EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, initially ±globular, not motile, branched; showing gravitropism; acquisition of phenylalanine lysase* [PAL], flavonoid synthesis*, 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, growth 3-dimensional*, cuticle +*, plane of first cell division transverse [with respect to long axis of archegonium/embryo sac], sporangium and upper part of seta developing from epibasal cell [towards the archegonial neck, exoscopic], with at least transient apical cell [?level], initially surrounded by and dependent on gametophyte, placental transfer cells +, in both sporophyte and gametophyte, wall ingrowths develop early; suspensor/foot +, cells at foot tip somewhat haustorial; sporangium +, single, terminal, dehiscence longitudinal; meiosis sporic, monoplastidic, MTOC [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 [1C] <1.4 pg, main telomere sequence motif TTTAGGG, KNOX1 and KNOX2 [duplication] and LEAFY genes present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes [precursors for starch synthesis], tufA, minD, minE genes moved to nucleus; mitochondrial trnS(gcu) and trnN(guu) genes +.
Many of the bolded characters in the characterization above are apomorphies of 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.
Sporophyte well developed, branched, branching apical, dichotomous, potentially indeterminate; hydroids +; stomata on stem; sporangia several, terminal; spore walls not multilamellate [?here].
TRACHEOPHYTA / VASCULAR PLANTS
Sporophyte long lived, cells polyplastidic, photosynthetic red light response, stomata open in response to blue light; plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; plant endohydrous [physiologically important free water inside plant]; PIN[auxin efflux facilitators]-mediated polar auxin transport; (condensed or nonhydrolyzable tannins/proanthocyanidins +); xyloglucans with side chains uncharged [?level], in secondary walls of vascular and mechanical tissue; lignins +; roots +, root hairs and root cap +; stem apex multicellular [several apical initials, no tunica], with cytohistochemical zonation, plasmodesmata formation based on cell lineage; vascular development acropetal, tracheids +, in both protoxylem and metaxylem, G- and S-types; sieve cells + [nucleus degenerating]; endodermis +; stomata numerous, involved in gas exchange; leaves +, vascularized, spirally arranged, blades with mean venation density ca 1.8 mm/mm2 [to 5 mm/mm2], all epidermal cells with chloroplasts; sporangia 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; archegonia embedded/sunken [only neck protruding]; suspensor +, shoot apex developing away from micropyle/archegonial neck [from hypobasal cell, endoscopic], root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Sporophyte growth ± monopodial, branching spiral; roots endomycorrhizal [with Glomeromycota],lateral roots +, endogenous; G-type tracheids +, with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangium dehiscence by a single longitudinal slit; cells polyplastidic, MTOCs diffuse, perinuclear, migratory; blepharoplasts +, paired, with electron-dense material, centrioles on periphery, male gametes multiciliate; nuclear genome size [1C] = 7.6-10 pg [mode]; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; mitochondrion with loss of 4 genes, absence of numerous group II introns; LITTLE ZIPPER proteins.
Sporophyte woody; stem branching 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 R-Put-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 randomly oriented, 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; T +, petal-like, each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], each theca dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, endothecium +, cells elongated at right angles to long axis of anther; tapetal cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine lamellate only in the apertural regions, thin, compact, intine in apertural areas thick, pollenkitt +; nectary 0; carpels present, superior, free, several, spiral, ascidiate [postgenital occlusion by secretion], stylulus at most short [shorter than ovary], hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry; suprastylar extragynoecial compitum +; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across, nucellar cap?; megasporocyte single, hypodermal, functional megaspore lacking cuticle; female gametophyte lacking chlorophyll, four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; ovule not increasing in size between pollination and fertilization; pollen grains bicellular at dispersal, germinating in less than 3 hours, siphonogamy, pollen tube unbranched, growing towards the ovule, between cells, growth rate (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 gametophytes tricellular, gametes 2, lacking cell walls, ciliae 0, 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 +, ?diploid, 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 [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 monosporic [spore chalazal], 8-celled, bipolar [Polygonum type], 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] (present).
[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, often with median adaxial ridge and inflexed apex ["hooded"]; 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 Lamiales, see discussion under Gentianales.
LAMIALES Bromhead Main Tree.
Cornoside, verbascosides [caffeoyl phenylethanoid glucosides (CPGs), caffeic acid esters, = acteosides], methyl- and oxygenated flavones +, iridoids 0; eglandular hairs multicellular; leaves opposite; inflorescence cymose/determinate/closed; K connate; anther sacs with placentoids; chalazal endosperm haustorium +, cotyledons incumbent; protein bodies in nuclei; mitochondrial coxII.i3 intron 0. - 24 families, 1,059 genera, 23,810 species.
Age. Estimates of the age of crown-group Lamiales are about 61.5 m.y.a. (Tank et al. 2015: Table S2), 77 m.y. (Magallón et al. (2015), (96-)87(-77) m.y. (Wikström et al. 2015), (105.3-)93(-80.5) m.y. (Tank & Olmstead pers. comm.), ca 97 m.y. (K. Bremer et al. 2004a), 100.6-97.5 m.y.a. (Nylinder et al. 2012: suppl.), and (104-)101.6(-98.2) m.y. (Roalson & Roberts 2016).
Note: Boldface denotes possible apomorphies, (....) denotes a feature common in the clade, exact status uncertain, [....] includes explanatory material. Note that the particular node to which many characters, particularly the more cryptic ones, should be assigned is unclear. This is partly because homoplasy is very common, in addition, basic information for all too many characters is very incomplete, frequently coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there are the not-so-trivial issues of how character states are delimited and ancestral states are reconstructed (see above).
Evolution: Divergence & Distribution. Lamiales contain ca 12.3% eudicot diversity. Most of this diversity is concentrated in families whose members are herbaceous to shrubby and have rather large, monosymmetric flowers, and about half have fruits with many rather small seeds (Sims 2013), and although about half the species have only eight or fewer seeds per fruit, they are not very big.
For a useful general discussion, including suggestions of apomorphies for some clades, see Soltis et al. (2005b); Kadereit (2004b) provided a summary of the order and its evolution. Endress (2011a) suggested that a key innovation somewhere in Lamiales was tenuinucellate ovules. Ovule number is notably variable in the basal clades and will be difficult to optimize. The four clades that are successively sister to other Lamiales either lack iridoids or have iridoids distinctively different (Oleaceae) from those in the other members of the clade, so iridoid (re)aquisition is pegged well within Lamiales; whether or not Carlemanniaceae have iridoids is unknown.
Taxa with 4-merous or predominantly 4-merous flowers are common in the basal pectinations of the Lamiales tree (see also Mayr & Weber 2006). Carlemanniaceae have both 4- and 5-merous flowers, while Calceolariaceae, on the other hand, have 4-merous flowers, each lip representing two completely connate petals, although some have interpreted their flowers as being 5-merous (Mayr & Weber 2006 and references). Monosymmetry is unlikely to be plesiomorphic in the order (c.f. Ronse de Craene 2010 and references), but it is very interesting that the evolution of corolla asymmetry has happened in a stepwise fashion, and may be evident as early (branching-wise) as in Oleaceae (Zhong & Kellogg 2015). Floral evolution in basal Lamiales is not simple, and where changes in floral meristicity and floral symmetry are to be placed on the tree is unclear.
Endress (2001b) suggested that families such as Orobanchaceae, Lamiaceae and Acanthaceae form a clade with strongly monosymmetric flowers that mostly lack a staminode, but such a grouping is not obviously consistent with the relationships being recovered. The tree in Magallón et al. (2015) has numerous ages for nodes in this clade, but their topology (see below) differs from that used here.
Confirmation of the phylogenetic positions of Carlemanniaceae, placed sister to Oleaceae, and of Plocospermataceae, as well as studies of their anatomy, chemistry, floral development, etc., and also resolution of relationships within Oleaceae, are important for understanding the evolution of the chemistry and floral morphology in particular of Lamiales as a whole (c.f. Endress 2001). Thus, given their position, one might expect Carlemanniaceae to lack iridoids - at least, to lack route II decarboxylated iridoids - and to have only a single (micropylar) endosperm haustorium. As might be anticipated, there is little morphological support for internal nodes in much of Lamiales and also for several of the families, and this is likely to be true whatever the relationships in the order.
For the complex pattern of variation in a number of other characters in this part of the tree, see the Gentianales page.
Ecology & Physiology. Carnivory, direct or indirect, has arisen three times in Lamiales (Lentibulariaceae, Byblidaceae, Plantaginaceae), and Martyniaceae may also be carnivorous.
Genes & Genomes. The pattern of duplication of the FLO=LFY and DEF=AP3 genes within Lamiales is largely congruent with the relationships discussed above; duplication occurred in the representatives of Phrymaceae, Verbenaceae, Paulowniaceae and Orobanchaceae examined, but not in those of Plantaginaceae or Oleaceae (Aagard et al. 2005).
Chemistry, Morphology, etc. For other characters that may clarify the relationships of Lamiales, see Gentianales.
A great deal of work on characterising iridoids and understanding their distribution in Lamiales has been carried out by S. R. Jensen and collaborators. The presence of cornosides and iridoids in Lamiales is largely mutually exclusive, except in Martynia louisiana (Jensen 1992, 2000a, 2000b). Verbascoside, a disaccharide derivative of the hydroxycinnamic acid, caffeic acid (= caffeoyl phenylethanoid glycoside), is common. It and trisaccharide derivatives (over 325 structures altogether - S. R. Jensen, pers. comm.) are phenylpropanoid glycosides, a class of compounds usually with a central glucose, a C6C2 unit, commonly dihydroxyphenyl-ß-ethanol, and a C6C3 unit, hydroxycinnamic acid (Mølgaard & Ravn 1988). Such compounds are very rarely found elsewhere; an exception is Cassinopsis (Cometa et al. 1993), which is sister to all other Icacinaceae (Byng et al. 2014; Stull et al. 2015).
Nodal anatomy needs study. Neubauer (e.g. 1977, 1978) suggested that the single trace often divided immediately into three or more, and this nodal type is indeed common in the order. Bailey (1956) recorded 2:2 nodes in Lamiaceae, and other nodal morphologies occur, e.g. in Gesneriaceae, Bignoniaceae, etc. Intermediary cells with distinctive plasmodesmata associated with the ultimate leaf veins may be plesiomorphic in Lamiales; their presence is linked with the transport of raffinose and stachyose, oligosaccharides commonly found in phloem exudate in the order (Turgeon et al. 2001; Turgeon 2010a). Leaf teeth have a glandular apex, with one accessory vein proceeding into the tooth, the other going above it.
Taxa with tricellular pollen grains are scattered throughout the order. For integument thickness, for which I have no generally comparable information but which may be of systematic importance, see also Hjertsen (1997) and Fischer (2004b). A chalazal hypostase is common - e.g. Buddleja, some "scrophs" - but the level of this feature is unknown. Oleaceae seem to have a rather diferent embryo development from that of other Lamiales studied (Yamazaki 1974). A long, narrow suspensor may be common in Lamiales (di Fulvio 1979; Maldonado de Magnano 1987), but I do not know the general distribution of this character - it is certainly not found in Loganiaceae. Details of endosperm development and of endosperm haustoria are variable, but there is little obvious phylogenetic signal in the former. Thus endosperm development in Orobanchaceae is overall rather similar - four cells or nuclei at the micropylar end, two at the chalazal - but in Bignoniaceae, Incarvillea differs greatly from the rest, as does Gratiola (Plantaginaceae) from other ex-Scrophulariaceae s.l. (see e.g. Mauritzon 1935a; Krishna Iyengar 1940a, 1942 and references). The seed is ruminate in various ways (Hartl 1959, 1965-1974; Hilliard 1994). Seed pedestals, developed from the funicle and/or placenta, are scattered, being known from e.g. Tetrachondraceae, Calceolariaceae, Orobanchaceae and Paulowniaceae (Rebernig & Weber 2007; Hilliard 1994).
For general information, see Kadereit (2004a), for chemistry, see Harborne and Williams (1971: scutellarein, etc.), Zindler-Frank (1978: oxalate accumulation), Young and Siegler (1981: anthraquinones), Mølgaard and Ravn (1988: caffeoyl esters), Tomás Barberán et al. (1988: flavone glycosides), Scogin (1992: acteoside), Jensen (1992), and Grayer et al. (1999: general). For proteinaceous nuclear inclusions, see Bigazzi (1984, 1989a, 1989b, 1993, 1995) and Speta (1977, 1979). Information on a number of families recognised here is to be found under Scrophulariaceae in the old sense - see e.g. Schmid (1906: ovules), Hartl (1956: placentation), and Hartl (1965-1974), Fischer (2004b), and Rahn (1996: Plantago), all general. For a sumary of inflorescence morphology, see Weber (2013), for some gynoecial variation, see Shamrov (2014b).
Phylogeny. Oxelman et al. (1999a), Mueller et al. (2001) and Hilu et al. (2001) among others suggested that Plocospermataceae are sister to other Lamiales. Savolainen et al. (2000b, rbcL data alone; see also H.-L. Lee et al. 2007, Plocospermataceae not included) placed Carlemannia as sister to Oleaceae (only 1 species in analysis) with moderate support, and Bremer et al. (2001) found that the two genera formed a sister group that was part of a trichotomy at the base of Lamiales; Oleaceae (Ligustrum only included) and [all other Lamiales] completed the trichotomy, while Plocospermataceae again were not studied. A sister relationship [Carlemanniaceae + Oleaceae] is also supported by Yang et al. (2007: 1.0 p.p., Plocosperma included, but sampling still very poor; Refulio-Rodriguez & Olmstead 2014), and that seems the best place to put the family. The peltate, glandular hairs with unicellular stalks and flowers with two stamens (their position is not entirely certain) of Carlemanniaceae also suggest Lamiales, and anatomical features (see below) are consistent with this relationship.
S. Andersson (2006, two genes, sampling poor) found 75% jacknife support for the clade [Calceolariaceae + Gesneriaceae], and 100% support for that clade as sister to remaining Lamiales, even though Mayr and Weber (2006) did not think that the two families were particularly near each other. However, chemistry and morphology also suggest a close relationship between the two, and their position as sister to the remaining Lamiales. Qiu et al. (2010), Soltis et al. (2011) and Refulio-Rodriguez and Olmstead (2014) suggest that Peltanthera may fall outide the [Calceolariaceae + Gesneriaceae] clade (see below, but c.f. Perret et al. 2012).
Relationships in the "Scrophulariaceae" - Acanthaceae - Bignoniaceae - Lamiaceae area have been uncertain for some time, see e.g. Wagstaff and Olmstead (1997), Olmstead et al. (2001), and Xia et al. (2009). B. Bremer et al. (2002) analysed variation in three coding and three non-coding regions of the chloroplast genome; their sampling was sketchy, so the support for some family groupings is difficult to evaluate; Freeman and Scogin (1999) focussed on the old Scrophulariaceae, but the pattern of relationships they found was unclear. A tree in K. Müller et al. (2004) suggested that at least a partial resolution of relationships was in sight, although sampling was again poor (this study focused on Lentibulariaceae); the three families then known or suspected to be carnivorous (Byblidaceae, Lentibulariaceae and Martyniaceae) were not immediately related. Rahmanzadeh et al. (2004), Albach et al. (2005) and Oxelman et al. (2005) began to clarify the contents of the separate clades that used to be subsumed in Scrophulariceae s. l. (see also Tank et al. 2006 for a summary). Thomandersia, from tropical Africa and previously usually included in Acanthaceae, appeared to go near Schlegeliaceae, from tropical America and previously usually included in Bignoniaceae, however, support for this association was weak (Wortley et al. 2005a and especially 2007a). Characters like the vasculature of the floral nectary and petiole, also the nectaries on the outside of the calyx, might link the two.
Lamiaceae and Verbenaceae were initially separated on the distinctions more or less herbaceous vs. more or less woody and style (often) gynobasic vs style terminal. However, gynoecial morphology had long suggested (Junell 1934) a separation along the lines of those followed today: inflorescence branches cymose vs inflorescence racemose and stigma bifid vs. more or less capitate. Many Lamiaceae have a single layer of sclerenchymatous, bone-shaped cells on the inside of the mesocarp, others have thicker pericarp walls, and the cells are often crystalliferous, while the pericarp anatomy of Verbenaceae is more complex (Ryding 1995). There may be differences in seed coat anatomy: the testa of at least some Verbenaceae has the hypodermal layer(s) thickened, while in Lamiaceae it is the exotestal cells that are thickened, particularly on their inner periclinal and anticlinal walls (Rohwer 1994a). The molecular relationships of Verbenaceae s. str. and Lamiaceae were for a time unclear (e.g. Olmstead et al. 2001, only one member of each sampled); see Wagstaff & Olmstead (1997) for more information. Petraea (Verbenaceae) was sister to Bignoniaceae in some early molecular phylogenies (Wagstaff & Olmstead 1997), similarly, Nie et al. (2006) linked Verbenaceae with Bignoniaceae, and Phrymaceae went with Paulowniaceae. Phrymaceae have remained cladistically close to Paulowniaceae (see below ), although they were included in Verbenaceae by Cronquist (1981) and others in the past, in part because they have a similar racemose inflorescence and gynoecium (see Cantino 2004). Indeed, the gynobasic style and four nutlets that were supposed to characterize Lamiaceae may have evolved more than once (Cantino 1992a), and a considerable number of ex-Verbenaceae are now included in Lamiaceae (Cantino et al. 1992a, b).
Amyloid is found in both Pedaliaceae and Acanthaceae, a family that has sometimes been weakly associated with Pedaliaceae in molecular analyses (Soltis et al. 2005b and references), and both Martyniaceae and Pedaliaceae, perhaps not immediately related, have 10-hydroxylated carboxylic iridoids. Refulio-Rodriguez and Olmstead (2014) link all three families, although support is weak. Byblidaceae may be sister to Lentibulariaceae (e.g. Albert et al. 1992), although K. Müller et al. (2004) found no association between the two, nor of either with any Lamiales with viscid indumentum like that of Martyniaceae and Pedaliaceae, a feature which could perhaps be considered to be "precursory" to insectivory. On the other hand, Müller et al. (2004) found a weak association of Lentibulariaceae and Bignoniaceae. Soltis et al. (2007a) found few strongly supported relationships in the bulk of the order; Wortley et al. (2005b), who had sequenced over 4600 bp, estimated that at least 10000 bp more would need to be added to resolve relationships within the clade.
Although focusing on Triaenophora (ex "scroph", now Orobanchaceae s.l.), the relationships that Albach et al. (2009) found are broadly consistent with those suggested by others and the phylogeny of Schäferhoff et al. (2010), in part followed here. The bulk of the free-living Scrophulariaceae are paraphyletic at the base of the iridoid-containing clade of Lamiales, Lamiaceae and Verbenaceae not sister taxa, the insectivorous and putatively insectivorous clades in Lamiales are all unrelated, etc. (Schäferhoff et al. 2010). The recent discoveries of Pereira et al. (2012) have added another phylogenetically isolated carnivorous clade (in Plantaginaceae). Albach et al. (2009) cast doubt on the monophyly of Phrymaceae (see also Schäferhoff et al. 2010); taxon limits in this area have had to be narrowly drawn, the result of keeping Orobanchaceae separate. The tree still lacked resolution, especially around the Bignoniaceae-Verbenaceae area.
Recent findings by McDade et al. (2012: focus on Acanthaceae) apparently contradict part of the tree found by Schäferhoff et al. (2010). In particular, Byblidaceae, Stilbaceae and, surprisingly, Thomandersiaceae all occur on the tree between Plantaginaceae and Scrophulariaceae (support is strong), and Linderniaceae are sister to Scrophulariaceae (support is weak). Although Bell et al. (2010) recovered a clade [Oleaceae [Byblidaceae, Plantaginaceae, The Rest (including Gesneriaceae)]], support along the spine was rather weak for the most part. On the other hand, Perret et al. (2012: focus on Gesneriaceae) found relationships more similar to those in Schäferhoff et al. (2010), although the two carnivorous clades Byblidaceae and Lentibulariaceae were sister taxa.
Refulio-Rodriguez and Olmstead (2008: summary) suggested that substantial progress in disentangling relationships around Lamiacae-Verbenaceae and Scrophulariaceae s.l. might be on the horizon (see also Xia et al. 2009). Details of their findings (Refulio-Rodriguez & Olmstead 2014) largely agree with those of Schäferhoff et al. (2010), although more genes were analyzed and support values are usually higher. In particular, nodes along the back-bone of the tree up to [Stilbaceae + The rest] all have very strong support. Resolution along much of the rest of the backbone remains weak, and family groupings also have little support (see also Z.-D. Chen et al. 2016). The family groupings in the part of the tree [Byblidaceae + The Rest] are those of Refulio-Rodriguez and Olmstead (2014), but for the most part they await confirmation; relationships suggested by Wikström et al. (2015) are rather different. However, a clade including Lamiaceae, Orobanchaceae, etc., was retrieved by McDade et al. (2012), although many of the internal support values were low. It had moderate-good support in Refulio-Rodriguez and Olmstead (2014; see also Z.-D. Chen et al. 2016; ), and with rather higher internal support values. Genera are still being added to this clade, and some relationships within it are not entirely clear; for further discussion, see below.
Two other genera have sometimes been associated with Lamiales. Lens et al. (2008a) and Weigend et al. (2013b) suggested that Vahlia was sister to all other Lamiales, although support was weak and Plocosperma was not included. However, Vahlia is perhaps more likely to be sister to Solanales (Refulio-Rodriguez & Olmstead 2014). The position of Hydrostachys within the asterids has also not been easy to determine. Here it is included in Cornales, and there is a discussion of its relationships there; Burleigh et al. (2009) suggested that it was a member of Lamiales, and its morphology is in general agreement with such a position. If it should end up in Lamiales, it is likely to be towards the basal part of the tree.
Classification. R. Olmstead (pers. comm.) has been compiling a synoptical classification of Lamiales from which some of the numbers of taxa included in the families below are taken. The limits of families like Scrophulariaceae have long been problematic (Thieret 1967 for a summary), and Olmstead (2002) provided a readable account of some of the changes in our ideas of relationships in the Scrophulariaceae s.l. in particular.
Despite the lack of morphological support for some of the families, little is to be gained and more lost if their limits are much expanded.
Includes Acanthaceae, Bignoniaceae, Byblidaceae, Calceolariaceae, Carlemanniaceae, Gesneriaceae, Lamiaceae, Lentibulariaceae, Linderniaceae, Martyniaceae, Mazaceae, Oleaceae, Orobanchaceae, Paulowniaceae, Pedaliaceae, Peltantheraceae, Phrymaceae, Plantaginaceae, Plocospermataceae, Schlegeliaceae, Scrophulariaceae, Stilbaceae, Tetrachondraceae, Thomandersiaceae, Verbenaceae.
Synonymy: Acanthales Berchtold & J. Presl, Antirrhinales Döll, Aragoales D. Don [?status], Bignoniales Berchtold & J. Presl, Byblidales Reveal, Callitrichales Link, Carlemanniales Doweld, Fraxinales Berchtold & J. Presl, Gesneriales Berchtold & J. Presl, Globulariales Dumortier, Hippuridales Link, Jasminales Berchtold & J. Presl, Lentibulariales Berchtold & J. Presl, Ligustrales Bischof, Myoporales Berchtold & J. Presl, Oleales Berchtold & J. Presl, Orobanchales Berchtold & J. Presl, Pedaliales Berchtold & J. Presl, Pinguiculales Dumortier, Plantaginales Berchtold & J. Presl, Rhinanthales Dumortier, Scrophulariales Lindley, Selaginales Martius, Stilbales Martius, Utriculariales Döll, Verbascales Döll, Verbenales Berchtold & J. Presl
PLOCOSPERMATACEAE Hutchinson Back to Lamiales
Shrubs or trees; cork?; vessels in radial multiples; large groups of fibres in outer cortex at nodal region; petiole bundle annular; styloids +; hairs unicellular, calcified and/or with cystoliths, also bicellular, club-shaped, glandular; cuticle wax crystalloids 0; petiole articulated near base; plant cryptically dioecious; inflorescences axillary; bracteoles 0; flowers 5-6-merous; staminate flowers: anthers extrorse, versatile, with largely separate thecae; nectary 0; pistillode +; carpellate flower: staminodes +; nectary +; stylar fusion postgenital, placentation parietal, style twice divided, stigmas not expanded; ovules 2/carpel; seeds with tuft of hairs at chalazal end, hairs multicellular; coat ?; endosperm ?development, slight; n = ?; protein bodies in nucleus?
1 [list]/1: Plocosperma buxifolia. Central America (map: from Leeuwenberg 1967).
Evolution: Divergence & Distribution. Diversification in Plocospermataceae seems to have slowed down (Magallón et al. 2018).
Chemistry, Morphology, etc. Plocospermataceae are poorly known. Jensen (1992) recorded verbascosides and cornoside from Plocosperma, but not iridoids.
Struwe and Jensen (2004) described the inflorescence as being a congested raceme or dichasium, and this, and the apparent absence of nectaries in the staminate flowers, should be confirmed. For ovule position, see Leeuwenberg (1967).
See also D'Arcy and Keating (1973: as Lithophytum, esp. anatomy), M. Endress et al. (1996), and Struwe and Jensen (2004), both general, for information.
Previous Relationships. Plocospermataceae were included in Gentianales by Takhtajan (1997), probably because Plocosperma had long been associated with Loganiaceae. Cronquist (1981) included the genus in his Apocynaceae, probably because of the hairs on its seeds.
[[Carlemanniaceae + Oleaceae] [Tetrachondraceae [[Peltantheraceae [Calceolariaceae + Gesneriaceae]] [Plantaginaceae [Scrophulariaceae [Stilbaceae [[Byblidaceae + Linderniaceae] [[Pedaliaceae, Martyniaceae, Acanthaceae] [Bignoniaceae [[[Schlegeliaceae + Lentibulariaceae] [Thomandersiaceae + Verbenaceae]] [Lamiaceae [Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]]]]]]]]]]]]]: phloem loading via intermediary cells [specialized companion cells with numerous plasmodesmata, raffinose etc. involved]; cells in heads of glandular hairs with vertical walls only; flowers 4-merous [?: reverses to 5-merous....]; placentation axile.
Age. Janssens et al. (2009) give a date of 95±11.9 m.y. for this node, Magallón et al. (2015) an age of ca 71 m.y., Bell et al. (2010) an age of ca (78-)74, 69(-61) m.y., while Magallón and Castillo (2009) offer estimates of ca 62.8 m.y., Nylinder et al. (2012: suppl., c.f. topology) of about 97.1-74 m.y. and Wikström et al. (2015) an age of (89-)79(-69) m.y.; ca 56.2 m.y. is the age in Tank et al. (2015: Table S2), while at around 53.9 m.y.a., the estimate by Naumann et al. (2013) is the youngest.
Evolution: Divergence & Distribution. There may be low-level and symmetrical expression of CYCLOIDEA2-like genes in Oleaceae (Zhong & Kellogg 2015), perhaps the beginning of changes that led to the development of monosymmetric flowers, and this novelty could perhaps be placed at this node. Hileman (2014; also Hileman & Cubas 2009) discusses the evolution of monosymmetry in Lamiales; there disymmetry is included in monosymmetry (see Hileman 2014: c.f. Fig. 2b).
Chemistry, Morphology, etc. Note that the arrangement of the sepals (and petals) is orthogonal in Oleaceae and Calceolariaceae, while that of Tetrachondraceae (and of 4-merous Veronica) is diagonal (Mayr & Weber 2006). For phloem loading, see Turgeon et al. (1993), Rennie and Turgeon (2009) and Davidson et al. 2010).
