkman (2005): [Schizanthoideae [Goetzioideae, Duckeodendron [[Cestroideae/Browallioideae, including Benthamiella et al.; their relationships have previously been unclear], Petunioideae, Schwenckioideae [Nicotianoideae + Solanoideae]]]], but support is strong for relationships between the last pair of taxa alone. Särkinen et al. (2013) added Reyesia to the taxa at the base of the tree whose inter-relationships are uncertain. Indeed, in this last study, [Petunioideae + Nicotianoideae] was the only well supported clade along the spine, although there was a weakly supported [Schwenkieae, Petunioideae, Cestroideae], even if in the latter it was unclear if Benthamiella was to be included. In a tree used for dating, clades including Cestrum, Browallia, Benthamiella, etc. and Schizanthus, Duckeodendron, etc., were successively sister to the rest of the family, made up of [Petunioideae [Nicotianoideae + Solanoideae]] (Särkinen et al. 2013: for details of the phylogeny, see add. file 2; Dupin et al. 2017).
Petunioideae. For the phylogeny of Brunfelsia, which moved to the Antilles, where it radiated, from South America, see Filipowicz and Renner (2012). Nicotianoideae. For a phylogeny of Nicotiana, sister to the largely Australian Anthocerideae, see Clarkson et al. (2004); the eastern Andean section Tomentosae are sister to the rest of the genus.
Solanoideae. The limits of Solanum are to be expanded to include Cyphomandra and Lycopersicon (see Bohs 2005, 2007; Levin et al. 2006; Weese & Bohs 2007 [three genes, S. thelopodium sister to the rest, or unresolved in Bayesian analysis], Poczai et al. 2008; Särkinen et al. 2013, 2015: Thelopodium sister to the rest). Relationships within the speciose subgenus Leptostemonum, characterised by stellate hairs and prickles, are outlined by Stern et al. (2011) and Vorontsova et al. (2013: African taxa); there have been three invasions of the Old World (Aubriot et al. 2016a). Särkinen et al. (2015) tackle relationships within the large black nightshade clade (morelloid Solanum species). Tepe et al. (2016) discuss relationships in the potato clade, made up of ca 11 sections and 194 species, most of which are in section Petota which includes the potato, Solanum tuberosum, although at around 112 species section Petota is less than half the size it was twenty five years ago. Jaltomata is sister to Solanum; major clades in the former genus are characterised by fruit colour (Miller et al. 2011). For relationships within the distinctive Nolana, see Tago-Nakawaza and Dillon (1999), Dillon et al. (2007, 2009), Tu et al. (2008) and Guerrero et al. (2013); N. sessiliflora may be sister to the rest of the genus. Lycium may be paraphyletic and will need to be expanded to include Phrodus and Grabowskia (Levin & Miller 2005; Levin et al. 2007; Levin et al. 2009). Relationships around Physalis are still poorly understood (Whitson & Manos 2005; Zamora-Tavares et al. 2016). The distinctive Sclerophylax is to be included in Solanoideae (Olmstead et al. 2008). Orejuela et al. (2017) discuss relationships in Solandreae; those along the spine are not well supported making generic delimitation a perilous occupation.
Classification. For the main outlines of the classification above, see Olmstead et al. (2008). For the circumscription of Lycium, see Levin et al. (2011). Knapp et al. (2004a) provide an infrageneric classification of Nicotiana that deals with the hybrid origin of some clades; these are put in sections separate from those to which their parents belong. Solanaceae Source includes information currently mostly about Solanum, but its coverage will expand.
Previous Relationships. Hutchinson (1973) placed Duckeodendraceae in Boraginaceae, but doubtfully; Cronquist (1981) kept it as a poorly-known family; Takhtajan (1997) placed it as a separate family in Solanales. Its carpels are oblique to the main axis of the flower (Kuhlmann 1934), as is appropriate for Solanaceae.