[Carlemanniaceae + Oleaceae]: C valvate; A 2; pollen tricolpate; stigma ± clavate; exotestal cells ± palisade, endothelium persistent.
Age. The age of this clade was estimated to be (83.7-)69.4(-54.7) m.y. (Tank & Olmstead pers. comm.).
CARLEMANNIACEAE Airy Shaw Back to Lamiales
Perennial herbs or shrubs; chemistry?; pericyclic fibers few; nodes?; cuticle waxes 0; lamina margins toothed; inflorescences terminal and axillary; flowers weakly obliquely monosymmetric, 4- or 5-merous, (heterostylous - Silvianthus); K members unequal or not, ± linear, aestivation open?, C aestivation induplicate-valvate; anthers connivent around the style, latrorse, ?attachment; ovary inferior, nectary on top, style clavate; ovules many/carpel; fruit fleshy-capsular, loculicidal, or 5-valved [valves correspond to calyx segments], opening widely, exposing the placenta - Silvianthus, K persistent; exotestal cells with radial walls thickened, interior cells unthickened, or polygonal, all walls thickened [Carlemannia], (endothelium persistent - Silvianthus); endosperm +, ruminate [Silvianthus], embryo small; n = 15, 19; protein bodies in nucleus?
2 [list]/5. E. Nepal eastwards to Myanmar, Thailand, Laos, Vietnam, S.W. China, Sumatra (map: Fl. China 19. 2011).
Chemistry, Morphology, etc. Fruit dehiscence does not really make sense - 5 valves from a two-carpellate gynoecium?
Some information is taken from Tange (1999); Thiv (2004) provides a general account, and Yang et al. (2007) information on chromosome numbers, etc.
Carlemanniaceae are very largely unknown.
Previous Relationships. Carlemanniaceae have usually been associated with Caprifoliaceae or Rubiaceae in the past. However, characters such as superficial cork, two stamens with connivent anthers and two carpels each with many ovules would remove Carlemanniaceae from Caprifoliaceae, and the toothed, exstipulate leaves, 2 stamens, anomocytic stomata, and absence of raphides from Rubiaceae (Solereder 1893; Airy Shaw 1965). Carlemanniaceae were included in Caprifoliaceae by Cronquist (1981) and in Rubiales by Takhtajan (1997).
OLEACEAE Hoffmannsegg & Link, nom. cons. Back to Lamiales
Woody; route I iridoids [deoxyloganic acid, loganin, etc. precursors], verbascoside or variants, myricetin, orobanchin, sugar alcohol mannitol +; wood with minute calcium oxalate crystals; (vessel elements with scalariform perforation plates); fibre tracheids +; libriform fibres 0; foliar crystals of various types, inc. styloids and raphides (0; druses); petiole bundle arcuate; sclereids + (0); cuticle deeply furrowed (waxes ribbons, platelets); (serial [superposed] axillary buds +); branching from previous innovation; leaf margins entire to toothed, (secondary veins palmate); flowers 4-merous; K valvate, initiation orthogonal; anther thecae ± back-to-back; tapetal cells often 3< nucleate; pollen (grains tricellular), intine thickening at the apertures [= oncus] [?first two tribes?]; (style short), stigma dry; ovules apical, (hemitropous), epitropous or apotropous, integument 7-8 cells across, (postament +), hypostase +; testa often vascularized, exotesta moderately and evenly thickened, (endotesta fibrous), (endothelium ?not persistent); endosperm +/0, first division asymmetrical; nuclear genome [1C] (851-)1471(-2919) Mb; protein bodies in nucleus crystalline-globular; 9 bp deletion in ndhF.
24 [list]/615 (790) - five tribes below. More or less worldwide, especially East Asia (map: from Meusel et al. 1975; Australia's Flora Online xii.2012).
Age. The age of crown-group Oleaceae is (73-)60.1(-49.2) m.y. (Tank & Olmstead pers.comm.).
1. Myxopyreae Boerlage
Myxopyroside iridoids [carbocyclic]; inverted cortical bundles in corners of angled stem (Dimetra not); petiole bundles three, arcuate; (K initiation diagonal, C contorted, early tube formation - Nyctanthes); (G collateral); placentation ± basal; ovules 1(-3)/carpel, integument to 20 cells across [Nyctanthes]; (megaspore mother cells several, embryo sac bisporic, 8-nucleate [Allium type]); fruit a berry or schizocarp; endosperm cellular [Nyctanthes]; n = 11, 12; germination epigeal.
3 (Myxopyrum, Dimetra, Nyctanthes)/7. Indo-Malesia.
Synonymy: Nyctanthaceae J. Agardh
2. Fontanesieae L. Johnson
Route 1b iridoids [carbocyclic and seco-iridoids]; pits ± vestured; petiole bundle annular; C free, imbricate; ovule 1/carpel; fruit a samara; testa crushed; n = 13.
1/2. Sicily, W. Asia, China.
3. Forsythieae L. Johnson
Cornosides, route 1b iridoids [forsythide - carbocyclic]; pith chambered; tapetal cells binucleate; ovules 1-several/carpel, integument 10< cells across, nucellar cap ca 2 cells across; archesporial cells several; fruit a samara or capsule; n = 14.
2/8. S.E. Europe, East Asia.
[Jasmineae + Oleeae]: route 1b/1c irioidoids [secoiridoids - oleoside]; leaves odd-pinnate to simple; ovules 2(-4)/carpel; fruit fleshy; suspensor very long.
Age. The age of this node may be (52-)48, 39(-35) m.y. or (Wikström et al. 2001) or (62-)45, 41(-24) m.y. (Bell et al. 2010) - but see below.
4. Jasmineae Lamarck & de Candolle
(K, C to 14 or more), first 4 K initiation diagonal, C quincuncial-imbricate, tube formation early; endothelium 0; (megaspore mother cells several, several elongated embryo sacs developing); fruit bilobed, berry or circumscissile capsule; seed coat multilayered, mesotesta with wholly thickened or band-thickened anticlinal walls; endosperm free-nuclear; n = 11-13; 21kb chloroplast inversion.
1/225-450 (Jasminum: inc. Menodora). Tropical to warm temperate Old World, some in America. [Photo - Flower.]
Synonymy: Bolivaraceae Grisebach, Jasminaceae Jussieu
5. Oleeae Dumortier
Flavone glycosides +, (carbocyclic iridoids); vessel elements in multiples; (pits vestured), (torus-margo pits +), libriform fibres + (0); fibre tracheids 0 (+); marginal parenchyma +/0; (indumentum of peltate scales); lamina (with flat abaxial glands - Ligustrum), vernation conduplicate [Chionanthus]; (plant dioecious); K (diagonal), (open), C valvate, (imbricate), (free), (0), tube formation late (early - Ligustrinae); (A 4 or more); (embryo sac bisporic [the chalazal dyad] and 8-celled [Allium type]); (fruit a samara); n = (20) 23; germination epigeal or hypogeal.
17/415: Noronhia (105), Chionanthus (60-120), Fraxinus (45-65), Ligustrum (50), Olea (33). Tropical and subtropical, inc. New Zealand and Hawaii.
Age. Wood identified as Oleinae has been found in the Deccan Traps 67-65 m.y. (Srivastava et al. 2015: Rhamnaceae and Rutaceae also possibilities; Wheeler et al. 2017). Samaras of Fraxinus have been reported from mid-Eocene deposits in Tennessee that are some 44 m.y.o. (Call & Dilcher 1992).
Synonymy: Forestieraceae Meisner, Fraxinaceae Vest, Ligustraceae G. Meyer, Schreberaceae Schnizlein, Syringaceae Horaninow
Evolution: Divergence & Distribution. Some molecular dates are incompatible with the fossil record; see above.
Much diversification within Oleaceae occurred during the Caenozoic (Besnard et al. 2009a). The Hesperelaea clade, from Guadalupe Island, west of Baja California, but now extinct, is probably older than Guadalupe Island - (27.5-)19.7(-12.5) versus (9-)7(-5) m.y. - and is likely to have moved there from the mainland (Zedane et al. 2015). Picconia excelsa, from the Madeiras Islands, may be a component of the old laurel forests there, however, Palaeo-Macaronesia is likely to be 60 m.y. or more old (Gelmacher et al. 2005; Fernández-Palacios et al. 2011).
Pollination Biology & Seed Dispersal. For the evolution of wind pollination, dioecy, etc., in Fraxinus, see Wallander (2013).
Plant-Animal Interactions. Caterpillars of some Sphinginae are quite common on Oleaceae (and the same genera may also be found on Solanaceae: Forbes 1958).
Genes & Genomes. There have been genome duplications in the clade leading to Olea europea 28 and 59 m.y.a. (Turgay Unver et al. 2017), so the older one could be quite deep in the family.
For the reorganization of the plastid genome in Jasminum s.l. and with a reduction in size of the small single copy portion, see H.-L. Lee et al. (2007). The chloroplast gene accD (= ORF512, zpfA) has been lost (Doyle et al. 1995 and references) in at least some Oleaceae.
Chemistry, Morphology, etc. The route I secoiridoids are unlike other route I secoiridoids, e.g. those in Gentianaceae (Jensen 1992; Jensen et al. 2002; see also Gousiadou et al. 2015). Damtoft et al. (1995) noted that the secoiridoids of Fontanesia (loganic acid, etc., and 5-hydroxylated derivates like swertiamarin) were produced by a somewhat different biosynthetic pathway than the oleoside-type secoiridoids common elsewhere in the family. Abeliophyllum, in a clade possibly sister to rest of Oleaceae, has cornosides and verbascosides, and some lack iridoids; these features may be plesiomorphies - but certainly not if Myxopyreae are sister to the rest of the family (see below); absence (= loss) or iridoids occurs elewhere in the family (Jensen et al. 2002). There is a single report of cornosides from the [Jasmineae + Oleeae] clade (Jensen et al. 2002).
At least some species of Osmanthus (and the related Picconia/Chionanthus retusus) have lignified, torus-bearing, intervascular pit membranes (Coleman et al. 2004: Dute et al. 2010b; Dute 2015; Nguyen et al. 2017). Govil (1973) showed how the lateral bundles of the petiole in Nyctanthes were derived from the cortical vascular system. The diversity of crystal types in the vegetative plant (other than the wood) is very great, but druses, the crystal form in which calcium oxalate commonly occurs elsewhere, are uncommon here (Lersten & Horner 2008a, 2009a, esp. b). Crystals are often clustered in epidermal cells at the bases of trichomes, an unusual distribution pattern (Lersten & Horner 2009b). Groups of few-celled secretory hairs may form extrafloral nectaries (Zimmermann 1932).
The calyx is sometimes diagonally oriented (Sehr & Weber 2009). There is variation in corolla tube initiation, both early and late initiation being known in the family (Sehr & Weber 2009). Nectar is reported to be secreted from the ovary in Syringa and Ligustrum (Weberling 1989). Osmophores are common and their absence from the anthers may be of systematic interest (Nilson 2000: sampling?); orbicules may be absent (Vinckier & Smets 2002a). There is infrageneric variation in the orientation of the two carpels; however, the two stamens are always borne in the plane of the ovary septum (Eichler 1874). Baillon (1891) illustrated both epitropous and apotropous ovules. Ghimire and Heo (2014a) suggested that the integument of Abeliophyllum was 5-7 cells across, but from their Fig. 3d (for example), it is at least 10 cells across; they also describe the integument of the whole family as being multiplicative. Indeed, the seed coat may be 14-20 or so cells across, the outer epidermis being enlarged (Patel 1963) .
For more information, see Green (2004: general), Jensen et al. (2002 and references: iridoids), Baas et al. (1988: wood anatomy), Song and Hog (2012: some petiole anatomy, Naghiloo et al. (2013: inflorescence morphology), Sehr and Weber (2009) and Dadpour et al. (2011), both floral ontogeny, the latter also some inflorescence morphology. Bigazzi (1989a: protein nuclear inclusions), Kiew and Baas (1984) and Rohwer (1994b: both Nyctanthes), Andersson (1931), Kapil and Vani (1966) and Maheswari Devi (1975), all embryology, and Rohwer (1993b, 1996: fruit and seed).
Phylogeny. Wallander and Albert (2000: some morphology also) found a [Jasminieae + Oleeae] clade, the two tribes with a fair bit of internal resolution; relationships of the other three tribes were unresolved. H.-L. Lee et al. (2007), however, found Myxopyreae to be sister to the rest of the family (100% bootstrap support), with Fontanesieae, Forsythieae and [Jasmineae + Oleeae] forming a tritomy; they emphasized the complex pattern of chloroplast inversions in Jasmineae. Kim and Kim (2011) suggested a quite well supported set of groupings [[Fontanesieae + Jasmineae] [Oleeae + Forsythieae]]; unfortunately, they did not sample other members of the family. The position of Jasmineae and Forsythieae is switched from that followed here in Z.-D. Chen et al. (2016), but support was not strong.
Franzyk et al. (2001) noted that Myxopyrum and Nyctanthes, both in Myxopyreae, had similar iridoids. Besnard et al. (2009a) and Guo et al. (2011) examined relationships in some Oleeae, while Hong-Wa and Besnard (2013, see also 2014) found considerable geographical signal in the clades they obtained in a study of relationships around Noronhia and other Oleinae - although polyploidy presented a problem in their analyses. The extinct genus Hesperelaea was placed in a clade with Forestiera and Priogymnanthus by Zedane et al. (2015). For the phylogeny of Fraxinus, see Wallander (2013 and references).
Classification. The tribes recognised above are those of Wallander and Albert (2000). Generic limits in Oleeae in particular need much attention; Olea itself, Osmanthus, and Chionanthus are all polyphyletic (Besnard et al. 2009a; Guo et al. 2011). Thus Chionanthus had included Linociera, but this is questionable; Hong-Wa and Besnard (2013) have begun the necessary process of generic realignments in this area.
Previous Relationships. The position of Nyctanthes has been uncertain, and it was often included in Verbenaceae in the old sense; Filonenko et al. (2010) considered the genus to be separate from both families.
[Tetrachondraceae [[Peltantheraceae [Calceolariaceae + Gesneriaceae]] [Plantaginaceae [Scrophulariaceae [Stilbaceae [[Byblidaceae + Linderniaceae] [[Pedaliaceae, Martyniaceae, Acanthaceae] [Bignoniaceae [[[Schlegeliaceae + Lentibulariaceae] [Thomandersiaceae + Verbenaceae]] [Lamiaceae [Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]]]]]]]]]]]]: plants ± herbaceous; enhanced but symmetrical expression of CYCLOIDEA2-like genes; C and A initiated simultaneously, or A before the C; seeds <4 mm long; endosperm also with chalazal haustoria; deletion in the matK gene.
Age. The age of this node is around 87 m.y. (K. Bremer et al. 2004a), (94.5-)81.6(-70.5) m.y. (Tank & Olmstead pers. comm.), (84-)74(-64) m.y. (Wikström et al. 2015), ca 66.7 m.y. (Magallón et al. 2015) or as little as ca 53.5 m.y.a. in Tank et al. (2015: Table S1, S2).
Chemistry, Morphology, etc. For information on the matK deletion, see Hilu et al. (2000); the sampling needs to be improved.
TETRACHONDRACEAE Wettstein Back to Lamiales
Creeping to erect herb; sorbitol +; cork?; nodes with split laterals; hairs moniliform [Polypremum]; leaves amphistomatic; leaf bases connate or connected by membranaceous stipules; (inflorescence of 1-2 axillary flowers - Tetrachondra), bracteoles two or more pairs; flowers rather small [<5 mm across], 4-merous; K initiation diagonal [Polypremum], C with very short tube; stamens free, ?thecae; pollen in tetrads, 6-sulcate, psilate; nectary 0; G transverse [when 2 pairs bracteoles], (ovary 4 partite, slightly inferior, placentae peltate - Polypremum), style (gynobasic - Tetrachondra), (0 - Polypremum), stigma small, subglobose; ovules (2/carpel, basal - Tetrachondra), or many, integument 3-4 cells across [Polypremum]; fruit with persistent green K, either a schizocarp, or a loculicidal (+ septicidal) capsule; seed pedestals +; testa thin, endothelial cells with persistent thickened inner walls; endosperm copious; n = 10, 11, protein bodies in nucleus?
2 [list]/3. Patagonia, New Zealand (Tetrachondra), S. U.S.A. to South America (Polypremum procumbens) (map: from Fl. Neotrop v. 81. 2000). [Photo - Polypremum Flower.]
Age. Crown-group Tetrachondraceae are ca 46 m.y.o. (K. Bremer et al. 2004a), (68.4-)39.7(-14.2) m.y. (Tank & Olmstead pers. comm.) or (61-)39(-18) m.y. (Wikström et al. 2015).
Evolution: Divergence & Distribution. Wagstaff et al. (2000) found that the sequences of the two species of Tetrachondra, from the Antipodes and S. South America, were almost identical - the distribution is probably recent.
Chemistry, Morphology, etc. Polypremum has both micropylar and chalazal endosperm haustoria; this should be checked in Tetrachondra, a very poorly known genus. The embryo sac of Polypremum protrudes through the nucellar epidermis (Moore 1948).
For general information, see Wagstaff (2004a), some additional information is taken from Mayr & Weber (2006), and Sehr and Weber (2009), also chemistry (Harborne & Williams 1971 - scutellarein +, c.f. Gelsemium!; Jensen 2000a), endothelium presence (absent in Loganiaceae), endosperm type, etc., of Polypremum are right for a position in Lamiales.
Phylogeny. The [Polypremum + Tetrachondra] clade is strongly supported (Oxelman et al. 1999a); see also Wagstaff et al. (2000).
Previous Relationships. Tetrachondra was placed in Boraginales by Takhtajan (1997: two ovules/carpel, gynobasic style in common) and in Lamiaceae by Cronquist (1981: ditto). Polypremum has always been associated with Loganiaceae s.l.; Takhtajan (1997) included it in his Buddlejaceae.
[[Peltantheraceae [Calceolariaceae + Gesneriaceae]]] [Plantaginaceae [Scrophulariaceae [Stilbaceae [[Byblidaceae + Linderniaceae] [[Pedaliaceae, Martyniaceae, Acanthaceae] [Bignoniaceae [[[Schlegeliaceae + Lentibulariaceae] [Thomandersiaceae + Verbenaceae]] [Lamiaceae [Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]]]]]]]]]]] / Core Lamiales: mycorrhizae usu 0; shikimic-acid derived anthraquinones, 6- and/or 8- hydroxylated flavone glycosides + [? Tetrachondraceae], storage substances stachyose and other oligosaccarides; inflorescence indeterminate/open; flowers vertically monosymmetric; K ± asymmetric, C usu. ± bilabiate, 2-lobed upper lip, 3-lobed lower lip [= 2:3], asymmetrical expression of CYCLOIDEA2-like genes, adaxial lobes outside the others in bud [ascending cochleate], tube formation late; A 4, didynamous, placentoids +; pollen tubes lacking callose [?level]; ovules many/carpel; second division of the endosperm longitudinal, suspensor large.
Age. Bell et al. (2010: note topology) estimated an age of (72-)64, 61(-56) m.y. for this node and Magallón et al. (2015) an age of ca 58.1 m.y.; the age in Bremer et al. (2004) is around 78 m.y., in Wikström et al. (2015) it is (76-)65(-56) m.y., and in Wikström et al. (2001: note topology) it is (60-)56, 45(-41) m.y. old. However, Tank et al. (2015: Table S1) suggest that this node is only ca 43.9 m.y. old.
Martínez-Millán (2010), using a rather scanty fossil record, suggested an Oligocene age for diversification within Lamiales - this would be at this node, since fossil Oleaceae are known from the Eocene.
Evolution: Divergence & Distribution. Many core Lamiales are herbaceous or shrubby and have often quite large monosymmetric, bilabiate flowers, and about equal numbers of species have fruits with many small seeds or with about eight or fewer (but still not very big) seeds. This clade includes the bulk of the diversity within Lamiales, and overall diversification rates are high (Magallón & Sanderson 2001; Magallón & Castillo 2009; Tank et al. 2015), although rates and patterns of diversification of clades in core Lamiales vary considerably. High speciation rates are common in other non-mycorrhizal groups, many of which are herbaceous (Maherali et al. 2016), and also in herbaceous clades per se (e.g. Eriksson & Bremer 1992; S. A. Smith & Donoghue 2008). Monosymmetric flowers may be a key innovation in Lamiales (Endress 2011) and would be pegged to this level, so several things could be driving diversification here.
Monosymmetry may be associated with a shift from determinate paniculate to indetereminate racemose or thyrsoid inflorescences, monosymmetric flowers being lateral on the inflorescence (Degtjareva and Sokoloff 2012). A didynamous androecium, with stamens in two pairs of unequal lengths, is common; the fusion, or at least close attachment, of the paired anthers may improve pollen removal from the flower (Ren & Tang 2010). For the stepwise evolution of the expression patterns in CYC and RAD genes, involved in the expression of monosymmetry but also expressed in more basal polysymmetric clades, see Zhong and Kellogg (2015). If the position of Peltanthera, with five stamens and a more or less polysymmetric flower, is confirmed (see below), optimisation of monosymmetry on the tree becomes interesting; understanding the floral development of the genus will be important.
Ecology & Physiology. The establishment of arbuscular mycorrhizal associations has a considerable effect on plant defences, upregulating some and downregulating others (e.g. Jung et al. 2012). It is not surprising that both parasitic and insectivorous members of Lamiales are largely non-mycorrhizal (Brundrett 2004 and references), but absence of mycorrhizae is common in general here (Brundrett 20018, 2017b). There is a connection between the herbaceous habit, thin roots, high specific root lengths (i.e. long roots per unit of biomass), and the absence of mycorrhizae (Ma et al. 2018).
Pollination Biology. The evolution of monosymmetric flowers may be connected with the evolution of bee clades like euglossine and bumble bees (ages: 71-40 m.y.a. for plants, 75-65 m.y.a. for bees), derived and generalist bees that can handle complex flowers (Westerkamp & Claßen-Bockhoff 2007; Zhong & Kellogg 2014 and references).
Genes & Genomes. It appears that CYC genes have duplicated independently within the clade and become separately involved in the development of the strongly monosymmetric flowers of Antirrhinum, Mimulus and Gesneriaceae (e.g. Damerval & Manuel 2003; Gübitz et al. 2003; Preston et al. 2011b). However, recent work suggests that recurrent duplications may not play a direct role, but CYC2-like and RAD-like genes have very asymmetric patterns of expression in the corolla of members of core Lamiales with monosymmetric flowers, but not in the more basal clades examined (Zhong & Kellogg 2014, 2015).
Chemistry, Morphology, etc. For callose, see Prospéri and Cocucci (1979: Oleaceae, etc., not sampled, ?Gesneriaceae). For the distribution of various flavone glycosides, see Tomás-Barberán et al. (1988): Mimulus and Orobanche lack the glycosides of Lamiaceae, Verbenaceae, Scrophulariaceae and Plantaginaceae, while those of Lentibulariaceae are somewhat different, variation broadly consistent with phylogenetic relationships here.
Westerkamp and Claßen-Bockhoff (2007) outline the morphological variation of the corolla. Monosymmetry of the 2:3 type is common and there are four stamens which are often didynamous and sometimes with connivent anthers; for staminodes and stamen reduction in general, see Endress (1998) and Song et al. (2009: molecular mechanisms). Nectary vascularization varies. Nectaries may be vascularized by branches from the main carpellary vascular traces, as in Schlegeliaceae, some Pedaliaceae, Verbenaceae, or separately from the gynoecium, as in Bignoniaceae, Acanthaceae, and other Pedaliaceae. This suggests that either the distinction between gynoecial and receptacular nectaries (Smets 1988; Smets et al. 2003) is overly simplistic and/or there is homoplasy in this feature. There are septal vascular bundles, the gynoecial vascular system forming a sort of figure of 8 in transverse section, in Bignoniaceae and Schlegeliaceae, while in taxa like Acanthaceae there are no septal bundles, the gynoecial vasculature being almost in a circle (there are of course placental bundles: see Wortley et al. 2005a for details). Knowledge of the distribution of this character needs to be extended. The level at which to peg a character "embryo suspensor large" [sic] is unclear. There is much about ovules, seeds, etc. on various taxa, esp. Scrophulariaceae sensu latissimo and Lentibulariaceae, in Takhtajan (2013).
[Peltantheraceae [Calceolariaceae + Gesneriaceae]]: ?
Age. The age for this node is ca 71 m.y. (K. Bremer et al. 2004a), (80.2-)65.5(-48.8) m.y. (Tank & Olmstead pers. comm.), or (68-)52(-32) m.y. (Wikström et al. 2015).
Phylogeny. Peltanthera has been placed with Gesneriaceae (e.g. Oxelman et al. 1999a; see also Clark et al. 2010), and is perhaps to be included in the family, but c.f. Soltis et al. (2011). More recently Perret et al. (2012), in a study focusing on Gesnerioideae, found the well supported clade [Peltanthera [Sanango + Gesneriaceae s. str.]]. However, Refulio-Rodriguez and Olmstead (2014) found strong support for the position of Peltanthera as sister to the whole group, a relationship that is followed here.
Chemistry, Morphology, etc. See Weber (2013) for inflorescence morphology; the ultimate units of the inflorescence of Peltanthera are not so very different from the pair-flowered cymes that characterize the rest of the clade.
PELTANTHERACEAE Molinari Back to Lamiales
Small tree; cornoside derivatives +; nodes 3:3; petiole bundle ± flattened-annular, with (medullary and) wing bundles; lamina bundle sclerenchyma slight; hairs branched-moniliform; leaves not joined at the base; lamina vernation involute; inflorescence axillary, much branched; flower ± polysymmetric, "small" [<5 mm long], bracteoles 0; K ± free, C valvate; A 5, anther thecae confluent, appearing to be peltate; nectary small; stigma capitate; capsule loculicidal; seeds dust-like, cells in longitudinal rows, longitudinally ridged [from cell walls]; n = ?
1 [list]/1: Peltanthera floribunda. Costa Rica to Bolivia (Map: from Fl. Neotrop. v. 81. 2000; TROPICOS ii.2013).
Evolution: Divergence & Distribution. Given the sister-group relationships in this part of the tree, Peltanthera has diversified very little.
Chemistry, Morphology, etc. Peltanthera is very similar in wood anatomy to Buddleja, but both genera are woody (Carlquist 1997c).
See Hunziker and di Fulvio (1957) and Norman (2000) for general information, Carlquist (1997c) for wood anatomy, and Jensen (2000a) for chemistry. Peltanthera floribunda is a poorly known species.
[Calceolariaceae + Gesneriaceae]: leaves rather soft, leaf bases joined by a slight ridge, lamina margin serrate; inflorescence branches pair-flowerered cymes; endothelial cells in longitudinal rows; endosperm longitudinally furrowed [aulacospermous].
Age. Ages for this node are (108.6-)87.7, 46.7(-26.2) m.y. (Nylinder et al. 2012), (74.6-)58.5(-41.7) m.y. (Tank & Olmstead pers. comm.), ca 48.6 m.y. (Magallón et al. 2015), or a mere 39.6 m.y.a. (Tank et al. 2015: Table S2).
Chemistry, Morphology, etc. In paired-flower cymes the two flowers of the flower-pair have the same orientation. Since the flower in front of the terminal flower is sometimes subtended by a "bracteole" that can be interpreted as the bract of that flower, the flower opposite it being totally suppressed, what appears to be a rather strange dichasial cyme is then a modified "panicle" (Weber 1973; Haston & Ronse De Craene 2007). Both Calceolariaceae and Gesneriaceae have at least some taxa with septicidal capsule dehiscence, but how the distribution of this character might appear on a combined tree of the two is unclear.
CALCEOLARIACEAE Olmstead Back to Lamiales
Herbs to shrubs; cork?; wood rayless; nodes 1:1; pericyclic fibres 0; petiole bundle(s) arcuate; (lamina margins entire); flowers 4-merous, strongly monosymmetric; K orthogonal, valvate, C bilabiate, abaxial lobe saccate, (adaxial "lip" strongly bilobed - Calceolaria triandra), elaiophores on inside of abaxial lip [pads of hairs] (0); A 2 [lateral pair] (3 [inc. abaxial member - C. triandra]), thecae (parallel) divergent, confluent on dehiscence or not, (theca 1), staminodes 0; nectary 0; (G semi-inferior), stigma small or capitate or obscurely bilobed; ovules with integument 3-4 cells across; capsule both septicidal and loculicidal; seed pedestals +; testa with anticlinal walls sinuous (straight); endosperm +; n = (8) 9.
2 [list]/260: Calceolaria (240-270). Upland tropical and W. temperate South America, Brasil, also New Zealand (some Jovellana) (map: from Sérsic 2004). [Photo - Habit, Flower.]
Age. Crown group diversification began (27-)15(-4) m.y.a. (Renner & Schaefer 2010), (37.6-)21(-6.8) m.y. (Tank & Olmstead pers. comm.), or (51.3-)30.8, 12.9(-5.1) m.y. (Nylinder et al. (2012).
Evolution: Divergence & Distribution. The bulk of the diversity in the family is included in Calceolaria, common along the Andes, and its crown group age may be as recent as (6-)5(-1) m.y. (Renner & Schaefer 2010), which suggests rapid diversification within the genus (see also Cosacov et al. 2009; Madriñán et al. 2013). Mean ages for the split between the South American and New Zealand clades of Jovellana range from 9.3-5.3 m.y. - probably long distance dispersal was involved (Nylinder et al. 2012).
Perhaps the development of nototribe pollination mechanisms was a key innovation here (Cosacov et al. 2009).
Pollination Biology & Seed Dispersal. Pollination in Calceolaria has been studied in detail, in partticular by Sérsic (2004). Oil from oil glands or from specialised hairs is a common reward in the genus, and sternotribic flowers of Calceolaria that are pollinated by Centris bees seem to be plesiomorphous; species with such flowers are diploid and are basically Chilean (Cosacov et al. 2009). Smaller Chalepogenus bees are the other main pollinators (both are anthophorids). Flowers with a closed mouth are visited by larger bees, those with an open mouth by smaller bees (see Murúa & Espíndola 2015 for morphometric analyses; also Rasmussen & Olesen 2000; Possobom & Machado 2017a and references). Bombus and Xylocopa visit flowers that lack oil; pollen is their reward. Specialised food bodies on the lower lip are the reward for species that are pollinated by non-nectarivorous birds like the fruit- and seed-eating charadriform Thinocorus rumicivorous (Vogel 1974; Sérsic & Cocucci 1996; Rasmussen & Olesen 2000). All told, about 4/5 of the genus have oil flowers (Sérsic 2004), and the ability to produce oil has been lost several times (Renner & Schaefer 2010). Oil glands were acquired after the split of Calceolaria from Jovellana, which lacks oil glands (Renner & Schaefer 2010).
Chemistry, Morphology, etc. There has been much discussion over the basic floral meristicity, but flowers in the family seem to be best interpreted as being 4- rather than modified 5-merous (Mayr & Weber 2006: superb micrographs; c.f. e.g. Sérsic 2004). From vasculature, etc., each lip of the flower seems to be formed from two petals; these primordium pairs may become connate only rather late in floral development (Mayr & Weber 2006). For floral development, see also Endress (1999).
Some information is taken from Weber (1973: inflorescence) and Molau (1988), Ehrhart (2000), and Fischer (2004b), all general, in Scrophulariaceae; see also Tank et al. (2006).
Phylogeny. For a phylogeny of the family, see S. Andersson (2006).
Classification. Porodittia, with three stamens, is a synonym of Stemotria, but neither name is needed as Stemotria is clearly derived from within Calceolaria, thus P. triandra = C. triandra (S. Andersson 2006). The limits of the sections need adjusting.
Thanks. I am grateful to Pamela Puppo for comments.
GESNERIACEAE Richard & Jussieu, nom. cons. Back to Lamiales
Distinctive verbascosides [e.g. sanangoside]; nodes trilacunar or thereabouts; petiole bundle annular; stomata anisocytic; A 4 + staminode; (dust seeds +).
147(+) [list]/3,460 - three subfamilies below. Largely tropical.
Age. Estimated ages for crown-group Gesneriaceae are (67.6-)49.2(-30.6) m.y. (Tank & Olmstead pers. comm.), (68.1-)57.5(-45.1) m.y. (Perret et al. 2012), ca 71.9 m.y. (Petrova et al. 2015, and (81.3-)73.1(-51.9) m.y. (Roalson and Roberts 2016).
1. Sanangoideae A. Weber, J. L. Clark & Mich. Möller
Shrub or small tree; vessel elements with scalariform perforation plates; nodes 7:7 + split lateral; stem with cortical bundles; petiole bundle with inverted adaxial bundles; lamina bundle with sheathing sclerenchyma; stomata in groups; lamina quite coriaceous; flower weakly monosymmetric; K ± free; anther thecae confluent; G semi-inferior, placentation axile, style short, stigma capitate-lobed; capsule loculicidal + septicidal; n = 8.
1/1: Sanango racemosum. Ecuador to Bolivia, Venezuela (Map: from Norman 1994; TROPICOS ii.2013).
[Gesnerioideae + Didymocarpoideae]
Usu. herbs or weak-stemmed trees (trees), often epiphytes [ca 700 spp.]; hairs often dense, soft, of stalked glands, or with thickened terminal cells; (cambium storied); (vessel elements with scalariform perforation plates); nodes 1:1 (+ split laterals), 3 or more:3 or more + split laterals); petiole bundle(s) also arcuate; lamina bundle lacking sheathing sclerenchyma; (stomata in groups); leaves (anisophyllous; two-ranked; spiral), lamina vernation involute, (margins entire); inflorescence axillary (terminal); flowers strongly monosymmetric (polysymmetric); K connate, C with abaxial lobe(s) outside others in bud [= descending cochleate] or quincuncial, (C spurred); A (5, 2, staminode 0, 3), anthers connivent, (thecae apically confluent); nectary vascularized; placentation intrusive parietal, placentae ± bilobed, triangular, usu. covered by ovules, stigma broadly bilobed to trumpet-shaped, wet or dry; integument 3-5 cells across; fruit a septicidal capsule; exotestal cells variously elongated and thickened, endotestal cells at most simply persisting; nuclear genome [1C] (251-)1118(-4220) Mb; GCyc duplication.
147/3,460. Largely tropical.
Age. Crown-group core Gesneriaceae may be a mere (47-)44, 34(-31) m.y. (Wikström et al. 2001) or (60.5-)44.7(-37.1) m.y. (Perret et al. 2012); however, Bell et al. (2010: note relationships) give an age of (66-)56, 52(-44) m.y., Petrova et al. (2015) ages of (67-)65.5(-55) m.y., and Roalson and Roberts (2016) ages of (77.1-)69.7(-48.2) m.y. for this node, all rather older.
2. Gesnerioideae Link
3-desoxyanthocyanins +, chalcones, aurones 0; seeds without surface ornamentation, cells much elongated, spirally arranged (ornamented; shorter; not spirally arranged); endosperm conspicuous; GCyc2 gene lost.
75/960 - five tribes below. Predominantly Neotropical, a few S.W. Pacific, East Asia. [Photo - Flower.]
Age. Crown-group Gesnerioideae can be dated to (48.7-)36.2(-32.3) m.y.a. (Perret et al. 2012), (66.2-)46.8(-40.3) m.y. (Roalson & Roberts 2016) or ca 41.9 m.y. (Petrova et al. 2015).
2a. Coronanthereae Fritsch
Trees to ± shrubby-herbaceous, (rooting from the nodes); stomata anomocytic (paracytic); (inflorescence racemose - Pagothyra); (flowers polysymmetric); (C fringed); (A 2 [adaxial pair]; 5); nectary embedded in G wall, vascularized from A traces; capsules septicidal (and loculicidal), (placentae fleshy), (fruit a berry); n = 37(-45); gcyc duplication.
9/23: Coronanthera (11). Solomon Islands, Antilles, New Caledonia, S. South America (map: red, from Burtt 1998).
Age. Crown-group Coronanthereae are (32.2-)9.5(-7.6) m.y.o. (Perret et al. 2012) or as much as (40.3-)23.2(-19.3) m.y. (Roalson & Roberts 2016).
2b. Titanotricheae W. T. Wang
Scaly rhizomes +; (stomata anomocytic); ± anisophyllous; inflorescence racemose, branched, with bulbils; testa striate-reticulate; n = 20.
1/1: Titanotrichum oldhamii. China, Japan, Taiwan (map: green above, from Fl. China v. 18. 1998).
2c. Gesnerieae Dumortier
(Plant with scaly rhizomes; tubers; moniliform root tubers); (raphides, styloids +); (nodes 3:3, split-laterals - Episcieae); (petiole bundles deeply arcuate to annular (medullary bundles +)); (stomata on raised mounds, usually single [= stomatal turrets]); (leaves spiral); (flowers resupinate); (K ± free), (C margins fimbriate); ovary superior to inferior, nectary vascularized from numerous vascular bundles in wall; fruit various, berry, loculicidal or septicidal + loculicidal capsule, with fleshy placentae or funicles ["display capsule"] or not; n = (8) 9 (10) 11 (12) 13-14 (16), polyploidy rare.
53/1500: Drymonia (140+), Alloplectus (75+), Nautilocalyx (70+), Paradrymonia (70+), Gesneria (60), Sinningia (60), Columnea (s.l. = 270+, s. str., 75+, + 4 genera, inc. Dalbergaria , Tricantha [75+]), Gesneria (50). New World (map: from Brummitt 2007, in part). [Photo - Leaves, Flower.]
Age. The crown-group age of Gesnerieae is (36.9-)31.7(-24.8) m.y. (Perret et al. 2012), ca 22.5 m.y. (Petrova et al. 2015), or (29.9-)27.3(-25.2) m.y. (Roalson & Roberts 2016).
Synonymy: Belloniaceae Martynov, Besleriaceae Rafinesque
7/225: Besleria (150). Tropical America, esp. northern Andes.
Age. The age of crown-group Beslerieae is ca 14 m.y. (Perret et al. 2012), ca 16 m.y. (Petrova et al. 2015), or (28.8-)22.6(-18.2) m.y. (Roalson & Roberts 2016).
Age. Crown-group Napeantheae are (12.7-)10(-7.1) m.y.o. (Roalson & Roberts 2016) or ca 5.5 m.y.o. (Perret et al. 2013).
3. Didymocarpoideae Arnott (= the old Cyrtandroideae)
(Plant body = leaf + inflorescence unit[s]); 3-desoxyanthocyanins 0, chalcones, aurones +; ?stomata; ovary wall not richly vascularized, nectary vascularized from A traces; testa cells little elongated; endosperm slight, cotyledons unequal, one accrescent.
71: 2,350 - two tribes below. Predominantly Old World, esp. South East Asia-Malesia and the Pacific (map: from van Steenis & van Balgooy 1966 [Malesia and Pacific]; Hilliard & Burtt 1971 [Africa].)
Age. The crown-group age of this clade is (54-)42(-28) m.y. (Perret et al. 2012), ca 61.2 m.y. (Petrova et al. 2015), or (75-)67.4(-46.6) m.y. (Roalson & Roberts 2016).
3a. Epithemateae C. B. Clarke
Dihydroxyphenolics [e.g. acteoside] 0; secretory canals; (medullary bundles + - Rhynchoglossum); cymes lacking bracteoles; (abaxial C lobe inside others in bud); (A 2 [adaxial pair]); (nectary variously vascularized); (placentation axile), ovary short, abruptly narrowed into the style; integument 2-3 cells across [Platystemma]; endosperm ?0; n = (8-)10(-12); (seedling primary root not developed).
6/80: Monophyllaea (35+). Predominantly Indo-Malesia, 1 sp. West Africa, 1 sp. (Rhynchoglossum azureum) southern Mexico to Peru.
Age. The age of crown-group Epithemateae is (74.1-)64.7(-48.5) m.y. (Roalson & Roberts 2016).
3b. Trichosporeae Nees
(Plant woody); (nodes 1:1 with split laterals; 3:3 with split laterals; 5:5); (sclereids +); A (2 [abaxial pair, as in Streptocarpus]), staminodes 0-3, (anthers not coherent); placentae lamelliform-recurved, ovules restricted to distal end, ovary gradually narrowed into the style; (ovules hemitropous); (fruit with septicidal and loculicidal dehiscence), (± elongated, twisted), (circumscissile), (a berry); (testa cells with [extremely long] hairs); n = (4, 8) 9-11 (12, 13) 14-17, etc., polyploidy not uncommon.
82/2,275: Cyrtandra (652-818), Aeschynanthus (185), Streptocarpus (175), Primulina (150), Paraboea (130), Codonoboea (120), Agalmyla (100), Didymocarpus (100), Oreocharis (85), Henckelia (56), Microchirita (36). S. Europe (scattered), Old World, mostly Sri Lanka to Malesia (especially southern China) and the Pacific to Hawaii.
Age. Crown-group Trichosporeae are (72.8-)63.6(-43.6) m.y.o. (Roalson & Roberts 2016).
Synonymy: Cyrtandraceae Jack, Didymocarpaceae D. Don, Ramondaceae Godron
Evolution. Divergence & Distribution. Roalson and Roberts (2016) give dates for numerous clades in the family in the course of their discussion about diversification within it; Perret et al. (2012) give ages for tribes in Gesnerioideae and Petrova et al. (2015) dates throughout the family, mostly rather younger than those in Roalson and Roberts (2016).
Within Gesnerioideae-Coronanthereae there seems to have been one (Smith et al. 2006) or two (Woo et al. 2011) E. to W. dispersal events across the Pacific. Diversification in the New World Gloxinieae occurred some 30-20 m.y.a. (Roalson et al. 2008b: see also biogeographic relationships; estimate in Perret et al. 2012 somewhat younger at (25.0-)21.7(-14.8) m.y.). Didymocarpoideae-Didymocarpeae: Möller and Cronk (2002) discussed biogeographic relationships within the large African genus Streptocarpus. Cyrtandra, with its baccate fruits, is a very speciose genus found throughout Malesia, diversification beginning ca 48 m.y.a., although at ca 17.3 and 11.1 m.y.a, other estimates are very much younger (M. A. Johnson et al. 2017; Roalson & Roberts 2016), and it is particularly speciose in places like New Guinea (Clark et al. 2009). It is also widely distributed in the Pacific, the species there forming a single clade, and it has been called a "supertramp" genus (Cronk et al. 2005), although surprisingly, perhaps, it is absent from the New Caledonian mainland (c.f. Psychotria s.l.). Fiji may have been the first area in the Pacific to be colonized (from the west) 11.4-8.9 m.y.a. (Clark et al. 2009), and the orange-fruited C. taviunensis is sister to the rest of the Pacific species (Johnson et al. 2017). The Hawaiian colonization, also from the west, was independent of that of the other Pacific islands and radiation there has happened within the last 5 m.y. (Clark et al. 2009; see also Roalson & Clark 2016 and Johnson et al. 2017 for more ages). There are several (5-11) Fijian clades, and as relationships become clarified numerous dispersal events in the Pacific and even within the Hawaiian archipelago are needed to explain the distribution of the genus, and most of these are west to east (Johnson et al. 2017). Indeed, species that can grow at low altitudes near the coast may be important in range extensions, with subsequent diversification in upland forest habitats (Johnson et al. 2017) - shades of E. O. Wilson's taxon cycles in Melanesian ants (Wilson 1961). There are now ca 60 endemic species on the Hawaiian islands, many very localized and kept apart via post-zygotic barriers such as reduced survivorship of seedlings; the species may have arisen in allopatry (Johnson et al. 2015; Lim & Marshall 2017: pattern of diversification on the islands). In both Hawaii and Fiji up to eight species may grow in sympatry.
There is extensive diversification in both flower and fruit in the speciose Gesnerioideae-Episcieae (Clark et al. (2011, 2012) and in floral variation in Petrocosmea (Didymocarpoideae), with both strongly monosymmetric (specialization, coevolution[?]) and almost polysymmetric (generalist) flowers, unfortunately, nothing seems to be known about their pollinators, although buzz pollination for at least some seems likely (Z.-J. Qiu et al. 2015). Roalson and Roberts (2016) noted five major increases in diversification rates in the family, including Pacific Cyrtandra. The others include Beslerieae, core Nematanthus, core Columneinae and core Streptocarpus. In the New World clades pollination by humming birds, accompanied by shifts in corolla colour to red, have been important, and Columneinae are epiphytic, although how that might interact with diversification is unclear; in the Old World bird pollination is less important and shifts in corolla colour have been back and forth between white and purple. In core Streptocarpus (African) the distinctive unifoliate growth habit, or perhaps more general variation in growth form, seems to have spurred diversification (Roalson & Roberts 2016).
The centres of diversity of both neotropical Gesneriaceae and of hummingbirds are in the Colombia-Ecuador region (Weber 2011; Ericaceae-Vaccinieae are also abundant here), but bird-pollinated Gesneriaceae are spread throughout Central and South America. Roalson and Roberts (2016) dated three major clades dominated by hummingbird pollination to 22.4[Columneinae]-15.2 m.y.a., while Serrano-Serrano et al. (2017) noted that diversification in Gesnerioideae increased (25.5-)18.5(-5) m.y.a. and that hummingbirds may have arrived in South America 25-20.3 m.y.a., so the birds may have spurred this diversification. Serrano-Serrano et al. (2017) estimated that there have been (41.5-)31.5(-21.5) shifts to hummingbird from insect (bee) pollination, the latter probably being the original condition for Gesnerioideae, and these shifts were often near the base of large clades that subsequently had very high subsequent diversification rates. The shifts had occurred throughout the range of the subfamily and in different biomes; overall ca 60% of Gesnerioideae they studied (351/590) were bird-pollinated (Serrano-Serrano et al. 2017), so Wiehler's (1978) estimate of some 600 bird-pollinated species in the subfamily seems to be on the mark. Serrano-Serrano et al. (2017) discuss other factors, including the adoption of the epiphytic habit, that may also have increased speciation. Zingiberales-Heliconiaceae, also commonly pollinated by hummingbirds and around 29-22 m.y.o. is another hummingbird-plant association that is quite old, as are bird-pollinated , ca 14 m.y.o.; Ericaceae-Vaccinieae may be a third case. For the diversity of bird-pollinated taxa of Gondwanan origin in tropical and premontane parts of the northern Andes, see Gentry (1982), and for hummingbird pollination in generak, see below.
Ecology & Physiology. Although many Gesneriaceae are almost succulent or quite delicate herbs, a surprising number grow on exposed rocks (Haberlea rhodopensis and Boea hygrometrica are examples) and are homoiochlorophyllous (their chloroplasts do not break down) resurrection plants tolerating extreme dessication (Burtt 1998; Bogacheva et al. 2013; Gall & Oliver 2013 for literature). Along with sucrose, involved in stabilizing phospholipid bilayers in such situations (e.g. Proctor & Tuba 2002; Gaff & Oliver 2013), galactose oligosaccharides are quite abundant in the dried leaf (Albini et al. 1999; see also Navari et al. 1995). In a genome-level analysis of Boea hygrometrica the resurrection syndrome includes protection of the photosynthetic apparatus during drying and the rapid resumption of protein synthesis upon wetting, in part achieved by regulatory changes (Xiao et al. 2015; see also L. Wang et al. 2009); the authors note that both seeds and pollen tend to be dessication tolerant (the "source" of genes involved in dessication tolerance in other taxa - e.g. Oliver et al. 2005; Gaff & Oliver 2013; Costa et al. 2017). The genome is not particularly small, unlike those of at least some other extremophiles (Baniaga et al. 2016), although it may also be quite large in other angiosperm xerophytes (e.g. Farrant et al. 2015). For dessication tolerance in Haberlea rhodopensis, see Gechev et al. (2013).
Epiphytes are common, with well over 400 epiphytic species in neotropical Episcieae alone (Madison 1977; Weber 1978; Gentry & Dodson 1987); adoption of the epiphytic habitat seems not to be associated with the evolution of extreme dessication tolerance, although the epiphytic habitat is associated with water stress, as in Orchidaceae. Although Zotz (2013) estimated that there were only 570 epiphytic species in the whole family, of which he noted that ca 275 were in the Old World Aeschynanthus and Agalmyla, a figure of ca 700 species seems likely (Melastomataceae and Piperaceae are the other two big epiphytic families in broad-leaved angiosperms). The evolution of epiphytism within Coronanthereae is described by Salinas et al. (2010).
Water calyces are known from some Gesneriaceae (Carlson & Harms 2007).
Pollination Biology & Seed Dispersal. Considerable work has been carried out on pollination in Gesneriaceae - birds and bees are the major pollinators here. Wiehler (1978) estimated that perhaps 60% of neotropical Gesnerioideae - some 600 species - were humming-bird pollinated, including large genera like Columnea s.l. with well over 200 species, and he divided the floral morphologies involved into three common and one less common "types" - rather narrowly tubular; strongly and broadly bilabiate; with a narrow mouth and an asymmetrically swollen tube; and tubular, with the limb more or less rotate. Thus Perret et al. (2007) found that hummingbirds pollinated perhaps 2/3 of the ca 80 species of Sinningieae (= Ligeriinae), a group centred in the Atlantic Forest of Brazil, while Serrano-Serrano et al. (2015) looked at the complex interaction of floral traits associated with pollination (including flower size and resupination) and climate of some Gesnerioideae there. Diversification in bird-pollinated Gesneriaceae-Gesnerioideae increased (25.5-)18.5(-5) m.y.a. (Serrano-Serrano et al. 2017), and Roalson and Roberts (2016) suggested that hummingbird-pollinated clades in Columneinae were ca 22.4 m.y. old.
Another ca 30% of Gesnerioideae (ca 300 spp.) may be pollinated by euglossine bees of both sexes (c.f. Orchidaceae where male bees seeking scents are involved), and in these flowers the spreading corolla lobes sometimes have long-fimbriate margins (Wiehler 1978); divergence within euglossine bees began 42-27 m.y.a. (Ramírez et al. 2010) or (38-)26, 25(-17) m.y.a. (Cardinal & Danforth 2011; Martins et al. 2014a). Bee pollination is probably the original condition for Gesnerioideae, and Serrano-Serrano et al. (2017) estimated that there were later (95-)76(-58) switches from hummingbird back to bee pollination starting ca 5 m.y. after the evolution of bird-pollinated flowers, however, diversification in those clades was not great; overall ca 40% of Gesnerioideae (231/590) were insect pollinated, and the great majority of these are likely to be bee pollinated. Clark et al. (2015) described the floral morphologies associated with particular pollinators in Drymonia. Here the plesiomorphic condition is to have campanulate corollas and anthers with poricidal dehiscence, the visitors being euglossine bees. In a number of taxa the corolla was constricted in various ways, a condition that had arisen independently eight or so times, and the anthers opened by longitudinal slits - the normal condition for the family, but here derived - and the visitors were hummingbirds. Roalson et al. (2003) explored the diversity of floral morphology in Achimenes, while Alexandre et al. (2015) looked at the genetic background of changes of the elements of pollination syndromes in Rhytidophyllum - unlinked genes with at least moderate effects were involved.
Martén-Rodríguez et al. (2015, see also 2009, 2010) discussed the pollination of Antillean Gesneriaceae-Gesneriinae, comparing it with that of mainland taxa (belonging to other subtribes), noting that generalized and bat-pollinated taxa were proportionally more common on the islands (see also Alexandre et al. 2015; Serrano-Serrano et al. 2017, etc.). Self compatability is quite high in herbaceous, bird-pollinated Gesnerioideae, higher than in other bird-pollinated taxa considered (Wolowski et al. 2013).
Bird pollination is relatively less common in Old World Gesneriaceae, but it is likely to predominate in Aeschynanthus, which has some 185 species. Harrrison et al. (1999) discuss floral diversification in Streptocarpus, which includes species with strongly monosymmetric flowers as well as Saintpaulia, with almost polysymmetric flowers, so encompassing very different floral morphologies and pollinators. For instance, the almost polysymmetric Saintpaulia-type flowers have the buzz pollination syndrome (Clark et al. 2011).
More or less polysymmetric flowers - the corolla is radial and rotate, although the androecium is often technically monosymmetric - have arisen independently several times in the family, the ten or so genera involved not being immediately related (e.g. Burtt 1970; Smith et al. 2004a), indeed, polysymmetric flowers are notably abundant here compared with some other core lamialean families (Endress 1997a). For floral development in Bournea, early monosymmetric, later polysymmetric, floral symmetry genes being expressed early and down-regulated later, see Zhong and Kellogg (2015). Relatively little is known about the pollination of such flowers, although buzz-pollination has sometimes been recorded (Clark et al. 2011 and references).
Flowers with inverted orientation are known from some Episcieae (= Gesnerieae) (Clark & Zimmer 2003); they seem to have evolved ca 3 times. This inverted orientation is evident from the very earliest stages of the ontogeny of the flower, and since there is no twisting of the pedicel (Clark et al. 2006), they are not resupinate by some definitions (see also Serrano-Serrano et al. 2015 for the diversification of resupinate clades).
There is rather strange synchronized flowering in Monophyllaea glabra, all the plants in a population starting to flower simultaneously, whatever their size (Ayano et al. 2005).
Many Gesneriaceae have capsular fruits with wind dispersed seeds. Splash-cup dispersal is quite common, occurring in around 190 or more species from the New World alone. The species involved grow in damp, forest floor/stream side type conditions; a persistent calyx may form the cup (Ertelt 2013). In the New World birds and perhaps other animals may disperse Gesneriaceae, either eating fleshy fruits in their entirety or the glistening black seeds exposed on a fleshy placenta or swollen funicles, in turn displayed against the coloured inside of the capsule wall (and sometimes surrounded by a coloured calyx). Other variants of fleshy capsule/drupe fruit type are quite common (Weber 2004b; Clark et al. 2006, 2012). In the Old World, the speciose Cyrtandra has berries.
Plant-Animal Interactions. Gesneriaceae are not often eaten by lepidopteran caterpillars (Ehrlich & Raven 1964). In both the Old and New World tropics, some epiphytic Gesneriaceae may live in ant gardens (Orivel & Leroy 2011).
Vegetative Variation. Variation in growth patterns in this family is considerable (see Weber 2004 for a useful survey). The architecture of some Didymocarpoideae (= the old Cyrtandroideae) is particularly diverse and distinctive. Streptocarpus (Didymocarpeae) shows much variation in growth patterns. Some species have only a single, huge, ever-growing cotyledon, although an abscission zone forms when growing conditions become unfavourable, a part of the leaf being lost. Others species are shrubs over 1 m tall (e.g. Hilliard & Burtt 1971; Jong & Burtt 1975; Nishii et al. 2015). The evolution of growth form here has many parallelisms - thus the unifoliate growth form has evolved more than once - and reversals, as well as being linked with other life history variables, such as age to flowering and flowering periodicity (Möller & Cronk 2001). Jong and Burtt 1975) thought that the ever-growing cotyledon of Streptocarpus, which they called a phyllomorph, was an example of the evolution of morphological novelty. However, Kaplan (1997, 1: ch. 6) suggested that such cotyledons were an extreme example of the dominance of the leaf in development, the apical meristem effectively having been evicted - perhaps the same story from a different perspective. Harrison et al. (2005a) found that genes involved in shoot development were now expressed on the petiole (= petiolode) in rosulate species of the genus, plants producing leaves, etc., from the petiole, but these genes were not expressed in strictly unifoliate species. Mantegazza et al. (2009) also suggested that the developmental pathways controlling meristem development appear to have become relocalised (see also Nishii & Nagata 2007). Foliar meristem activity ceases on flowering, so unifoliate species are monocarpic (Jong 1978: Hilliard & Burtt 1971). The petiolode of Streptocarpus, at least, is unifacial, although not at the seedling stage, when it is bifacial (Tononi et al. 2010). Interestingly, caulescent species, although looking rather ordinary vegetatively, just like the unifoliate and rosulate species initially lack an embryonic shoot apical meristem (SAM), and their SAM develops post-embryogenically (Hilliard & Burtt 1971; Imaichi et al. 2007); leaves of these caulescent species also show prolonged basal meristem activity (Nishii et al. 2010). This prolonged foliar meristem activity involves the expression of KNOX1 genes, so maintaining an undifferentiated state in the leaves (Nishii et al. 2010). Jong et al. (2012) discussed the morphology and anatomy of two woody Madagascan species of the genus. Interestingly, Microchirita initially develops a single large cotyledonary leaf, and flowers may develop at the apex of its petiole, but the normal plant body here is a herb to shrublet with opposite leaves that have flowers in their axils or along the petioles; the result is there can be much variation within a single population (Puglisi & Middleton 2017). Beaufort-Murphy (1984: check taxa and classification) found that Cyrtandroideae were much more responsive to growth hormones than than Didymocarpoideae.
Within Epithemateae, too, anisophylly is common. The plant body of many species of Monophyllaea is rather like that of Streptocarpus, consisting of a single, ever-growing structure that is derived from a single cotyledon. A meristem develops at the base of the cotyledon blade, and inflorescences later develop at the base of the phyllomorph; in some species (= the old genus Moultonia) the flowers arise along the midrib of the phyllomorph blade rather than from separate inflorescences (Burtt 1978; Imaichi et al. 2001; see also Tsukaya 2005; Ishikawa et al. 2017). The cotyledon that keeps on growing is the one that is exposed to more light (Saueregger & Weber 2005). In some species of Monophyllaea the plant body becomes more complex by repetition of the cotyledonary unit. Ishikawa et al. (2017) discuss differences in the development of the phyllomorphs in Streptocarpus and Monophyllaea, and there is also variation in whether the first root is exogenous or endogenous (Ayano et al. 2005; Imaichi et al. 2007).
The radicle of the seedling may not develop in Monophyllaea, and this has also been noted in other Epithemateae (Imaichi et al. 2001). Taxa like Rhynchoglossum have two-ranked leaves with very aymmetrical blades; vegetatively they look rather like Begonia or Pentaphragma, which grow in similar habitats in the same general area.
Monophylly and some forms of anisophylly seem to be adaptations for life on rocks and/or shady conditions. Monophyllous Gesneriaceae grow in on rocks in cracks and the single leaf hangs down and covers the rock surface quite efficiently; that the better lighted cotyledon of Monophyllaea is the one that develops make sense in this context. Plants whose stems consist of sprays of alternating leaves - if they are opposite, then there is often strong anisophylly, as in Pilea (Urticaceae) - are also common in such situations; again, a photosynthetic surface covering the rock is deployed. For anisocotyly in general - more accurately, one cotyledon is accrescent - and its development in Didymocarpoideae, see Burtt (1970) and Saueregger and Weber (2004).
Chemistry, Morphology, etc. Secondary metabolites (lack of iridoids, presence of the caffeoyl phenylethanoid glycoside, sanangoside) seem to suggest an association between Sanango and Gesnerioideae in particular (Jensen 1996).
There is quite a lot of anatomical variation to be integrated with the clades above; this would surely repay the effort involved. For example, stem sclereids are common; Aeschynanthus has strongly U-thickened sclereids in the pericycle, other taxa lack fibres or sclereids in the pericyclic position; some taxa have lignified hairs; and Gesneria has a U-shaped petiole bundle cradling a unmedullated circle of vascular tissue, and there are also two wing bundles, while in other taxa the petiole bundle may be annular, with adaxial bundles. Nodal anatomy is quite variable (see also Howard 1970; Jong et al. 2012). (In addition to its distinctive anatomy, Gesneria has spirally-inserted serrate leaves with an almost coriaceous texture - it looks quite ungesneriaceous.)
Song et al. (2009) found that CYC2 genes were involved in repression of the growth of both the single adaxial stamen and the abaxial stamen pair in Opithandra, so resulting in a flower with but two functional stamens, the adaxial stamen pair - c.f. Lentibulariaceae, where it is the abaxial stamen pair that remains fertile.
For more information, see Weber (1978 and references: Klugieae, Loxonieae), Burtt and Wiehler (1995), Wiehler (1983), Weber (2004a: excellent account, 2004b: history of classification), all general, Kvist and Pedersen (1986: phenolics), Wiehler (1970: vegetative anatomy, esp. Gesnerioideae), Weber (1973: inflorescence), Trapp (1956b: androecium), C. L. Wilson (1974a, b: nectary vascularization), Skog (1976: Gesnerieae s. str.), Citerne et al. (2000), Smith et al. (2004a), and Zhou et al. (2008: all molecular details of floral development), Erbar (2014: nectaries), Hildebrand (1872: seed hairs - chalazal prolongation, also micropylar - in Aeschynanthus) and Beaufort-Murphy (1983: seeds under the S.E.M.), and Skog (1984), Möller and Kiehn (2004) and Christie et al. (2012), all cytology, considerable infra-generic variation. Pan et al. (2002) discussed the floral development of Titanotrichum (see below for phylogeny). Pollen variation is either uninformative or suggests problems in everything from species delimitation on up (Schlag-Edler & Kien 2001).
Dickison (1994), Jensen (1994, 1996), Norman (1994), and Wiehler (1994) all deal with Sanango.
Phylogeny. For an extensive summary, see Möller and Clark (2013). The relationships of Peltanthera are dealt with above; it has support as sister to [Calceolariaceae + Gesneriaceae]. Sanango is sister to [Gesnerioideae + Didymocarpoideae] (e.g. Perret et al. 2012; Refulio-Rodriguez & Olmstead 2014); within Epithematoideae, Epithemateae are sister to Trichosporeae, and their monophyly is well established - see Smith (1996), Smith et al. (1997a, b), Y.-Z. Wang et al. (2010), etc., and especially Mayer at al. (2003).
Didymocarpoideae. Within Trichosporeae, Haberlea and Ramonda, temperate, European, and with polysymmetric flowers and five stamens, may be sister to the rest (e.g. Mayer et al. 2003), or more likely near the base of the clade (Wei et al. 2010; Y. Z. Wang et al. 2010); they have dihydrocaffeoyl ester found nowhere else in flowering plants (Jensen 1996). Indeed, Möller et al. (2009) placed a number of small Asian and European clades all with four or five, rarely two, stamens as basal in Didymocarpoideae. Of these, the odd Jerdonia, from the Western Ghats, India, has pollen in tetrads, four parietal placentae, large seeds with alveolate endosperm, and n = 14 (Burtt 1977b); it may be sister to the rest of the subfamily (Möller et al. 2009). Wang et al. (2010: Jerdonia not included) found that Corallodiscus, the Ramonda clade, and Streptocarpus are successive branches in the phylogeny; taxa with radially symmetric flowers are scattered through the tree, while Z.-D. Chen et al. (2016: Chinese taxa) found a similar position for Corallodiscus.
Didymocarpus itself has been dismembered (Weber & Burtt 1998) and many species placed in Henckelia, although the limits of the latter were unclear (Möller et al. 2009; see also Middleton et al. 2013)). Within the diverse Cyrtandra, particularly speciose in places like New Guinea, all Pacific species studied are members of a single clade with a long branch, and within this clade Hawaiian species are monophyletic and possibly sister to the rest (Cronk et al. 2005; J. R. Clark et al. 2009; Atkins et al. 2013). The long branch of the Pacific species has been broken up by a clade of species from the Solomon Islands, and other clades of Solomon Islands species are in both the Pacific and Malesian parts of the tree (J. R. Clark et al. 2013). For relationships in Streptocarpus, which includes i.a. Saintpaulia, see Möller and Cronk (2001) and in particular the comprehensive analysis by Nishii et al. (2015). For a study of Aeschynanthus linking seed morphology and geography, see Denduangboripant et al. (2001). For a phylogeny of Chirita (= Henceklia) and relatives, see Y.-Z. Wang et al. (2011) and in particular Weber et al. (2011), and for relationships in an expanded Oreocharis, see Möller et al. (2011b). Puglisi et al. (2016) exmined relationships in Loxocarpinae. For the phylogeny of Petrocosmea, see Z.-J. Qiu et al. (2015).
Epithemateae are perhaps to include Cyrtandromoea (molecular data; branch lengths are long), but that genus is also sometimes placed in "Scrophulariaceae" - and it does have iridoids and is otherwise chemically similar to the latter; it also has endosperm, an exotesta with laminated, U-shaped thickenings in transverse section, the seeds are isocotylous, and the gynoecium is bilocular (Burtt 1965: q.v. for a revision). Burtt placed the genus in Scrophulariaceae and linked it with Leucocarpus (now in Phrymaceae). Chemistry - Napeanthus (Gesnerioideae) is also similar. More work is needed on these taxa. For Didymocarpoideae phylogeny, see also Möller et al. (2011a).
Gesnerioideae. Kotarski et al. (2007) found 80% bootstrap support for the position of Coronanthereae as sister to other Gesnerioideae, and Titanotrichum was sister to the remainder. Other studies also place the Old World but more or less isocotylar Titanotrichum basal in Gesnerioideae (C.-N. Wang et al. 2004: substantial amount of molecular data; c.f. D. Soltis et al. 2000; Albach et al. 2001), although that genus has also sometimes been placed in "Scrophulariaceae". Besleria and Napeanthus (n = 16) may also be near the base of the Gesnerioideae. In general agreement with these earlier studies, Perret et al. (2012) found basal relationships in Gesnerioideae to be [[Napeantheae + Beslerieae] [Coronathereae [Sinningieae + the rest]]]; Titanotrichum was sister to Napeanthus, and although neither Shuaria nor Cyrtandromoea were included in their study, there is little doubt about the placement of the former genus. See also de Araujo et al. (2016) for relationsips in this area. Serrano-Serrano et al. (2017) recovered the relationships [[Napeantheae + Beslerieae] Titanotricheae [Coronathereae + Gesnerieae]]]
For a phylogeny of Coronanthereae, see Smith et al. (2006) and Woo et al. (2011). Shuaria, a woody plant superficially similar to Sanango that sometimes also has "alternate" leaves, was placed firmly in Beslerieae (Clark et al. 2010; Serrano-Serrano et al. 2017). Relationships along the spine of Gesnerieae remain only weakly supported (e.g. Woo et al. 2011; Perret et al. 2012; de Araujo et al. 2016). However, there seem to be five well supported clades, Ligeriinae (= the old Sinningieae), Sphaerorrhizinae, Gesneriinae, Gloxiniinae, and Columneinae (= the old Episcieae) (Perret et al. 2012). For other relationships in Gesnerieae, see Smith (2001), Zimmer et al. (2002) and Smith et al. (2004a, b). See Skog (1976) for a revision of Gesneria and relationships in Gesneriinae. For the phylogeny and biogeographic relationships of Gloxiniinae, see Roalson et al. (2005 a, b; 2008b: relationships in Central America and the Antilles). For diversification in Beslerieae, see Roalson and Clark (2006) and in Ligeriinae, see Perret et al. (2003, 2006: the limits of Sinningia need adjusting). For relationships within Columneinae, see Clark and Smith (2009) and in Columnea itself, see Smith et al. (2013) and Schulte et al. (2014). For relationships around Alloplectus, now much reduced in size, see Clark and Zimmer (2003).
For a preliminary study of relationships in the complex Episcieae, see Clark et al. (2012); Smith and Clark (2014) found that a number of species were placed outside recognized genera.
Classification. Perret et al. (2012) were undecided as to the circumscription of the family, sometimes suggesting that it be broadened to include Peltanthera and Sanango, sometimes suggesting that those genera might be excluded. However, Peltanthera seems not to be immediately associated with Gesneriaceae (Refulio-Rodriguez & Olmstead 2014), while Sanango is. Weber et al. (2013) include it in the family, for which they provide a formal classification down to the subtribal level, which is being followed here (I will stop at tribes); the old tribes of Didymocarpoideae were decidedly unsatisfactory (Möller et al. 2009). See also the World Checklist and Bibliography of Gesneriaceae (Skog & Boggan 2005 a, b) and The Genera of Gesneriaceae (Weber & Skog 2007).
As might be expected of a family in which there are conspicuous flowers and much obvious adaptation to pollinators, many old genera that were based on floral characters have turned out to be unsatisfactory. Thus Clark et al. (2012) found that six of fifteen genera of Episcieae for which they sampled two or more species were para- or polyphyletic and Möller et al. (2011a) found that only 12/29 genera for which they sampled more than one species were monophyletic. However, much-needed changes are underway, and some changes in generic limits in New World Gesneriaceae are clearly explained in a series of articles in Gesneriads 56(3). 2006.
Some genera, perhaps most notably Chirita, are polyphyletic. For generic limits around Paradrymonia, see Mora and Clark (2016). Primulina, originally monotypic, has been greatly expanded in the course of understanding the limits of Chirita (Weber et al. 2011). There are also many monotypic genera, some of which are needed (Smith & Clark 2013), but others are not, thus Oreocharis has been expanded to include eleven mostly very small Chinese genera (Möller et al. 2011b). The huge Didymocarpus itself has been dismembered (Weber & Burtt 1998), species that had been included there being assigned to 27 genera (including two in Plantaginaceae); many species were placed in Henckelia, although this was not monophyletic, and it is now considerably restricted (Middleton et al. 2013). The limits of Paraboea have been adjusted (Puglisi et al. 2011), while Puglisi et al. (2016) revise generic limits in Loxocarpinae as a whole. Streptocarpus has been expanded, now including Saintpaulia, etc. (Nishii et al. 2015); chromosome number was the only feature characterizing the two major clades in the genus, hence the limits of the genus.
The large genus Cyrtandra has been broken up into some 40 sections, although the form any final classification here will take is unclear (Atkins 2013).
Previous Relationships. The limits of Gesneriaceae have by and large been quite stable, although Sanango has previously been placed in Loganiaceae or Buddlejaceae and it is still unclear if a few genera belong here or elsewhere in Lamiales (see above).
[Plantaginaceae [Scrophulariaceae [Stilbaceae [[Byblidaceae + Linderniaceae] [[Pedaliaceae, Martyniaceae, Acanthaceae] [Bignoniaceae [[[Schlegeliaceae + Lentibulariaceae] [Thomandersiaceae + Verbenaceae]] [Lamiaceae [Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]]]]]]]]]]: route II decarboxylated iridoids as glucosides [aucubin, catalpol widespread], 6- or 8-hydroxyflavones or 6 methoxyflavones +, cornosides 0; inflorescence racemose [lateral and main axes of inflorescence indeterminate]; (embryo sac haustoria +).
Age. Bremer et al. (2004) suggested an age of ca 76 m.y. for this node, Tank and Olmstead (2017) an age of (81.3-)70.2(-60.1) m.y., Cusimano and Wicke (2016) an age of (71.5-)65.9, 60.3(-56.7) m.y., Wikström et al. (2015) an age of (72-)62(-53) m.y., and Magallón et al. (2015: note topology) an age of around 52.9 m.y.; the age of (51.7-)31.5(-12.8) m.y. suggested by Naumann et al. (2013) is substantially younger.
Evolution. Divergence & Distribution. Node ages in Tank et al. (2015: Table S2) within this large clade are all less than 40 m.y., even if details of the tree topology there differ from those here.
Plant-Animal Interactions. Caterpillars of Nymphalinae-Melitaeini and -"Kallimini" (Juononiini, Victorinini) butterflies are quite common on plants in this group (see also Plantaginaceae, Acanthaceae and Orobanchaceae below). They may have moved here from the Urticaceae group of families (Rosales) around about the K/P boundary, a shift that may have been followed by an increased diversification rate (Fordyce 2010). Some Melitaeini in turn adopted members of Asteraceae as food plants (Nylin & Wahlberg 2008; Wahlberg et al. 2009; Nylin et al. 2014).
Chemistry, Morphology, etc. For the synthetic pathway of route II iridoids, see Jensen et al. (2002); 8-epi-irodial, 8-epi-iridotrial and 8-epi-deoxyloganic acid are the precursors. Iridioid acquisition seems best placed here, with an independent origin in Oleaceae (modified route I iridoids - Jensen et al. 2002). Flavonoid 7-O-glucosides and glucuroides are scattered in Lamiaceae, Pedaliaceae, and Plantaginaceae (Noguchi et al. 2009).
Extrafloral nectaries in this clade commonly consist of scattered multicellular trichomes (Zimmermann 1932).
PLANTAGINACEAE Jussieu, nom. cons. Back to Lamiales
Herbs (shrubs; rooted aquatics); (cardenolides [Digitalis], phloem loading not via intermediary cells, raffinose etc. not involved, mannitol, sorbitol +, iridoids 0), little oxalate accumulation; cork initiation various; (wood rayless); (leaf endodermis +); hairs with gland head not often vertically divided, (with cystolith); leaves also spiral, simple to compound; (inflorescence branches pair-flowered cymes), (bracteoles 0 - Antirrhineae); (corolla spurred; 0), (descending cochleate); stamens (2 [adaxial pair] + 2 staminodes [Trapella]; 2; 5-8), thecae parallel, end-to-end, sagittate, or on connective arms, confluent [Penstemon] or not, connective well developed, placentoids usu. 0, (staminode + - esp. Cheloneae, Antirrhineae); pollen exine tectate and reticulate; (placentation intrusive parietal), stigma (slightly) capitate or bilobed, dry (wet); ovules (>1/carpel), (campylotropous?), integument 3-22 cells across [3-6 cells in Gratioleae]; fruit a septicidal capsule (loculicidal - Veronica), (poricidal - Antirrhineae), (circumscissile); seeds (1-)many, (pedestals +), (variously sculpted/winged), exotestal cells with inner walls ± thickened, when winged, cells with reticulate thickenings, (mesotesta to 4 cells across); endosperm +/0, mannose-rich polysaccharides + [?distribution], (embryo chlorophyllous), (short), (curved), (suspensor long); n = 6-10+; nuclear genome [1C] (313-)947(-4523) Mb; protein bodies in nucleus amorphous (not - Angelonieae and Gratioleae].
Ca 90 [list]/1,900: Veronica (ca 450), Penstemon (275), Plantago (275), Linaria (150: tubular protein bodies), Bacopa (55), Stemodia (55), Russelia (50), Callitriche (30). Mostly temperate (map: from van Steenis & van Balgooy 1966; Hultén 1971; Meusel et al. 1978; Frankenberg & Klaus 1980; Hong 1983; Heide-Jørgensen 2008). [Photos - Callitriche Habit, Hippuris Habit, Veronica Flower.]
Age. Bell et al. (2010: note sampling) suggested an age of (57-)46, 42(-34) m.y. for crown Plantaginaceae; an age of ca 66 m.y. was suggested by Bremer et al. (2004), (79.2-)66.5(-53.1) m.y. by Tank and Olmstead (2017) and an age of (62-)50(-37) m.y. by Wikström et al. (2015); Meudt et al. (2015b) dated a clade [Globularia + Veronica] to ca 28 m.y., while the age of a clade [Globularia [Plantago + Digitalis]] was estimated as ca 27.5 m.y.a. (Affenzeller et al. 2018).
Evolution: Divergence & Distribution. Clades of Plantaginaceae such as Hebe (deeply embedded in Veronica), Ourisia, Penstemon and Globularia have radiated, sometimes very extensively, in alpine habitats in various areas throughout the world (Madriñán et al. 2013; Hughes & Atchison 2015; Affenzeller et al. 2018). Indeed, Hebe, centred in New Zealand but absent from New Caledonia, is the largest lineage of woody angiosperms there (Wagstaff & Garnock Jones 1998), although the distributions of its segregates are unlikely to have anything to do with Gondwanan vicariance and the microphylly of some of the species is unlikely to have been inherited from gymnosperm ancestors (c.f. Heads 1994 and references). In Veronica s.l. no correlation was initially found between speciation rates and rate of molecular evolution (K. Müller & Albach 2010). However, in a comprehensive study Meudt et al. (2015b, q.v. for dates, etc.) found genome size to be reduced in polyploid taxa, there were smaller genomes in annuals than perennials, and decrease in genome size was linked with increased diversification rates. For more on the evolution of Veronica, see also Rojas-Andrés et al. (2015).
The Plantago clade is 5-17 m.y. old (Cho et al. 2004; Rønsted et al. 2002b); for relationships within it, see Rønsted et al. (2002b, also Rahn 1996: morphological analysis). The mucilaginous seed coats of Plantago may have facilitated the three dispersals of this genus from Australia to New Zealand (Tay et al. 2010). Within Antirrhineae there are perhaps four independent connections between Californian and Mediterranean members of the tribe that have been dated to some time in the Miocene around (30-)21-19(-4) m.y.a., mostly well before the origin of the Mediterranean climates that they now prefer (Vargas et al. 2014).
For the biogeography of Antirrhineae, world-wide but mostly Mediterranean, see Ogutcen and Vamosi (2016); long distance dispersal accompanied by polyploidy may be involved.
Details of characters like the distribution of R-Put morphologies and the timing of androecium initiation remain to be clarified, and morphological/developmental synapomorphies for Plantaginaceae may yet be found.
Ecology & Physiology. Philcoxia, a recently described white sand endemic from Brasil, was suspected of being carnivorous (Fritsch et al. 2007). This has been confirmed by Pereira et al. (2012): Nematodes stick to the glandular secretions covering the leaves, which are underground, and are then digested by the plant; phosphatase activity has been detected in the hairs. The plants lack mycorrhizae, as is common when there is carnivory - but absence of mycorrhizae is a feature of core Lamiales in general... (see also papers in Ellison and Adamec 2018).
Extreme dessication tolerance is known from several species in a few genera in the Lindernieae area (Gaff & Oliver 2013), of which Craterostigma, whose walls reversibly collapse as the plant dries, has been quite extensively studied (e.g. Vicré et al. 2004a). The plants are homoiochlorophyllous, retaining their photosynthetic apparatus and chlorophyll, during the drying process, and as in other dessication-tolerant angiosperms late embryogenesis abundant proteins have been coopted in the process, and also water-stress-related genes also found in dessication-sensitive plans are involved, but they are expressed differently (Rodriguez et al. 2010). Chamaegigas intrepidus is a dessication-tolerant aquatic(!) in seasonal pools on African inselbergs (Porembski & Barthlott 2000).
The submersed (at least for part of its life) aquatic Litorella uniflora (= Plantago) is a CAM plant (Keeley 1998).
Pollination Biology & Seed Dispersal. Floral morphology is very variable (see Reeves & Olmstead 1998), but Plantaginaceae are pollinated mainly by large insects and birds. Some kind of spur has evolved two to three times in Antirrhineae (Glover et al. 2015), and Vogel (1998b) discussed how nectar gets in to the spur. Guzmán et al. (2015) thought that the tribe as a whole could be characterized by a personate corolla, with its mask-like face, and in a number of species the pollinators (bees) have to exert substantial force to open the tube. The South American Monttea and Angelonia have weakly bisaccate oil-producing corollas; in the latter genus the visiting bees have either their front (Centris) or middle (Tapinotaspis) legs elongated (Sérsic & Cocucci 1999; Machado et al. 2002; Martins et al. 2013). At least 30 species in Angelonieae produce oil from hairs inside the corolla, although the bees may sometimes also pick up nectar or pollen; there may have been four or five gains of oil pollination (Martins & Alves-dos-Santos 2013; Martins et al. 2014b, see also 2013; Possobom & Machado 2017a and references). Collinsia has remarkable papilionoid flowers. The distinctively bicolored and erect standard is formed from the two adaxial petals, while the three other petals are flat-coloured, the median abaxial petal forming a keel that encloses the stamens. Indeed, the overall colour scheme and functional floral morphology is very like that of some species of Lupinus (see Armbruster et al. 2009a; Baldwin et al. 2011; Armbruster 2014 for floral evolution and pollination; Kampny 1995, as Scrophulariaceae, for pollination).
P. Wilson et al. (2006, 2007; see also Wessinger et al. 2016) discussed the up to 21 shifts from bee to bird pollination in Penstemon s.l., a speciose North American genus often with a prominent bearded staminode, noting morphological changes that both facilitate hummingbirds and prevent bees pollinating the flowers (see also Castellanos et al. 2004: results not always straightforward). Over 40 species are pollinated by hummingbirds, but none of the bird-pollinated clades is of any size, as is common in more temperate bird-pollinated groups, at least (Abrahamczyk & Renner 2015: ten shifts). Bird pollination has evolved from bee pollination, and there have apparently been no switches in the opposite direction (see also Barrett 2013). For pollination - in New World taxa, hummingbirds involved again - in Antirrhineae, see Ogutcen et al. (2017) and Guzmán et al. (2017).
Pollination in the aquatic Callitriche may be by wind or under water (= hypohydrophily), or self pollination may occur; the latter two mechanisms evolved once in the genus. In self pollination the pollen grains germinate in the anthers of a staminate flower and grow through the stem, etc., to the ovules of an adjacent carpellate flower (Osborn & Philbrick 1994; Philbrick & Les 2000; X.-F. Wang et al. 2011). Although in gross morphology the species of the genus are quite similar, the pollen of C. hermaphroditica, which is hypohyrophilous, may entirely lack exine, and the grains germinate in the anthers (Osborn & Philbrick 1994) - pollen grain + tube makes a better search vehicle? There have been several transitions from aquatic to terrestrial habitats (Ito et al. 2017b).
Muñoz-Centeno et al. (2006) discuss seed morphology in the context of the phylogeny of Plantago; the seeds have mucilaginous coats (see also Western 2011 for myxospermy in the family).
Plant-Animal Interactions. For feeding preferences of a variety of insect groups that might suggest that the erstwhile Plantaginaceae s. str. and Scrophulariaceae s. l. are close, see Airy Shaw (1958), Allen (1960, 1961) and Tempère (1969). Allen (1960) found different insects eating Plantaginaceae s. str. and Scrophulariaceae s. str. (see also below). Larvae of Nymphalinae-Melitaeini butterflies are commonly found here and on Orobanchaceae, but not on Scrophulariaceae s. str. (Wahlberg 2001). Agromyzid dipteran leaf miners have diversified on Plantaginaceae (Winkler et al. 2009).
Genes & Genomes. For genome size, etc., and the evolution of Veronica, see above.
Bakker et al. (2006a) found major increases in the rate of evolution of the mitochondrial gene nad1 in Plantago and Littorella; Plantago has substitution rates at synonymous sites in the mitochondrial genome that are 3,000-4,000 times those of nearly all other angiosperm clades (Cho et al. 2004; Mower et al. 2007). At least three mitochondrial genes have recently been transferred from Cuscuta to species of the Plantago coronopus group, although for the most part they do not seem to be functional there (Mower et al. 2010). The cox1 intron is common in the family, and the cox1 gene itself has been been lost twice in Plantago, a loss not recorded in any other angiosperms (Sanchez-Puerta et al. 2008).
Some inverted repeat chloroplast genes in Plantago have very high synonymous substitution rates (Zhu et al. 2015).
Economic Importance. For Digitalis, a source of important drugs, see Luckner and Wichtl (2000).
Chemistry, Morphology, etc. Both Digitalis (and its synonym, Isoplexis) have cornosides. Iridoids with an 8,9 double bond - rather uncommon - occur in a number of genera (Jensen et al. 2007). At what level this character might be an apomorphy is unclear; they are to be found in both Veronica and Plantago (Rønsted et al. 2000). Veronica has mannitol (Taskova et al. 2012), while Plantago has sorbitol. P. Pedersen et al. (2007), Jensen et al. (2008a) and Maggi et al. (2009) report on some chemistry of ex-Hebe/Hebe s.l..
Penstemon is reported () to have a storied cambium. Veronica lyallii has successive subhypodermal phellogens (Gray 1937), while Besseya and Plantago have a foliar endodermis. Buds or branches may develop from the petioles of Philcoxia (Scatigna et al. 2015). R-Put morphology may be of interest. The cell walls in the heads of the glandular hairs are variously oriented. Lindernieae were until very recently included in Plantaginaceae but the heads of their glandular hairs are divided by vertical partitions. However, Russelia and some species of Penstemon, still in Plantaginaceae, also have such hairs (Raman 1991 and references).
Penstemon and a few other genera have paired-flower cymes (Weber 2013). The development of the petaloid calyx of Rhodochiton is not connected with the expression of B-class genes (Landis et al. 2012).
There has been much work on molecular aspects of floral development in Plantaginaceae (e.g. Hileman & Cubas 2009, Hileman 2014). Antirrhinum majus is a model organism used for understanding the development of monosymmetric flowers and the involvement of the CYC gene in this (e.g. Rosin & Kramer 2009; Preston et al. 2011 for references); duplication of the gene is evident in Antirrhineae, but not in Digitalis (Gübitz et al. 2003). Although similar genes are involved in the development of monosymmetric flowers in Senecio vulgaris (Asteraceae), they are expressed differently (see also discussion under Euasterids). Floral evolution in the Veronica/Plantago clade is becoming better understood. Veronica has an open, 4-lobed corolla, but only two stamens; some species have two main veins in the adaxial corolla lobe, perhaps suggesting that it is formed by the fusion of the two adaxial lobes of other members of the family. Wulfenia, sister to Veronica, has tubular and rather weakly lipped (2 + 3) flowers. Aragoa has 4-merous, polysymmetric flowers, but with five sepals. The flowers of Plantago, sister to Aragoa (e.g. Bello et al. 2002b), are small, polysymmetric, and in dense spikes; they have four sepals, petals and stamens, and are wind pollinated. Their evolution is connected with the degeneration of some floral symmetry genes, e.g. Cycloidea (Preston et al. 2011a). Bello et al. (2004) discuss floral evolution in the Plantago area, also emphasizing the evolution of polysymmetry. Sibthorpia has 5-8-merous, polysymmetric flowers; polysymmetric flowers have been derived from monosymmetric flowers several times in this family. Linaria has flowers with a single well-developed abaxial spur, but the polysymmetric Peloria mutant of Linaria vulgaris with five spurs is the result of epigenetic inactivation by methylation of the cycloidea gene which controls monosymmetry in Antirrhinum (Cubas et al. 1999).
In a number of taxa in Plantaginaceae the androecium is initiated before the corolla, but other patterns also occur, so the timing of androecium initiation is perhaps unlikely to be a synapomorphy for the family (Bello et al. 2004, c.f. Judd et al. 2002). Veronica/Plantago, as well as Digitalis, are members of a clade that has descending-cochleate aestivation (Bello et al. 2004), i.e. in bud the abaxial corolla lobes are outide the others. Petals have sometimes been lost in Synthyris (Hufford 1992b). Illustrations in Chatin (1874) suggest that the ovules of Veronica may be crassinucellate. The large, transversely elongated endothelial cells in vertical rows in Gratioleae cause their seeds to have longitudinal ridges, and the extotestal cells have hook-like thickenings.
For general information, see Rahn (1996: Plantago), Sutton (1988: Antirrhineae), Leins and Erbar (2004a: Hippuridaceae), Erbar and Leins (2004b: Callitrichaceae), Schwarzbach (2004: Plantaginaceae), Ihlenfeldt (2004) and Takhtajan (2013), both Trapellaceae, Fischer (2004b: Scrophulariaceae p. pte) and Wagenitz (2004: Globulariaceae). For chemistry, see Jensen (2005), Taskova et al. (2006), and Jensen et al. (2009c), for Trapella, see Oliver (1888), and for a general survey, see Thieret (1967). Additional information is provided by Kampny et al. (1993: floral development), De-yuan (1984): Veroniceae) and Tsymbalyuk and Mosyakin (2013), both pollen, Schmid (1906: ovules, Scrophulariaceae s.l.), Elisens (1985: seeds, considerable variation in Antirrhineae) and Ahedor and Elisens (2015: seeds, Gratiolinae), and Schrock and Palser (1967), Leins and Erbar (1988, 2010), and Endress (1999), all floral development.
Phylogeny. Plantaginaceae as here circumscribed initially had only rather weak support, e.g. Olmstead et al. (2001, as Veronicaceae: inclusion of Cheloneae and Hemimerideae may be the problem; for the latter, see Scrophulariaceae below), but see Oxelman et al. (2005: support stronger), and Tank et al. (2006, summary, as Veronicaceae), Z.-D. Chen et al. (2016), Chinese taxa, fair support, also Olmstead and Reeves (1995) and Reeves and Olmstead (1998).
Gratiolaceae were recognised as a distinct family by Rahmanzadeh et al. (2004), although only three species were examined; Rahmanzadeh et al. (2004) thought that Angelonieae might also be included and Limosella, here in Scrophulariaceae, was included without comment. Albach et al. (2005a) found relationships in a combined molecular tree to be [[Gratioleae + Angelonieae] [Cheloneae [Antirrhineae + The Rest]]]. However, Estes and Small (2008) placed Antirrhinum, along with members of Cheloneae and other tribes, in a clade sister to [Angelonieae + Gratioleae]; Limnophila was part of Gratioleae (1.0 p.p.), Limosella was not sampled. Kornhall and Bremer (2004) placed Limosella in Scrophulariaceae, but they did not look at other members of Gratiolaceae. Gratioleae, including Trapella (strong support for this position), and Angelonieae formed a clade sister to all other Plantaginaceae examined (see Gormley et al. 2015).
For the phylogeny of Antirrhineae, see Ghebrehiwit et al. (2003), Vargas et al. (2004), Guzmán et al. (2015) and Ogutcen and Vamosi (2016); some genera are not monophyletic, but both major patterns and details of relationships seem not to be stable yet. Fernândez-Mazuecos et al. (2013) discuss relatonships within Linaria (which is monophyletic). Bräuchler et al. (2004) discussed the phylogeny of the cardenolide-rich Digitalis (to include the bird-pollinated Isoplexis). For a phylogeny of Veroniceae, see Albach et al. (2004a, c, 2005c), Taskova et al. (2004, 2006), and Albach and Meudt (2010); the "new" molecular relationships are at least sometimes supported by other data such as chromosome number and iridoid type (Albach et al. 2004b, 2005c; Albach & Meudt 2010). The ca 125 species of the Hebe complex are found in New Zealand, except for a few from New Guinea (Albach et al. 2005b); the genus is polyphyletic. Albach (2008) discussed the limits of Veronica s.l., which is to include Hebe, etc.; for its chemistry, see Maggi et al. (2009 and references) and for its pollen, quite distinctive, see Tsymbaluk and Mosyakin (2013), Wulfenia is sister to the expanded genus (see also Bello et al. 2002b; Meudt et al. 2015b). For relationships in Plantago, which is to include Litorella, see Rahn (1996) and Rønsted et al. (2002b). Plantago is sister to the ericoid páramo shrublet Aragoa), both having more or less polysymmetric and 4-merous flowers (Bello et al. 2002b). Wolfe et al. (2006) outline phylogenetic relationships in Penstemon (see also P. Wilson et al. 2007; Wessinger et al. 2016); section Dasanthera may be sister to the rest of the genus. For the phylogeny of Collinsia and the related Tonella, see Baldwin et al. (2011) and for that of the ca 47 species of [Globularieae + Campylanthus], some 17 m.y.o., see Affenzeller et al. (2018: 9.6 m. - Poskea).
Classification. The circumscription of Plantaginaceae adopted here is broad on the one hand (it incorporates several highly divergent but small clades previously recognized as families, see above) but narrow on the other (it is but part of the old Scrophulariaceae). These small but florally very distinctive families are derived members of a clade that also includes numerous species with relatively large but undistinguished monosymmetric flowers. Maintaining them as distinct would entail the recognition of a number of other families that would be poorly characterised.
Rahmanzadeh et al. (2004) did not characterise their Gratiolaceae; they included the widespread Limosella (here Scrophulariaceae) and, somewhat hesitantly, Lindenbergia (here Orobanchaceae) along with 30 other genera. Souza and Lorenzi (2012) included ca 20 genera and 250 species in Gratiolaceae, among them the carnivore Philcoxia. Rahmanzadeh et al. (2004) thought that Angelonieae might also be part of their Gratiolaceae, but Souza and Lorenzi (2012) recognized an Angeloniaceae, often with oil flowers that have a spurred corolla (5 genera, with 30 species, were mentioned); Ourisia seems not to have been accounted for. Oxelman et al. (2005) located the majority of Gratiolaceae in Plantaginaceae; Limosella remained in Scrophulariaceae (see also Schäferhoff et al. 2010). Sampling of Plantaginaceae s.l. is still very poor, and little is gained by segregating at most poorly distinguishable clades as families. Campylanthaceae nom. nud. are mentioned in a flora of the Canary Islands (Muer et al. 2016); Campylanthus has flowers that seem to be held upside down, at least sometimes, and are more or less polysymmetric when viewed face-on, and there are two stamens.
Veronica is to be expanded to include Hebe, Parahebe, Synthyris, etc.; recognizing them would entail the recognition of ca 9 genera in the complex (e.g. Albach et al. 2004; Meudt et al. 2015b and references).
Previous Relationships. Both Cronquist (1891) and Takhtajan (1997) recognise several of the smaller families just mentioned, but they are in the same general part of their sequences; Cronquist had a notably broad circumscription of Globulariaceae and included a number of genera here placed in Scrophulariaceae. Trapella has been included in Pedaliaceae (e.g. Cronquist 1981), in part because its stoutly-spiny fruits appear to be so similar to those of Pedaliaceae.
Botanical Trivia. Linnaeus was initially so impressed with the distinctive morphology of the Peloria mutant, differing as it did so strikingly in floral (= generic) characters from Antirrhinum, that he proposed to place it in a genus of its own, but J. E. Smith sourly observed.
Thanks. I thank Dirk Albach for comments.
Synonymy: Angeloniaceae V. C. Souza, P. Dias & Udulutsch, Antirrhinaceae Persoon, Aragoaceae D. Don, Callitrichaceae Link, nom. cons., Chelonaceae Martynov, Digitalidaceae Martynov, Ellisophyllaceae Honda, Erinaceae Pfeiffer, Globulariaceae Candolle, nom. cons., Gratiolaceae Martynov, Hippuridaceae Vest, nom. cons., Linariaceae Berchtold & J. Presl, Littorellaceae Gray, Oxycladaceae Schnizlein, Psylliaceae Horaninow, Scopariaceae Trinius, Sibthorpiaceae D. Don, Trapellaceae Honda & Sakisaka, Veronicaceae Cassel
[Scrophulariaceae [Stilbaceae [[Byblidaceae + Linderniaceae] [[Lamiaceae [Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]]] [[Pedaliaceae, Martyniaceae, Acanthaceae] [Bignoniaceae [[[Schlegeliaceae + Lentibulariaceae] [Thomandersiaceae + Verbenaceae]] [Lamiaceae [Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]]]]]]]]]: cornosides at most uncommon.
Age. Bremer et al. (2004) suggested an age of ca 75 m.y. for this node, Tank and Olmstead (2017) an age of (76.8-)66.6(-57.4) m.y., and Wikström et al. (2015) an age of (67-)58(-49) m. years.
SCROPHULARIACEAE Jussieu, nom. cons. Back to Lamiales
Herbs to shrubs, (vines); harpagide, harpagioside [8ß-8α-methyl substituted iridoids] +, (secoiridoids +), little oxalate accumulation; nodes also 1:3 + girdling bundle; leaves (basally connate), (spiral above), lamina vernation flat, (± foliaceous, stipuliform structures +); inflorescence branches cymose; K unequal or not; anthers synthecous; tapetal cells binucleate; staminodia +/0; nectary small or 0; stigma capitate (lingulate), dry or wet; ovules many/carpel, campylotropous, integument 5-11(-12) cells across; fruit a capsule, septicidal (and apically loculicidal); seeds many, to 1.5 mm long; exotestal and endotestal cells with thickened inner walls; endosperm moderate; nuclear genome [1C] (349-)943(-1900) Mb; (protein crystal stacks in nucleus).
59 [list]/1,880 - 7 groups below. World wide (map: from Hultén 1958, 1971; van Steenis & van Balgooy 1966; Meusel et al. 1978; Leeuwenberg 1979; Hong 1983; Hilliard 1994; Norman 2000; Lebrun 1977, 1979 [Sahara]).
Age. Bremer et al. (2004: Buddleja included!) suggested an age of ca 68 m.y., Tank and Olmstead (2017) an age of (76.8-)66.6(-57.4) m.y., and Wikström et al. (2015) an age of (61-)50(-38) m.y. for this clade.
1. Hemimerideae Bentham
Annual to perennial herbs (shrublets); flowers strongly monosymmetric, (resupinate - Alonsoa); C spurs 0, 1, 2; staminodia 0; (pollen 3-, 6-8-colpate, 5-8-colporate); stigma capitate to weakly bilobed; seeds winged, testa alveolate; n = 7, 9.
6/150: Diascia (73), Nemesia (65). Africa-Madagascar, esp. South Africa, few tropical America.
Age. The Alonsoa-Nemesia split is estimated to be 62-59 m.y.o. (K. Bremer et al. 2004a) or 47.5-42 m.y.o. (Wikström et al. 2001); see Datson et al. (2008).
Synonymy: Caprariaceae Martynov, Hemimeridaceae Doweld
[[Aptosimieae [Myoporeae + Leucophylleae]] [Buddlejeae, etc. [Limoselleae + Scrophularieae]]]: ?
Age. Bell et al. (2010) estimated an age of (58-)53, 51(-45) m.y. for this clade (Buddleja was widely separated and sister to Paulowniaceae).
[Aptosimieae [Myoporeae + Leucophylleae]]: ?
2. Aptosimieae (Bentham) Bentham
(Annual) herbs to shrubs; flowers monosymmetric; staminode 0; pollen syncolporate, surface striate; stigma capitate-clavate to slightly bilobed; seeds rugose; endothelium with isodiamtric cube-shaped cells, walls equally thickened; n = ?
3/22: Aptosimum (20). Africa, drier areas, to India, Cape Verde Islands
[Myoporeae + Leucophylleae]: plant shrubby; lamina isobifacial, dorsiventrally flattened, pellucid gland dots +; pollen colpi diorate, surface reticulate (rugulate, etc.); style somewhat impressed.
3. Myoporeae Reichenbach
3A. Androya Perrier
Corolla subrotate, polysymmetric, tube very short; pollen colporate, surface smooth; stigma lingulate; ovules 2/carpel; capsule loculicidal; seeds two, winged.
1/1: Androya decaryi. Southern Madagascar.
3B. Other Myoporeae.
(hairs stellate); flowers strongly monosymmetric to polysymmetric; (ovary loculi often subdivided); stigmatic surface in a notch at tip of slender style (capitate); ovules (1-)2-8/carpel, pendulous to superposed, anatropous, epitropous; fruit a drupe or schizocarp; seeds 2-3 mm long; endosperm slight; n = 18.
4/240: Eremophila (215). Esp. Australia, a few species in tropical America, scattered from Mauritius to New Zealand, Hawaii. [Photo: Myoporaceae s. str. flower, also Myoporeae.]
Synonymy: Bontiaceae Horaninow, Myoporaceae R. Brown, nom. cons.
4. Leucophylleae Miers
Vascular tissue in a continuous ring; hairs usu. branched/stellate; stomata anisocytic; leaves (bifacial), (pellucid gland dots 0; foliar cavities +); flowers usu. weakly monosymmetric to polysymmetric; K divided to near base; (A 2, 5), anthers synthecous; style tips expanded and flattened, stigmas along the margins; ovules (1/carpel); (seeds to 2 mm long); n = 17.
1/20. S.W. U.S.A. to tropical America.
[Buddlejeae, etc. [Limoselleae + Scrophularieae]]: ?
5. Buddlejeae Bartling (inc. Teedieae Bentham, etc.)
Shrubs to trees; vessel elements with helical thickenings; (cork inner cortical/pericyclic); (?plant dioecious); flowers often polysymmetric; A (thecae separate), pollen (4-colpate), surface smooth, orbicules 0; (G 4-locular), stigma globose to ± bifid; hypostase +; (fruit a berry), seeds winged or not, (alveolate); exotestal cells ± longitudinally elongated, inner walls thickened; endosperm +, chalazal haustorium single large cell; n = 14, 15, 19, etc..
(Buddleja 108). The Americas, Asia, Africa and Madagascar.
Synonymy: Buddlejaceae K. Wilhelm, nom. cons., Oftiaceae Takhtajan & Reveal
[Limoselleae + Scrophularieae]]: testa alveolate.
6. Limoselleae Dumortier (inc. Manuleeae and Selagineae)
± Ericoid shrubs to (annual) herbs; (bract adnate to C [recaulescent]); (K 3-8), deeply lobed to connate; C often ± polysymmetric, adaxial lobes external in bud, (4:0 - Hebenstretia); A (2, 5), filaments (broadened upwards); pollen surface reticulate; nectary asymmetrical, adaxial (0); stigma lingulate, with marginal papillae (bifid), (punctate with terminal papillae); (ovules 1-)many/carpel, apotropous or epitropous, obturator +; fruit often a 2-seeded schizocarp (indehiscent), pedestals/cushion-shaped scars on the placentae, (funicles massive - Selago, etc.); seeds small (not alveolate); testa often rather thin, inner cuticle massively developed; n = 6-8(-10).
27/640: Selago (190), Jamesbrittenia (85), Manulea (75), Zaluzianskya (57), Sutera (49), Chaenostoma (46). Especially southern Africa, also temperate northern hemisphere (Limosella).
Synonymy: Hebenstretiaceae Horaninow, Limosellaceae J. Agardh, Selaginaceae Choisy, nom. cons.
7. Scrophularieae Dumortier
Annual herbs to shrublets; (A 5 - Verbascum), staminodes often well developed, (orbicules 0 - Verbascum); stigma ± capitate; n = 9, 13, 15-18.
6/575: Verbascum (360), Scrophularia (200). North Temperate, to the Caribbean, few Africa. [Photo - Flower].
Synonymy: Verbascaceae Berchtold & J. Presl
Evolution: Divergence & Distribution. Scrophulariaceae are very diverse in southern Africa, having some 700 species there (Johnson 2010).
Ecology & Physiology. The corms of Limosella grandiflora perennate in a state of extreme dessication (Gaff & Oliver 2013). Annual species are quite common in southern Africa, the ca 50 species of annuals in Nemesia representing 3-4 evolutionary origins of the habit (Datson et al. 2008). There are a number of vines in the family (see Sousa-Baena et al. 2018b and references).
Pollination Biology & Seed Dispersal. Scrophulariaceae include a number of species that have oil-flowers with oil-secreting hairs (Vogel 1974; Vogel & Cocucci 1995 for a list; Renner & Schaefer 2010; Martins et al. 2013; Possobom & Machado 2017a and references). Details of the pollination of the remarkable two-spurred oil-flowers of the southern African Diascia are quite well known. Several species of the melittid bee Rediviva collect oil from the oil-secreting hairs in the spurs using their sometimes remarkably elongated front pair of legs which have special hairs that absorb oils (Vogel 1984; Steiner 1990; Rasmussen & Olesen 2000; Steiner & Whitehead 1990, 1991; Johnson 2010; Kahnt et al. 2017). However, these long legs, which may have evolved some five times, seem not to be immediately associated with the spectrum of Diascia plants the bees visited for oils (Kahnt et al. 2017), thus Hollens et al. (2017) found both a long- and short-legged Rediviva visiting - and pollinating four species of Diascia with tubes of varying lengths, however, leg and spur length matched the frequency of visits by these bees matched spur length (see also Pauw et al. 2017). Interestingly, flowers of some Orchidaceae-Orchidoideae-Coryciinae (e.g. Disperis) from the same area are rather similar (mimics) and are also pollinated by the bees (Pauw 2006) as are some other species of oil flowers, including Alonsoa and Hemimeris, also Scrophulariaceae. Flowers of several species of Scrophularia are pollinated by wasps (see Kampny 1995: also pollination elsewhere in the family), and evolution of pollinator preferences has been studied in detail there (Navarro-Pérez et al. 2013).
Myxospermy is known from the family (?extent: Grubert 1974).
Plant-Animal Interactions. Mohrbutter (1937) noted both fungi and leaf miners that attacked members of the old Buddlejaceae and Scrophulariaceae placed here. For example, the dipteran agromyzid miner Amauromyza verbasci has been found on Verbascum, Scrophularia and Buddleja (Spencer 1990). Other insect herbivores also distinguish between Plantaginaceae and Scrophulariaceae (e.g. Allen 1960; Tempère 1969).
Chemistry, Morphology, etc. The iridoids harpagide and harpagioside, found quite commonly in Scrophulariaceae, are also scattered elsewhere in Lamiales, in Lamiaceae (inc. Caryopteris) and Pedaliaceae (Hegnauer & Kooiman 1978; Nicoletti et al. 1988; Georgiev et al. 2013); Soltis et al. (2005b) suggest that such acylated rhamnosyl iridoids characterise Scrophulariaceae. Secoiridoids are known from Manulea, which also has the more conventional verbascoside (Gousiadou et al. 2014). The chemistry of Buddlejaceae (see Jensen 2000b) and other Scrophulariaceae is similar (Houghton et al. 2003); for the chemistry of Myoporaceae s. str., see Ghisalberti (1994), and for that of Verbascum, see Georgiev et al. (2011). Nicodemia (= Buddleja) is reported to have tannin (Bate-Smith & Metcalfe 1957).
The wood anatomy of Buddleja is similar to that of Nuxia (Stilbaceae) and Peltanthera (Gesneriaceae), etc. (Carlquist 1997c), i.e. to taxa that are not immediately related. Some Scrophulariaceae have opposite leaves, an angled stem, and 1:3 nodes, however, I have not seen the little bundles of fibres that run along the ridges of otherwise similar stems in Linderniaceae. There are glands in the leaves of Leucophyllum and Capraria, c.f. those of Myoporeae s. str. (Lersten & Beaman 1998; Lersten & Curtis 2001). Scrophularia and Verbascum also have distinctive cells (idioblasts) in their leaves (Lersten & Curtis 1997) perhaps similar to these glands, although the clades to which they belong are not close.
Taxa with more or less polysymmetric flowers - sometimes rather like those of Silene, which some South African species may mimic (ref.?) - are common in almost all tribes. There are also taxa with five rotate corolla lobes and five stamens (Capraria) and four lobes and stamens (some species of Buddleja), and in both cases the flowers are fully polysymmetric. Flowers of Verbascum s. str. have five stamens, but those of Celsia, embedded in Verbascum (e.g. Ghahremaninejad et al. 2015), have only four. Hemimeris may have inverted (and inversostylous!) flowers, but the originally adaxial lobe of the corolla is patterned, i.e. it is not functionally different from the normal condition with patterning on the abaxial lobe and adjacent lateral abaxial lobes. The anthers may be straight or U-shaped, but they are not sagittate, and in taxa with confluent dehiscence the two thecae may be end-to-end after dehiscence. The pollen of Aptosimieae was described as being diporate (Oxelman et al. 2005), but Mosyakin and Tsymbalyuk (2015b) mention only a single pore. The micropylar haustorium of Buddleja ramifies through th integument, almost reaching the chalaza (Maldonado de Magnano 1986b). The alveolate testa can be either bothrospermous or aulacospermous, and some taxa have cushion-shaped scars on the placenta, often with a central umbo or pedestal (e.g. Hilliard 1994). These mark the place where the seeds fell off. Limoselleae with single ovules have much-thickened funicles.
Additional general information is taken from Rogers (1986) and Norman (2000), both Loganiaceae, Hilliard (1994, 1998: nearly all Limoselleae), Oxelman et al. (2004a: Buddlejaceae s. str., 2005), Theisen and Fischer (2004: Myoporaceae), Fischer (2004b: Scrophulariaceae p. pte); see also Jansen (1999) and Harborne and Williams (1971), both chemistry, Carlquist (1997c: wood anatomy), Rodríguez-Riaño et al. (2015: vascular anatomy of Scrophularia flowers), Tsymbalyuk and Mosyakin (2013) and Mosyakin and Tsymbalyuk (2015a, b, 2017), all pollen, Vinckier and Smets (2002a: orbicules), Junell (1961: gynoecium of Selagineae), Bendre (1975), Maheswari Devi and Lakshminarayana (1980) and Maldonado de Magnano (1987), all embryology, and Hartl (1959: seed coat/rumination); for floral development, see Armstrong and Douglas (1989) and Endress (1999).
Phylogeny. For early stabs at phylogenetic relationships, see B. Bremer et al. (1994) and Nickrent et al. (1998). The main issues are the relationships between the old Selaginaceae, Buddlejaceae and Myoporaceae and the Scrophulariceae that make up the rest of the clade.
The old Selaginaceae/Selagineae with but a single apical ovule per loculus link with Scrophulariaceae-Manuleéae, and although the latter have more ovules, these are very variable in both number and orientation (see also Junell 1961; Hilliard & Burtt 1977; Hilliard 1994). Kornhall et al. (2001: see also character optimisations, sampling good), found that Selagineae were embedded in Manuleéae, while Kornhall and Bremer (2004) found that the cosmopolitan aquatic Limosella was also to be placed with these often quite xeromorphic and largely southern African taxa.
Buddleja, ex Loganiaceae, is very much paraphyletic and includes Nicodemia, Emorya, and Gomphostigma (see especially Chau et al. 2017: basal relationships around ex-Gomphostigma, B. salviifolia, etc., unclear); several lines of evidence place it in Scrophulariaceae (e.g. Maldonado de Magnano 1986b). Oftia, with a racemose inflorescence, only four ovules/carpel, and a drupaceous fruit, the seeds with a very hard testa and copious endosperm (some information from Dahlgren & Rao 1971); it also has 4-colpate pollen (Niezgoda & Tomb 1975) and intraxylary phloem, not known from Teedia, its close relative. Teedia and Oftia have strong support as the sister group to Buddleja s.l. (Wallick et al. 2001, 2002), although Takhtajan (1997) placed the latter in its own family which, he thought, was related to Myoporaceae and Scrophulariaceae. Camptoloma is sister to other Buddlejeae (Oxelman et al. 2004).
The association of Leucophyllum with the old Myoporaceae is well established (e.g. Schwarzbach & McDade 2002; Gándara & Sosa 2013), and both have distinctive pollen - tricolpate, with each colpus diorate (Niezgoda & Tomb 1975; Mosyakin & Tsymbalyuk 2015b; c.f. Argue 1980). Within Leucophylleae, Leucophyllum is strongly paraphyletic, including Eremogeton and Capraria (Gándara & Sosa 2013: support poor to strong). Leucophyllum has only a single pellucid gland at the apex of the lamina and Eremogeton has none; Capraria also has leaf glands and pollen like that of other Myoporaceae and it fits nicely here (for leaf glands, see Lersten & Beaman 1998; c.f. also Henrickson & Flyr 1985; Lersten & Curtis 2001; Henrickson 2004). Androya (ex-Buddlejaceae) and Aptosimum may be around here. The tricolporate pollen of the former has been compared with that of Nicodemia (Loganiaceae s. str.), and it was a member of Loganiaceae s.l.. However, Kornhall et al. (2001) found that Androya it was sister to Myoporum, and it was well supported as sister to other Myoporeae in Oxelman et al. (2005) and Gándara and Sosa (2013). Originally placed in Oleaceae, its position here causes problems with character optimisations that I am ignoring for a while. Aptosimum and relatives, long considered a distinct little group, are sister to Myoporeae.
As the scope of phylogenetic studies in Scrophulariaceae has expanded, the broader picture of relationships has become clarified, fortunately, the topologies of the various studies are largely congruent. Kornhall et al. (2001) found that most other Scrophulariaceae were in a clade sister to Buddleja and immediate relatives, although Myoporum was outside this group. The more general relationships in Kornhall and Bremer (2004) are [Myoporum, etc. [[Buddleja, etc.] [[Scrophularia, etc.] + [Limoselleae, inc. Manuleéae, etc.]]]]. Finally, Oxelman et al. (2005) found the relationships [Hemimerideae (inc. Diascia) [[Myoporeae + Aptosimieae] [[Buddleja, etc.] [Limoselleae + Scrophularieae]]]].
Relationships in Scrophulariaceae-Hemimerideae are discussed by Oxelman et al. (1999b; see also 2004). [Diascia + Nemesia] may be sister to the rest of the tribe, but the position of the Alonsoa is unclear. For relationships within the South African Nemesia, see Datson et al. (2008: unreversed woody → herbs).
Limoselleae. Archibald et al. (2017) examined relationships in the African Zaluzianskya and relatives.
Scrophularieae: For relationships within Scrophularia and Verbascum, see Scheneurt and Heubl (2014 and references) and Ghahremaninejad et al. (2015) respectively.
Classification. Olmstead et al. (2001) suggested that recognition of Myoporaceae might make Scrophulariaceae paraphyletic; Chinnock (2007), monographing Myoporaceae s. str., suggested that they could well be included in Scrophulariaceae. Here I have largely followed Oxelman et al. (2005) for tribes; Myoporeae and Leucophylleae are kept separate, although they are clearly sister taxa and the combined clade has synapomorphies - except remember the problem with Androya.
Generic limits in Leucophylleae will need to be redrawn; a single genus for the tribe would work, but Gándara and Sosa (2013) propose the recognition of five. For the circumscription and sectional classification of Buddleja see Chau et al. (2017).
Previous Relationships. The limits of Scrophulariaceae have long been problematic (Thieret 1967 for a summary; Olmstead 2002 for a readable account of the implications of the findings of molecular data). Albach et al. (2005a) and Oxelman et al. (2005) are clarifying the contents of the separate clades that used to be subsumed in Scrophulariaceae s. l. (see also B. Bremer et al. 2002; Tank et al. 2006); for further details see the introduction to Lamiales above.
Members of the Scrophulariaceae of a generation ago are now to be found in Plantaginaceae and Orobanchaceae (these include most of the taxa that have moved), as well as in Stilbaceae, Phrymaceae, Mazaceae, and Linderniaceae. Other genera previously associated with Scrophulariaceae and thought to be links with other families include Nelsonia and its relatives (see Acanthaceae) and Paulownia (see Paulowniaceae). Buddleja (et al.) were included in Loganiaceae or placed in their own family.
Thanks. To F. Zapata, for useful comments on the family.
[Stilbaceae [[Byblidaceae + Linderniaceae] [[Pedaliaceae, Martyniaceae, Acanthaceae] [Bignoniaceae [[[Schlegeliaceae + Lentibulariaceae] [Thomandersiaceae + Verbenaceae]] [Lamiaceae [Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]]]]]]]]: ?
Age. This clade was estimated to be (70-)61, 54(-51) m.y.o. by Bell et al. (2010) and (64-)55(-47) m.y.o. by Wikström et al. (2015).
STILBACEAE Kunth, nom. cons. Back to Lamiales
Ericoid shrubs, ordinary shrubs, or herbs; (iridoids from deoxyloganic acid - C-8 iridoid glucosides), (cornosides +); cork just outside pericycle; vessel elements also with scalariform perforation plates; nodes ?; petiole bundle?; stomata?, cuticle waxes as rods or threads; lamina vernation revolute or not, (margins minutely toothed); inflorescence branches cymose, (plant cauliflorous), (flowers axillary); bracteoles as long as K; flowers often polysymmetric, (4) 5(-7)-merous; K bilobed or not (free), C lobes equal to unequal; stamens = sepals, (one fewer; staminode +), anther thecae confluent apically, or with separate parallel slits; ovary (apically) unilocular, [1 G infertile, or septum 0], or bilocular, stigma slightly bifid or punctate; ovules 1-2/carpel, ascending and/or descending, apo/epitropous, or many; micropyle long, integument several [ca 15?] cells across, hypostase +; embryo sac very long; fruit a loculicidal (and septicidal) capsule, (indehiscent), K and C persistent; (seeds with pedestals - Charadrophila); endosperm +, embryo cylindrical [always?]; n = 10, 12, 19; protein bodies in nucleus crystalline [Halleria].
11[list]/39: Nuxia (15). Most South Africa, the Cape Province, also to tropical Africa, Madagascar, the Mascarenes and Arabia (map: from Leeuwenberg 1975). [Photo - Nuxia Inflorescence, Halleria Flower.]
Age. Tank and Olmstead (2017) suggested an age of (60-)37.1(-13.3) m.y. for this clade.
Evolution: Pollination Biology. Oil flowers are quite common in the family (Vogel 1974; Renner & Schaefer 2010; Possobom & Machado 2017a and references).
Chemistry, Morphology, etc. The C-8 iridoid glucosides common in Stilbaceae are extremely uncommon elsewhere (Frederiksen et al. 1999); for unedoside, present in at least some genera of Stilbaceae, see Oxelman et al. (2004a). Indeed, some iridoids in Stilbaceae are like those of Loasaceae and Hydrangeaceae; all three have unedoside (Jensen et al. 1998).
By and large, the gynoecium is reminiscent of that of Scrophulariaceae-Manueleae. Thesmophora appears to have two collateral carpels, each with one descending ovule (Rourke 1993) - perhaps an abaxial carpel divided by a false septum.
For general information, see Dahlgren (in Dahlgren & van Wyk 1988,) Weber (1989: Charadrophila), Fischer (2004b: Bowkerieae) and Linder (2004: narrow circumscription), for anatomy and morphology, see Carlquist (1986) and Dahgren et al. (1979), and for embryology, see Junell (1934).
Phylogeny. Retziaceae and Stilbaceae come out together in rbcL trees (Wagstaff & Olmstead 1997); for another early study, see B. Bremer et al. (1994). Nuxia (ex Loganiaceae) is also placed here in molecular phylogenies (Backlund et al. 2000; Wallick et al. 2002), and this makes phytochemical sense (Frederiksen et al. 1999). The cauliflorous Halleria is also to be included in Stilbaceae (Olmstead et al. 2001). Genera like the gesneriad-like Charadrophila (the common name for this plant is "Cape gloxinia") and Scrophulariaceae-Bowkerieae (Bowkeria, Anastrebe and Ixianthes) are now members of the family. Charadrophila and Halleria may form a clade - but little support yet - that is sister to well-supported clades that includes the rest of the family (Oxelman et al. 2005). Thesmophora has not been included in these studies.
Classification. Rourke (2000) recognised two subfamilies, Retzioideae and Stilboideae, in Retziaceae, Kornhall (2004) recognized three tribes. However, the circumscription of the family has greatly changed from what it was ten years ago (see also Tank et al. 2006).
Synonymy: Halleriaceae Trinius, Retziaceae Choisy
[[Byblidaceae + Linderniaceae] [[Pedaliaceae, Martyniaceae, Acanthaceae] [Bignoniaceae [[[Schlegeliaceae + Lentibulariaceae] [Thomandersiaceae + Verbenaceae]] [Lamiaceae [Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]]]]]]]: ?
Age. This node is around 48 m.y.o. (Magallón et al. 2015: note topology).Evolution: Divergence & Distribution. Sensitive stigmatic lobes occur sporadically in this part of the tree (see also Endress 1994b).
[Byblidaceae + Linderniaceae]: bracteoles 0; x = 8, 9.
Chemistry, Morphology, etc. Flowers are either axillary or the inflorescence is racemose in this clade - not too much difference between the two!
BYBLIDACEAE Domin, nom. cons. Back to Lamiales
Rhizomatous and woody, or ephemeral herbs; cork?; young stem with separate bundles; nodes 1:1 or 1:3; stomata paracytic; leaves spiral, lamina linear, abaxially circinate or straight, veins parallel; flowers single, axillary; flowers subpolysymmetric; K connate only basally, C contorted, connate only basally, margins fimbriate; A ± monosymmetric, stamens 5, shortly epipetalous, anthers dehiscing by short slits or pores, epidermal cells ephemeral; nectary 0; stigma punctate to capitate (slightly bilobed); ovules 2-several/carpel, ± apical; exotestal cells tangentially somewhat elongated, anticlinal walls not uniformly thickened, mesotesta sclerenchymatous; endosperm starchy, copious; proteinaceous inclusions in the nucleus?
1 [list]/8. W. and N. Australia, S. New Guinea (map: from van Steenis 1971; FloraBase 2004). [Photos - Collection.]
Age. A single seed, now destroyed, from the Middle Eocene of South Australia may be assignable to this family (Conran & Christophel 2004).
Evolution. Ecology & Physiology. Although there is no evidence that the plant absorbs nutrients from the insects that often stick to it (Hartmeyer 1997, 1998; Mueller et al. 2001), Conran and Carolin (2004) note that mirid bugs are associated with the genus, and so there may be a relationship similar to that in Roridula (Ericales) where the mirid eats insects stuck to the plant and the plant absorbs nutrients from the excreta of the bug (see Wheeler & Krimmel 2015 for mirids).
Pollination Biology & Seed Dispersal. Although the flowers are basically polysymmetric, the stamens are held to one side of the flower. Buzz pollination is likely.
Chemistry, Morphology, etc. Byblis linifolia has leaves that are sometimes abaxially curled in bud and so are like those of Drosophyllum (Drosophyllaceae, Caryophyllales). However, the glandular hairs of Byblidaceae have the typical structure of those of core Lamiales and look like little parasols; those of Drosophyllum are vascularized and have irregularly arranged cells in the head.
Diels (1930b) drew the flower of Byblis with the odd sepal abaxial. Byblidaceae are often described as being bitegmic, but c.f. Diels (1930b) and Vani-Hardev (1972).
See Lloyd (1942), Juniper et al. (1989), Conran and Carolin (2004), McPherson (2008, 2010), Lowrie (2013: vol. 1), papers in Ellison and Adamec (2018), and the Carnivorous Plants Database for general information, also Wilkinson (1998: anatomy), Takahashi and Sohma (1981: pollen), Conran (1996: embryology), and Conran et al. (2002: chromosome numbers).
Previous Relationships. Roridula (see Roridulaceae - Ericales) has hitherto often been placed in the same family as Byblis as Byblidaceae and then included in Rosales, as by Cronquist (1981), or the two kept separate, but both placed in Byblidales, in Aralianae, as by Takhtajan (1997).
LINDERNIACEAE Borsch, K. Müller, & Eb. Fischer Back to Lamiales
Ephemerals to suffruticose perennials; iridoids 0; cork?; nodes 1:3; stems angled; leaves (basally connate), lamina venation also pamate, margins entire or serrate; (flowers single, axillary); (K free); C with glandular hairs on the inside; A curved, 4, staminode +/0, or A 2, the adaxial pair, also 2 large abaxial Z-shaped staminodes with an appendage, or staminodes much reduced, anthers connivent [?all], thecae parallel to ± head to head; pollen 3(-5)-colpate; stigma lobes sensitive; embryo sac spathulate, protruding through the micropyle, integument 3-4 cells across; capsule septicidal or -fragal; exotestal cells in longitudinal series [?all], seeds with ruminate endosperm [surface alveolate - bothrospermous - or furrowed - aulacospermous] (smooth); n also = 12-14, etc. [x = 7-9?].
17 [list]/255 (220): Vandella (55), Torenia (51), Crepidorhopalon (30), Lindernia (30). Pantropical to warm temperate (map: based on Fischer 1992; Lewis 2000).
Age. The clade [Torenia + Craterostigma] was dated to 45.6-)27.4(-10.2) m.y. (Tank & Olmstead pers. comm.).
Evolution. Ecology & Physiology. Although many Linderniaceae seem to be rather delicate little herbs, a number are dessication tolerant (poikilohydric). These include the remarkable Chamaegigas intrepidus, which grows in transient pools - it is an aquatic resurrection plant - on inselbergs and probably uses glycine and serine as nitrogen sources (Heilmeier & Hartung 2011). Fresh leaves of Craterostigma plantagineum store large amounts of the unusual sugar, 2-octulose, which is converted into sucrose as the leaf dries (Bianchi et al. 1993; Farrant 2000). For more information on dessication tolerance in the family, see Dinakar and Bartels (2012 and references).
Pollination Biology & Seed Dispersal. In some species the anthers of the abaxial stamens are yellow and lie against the abaxial lip; they appear to contribute to the attractive aspect of the lip. In other species the long, curved abaxial filaments, joined by the connate anthers, form a sort of balustrade across the mouth of the corolla. Various hairs develop on the knees of the abaxial anthers and inside the corolla, and the corolla may have projections, flanges, etc.; all in all, a complex little flower (see e.g. Magin et al. 1989; Rahmanzadeh et al. 2004 for photographs). It would be interesting to know details of pollination mechanisms for such flowers; small bees have been recorded as visitors (Magin et al. 1989). In Torenia fournieri, which has a less obviously distinctive floral morphology, the adaxial stamen pair elongate quickly and then more ot less protrude from the mouth of the corolla, while the abaxial pair has anthers which, when touched on lever-like lateral flanges, forcibly extrude their pollen (Armstrong 1992).
Chemistry, Morphology, etc. The nodes appear to be 1:3, rather than 3:3 as I originally thought. Small strands of lignified tissue are associated with the sharp ridges of the stems in the couple of species that I have seen. The glandular heads of the hairs on the corolla and the vegetative plant have vertical partitions, as is common in Lamiales.
For the floral development of Torenia, see Armstrong (1988). Lewis (2002) suggests that the anthers are extrorse and the ovules are straight; Fischer (1992), however, gives a floral diagram showing introrse anthers and describes the ovules as being anatropous to hemitropous. The embryo sac protrudes beyond the micropyle in some species of both Torenia and Lindernia, at least (Wardlaw 1955; Yamazaki 1955); the synergids can then be ablated easily in studies of fertilization (Higashiyama et al. 2006). The rumination of the endosperm is caused by inpushings of endothelial cells (alveoli); these can become confluent and the seeds then have longitudinal ridges.
For more information, see Fischer (1989, 1992, 2004b - the latter Scrophulariaceae pro parte), general, and Takhtajan (2013: ovule and seed).
Phylogeny. Rahmanzadeh et al. (2004: Micranthemum not included) recovered this clade with 100% bootstrap support. Albach et al. (2005a) analysed four genes, separate analyses of three of which and the joint analysis suggested that Linderniaceae were distinct from Plantaginaceae. Micranthemum, with only two stamens, was sister to Lindernieae, whose members made up the rest of this clade (Albach et al. 2005a). Oxelman et al. (2005) found that Micranthemum was sister to Torenia, the two in turn were sister to Stemodiopsis, the only three Linderniaceae they examined. In a more extensive analysis the relationships [Stemodiopsis [Lindernia, etc.] [Torenia, Craterostigma, Vandella, etc.], all with strong support, were obtained (Fischer et al. 2013). See also Tank et al. (2006) for a summary of our ideas of relationships within this clade, and for the inclusion of the Brazilian Cubitanthus, ex-Gesneriaceae, see Perret et al. (2012; not in the study of Fischer et al. 2013) - it was placed as sister to the African Stemodiopsis.
Classification. See Rahmanzadeh et al. (2004), Tank et al. (2006) and especially Fischer et al. 2013)for the composition of Linderniaceae; the generic list here is rather notional. If Micranthemum (Scrophulariaceae-Microcarpeae) belongs in this clade, some other genera may have to be included; Microcarpeae are often aquatic herbs whose flowers usually have only the abaxial stamen pair fertile, and in four other genera the filaments have "clavate geniculations at base" (Fischer 2004b: p. 402).
[[Pedaliaceae, Martyniaceae, Acanthaceae] [Bignoniaceae [[[Schlegeliaceae + Lentibulariaceae] [Thomandersiaceae + Verbenaceae]] [Lamiaceae [Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]]]]]]: ?
Age. This age of this clade was estimated to be (60-)51(-44) m.y. by Wikström et al. (2015: note topology) and (64.6-)57.1, 52.1(-48.9) m.y. by Cusimano and Wicke (2016: Sesamum).
[Pedaliaceae [Martyniaceae + Acanthaceae]]: ?
Previous Relationships. Martyniaceae and Pedaliaceae have often been combined (as Pedaliaceae, e.g. Cronquist 1981), but there is no current evidence that they form a monophyletic group. Differences in pollen (inaperturate and with platelets vs several colpi) and placentation (parietal vs axile) clearly separate the two morphologically. In addition, the remarkable branched spines, etc., on the fruits of Pedaliaceae develop as such while those of Martyniaceae become exposed as the outer layer of the fruit rots away.
PEDALIACEAE R. Brown, nom. cons. Back to Lamiales
Annual to perennial herbs, (stems ± succulent), (roots swollen) to small deciduous trees; 10-hydroxylated carboxylic iridoids [harpagoside], orobanchin, amyloid +; (cambium storied); pericycle also with sclereids (fibers few); petiole bundle interrupted-annular; hairs broadly capitate-stellate, mucilaginous; leaves (spiral - Sesamum), lamina margins toothed, lobed or entire, (venation palmate); flowers usu. axillary, (inflorescence branched, branches cymose); base of pedicel with paired nectaries [modified flowers], (not - Uncarinia); (C with spur); A (5), thecae ± confluent, at right angles to filaments, staminode + (0); pollen 5-13 stephanocolpate; G [2-4], with false septae, (8 loculi - Josephinia), stigma lobes broad, often sensitive, wet; ovules 2-many/carpel, (1 ovule/"loculus" - Josephinia), integument 7-20 cells across, hypostase +; fruit with hooks or glochidiate spines, etc., (heterocarpic), (schizocarp; nut; wind-dispersed); seeds winged or not, surface often sculpted, testa multiplicative, exotestal cells palisade or otherwise thickened, (mesotesta with crystals); endosperm slight, cotyledons with fat and cell walls with xyloglucans [thick, pitted - amyloid]; n = 8 (13); nuclear genome [1C] (337-)1145(-1648) Mb; protein bodies in nucleus?
15 [list]/70: Sesamum (19), Pterodiscus (13). Mostly Old World tropical, in coastal or arid habitats (map: from Ihlenfeldt & Grabow-Seidensticker 1979; FloraBase 2005; Australia's Virtual Herbarium xii.2012; Ihlenfeldt 1994b, 2010).
Age. The age of the clade [Uncarina + Sesamum] is estimated to be (39-)20.1(-6) m.y. (Tank & Olmstead pers. comm.).
Evolution: Pollination Biology & Seed Dispersal. The diversity of fruit morphology and dispersal "strategies" in this small family is remarkable, as is their variation in growth form (Ihlenfeldt 2010). Sesamum is myxospermous (Grubert 1974).For genome size, see Lyu et al. (2017: c.f. Tables S3 and S5).
Chemistry, Morphology, etc. The iridoid glycoside harpagoside, known from Harpagophytum and Rogeria, is scattered in other Lamiales such as Lamiaceae, Plantaginaceae, and quite commonly in Scrophulariaceae s. str. (Georgiev et al. 2013). The mucilage glands that are often so conspicuous normally have four apical cells.
The apparently single axillary flowers of some taxa appear to be reduced cymes, the paired nectaries at the base of the pedicel representing modified flowers (Manning 1991). Josephinia may have four carpels, each loculus being divided - an unusual combination for a euasterid. Although Rogeria is reported to occur in Brasil, this seems to be a mistake (Volker Bittrich, pers. comm.).
Some information is taken from Stapf (1895), Carlquist (1987b: wood anatomy), S. D. Manning (1991: U.S.A., general), and Ihlenfeldt (1967, 2004, 2010: general), also Jordaan (2011: seed coat of Harpagophytum - complex).
Phylogeny. Gormley et al. (2015) found good support for the relationships [Pedalieae [Sesamothamneae (monotypic) + Sesameae]] in a chloroplast analysis, but the first tribe was paraphyletic in an analysis using the external transcribed spacer, with Rogeria sister to the rest of the family, albeit with little support; in Sesameae, Sesamum was paraphyletic in both analyses, although more so in the first.
Synonymy: Sesamaceae Berchtold & J. Presl
[Martyniaceae + Acanthaceae]: ?
MARTYNIACEAE Horaninow, nom. cons. Back to Lamiales
Annual herbs, roots often tuberous (perennials; woody); petiole bundle deeply arcuate, also adaxial cortical and medullary bundles; plant long sticky-hairy; leaves also spiral, lamina margins toothed; (K free); A (2 + 2 staminodes - Martynia), connective with apical gland, staminode(s) +; pollen grain tricellular, inaperturate, exine made up of 20-40 platelets, adjacent or somewhat separate, with reticulate sculpture (smooth raised rings, surface inside smooth - Craniolaria); G with parietal placentation, placentae T-shaped, ovules at the end of the cross bar, stigma lobes sensitive; 2-many ovules/carpel; capsule with paired apical spurs or hooks [developing from sterile upper part of ovary], (± smooth), outer mesocarp ± fleshy, caducous, inner mesocarp woody, with crests and spines; seeds large [>10 mm long], (ca 3 mm long); testa ca 5 layers thick, exotesta subgelatinous, or inner and radial walls with cellulosic bands, inner layers lignified [Proboscidea], or exotesta only persistent, R-Put-like structures below [?bands of thickening - Martynia, no other cellular details], or lignified exotesta; endosperm at most thin; n = 15 (16, 18), nuclear genome size [1C] ca 0.49 pg.
5 [list]/16: Proboscidea (10). Tropical and subtropical America, rather scattered (for map, see Gutierrez 2011).
Age. The age of crown-group Martyniaceae is estimated to be (54.3-)51.5(-49.3) m.y. (Tank & Olmstead pers. comm.).
Evolution: Divergence & Distribution. The primary division in the family is between North American and South American taxa (Gutierrez 2011; Gormley et al. 2015).
Ecology & Physiology. Insects may stick to the very viscid indumentum of Martyniaceae, although there is no evidence that the plants are carnivorous (see Rice 2008; Plachno et al. 2009); c.f. Stylidiaceae (Asterales), which also have sticky hairs and which also may be carnivorous (Darnowski et al. 2006).
Seed Dispersal. The outer part of the pericarp rots away to expose the distinctive spiny/thorny fruits that are quintessential trample burrs; the anatomy of the fruit wall is complex (Horbens et al. 2014). The seeds of several Martyniaceae are very large compared with those of other core Lamiales.
Chemistry, Morphology, etc. Prieu et al. (2017) record Craniolaria and Martynia as having pantoporate pollen.
General information is taken from Stapf (1895), Ihlenfeldt (2004) and McPherson (2010, vol. 2, esp. photographs) and especially Gutierrez (2011); see also Carlquist (1987b: wood anatomy), Bretting and Nilsson (1988: pollen morphology), and S. Singh (1970: embryology, etc.). For the seed coat, see Ricketson & Schmidt 4981 (Proboscidea areania), Gentry & Zardini 48864 (Martynia annua).
Phylogeny. For relationships within Martyniaceae, see Gutierrez (2008, esp. 2011); the northen Proboscidea and Martynia form a clade sister to southern taxa in the family (see also Gormley et al. 2015: support moderate for monophyly of the southern taxa).
ACANTHACEAE Jussieu, nom. cons. Back to Lamiales
Quaternary methylammonium compounds, amyloid +; (cork cambium deep seated); stomata diacytic; nodes swollen [?level]; lamina margins entire to toothed; (inflorescence branches cymose), bracts large, conspicuous; K free or connate, often sharply pointed, (C lobes narrow); A (2; 2 + 2 staminodes; 5), staminode +/0; G lacking septal bundles; ovule with "thin" integument [?]; embryo sac long, curved, (apex of 4-nucleate sac growing out of the micropyle and eventually into the placenta); (zygote pushed back into the ovule by a long suspensor); capsule dehiscence explosive, walls cartilaginous, K persistent; testa with hygroscopic trichomes; endosperm development highly asymmetric, the two haustoria lying close to each other, second division of the endosperm transverse, primary endosperm 3-celled, linear, embryo often ± curved.
220 [list]/4,000 - four subfamilies below. Mostly tropical.
Age. Crown-group Acanthaceae may be slightly over 90 m.y.o. (Tripp et al. 2013b), (92.3-)81.9(-71.7) m.y. (Tripp & McDade 2014b), around 57 m.y. (Tripp & McDade 2014a), or (57.3-)49.3(-41.1) m.y. (Tank & Olmstead pers. comm.).
1. Nelsonioideae Pfeiffer
Herbs; gland-headed hairs with 2-celled heads; (leaves spiral); bracts spiral, (bracteoles 0 - Nelsonia); C with adaxial lobes of C outside others [= descending cochleate aestivation], (A 2), anthers variable (e.g. thecae ± separate); (pollen colpate); ovary (with parietal placentation - Elytraria); stigma broadly (unequally) lobed, (lobes large, sensitive - Elytraria); ovules (4-)many/carpel, campylotropous, endothelium +; antipodal cells persistent; funicular obturator +; seeds 2-many, ruminate, testa ± disorganised (± visible - Nelsonia); chalazal endosperm haustorium degenerates early, endosperm +, oily; n = 9.
5/172: Staurogyne (145). Tropical (warm temperate).
Age. Crown-group Nelsonioideae are estimated to be (81.5-)67.7(-53.8) m.y.o. (Tripp & McDade 2014b).
Synonymy: Nelsoniaceae Sreemadhavan
[Acanthoideae [Thunbergioideae + Avicennioideae]]: (wood rayless); (inverted vascular bundles in the pith); acicular fibres +; pollen usu. other than tricolpate or -colporate; ovules 2/carpel; endothelium 0, funicular obturator 0; endosperm 0, (amyloid [xyloglucans] in cotyledons +).
Age. Estimates of the age for this node are (50-)41, 38(-29) m.y. (Bell et al. 2010), (38-)35, 27(-24) m.y. (Wikström et al. 2001), (42-)32(-17) m.y. (Wikström et al. 2015), ca 54 m.y. (K. Bremer et al. 2004a) and (80.7-)70.9(-61.4) m.y. (Tripp & McDade 2014b).
2. Acanthoideae Eaton
Herbs (to shrubs); (benzoxazinones +); cystoliths + (0); petiole bundles arcuate, arranged in a circle, (annular); (leaf margins spiny); C often with abaxial lobe outside others in bud [= ascending cochleate aestivation], (slit-monosymmetric - rare); anthers sagittate, or thecae displaced and not opposite, (one theca ± reduced); pollen hideously variable, often porate; stigma dry, usu. bifid; ?funicular obturator; capsules obovoid; seeds flattened, usu. 4, (hairy), borne on hook-like hardened funicles [jaculators, retinacula]; exotesta palisade, (hypodermal cells thickened); both chalazal and micropylar haustoria +; cytologically very variable, x = ?7; nuclear genome [1C] ca (416-)1462(-2841) Mb.
217/3,220: Asystasia (70) - seven groups below. World-wide; most species are neotropical (map: from Brummit 2007). [Photo - Habit, Flower.]
Age. The age of crown-group Acanthoideae was estimated at (102-)79(-65) m.y.a. (Tripp et al. 2013b) or (80.1-)71.1(-61.9) m.y.a. (Tripp & McDade 2014b).
2A. Acantheae Dumortier
Nodes not swollen; A 4, anthers monothecous; pollen tricolpate.
21/500: Aphelandra (170), Blepharis (130).
[[Ruellieae + Justicieae] [BAWN clade]]: cystoliths +; pollen porate.
[Ruellieae + Justicieae]: pollen with false apertures.
2B. Ruellieae Dumortier
(Filament curtain +); C left-contorted; pollen often reticulate, with compound apertures; adaxial stigmatic lobe shorter than the abaxial lobe, to 0; (ovules 310 call layers across]; 2 [?mesotestal] layers sclerified [Dipteracanthus]; n = 6 and just about everything else in the family, 15-17 common, x = 8?
38/1185: Ruellia (355), Strobilanthes (350), Hygrophila (100), Dyschoriste (80), Hemigraphis (60), Sanchezia (60).
2C. Justicieae Dumortier
Pyrroloquinazoline alkaloids +; (flowers resupinate - Diclipterinae); parallel ridges on upper lip of corolla [rugula] holding style (0); A (2), thecae displaced, not opposite, connective expanded, with appendages, etc.; pollen tricolporate, hexapseudocolpate; embryo cell walls with xyloglucans [thick, pitted - amyloid]; n = (7, 9-13)14(15-18, 20 ...34).
Justicia (600), Ptysiglottis (60).
Synonymy: Justiciaceae Rafinesque
[Barlerieae + Andrographidae + Whitfieldieae + Nemacanthus] / BAWN clade: ?
2D. Barlerieae Nees
C quincuncial; seed with hygroscopic trichomes.
/420: Barleria (300), Petalidium (40). Pantropical.
2E. Andrographidae Endlicher
Pollen colporate, ornamented and thickened exine surrounding or over apertures; (ovules 3+/carpel); testa lacking hygroscopic hairs; endosperm ruminate.
2F. Whitfieldieae Reveal
(C left-contorted); pollen biporate, lenticular, granular around apertures (pantoporate); stigma capitate; seeds with concentric rings of ridges, (also hygroscopic trichomes + - Lankesteria); n = ca 21.
K united, 3 + 2; pollen tricolporate, intercolpal regions psilate/foveolate; seed with hygroscopic trichomes.
1/30. Africa, Madagascar, Arabia to Vietnam.
[Thunbergioideae + Avicennioideae]: C left-contorted; filament bases thickened; ovules 2/carpel, collateral, apotropous, apex of nucellus exposed, surrounded by short integumentary rim, embryo sac ± on surface of nucellus; cotyledons folded.
Age. The age of this node was estimated to be ca 86 m.y. (Tripp et al. 2013b) or (80.7-)70.9(-61.4) m.y. (Tripp & McDade 2014b).
3. Thunbergioideae T. Anderson
Twining vines (erect); (iridoids from deoxyloganic acid - C-8 iridoid glucosides, unedoside); rays 0 [Thunbergia], (intraxylary phloem/bicollateral vascular bundles +); petiole bundles arcuate or annular with wing bundles; lamina vernation strongly curved; inflorescence with axillary flowers, or fasciculate, 2 or more flowers in the median plane of the leaf/inflorescence bract, adaxial flowers opening first; bracts 0, bracteoles very large, connate or not; K a rim, (with up to 16 linear lobes), C (not contorted); (staminode +), anthers with lignified unicellular hairs (multicellular awns), sagittate, (thecae slightly displaced), dehiscing by (elongated) pores (slits), connective elongated, endothecium 0; pollen 4-8-brevicolpate or spiraperturate; (adaxial carpel aborting - Mendoncia), stigma wet, small and sub-bilobed to trumpet-shaped and with broad and often unequal papillate lobes; capsule also septifragal, (fruit a 1-2-seeded drupe - Mendoncia); chalazal endosperm haustorium 0, secondary haustoria develop, embryo cell walls with xyloglucans [thick, pitted - amyloid - Thunbergia], (cotyledons twice folded - Mendoncia, etc.); n = 9, 28.
Ca 5/190: Thunbergia (90), Mendoncia (90). Tropical America, Africa and Madagascar, fewer in South East Asia—Malesia. [Photo - Flowers.]
Age. Crown-group Thunbergioideae are estimated to be (59.5-)47.2(-34.5) m.y.o. (Tripp & McDade 2014b).
Synonymy: Mendonciaceae Bremekamp, Meyeniaceae Sreemadhavan, Thunbergiaceae Lilja
4. Avicennioideae Miers
Trees; betaines +, tanniniferous; wood with successive cambia, phloem islands occurring in bands of conjunctive tissue; vessels in radial multiples; nodes 3:3; petiole bundle annular; sclereids +; lamina thick, with salt glands on both sides, colleters +; inflorescence in dense thyrsoid spicate units[!]; flowers (polysymmetric), 4(-6)-merous; K ± free, C with nectar glands on tube; stamens = and alternating with C; pollen 3-colporate; (G with false septae), loculi apically confluent, stigma with 2 blunt lobes; placentation becoming free central, ovules apical, ± straight; fruit an achene, K persistent, green; seeds large; chalazal endosperm haustorium degenerates early, micropylar haustoria aggressive; embryo chlorophyllous, cotyledons induplicate-reduplicate; n = 18, 32; nuclear genome [1C] ca 509 Mb; embryo breaking the seed coat before the seed falls from the tree.
1/8 (species limits need attention). Mangroves throughout the tropics, but also warm temperate (map: from Moldenke 1960; Tomlinson 1986). [Photo - Flower]
Age. Ricklefs et al. (2006) dated ?crown-group Avicennia to ca 42 m.y.; (39.3-)38.7(-38.4) m.y. is the estimate in Tripp and McDade (2014b).
Avicennia is very common both as leaves (but no salt glands were seen) and wood in Late Middle Eocene deposits ca 39 m.y.o. on the Pacific side of Peru (Woodcock et al. 2017).
Synonymy: Avicenniaceae Miquel, nom. cons.
Evolution: Divergence & Distribution. For a careful discussion of dating in the family, and also dates for nodes other than those given above, see Tripp and McDade (2014b). Depending on the calibration, dates varied by a factor of about two; the dates here are those preferred by Tripp and McDade (2014b: several fossil calibrations, none far from the in-group, no secondary calibrations, etc.). Tripp and McDade (2014b) validated the identity of a surprisingly large number of fossils that had been attributed to the family.
There are more species of Acanthoideae in the New World, more genera in the Old World, but that is probably an artefact of taxonomists' minds (Tripp et al. 2013a) - of course genera don't mean very much. However, in six clades listed by Tripp and Tsai (2017) the overall disparity New World:Old World was 1,340:89. Nearly all intercontinental (11/13) movements seem to have been from the Old to the New World; they are prominent in Acanthoideae - probably long distance dispersal - and have occured within the last 20 m.y. or so (Tripp & McDade 2014b; see also Kiel et al. 2017). For the biogeography and ecology of the Justicieae-Tetramerium group, also with an Old World origin, especially the many species adapted to drier conditions, see Daniel (2008) and Côtes et al. (2015).
Physacanthus is apparently the product of an ancient hybridization event between Acantheae and Ruellieae and has characters of both; it lacks cystoliths, as do the former, but it has pollen with compound germinal apertures, as do the latter (Tripp et al. 2011, esp. 2013b). There may have been back-crossing to Ruellieae, remarkably, Physacanthus has remained heteroplasmic. The plants may be variegated, perhaps because of incompatibilities developing between organelles from plants with different genomes (Tripp et al. 2013b).
Borg et al. (2006) discuss the biogeography of Thunbergioideae and the evolution of some characters there, while Borg and Schönenberger (2011) mention possible floral/developmental apomorphies of Thunbergioideae and Avicennioideae. At least some of the features characterizing Nelsonioideae mentioned by Scotland and Vollesen (2000) - no retinacula or cystoliths, descending cochleate aestivation (i.e. the adaxial petals overlapping the abaxial petals in bud) - are likely to be plesiomorphies (see Eichler 1875; c.f. McDade et al. 2012), as is their sometimes rather undistinguished tricolpate or tricolporate pollen.
Ecology & Physiology. Many of the distinctive morphological features of Avicennia are common in other plants in the mangrove habitat in which it grows. These include the large, green, more or less viviparous embryos that are the units of dispersal, pneumatophores, and salt glands on both surfaces of the fleshy leaf (Tomlinson 1986), although this last feature is perhaps more widespread in non-mangrove halophytes (for the evolution of the mangrove habitat, see Rhizophoraceae. These salt glands have largely radially-arranged cells in their heads (Fahn 1979), and appear to be variants of the common glandular R-Put type in Lamiales. Robert et al. (2009, 2011) discuss the hydraulic architecture of the wood of Avicennia in which both xylem and phloem are organized in a three-dimensional network. For salt and water balance, see Reef and Lovelock (2015) and other papers in Ann. Bot. 115(3). 2015 and Nguyen et al. (2017).
C4 photosynthesis is reported from a number of species of Blepharis section Acanthodium (Sage 2004), and the other species of the section are C3-C4 intermediates or C4-like plants (Fisher et al. 2015). Heat and aridity seem to have promoted the evolution of C4 photosynthesis here within the last 10 m.y., and C4 plants grow predominantly in the Saharo-Sind and southwest African areas (Fisher et al. 2015).
Very fast germination (within 24 hours after imbibition) is reported from Blepharis persica, the radicle of which can reach 5 cm in length within 24 hours of wetting of the seed - perhaps a record (Gutterman 2000 and references; Parsons 2012). Namibia is a centre for genera like Barleria, Blepharis, Monechma, and Petalidium), and Petalidium in particular has diversified quite extensively (37/40 species) in the Namib Desert within the last 4.8-1.4 m. years. Such diversification is rather unusual in hyperarid climates worldwide (Tripp et al. 2017b). Most Blepharis grow in dry habitats, and some are very small, very spiny, and with remarkable growth forms.
In Mendoncia substantial amounts of fluid accumulate inside the bracteoles, i.e., it has water calyces (Magnaghi & Daniel 2017)
Pollination Biology & Seed Dispersal. Some 500-600 species of Acanthaceae are humming-bird pollinated (E. A. Tripp and L. McDade, pers. comm.; Tripp & Manos 2008). Tripp et al. (2013c) noted that in two New World groups, justicioids and Ruellia, diversification of the acanths was after diversification of the birds, suggesting that diffuse co-evolution was unlikely. In a study focusing on Ruellia, of which 100[46/146 species examined]-130 species may be bird pollinated, hummingbirds diversified considerably in the mid to late Miocene, but diversification of Ruellia began (13.5-)9.0(-8.3) m.y.a., i.e. most of this is decidedly younger (Tripp & McDade 2014a; Tripp & Tsai 2017). Speciation rates in bird-pollinated clades was higher than in clades pollinated by other animals, although reversals in the former were also more frequent (Tripp & Tsai 2017). For bird pollination in Aphelandra, see McDade (1992).
Tripp and Manos (2008) studied the pollination systems in the speciose Ruellia. They found that although flowers specialised for bird or bee pollination may reverse pollinators (bee to bird transitions are usually decidedly uncommon - Barrett 2013), sphingid-adapted flowers do not reverse, perhaps because they had entirely lost their floral pigments.
Full (180o) or partial resupination has evolved several times in Acanthoideae, and this is sometimes caused by the twisting of the corolla tube rather late in development (Daniel & McDade 2005), a rather unusual mechanism. Elytraria (Nelsonioideae) may also have inverted flowers, as may some species of Thunbergia with pendulous inflorescences (Dworaczek & Claßen Bockhoff 2016). The filament curtain, formed from decurrent filament ridges in the corolla tube and more or less connate filaments immediately above the adnate portion of the filaments, is found in Ruellieae and perhaps other taxa, too. The curtain divides the corolla tube vertically into compartments; there may be transverse ridges on the corolla tube near the base, the nectar then becoming enclosed in a separate chamber (Mantkelow 2000; see also Moylan et al. 2004b).
Capsules open explosively in all taxa except Avicennioideae and some Thunbergioideae. Witztum and Schulgasser (1995) discuss in detail capsule dehiscence in Acanthoideae with their distinctive jaculators (= retinacula); capsules may be hygrochastic or xerochastic (e.g. Sell 1969). Dehiscence was described in detail for the hygrochastic Ruellia ciliatiflora. When the capsule opens explosively massive backspin (ca 1660 Hz - revolutions/second) is imparted to the flattened seeds because they sit on the jaculator in a way that results in force from the opening capsule being applied below the centre of mass, and this backspin also gives the seeds some lift, and they can be dispersed up to 7 m (Cooper et al. 2018). Some seeds, "floppers", wobble when launched, and they do not travel so far, while more wobblers/seeds with much less backspin are found in other Acanthoideae (Cooper et al. 2018). There is some dispute as to whether Nelsonioideae have jaculators, but even if present, they are not functional, and although "rudimentary" jaculators are reported from the subfamily (Johri & Singh 1959; Roham Ram & Masand 1963), they are unlike jaculators in Acanthoideae (Daniel & McDade 2014). In a number of taxa the testa is mucilaginous, and the mucilage can form a layer impermeable to oxygen so inhibiting germination when there is too much water around because of flooding (Western 2011 for references), although mucilage may also facilitate seed dispersal after discharge. Overall, seed morphology shows considerable variation (Al-Hakimi et al. 2017). For ultra-fast germination, see above under Ecology & Physiology.
In some species of Strobilanthes all the individuals flower and fruit in synchrony and then die; this happens in a regular cycle every few years and can occur over very large areas (Janzen 1976). Both pollinators and seed dispersers (the seeds are rich in oils) are attracted to the plants in large numbers.
Plant-Animal Interactions. Gall-forming fruit flies of the Tephretidae-Tephrellini are found here (and on Verbenaceae and Lamiaceae: Korneyev 2005). Neotropical species of Avicennia host a diversity of gall morphotypes, although the plant itself seems to be little affected (Silva et al. 2017).
Larvae of Nymphalinae-Melitaeini butterflies commonly feed on Acanthaceae (Wahlberg 2001; Nylin & Wahlberg 2008). Mass defoliation of Avicennia by lepidopteran larvae seems to be not uncommon (Fernandes et al. 2009).
Genes & Genomes. Chromosome numbers are very variable here - see Daniel (2018 and references) for literature. Daniel (2000) thought that the base number for Acanthaceae, excluding Nelsonioideae, was x = 7. Lyu et al. (2017) give measurements of some genome sizes.
Chemistry, Morphology, etc. Mendoncia lacks iridoids.
Inverted vascular bundles in the pith, or anomalous secondary thickening where an internal and inverted cambium develops, are scattered in the family. Neither have yet been found in Nelsonioideae or Avicennioideae, although some species of the former have odd vascular anatomy in the stem and even the root (Rouler 1893; Schwarzbach & McDade 2002 for literature). Mendoncia belizensis has rather boraginaceous R-Put bases.
The inflorescence of Mendoncia is described as being pedunculate and dichasial (Magnaghi & Daniel 2017), the pedicels proper being short to absent, although in overall appearance it is fasciculate and with long pedicels; inflorescence morphology here needs to be confirmed, and whatever the outcome, what are described as peduncles are in fact pedicels. Thunbergia has extrafloral nectaries on the calyx as well as nectaries inside the corolla tube, and in Avicennia nectar is secreted from glands on the corolla tube (for details, see Tomlinson 1986). In Avicennia there may be fewer corolla than sepal lobes ("connation" of a pair of the former?). Bravaisia (Acanthoideae) is distinctive in that it has small bracteoles and rounded calyx and corolla lobes (the former are more or less scarious); the anthers have short basal appendages. There is discussion as to the nature of corolla tube initiation, which is probably usually more or less late, rarely early (c.f. Leins & Erbar 1997; Schönenberger & Endress 1998; see also Endress 1999 for floral development). Anther morphology is particularly variable in neotropical Justicia (Kiel et al. 2013, 2017). The diversity of pollen morphology in most of the family (not Nelsonioideae) is spectacular, and it also shows extensive homoplasy (e.g. Kiel et al. 2006). For variation within Strobilanthes s.l., see Carine and Scotland (2000) and Wang and Blackmore (2003), for that within Acanthoideae as a whole, see Raj (1961), Daniel (1998), Scotland and Vollesen (2000) and references, Daniel (2010), House and Bakewill (2016), Al-Hakimi et al. (2017) and many other papers. Many Isoglossinae (Justicieae) have distinctive "Gürtelpollen" (Kiel et al. 2006) - lenticular biporate pollen with a prominent circumferential band, but any functional significance of this is unclear. The [Acanthoideae [Thunbergioideae + Avicennioideae]] clade appears to lack a funicular obturator, but I am uncertain as to the polarity of this feature. The fruit of Avicennia is a capsule, according to Takhtajan (1997) and Schatz (2001), but it may open only as the seed germinates. For cotyledon folding, see Schwarzbach and McDade (2002).
Embryo sac development in some/most Acanthaceae is very distinctive. The tip of the embryo sac grows through the micropyle and eventually may lodge in the placenta, and this where the egg apparatus is formed (the movements of the polar nuclei are unclear). As the embryo develops, a very long suspensor forms and the embryo is pushed back into the endosperm - and so into the ovule and the developing seed (e.g. Mohan Ram & Masand 1963 and references). This is rather similar to comparable, but more extreme, behaviour in Loranthaceae. The ovule of Avicennia is reported to be straight; the embryo sac is extra-ovular, and the micropylar endosperm haustorium at least is also extra-ovular, being very much branched and reaching the placenta (Mauritzon 1934a; Padmanabhan 1964, 1970).
In Acanthoideae other than Acantheae, there is considerable variation in the details of endosperm development. There is often a central area in which divisions are free nuclear, walls being laid down subsequently, but in some taxa there is what is known as a "basal apparatus", an area in which walls are not laid down; this pattern of endosperm development occurs in no other angiosperms (Mohan Ram & Wadhi 1964; Johri et al. 1992 and references). In Nelsonioideae the central area is entirely cellular, but other details of endosperm and embryo sac development are like those just described (Johri & Singh 1959; Moham Ram & Masand 1963). This distinctive asymmetric endosperm development is also found in Lamiaceae-Nepetoideae (a parallelism).
For general anatomy, capsule dehiscence, etc., see van Tieghem (1908), for embryology, etc., see Mauritzon (1934a), and Wadhi (1970), and for stomata, see Rohweder et al. (1971). Nelsonioideae: some information is taken from Bremekamp (1955) and especially Daniel and McDade (2014). Thunbergioideae: for Thunbergia, etc., see Schönenberger (1999). Avicennioideae: for embryology, etc., of Avicennia, see Padmanabhan (1970, as Verbenaceae) and also Borg and Schönenberger (2011) and for wood anatomy, see Carlquist (1990b), for general information, see Tomlinson (1986) and Sanders (1997). Acanthoideae: for information on acicular fibres, see Bremekamp (1965: "raphidines"), for chemistry, see H. F. W. Jensen et al. (1988) and Sicker et el. (2000: benzoxazinones), for corolla aestivation, which shows interesting variation, see Scotland et al. (1994), for floral morphology, see Endress (1994b), for nectaries, see Vogel (1998c), and for some embryology, see Maheshwari and Negi (1955).
Phylogeny. The erstwhile Nelsoniaceae were placed sister to other Acanthaceae in Hedren et al. (1995), and this position seems quite firm (see esp. McDade et al. 2012). The position of Avicennia (Avicenniaceae) within Acanthaceae s.l. is also well established, if its exact position is less certain; all have the same distinctive endosperm development and swollen nodes. Avicennia has a rather weakly supported sister group relationship with Thunbergioideae (Schwarzbach & McDade 2002; Hilu et al. 2003), support coming mostly from the chloroplast genes (McDade et al. 2008). Relationships in Tripp and McDade (2014a) were [Nelsonioideae [Thunbergioideae [Avicennioideae + Acanthoideae]]], while in Z.-D. Chen et al. (2016) the positions of Avicennioideae and Thunbergioideae were reversed, although in neither was the position of Avicennioideae well supported. For more on phylogenetic relationships, see Scotland et al. (1995).
Within Nelsonioideae, Nelsonia and Elytraria are successively sister to the rest of the subfamily, within which there is quite a lot more structure (McDade et al. 2012, see also 2009; Daniel & McDade 2014; Wenk & Daniel 2009: position of Nelsonia uncertain).
For the phylogeny of Acanthoideae, see McDade et al. (2008: see also McDade & Moody 1999; McDade et al. 2000a; McDade et al. 2006; Tripp & McDade 2014a): Acantheae are sister to the rest. In Acantheae, McDade et al. (2005) found that taxa with one- and two-lipped corollas form separate clades, Old World and largely New World respectively. Barlerieae: The Indian Petalidium barlerioides is probably sister to the rest of the genus, which is mostly from the Namib Desert area (Tripp et al. 2017b). For Justicieae, mostly New World, see McDade et al. (2000b), Kiel et al. (2009), and in particular the very useful treatment by Tripp et al. (2013a) and the extensive study of the "justicioid" lineage by Kiel et al. (2017). In the latter, it was found that support along the backbone of the phylogeny was mostly strong. For relationships in the Tetramerium group, see Daniel et al. (2008) and especially Côrtes et al. (2015). Ruellieae: Ruellia is defined by pollen morphology, and it includes genera like Blechum, etc.; many taxa are cleistogamous (Tripp & Manos 2006; Tripp 2007). For relationships in Ruellia itself, see Tripp and Tsai (2017), and for those in Old World species of the genus, basal but a minority, see Tripp and Daryshire (2017). The Physacanthus is probably an ancient inter-tribal (Ruellieae X Acantheae) hybrid (Tripp et al. 2013b, see also above).
Borg et al. (2006) provide a phylogeny for Thunbergioideae.
Classification. The tribal classification of Acanthoideae follows that in McDade et al. (2008). Generic limits are difficult, as in other groups where genera have commonly been based on variations in corolla morphology that represent adaptations to particular pollinators (e.g. Daniel et al. 2008 and references; see also Côrtes et al. 2015); floral variation may be less reliable in marking genera than variation in e.g. seed and pollen (Kiel & McDade 2014). Furthermore, the very extensive variation in pollen morphology has led to the dismemberment of genera. Bremekamp (1944) broke up Strobilanthes into some 54 genera most of which have been returned to whence they came. Genera in Justicieae are being recircumscribed and have been assigned to subtribes (Tripp et al. 2013a), although recent work emphasizes the problems that have to be faced (Kiel et al. 2017); for genera in Nelsonioideae, see Daniel and McDade (2014). For a sectional classification of Old World Ruellia, see Tripp and Darbyshire (2017).
Species numbers seem particularly uncertain here, as Tripp et al. (2013a) suggest.
Previous Relationships. Nelsonioideae have often been placed in Scrophulariaceae s.l. or considered "intermediate" between Scrophulariaceae and Acanthaceae while Cronquist (1981) was uncertain of the relationships of his Mendonciaceae. Avicennia was often included in Verbenaceae, largely because it is woody, has a more or less cymose inflorescence, and a gynoecium with two ovules per carpel. Thomandersia has seeds with a structure described as a retinaculum, although capsule dehiscence is not explosive (see Thomandersiaceae).
[Bignoniaceae [[[Schlegeliaceae + Lentibulariaceae] [Thomandersiaceae + Verbenaceae]] [Lamiaceae [Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]]]]]: ?
BIGNONIACEAE Jussieu Back to Lamiales
Woody, trees or shrubs; C-4 carboxyl and ecarboxylated iridoids +; phloem stratified; cork also cortical; paratracheal-aliform parenchyma + (0); nodes 1:1-9; petiole bundles annular (also rib or adaxial bundles); stomata helicocytic [?level]; leaves twice-compound, lamina vernation conduplicate, margins entire (toothed); inflorescence branches cymose; flowers large; K often with nectaries, A (5, 2), thecae sagittate or head-to-head, usu. not confluent, tapetum amoeboid; pollen tricolpate, psilate, nonperforate; bundles in the ovary wall and also opposite septum, ovules in two groups in each loculus, (placentae lobed), stigma lobes broad, sensitive, wet; integument 4-10 cells across; fruit often with epidermal extrafloral nectaries; seeds many, winged, relatively large; wings 1-2 cells thick, cells with helical/annular(none/reticulate) thickenings; endosperm 0, micropylar haustoria 0; n = 20; nuclear genome [1C] (592-)1112(-1697) Mb; germination epigeal, phanerocotylar (cryptocotylar), cotyledons persistent, ± cordate basally, apex lobed.
110 [list]/790 - eight groups and unassigned genera below. Mainly tropical, esp. South America (map: from van Steenis 1977).
Age. Crown-groupo Bignoniaceae are estimmated to be (54.3-)51.5(-49.3) m.y.o. (Tank & Olmstead pers. comm.).
Fossil seeds and fruit of Bignoniaceae are known from the Eocene of Washington State and are ca 49.4 m.y.o. (Pigg & Wehr 2002).
1. Jacarandeae Seeman
Aliform parenchyma +; K ± free, staminode large, bearded; G with parietal placentation; fruit orbicular, angustiseptate; n = 18.
1(?2)/55: Jacaranda (50). Tropical America.
[Tourrettieae [Tecomeae [Bignonieae [[Catalpeae + Oroxyleae] [Crescentieae + Coleeae]]]]]: (vessel elements with reticulate and/or foraminate perforation plates).
2. Tourrettieae G. Don
Vines, climbing by tendrils; (leaves pedate);inflorescence racemose, bracteate; staminode 0.
2/6. Andes in South America and N. to Mexico. [Photo - Eccremocarpus Flower.]
[Tecomeae [Bignonieae [[Catalpeae + Oroxyleae] [Crescentieae + Coleeae]]]]: leaves once compound; (staminodes +, simple).
3. Tecomeae Endlicher
Distinctive C-4 formyl iridoids; (perforated ray cells).
12/55. Worldwide, not Arctic.
[Bignonieae [[Catalpeae + Oroxyleae] [Crescentieae + Coleeae]]]: ?
Age. An estimate of the age for the clade [Campsis, Catalpa] is (32-)25(-17) m.y. (Bell et al. 2010).
4. Bignonieae Dumortier
Lianes, climbing by leaf tendrils; (monofluoracetates +); (cambium storied); vascular pit borders usu. 0-3.9μm across, aliform-confluent xylem parenchyma +, rays tall [usu. >1 mm tall], ray cells perforated; anomalous secondary thickening + [morphologically variant phloem in deep wedges, the xylem cylinder 4- or more lobed] (normal); (stratified phloem 0); (prophyllar pseudostipules +); (leaves once-compound, ternate, (with 3 [1, 2, several] petiolular tendrils) (lamina vernation involute - Pyrostegia); fruit septifragal, with persistent septum and separate whip-like strands of woody tissue [= vascular bundles opposite septum], (indehiscent).
21/383: Adenocalymma (74), Fridericia (67), Amphilophium (47), Anemopaegma (45). America, largely tropical. [Photo - Distictella Flower.]
Age. Crown-group Bignonieae have been dated to (54.2-)49.8(-45.7) m.y., the crown clade that includes the tribe minus the monotypic Perianthomega being (52.2-)48.0(-43.9) m.y. old (Lohmann et al. 2012).
[[Catalpeae + Oroxyleae] [Crescentieae + Coleeae]]: (vasicentic or aliform parenchyma +).
[Catalpeae + Oroxyleae]: ?
5. Catalpeae Meisner
Leaves (spiral), simple; (A 2, staminodes 3).
2-3/11. North America, the Greater Antilles, East Asia.
6. Oroxyleae A. H. Gentry
(Flowers polysymmetric); (A 5); fruits septicidal.
[Crescentieae + Coleeae]: ?
7. Crescentieae G. Don
Cambium storied; (short shoots +); leaves spiral, palmately compound, (unifoliolate), (simple), (phyllodinous); (flowers bat-pollinated, ± cauliflorous); (placentation parietal); ovules with hypostase; (fruits ± indehiscent, and seeds not or barely winged).
12/147: Tabebuia (70). Central and South America and the Greater Antilles. [Photo - Amphitecna Flower.]
Synonymy: Crescentiaceae Dumortier
8. Coleeae Bojer
(Prophyllar pseudostipules +); leaves often whorled, (simple), (phyllodinous, articulated); flowers bat-pollinated, ± cauliflorous; (placentation parietal); fruits ± indehiscent; seeds ?not winged.
4/69 + 28 undescribed (Callmander et al. 2015). Madagascar and surrounding islands.
Evolution: Divergence & Distribution. The family is probably New World in origin, with five or six shifts to the Old World and one back to the New World (Olmstead et al. 2009; Olmstead 2013). Lohmann et al. (2012, q.v. for many dates) suggested that the ancestors of fossils assignable to Bignonieae from Central and North American (Panama, Washington State) as well as of North American Bignonia itself, might have arrived there by long distance dispersal. Interestingly, members of three clades which are surmised to have been involved in long distance dispersal are currently dispersed by animals; Olmstead (2013) thought that adaptation to animal dispersal had occurred after wind-assisted dispersal events.
Variation in wood anatomy in the family is optimised on a phylogenetic tree by Pace and Angyalossy (2013; see also Pace et al. 2015a) and the extensive variation of the distinctive variant phloem found in deep wedges in the secondary xylem in Bignonieae is placed in a phylogenetic context by Pace et al (2015b; see also below).
Ecology & Physiology. Bignoniaceae-Bignonieae are, along with Sapindaceae, perhaps the most ecologically important neotropical group of lianes, and include around 400 species (e.g. Gentry 1991); Sousa-Baena et al. (2014a) discuss the evolution of tendrils in Bignonieae. The plants climb using foliar tendrils, which can be grapnel-like as in the appropriately-named Dolichandra unguis-cati, and attachment may be aided by glue-like exudates, as in Bignonia capreolata, or by tissue ingrowth into irregularities of the support, as in Amphilophium crucigerum (Seidelmann et al. 2012). The phloem of the lianes is particularly distinctive and is of two types. More ordinary phloem is found on the periphery of the vascular cylinder, and it has narrow sieve tubes, more parenchyma, broad rays, etc., and is perhaps involved in storage. The variant phloem, found in the phloem wedges, has prominent fibres and very wide sieve tubes, and is probably more involved in translocation of the photosynthesate (Pace et al. 2011). Lianes in general tend to have extensive leaf areas considering the width of their stems, hence perhaps the importance of the variant phloem (e.g. Isnard & Feild 2015 and references). There are a number of differences between the wood of lianes, shrubs and trees in Bignoniaceae, lianes having i.a. a larger area of vessels, these vessels showing a great variation in size (= dimorphism); perhaps the narrower vessels remain fuctional when the wider vessels become cavitated (Gerolamo & Angyalossy 2017). For additional information about lianes and Bignoniaceae, see Angyalossy et al. (2015) and other references in Schnitzer et al. (2015).Bignoniaceae are also the second most speciose family in drier tropical forest types in America (Gentry 1988, 1991), and drier forests and the liane habit may be connected, having in common toleration/prevention of water stress, the whole family perhaps being adapted to drought (Punyasena et al. 2008).
Pollination Biology & Seed Dispersal. The large flowers of Bignoniaceae are animal pollinated, and the considerable variation in floral morphology and flowering phenology can be associated with the behaviour and type of visitor (Gentry 1974a, b, 1990; Alcantara & Lohmann 2010a, b; Alcantara et al. 2013). One of the commonest flower types in the New World is the Anemopaegma type, visited by euglossine bees (along with anthophorids); this may be ancestral in Bignonieae, and has an infundibular, straight corolla tube, nectar, and is magenta, yellow or white in colour (Alcantara & Lohmann 2010a). The nectarless Cydista type, otherwise rather similar florally, is also visited by euglossines. (Note that euglossine bees began diversifying some 42-27 m.y.a. - Ramírez et al. 2010.) Oroxylon is bat pollinated, and its flowers are almost polysymmetric and have five stamens; Fleming et al. (2009) list species in the family that are known to be pollinated by bats. Alcantara and Lohmann (2010a, b) found that, in general, flower size in the lianescent Bignonieae was larger in the past than it is is in extant species.
Dispersal syndromes are also quite diverse (Gentry 1983; 1990) but they are not particularly correlated with pollination syndromes. Thus Kigelia africana is bat-pollinated and has massive, sausage-shaped, indehiscent fruits that are eaten by everything from monkeys to elephants. Oroxylon is also pollinated by bats, but it has capsules and wind-dispersed seeds. Wind dispersal is common, and the seeds often have broad, papery wings. A number of taxa have seeds dispersed by water, including Dolichandrone, a mangrove plant; here the modified seed wing is corky and serves as a flotation device. In Crescentieae, Amphitecna and Crescentia (calabash) have spherical indehiscent fruits, Parmentiera has elongated fleshy fruits, although its seeds still have a small wing, and Spirotecoma and Tabebuia and relatives have elongated, dehiscent fruits and winged seeds.
Extrafloral nectaries are extremely common; these may be on reduced prophylls, on the tips of young leaflets, at the nodes, on the outer surface of the calyx and on the ovary; ants are attracted (e.g. Gonzalez 2011; Weber & Keeler 2013). Domatia are also common.
Vegetative Variation. Bignonieae are nearly all lianes with branched tendrils and distinctively rayed xylem (Lohmann 2006 for a phylogeny). Perianthomega has biternate leaves, it also has robust unbranched twining petioles, the three small scars at their ends representing leaflets. Elsewhere in Bignonieae the tendrils are variously-branched terminal or lateral petiolules of the compound leaves so common in the family, and Sousa-Baena et al. (2014a, also 2018b) discussed tendril morphology and evolution. As for the genetic control of tendril development here, Sousa-Baena et al. (2014b, 2018a) examined this in some detail, noting i.a. the activity of SHOOTMERISTEMLESS (a KNOX1 gene), PHANTASTICA and LEAFY/FLORICAULA (c.f. the IRL clade in Fabaceae; the latter gene is most important). Within Bignonieae, variation in the detail of the ray-like fluting the xylem which becomes channeled or lobed can be interpreted as complexity increasing by terminal addition and is mirrored by ontogenetic increases in the numbers of channels as an individual grows; the simple pattern in shrubby members, a polyphyletic group, results from a heterochronic reversal (Pace et al. 2009). Pace et al. (2011) note that the variant phloem that causes the fluting of the vascular cylinder has large-diameter sieve tubes and numerous fibres, hence contributing substantially to both translocation and stem support; regular phloem has much narrower sieve tubes.
Palmate leaves have arisen more than once within Bignoniaceae, but are known only in New World taxa. The New World Tabebuia s.l., which has opposite, palmate leaves, is polyphyletic (Grose & Olmstead 2007b); a number of taxa - some apparently very different vegetatively - are derived from it. These include Amphitecna, with spiral, simple leaves like those of Crescentia. The petioles are short and the lamina has distinctive, widely spreading venation; they are phyllodinous, and in some species of Crescentia palmate leaflets are borne on the end of a lamina-like petiole confirming the morphological nature of the latter. Parmentiera and Spirotecoma, both with more ordinary opposite palmately-compound leaves, are also close; all four genera have bat-pollinated flowers. They are part of a clade of palmately-leaved taxa (Grose & Olmstead 2002, 2007a; see expanded Crescentieae above).
The simple and clearly petiolate leaves of Catalpa (opposite or whorled) and Chilopsis (spiral: the two genera hybridise), have a very different morphology from those of Crescentia, etc.; they appear to be more conventionally simple.
Chemistry, Morphology, etc. Pace et al. (2016) summarize variation in wood anatomy in the family.
There are four main carpel bundles, but only two in "Scrophulariaceae" (Armstrong 1985), Gesneriaceae, etc.. In Tourrettieae, Tourrettia has sub four-locular ovaries each loculus with a single rank of ovules, while Eccremocarpus has parietal placentation. Ovule shape varies considerably, some species having a long chalazal beak; Pereira abd Bittencourt (2016) note that details of the deposition of callose around the megaspores and also nucellar protrusion may be of systematic interest. Endosperm development also varies, thus Incarvillea has a huge micropylar endospermal cell (Mauritzon 1935). A number of Bignonieae with septifragal dehiscence also have cracks in the loculicidal position along the backs of the valves.
For general information, see Manning (2000) and Fischer et al. (2004a: the classification is very "classical", c.f. e.g. Lohmann 2006 and esp. Lohmann & Taylor 2014). For toxic monofluoracetates, see Lee et al. (2012) and for iridoids, von Poser et al. (2000), for wood anatomy, see Rogers (1984: comparison with Rubiaceae), Gasson and Dobbins (1991: lianes and the rest compared) and especially Pace and Angyalossy (2013) and Pace et al. (2015a, b), and for nodal anatomy, see Trivedi et al. (1976). For information on pollen, which is very variable, see Gentry and Tomb (1979) and Burelo-Ramos et al. (2009: Pithecocteniinae), for tapetum, Huysmans et al. (1998), for some embryology, see Bittencourt and Mariath (2002), for seed anatomy, including that of Schlegliaceae and Paulowniaceae, see Lersten et al. (2002), and for protein bodies in the nucleus, see Bigazzi (1995).
Phylogeny. The basic phylogenetic structure within the family is [Jacarandeae [Tourrettieae [Bignonieae + the rest]]] (Olmstead et al. 2002). This has been further amplified by Olmstead et al. (2009: ca 3/4 of the genera sampled, three genes), although some relationships of major groups like Tecomeae remain poorly supported.
For a comprehensive (2-gene + morphology) phylogeny of Bignonieae, see Lohmann (2006a, 2012); [Perianthomega [[Adenocalymma + Neojobertia + The Rest]] is the basic phylogenetic structure. Major clades are supported by a mixture of floral and vegetative characters (Lohmann 2002, esp. 2006); the limits of Adenocalymma are being reworked (Fonseca & Lohmann 2018). Bignonieae may be close to Oroxylum and relatives - which have bicompound leaves and septicidal capsules - and Catalpa - which has only two stamens (Olmstead et al. 2002). Coleeae as narrowly delimited here are restricted to Madagascar, and their phylogeny and fruit evolution has been examined by Zjhra et al. (2004) and especially Callmander et al. (2015); they are part of a larger and well supported clade that includes Kigelia, Spathodea, etc.. Coleeae and Crescentieae have taxa with similar flowers and fruits and "simple" leaves, but latter are different morphologically. Relationships between the New World Tabebuia, with opposite, palmately-compound leaves and its relatives have been clarified. Amphitecna and Crescentia, both with spiral, simple leaves, are probably derived (Grose & Olmstead 2007a, b). Delostoma may be sister to the [Bignonieae [[Catalpeae + Oroxyleae] [Crescentieae + Coleeae]]] clade (Pace et al. 2015a).
Classification. The tribes above are those recognised by Olmstead et al. (2009). Note, however, that their tribal classification is not exhaustive in that not all genera are assigned to tribes, partly because their phylogenetic position is still ambiguous (e.g. Argylia, Delostoma). Crescentieae have been expanded to include Tabebuia, etc. (the Tabebeuia alliance of Grose & Olmstead 2007a, b), the expanded clade being characterized by palmate leaves. Coleeae, too, could well be expanded to include genera like Kigelia, Spathodea, etc. (but see Callmander et al. 2015).
Over-reliance on characters associated with pollination and dispersal syndromes as markers of generic distinctness has caused serious problems with generic limits (see Lohmann 2003, 2006), however, generic limits in Bignonieae, close to half the family, have now been reworked (Lohmann & Taylor 2014).
There is a species level checklist for the family (Lohmann & Ulloa 2007).
Thanks. I am grateful to L. Lohmann for comments.
[[[Schlegeliaceae + Lentibulariaceae] [Thomandersiaceae + Verbenaceae]] [Lamiaceae [Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]]]]: ?
[[[Schlegeliaceae + Lentibulariaceae] [Thomandersiaceae + Verbenaceae]]: ?
[Schlegeliaceae + Lentibulariaceae]: ?
Phylogeny. For sampling, and support for this odd couple, see Refulio-Rodriguez and Olmstead (2014).
SCHLEGELIACEAE Reveal Back to Lamiales
Woody shrubs or vines, often epiphytes, (large trees); pericyclic sheath sclereidal; nodes 1:3; petiole bundle solid or (almost) annular, with wing bundles, pericyclic lignification 0; sclereids +; stomata variable; lamina margins entire or serrate/spiny; (inflorescence branched); flowers quite large; nectaries on outside of K; staminode +/0; nectary vascularized from carpellary bundles/0; placentae swollen, (placentation intrusive parietal, placentae uni- or bilobed); fruit a berry, K persistent to ± accrescent; seeds compressed or angular; exotestal cells with scalariform thickenings on the inner periclinal wall or mucilaginous with outer periclinal wall absent; endosperm +/0, cotyledons slightly over half the length of the embryo; n = 20; seedlings epigeal and phanerocotylar, cotyledons lobed.
4 [list]/28 (37): Schlegelia (15), Gibsoniothamnus (11). Mexico to tropical, esp. N.W., South America, Antilles (map: from Gentry 1980; Tropicos iii.2014). [Photo - Flower, Flower, Fruit.]
Chemistry, Morphology, etc. For wood anatomy, see Gasson and Dobbins (1991); there are no obvious differences in wood anatomy between Schlegeliaceae and Bignoniaceae. Schlegelia may have anomocytic or paracytic stomata, while those of Gibsoniothamnus are anisocytic or cyclocytic. There are often quite conspicuous "glands" on the lower surface of the lamina - these are hairs with the normal lamialean structure of radially-arranged cells in the head. Gibsoniothamnus may be anisophyllous (c.f. Thomandersia).
Winged seeds have been reported for e.g. Schlegelia (Fischer 2004b), but the combination of winged seeds and baccate fruits seems rather improbable; Gentry (1973) described the seeds of Schlegelia as being angular. I have not seen the Cuban Synapsis.
Some information is taken from Burger and Barringer (2000), Barringer (2004: Gibsoniothamnus), and Fischer (2004b: under Scrophulariaceae), all general, Leinfellner (1973: gynoecium of Schlegelia), and Armstrong (1985: floral anatomy). Gibsoniothamnus parvifolius: Herrera 672, - leaf, stem, seed; G. allenii: McPherson 11069 - leaf, seed; Schleglia darienensis: Neill et al. 11411 - seed.
Previous Relationships. Schlegelia and relatives have usually been included in Bignoniaceae or in Scrophulariaceae s.l., being "transitional" between the two (Cronquist 1981).
LENTIBULARIACEAE Richard, nom. cons. Back to Lamiales
Herbs, as rosettes, etc., (annuals); carnivorous [insectivorous]; (verbascoside 0 - Utricularia); primary and other roots poorly developed, root cap 0, or roots 0; plants often Al-accumulators, little oxalate accumulation; ?cork; vessel elements?; stomata also anisocytic; hairs variously secreting mucilage and digestive enzymes; leaves spiral/(0), lamina margins entire, vernation circinate [Pinguicula heterophylla]/elongated eel trap-like structures/sensitive traps +; (inflorescence umbellate - Pinguicula); K 2, 4, 5, C quincuncial [abaxial lobe outside the others in bud - ascending cochlear], etc., tube formation early [Pinguicula], with an abaxial spur, nectar produced by glandular hairs; A 2 [the abaxial pair], (± free - Pinguicula), filaments stout [always?], thecae confluent, (superposed), epidermal cells ephemeral; tapetal cells 2(-3)-nucleate; staminode 0; pollen (grains tricellular), (4-10-zonocolporate, etc. - Pinguicula); G placentation free-central or basal, style hollow, short [up to as long as the ovary, often 0], stigma lobes broad, (sensitive), (one lobe only), wet; ovules (1< carpel), integument 2-6 cells across; (embryo sac protrudes beyond the micropyle, haustorial), (antipodal cells persisting); fruit a capsule of various types, (seeds with pedestals); exotestal cells variously thickened, elongated, and/or protruding; 0, embryo chlorophyllous, cotyledons 1, some Pinguicula (undifferentiated - many Utricularia/to 15 cotyledon-like structures - some Utricularia); germination (hypogeal - some Pinguicula); n = 6-12+; chromosomes 0.2-2.3µm long, nuclear genome size [1C] 0.065-1.55 pg/(61-)476(-1722) Mbp.
3 [list]/350: Utricularia (240), Pinguicula (80), Genlisea (30). World-wide, but introduced into Hawaii? (map: from Hultén 1958, 1962, 1971; Taylor 1989). [Photo - Flower.]
Age. Crown-group Lentibulariaceae have been dated to (41-)38, 28(-25) m.y.a. (Wikström et al. 2001), ca (54-)42, 37(-28) m.y.a. (Bell et al. 2010), ca 40 m.y.a. (Ibarra-Laclette et al. 2013) and ca 47 m.y.a. (Silva et al. 2017).
Evolution: Divergence & Distribution. South America and the Antipodes harbour most diversity within Utricularia, and Silva et al. (2017) flesh out possible scenarios for diversification following a suggested South American origin. Fleischmann et al. (2010) examine character evolution in Genislea.
Ecology & Physiology. As befits their carnivorous proclivities, Lentibulariaceae are notably prominent in wet, acid habitats, Piguicula, for instance, growing in acid bogs. The ancestral habitat of Utricularia is terrestrial, although the fully aquatic lifestyle has evolved there more than once, some species living happily as members of the ephemeral flora of ponds on African inselbergs (Seine et al. 1996) or in bromeliad tanks (embryos may be viviparous here - Plachno & Swiatek 2009), and there are also a few rheophytes and epiphytes (Silva et al. 2017). Tubers, apparently modified rhizomes, store water in a few American species of the genus (Rodrigues et al. 2017).
Pinguicula has fly-paper traps, and the plants may smell, so perhaps attracting potential prey (Fleischmann 2016 and references). Even pollen landing on the leaves may be digested (Rice 2011), while according to the english summary of Titova (2012: p. 1162) the cotyledons of P. vulgaris have the "ability to flap and digest insects". Mirid bugs have been found on Pinguicula, and this may have implications for plant protection and/or nitrogen uptake (see Wheeler & Krimmel 2015 for mirids). Genlisea has long, spirally-twisted structures (= modified leaves, see below) that function rather like eel traps; prey are passively trapped as they swim up the spiral, their exit being blocked by backwardly-pointing hairs, and a few species of Utricularia have passive traps rather like those of Genlisea (Westermeier et al. 2017).
Nearly all species of Utricularia, whether growing in water or moist soil, have suction traps (for their morphology, see Merl 1915; Franck 1976; Reifenrath et al. 2006; Westermeier et al. 2017). Fewer studies have beeen carried on on terrestrial Utricularia, although Westermeier et al. (2017) is a notable exception. When water is pumped out of the bladder, the traps are under negative pressure (e.g. Adamec & Poppinga 2016). The trapdoor itself may be convex, i.e. it bulges outwards, and the entrance is short, or the trapdoor forms a ± acute angle between the upper and lower sides of the entrance, and the entrance tube is long (Westermeier et al. 2017). In aquatic species, the stimulation of sensitive hairs at the mouth of the trap leads to the rapid inversion of curvature of the door (to concave) and its opening in around 300–700 µs, water being sucked in the short mouth at a rate of around 2.7 m s-1 (Singh et al. 2011). Recovery may take up to half an hour, but is often much faster (see Westermeier et al. 2017 for details of the timing of the various phases of trap activity, videos, etc.). Jobson et al. (2004) and Laakkonen et al. (2006) suggest a possibly associated change in cytochrome c oxidase that may increase respiratory capacity so providing the energy needed for the rapid movements of the traps. Vincent et al. (2011; see also Singh et al. 2011) distinguish between a slow, energy-dependent phase in which water is pumped out of the trap, the trap becoming deformed and elastic energy being stored in the trap body, and a fast but passive phase in which the trap door opens and closes in less than a millisecond, with water and contained prey rushing inside. Westermeier et al. (2017) describe a variety of trap morphologies (obliquity of the trapdoor, length of the entrance tube, R-Put position) and behaviours (does the trap deform before opening?) in the genus, and plot the complex variation that they describe on a tree. Spontaneous opening of traps without stimulation by prey is common (Adamec 2011a; Adamec & Poppinga 2016). For the vascularization of the traps of Genlisea and Utricularia, see Plachno et al. (2017), although it is unclear how the vascular system functions. Inside the trap are 2-armed hairs near the mouth and X- or H-shaped 4-armed hairs further in, although there are also 1- and 3-armed hairs (e.g. Taylor 1989).
What do the traps do? One tends to think of small water animals swimming around, triggering the opening of the traps, and meeting their death - indeed, I have even seen a small ant trapped in a bladder; its head and thorax were inside. However, the exact role of the traps in the life of the plant is uncertain. Sirová et al. (2017, see also 2018) observed that in their experience traps rarely caught anything, but all of them had microbial commensals inside them, and they found 4,500 microbial taxa in the traps and their periphyton. Indeed, the relationships between plant and algae - and potential animal prey, too - have been difficult to elucidate, and diatoms and other algae may be common in the bladders (Jobson & Morris 2001; Alkhalaf et al. 2011; Adamec 2012; Plachno et al. 2014). Some Utricularia may eat aquatic algae, especially if the water is very acid, and algae may predominate in traps in such environments (Peroutka et al. 2008a). Nitrogen from 15N-labelled phytoplankton may move into the plant (Alkhalaf et al. 2009), and some bacteria in the traps are able to fix nitrogen, even if the high nitrogen concentration in the traps represses this activity (Sirová et al. 2014). The diverse microbial community in the traps can also aid in the uptake of phosphorus by the plant (Sirová et al. 2009). The plant may support the microbial community nutritionally when there is no prey in the traps (Adamec 2011a), carbon recently fixed by the plant ending up in the young traps and in the microorganisms there (Sirová et al. 2010). Recently Sirová et al. (2017) described bacteria that could variously break down protein, amino acids, cellulose, etc., and methanotrophs that seemed to keep the traps free of methane. A protozoan community (euglenids, Tetrahymena), species-poor but often present in very high numbers, along with predatory bacteria (Bacteriovoracaceae) kept the numbers of bacteria down. Wheeler and Carstens (2018) looked changes in gene expression categories in Genislea aurea and Utricularia gibba, finding notably more in the latter than in the former.
For further details of the morphology of Lentibulariaceae as it relates to their carnivorous proclivities, see Lloyd (1942) and Juniper et al. (1989) in particular; note that secretory glands throughout the family are attached to single epidermal cells and have no contact with vessels. Peroutka et al. (2008b) discuss aspects of the functional biology of Lentibulariaceae (see also Rice 2011; Adamec 2011a, b).
Pollination & Seed Dispersal. There are some very distinctive flower types among the 63 species of Australian Utricularia (Lowrie 2013: vol. 3).
Utricularia may be myxospermous (Grubert 1974). The diversity of capsule type and especially testa morphology within Utricularia in particular is staggering (Taylor 1989).
Vegetative Variation. Pinguicula, alone among Lentibulariaceae, has roots, if often rather poorly developed (Adlassnig et al. 2005); ordinary roots do not occur in either Genlisea and Utricularia. The vegetative morphology of some species of Utricularia in particular can be difficult to interpret in conventional terms (e.g. Arber; Rutishauser & Sattler 1989; Rutishauser 2016: summary). There the embryo is usually undifferentiated, although some exceptions are mentioned by Plachno and Swiatek (2010). Its early development can seem almost disorganized, with no obvious primordia evident (Kondo et al. 1978); cotyledons and radicle are not apparent, or there can be up to 15 cotyledon-like structures. Small fragments of the "leaves" or even the cut peduncle can regenerate the whole plant (Merl 1915); Chormanski and Richards (2012) describe the construction of U. gibba in detail; the plant is made up of stolons and dichotomously-branching leaf-like structures that bear the traps. The suction bladder-traps in Utricularia have no parallel in other flowering plants (see e.g. Sattler & Rutishauser 1990; Plachno & Swiatek 2010 for development), although Kaplan (1997, vol. 2: chap. 14, 17; e.g. also Lloyd 1942) suggested that the various structures bearing traps in Lentibulariaceae are all basically foliar in nature. For instance, the spiralling, positively geotropic passive traps of Genlisea are borne in the same phyllotactic sequence as its leaves, and the prolonged apical growth of these traps is like that of the leaves of some species of the morphologically much less problematic Pinguicula. Some species of Utricularia have single traps on the ends of elongated leaf-like structures, and these may be positively geotropic (Taylor 1989, c.f. Genlisea). There are also quite commonly much more conventional leaf-like structures in Utricularia itself, and U. kuhlmannii (+ U. trichophylla) was even described as having odd pinnate leaves by Merl (1915; see also Troll & Dietz 1953), while other taxa may have deeply cordate leaf blades, etc.. Rhizome- and tuber-like structures occur in some taxa (Rodrigues et al. 2017).
Bacterial/Fungal Associations. Utricularia gibba has lost its endomycorrhizal-specific genes (Ibarra-Laclette et al. 2013; Delaux et al. 2014).
Genes & Genomes. Some species of Genlisea, e.g. G. tuberosa, have the smallest genomes known from angiosperms, the chromosomes of that species being bacterium-sized and only 0.2 µm long, close to the resolution limit of light microscopes. However, there is substantial variation in genome size - 60Mb—1.5Gb/63.6-1722 Mbp - within the family, genomes of Pinguicula in particular being larger, although within Genislea alone there is the whole range of variation in the family (Greilhuber et al. 2006; Fleischmann et al. 2014; Silva et al. 2017). Ibarra-Laclette et al. (2013, see also 2011; Leushkin et al. 2013; Carretero-Paulet et al. 2015) found that almost all the non-genic DNA in the tiny genome of U. gibba had been lost. However, gene number and overall functionality was similar to that in genomically more obese plants - although Leushkin et al. (2013) suggested that G. aurea had only 1/2-2/3 the genes of two other lamiids with which they compared it - and there was evidence of three (?two - Lan et al. 2017) rounds of genome duplications (with n initially = 6, or 8?) beyond the palaeohexaploidy event of the core eudicots and since the divergence of Solanales (Ibarra-Laclette et al. 2013). Around two thirds of the genes in G. aurea were the only members of their family, while in the three other rosids compared over 50% of the genes had two or more members per family (Leushkin et al. 2013). Interestingly, it is the diploids in Genislea that have the larger genomes (Fleischmann et al. 2014). At the same time tandem repeats seem to have played an important role in the evolution of the U. gibba genome and of numerous genes involved in carnivory there (Lan et al. 2017). There is extensive variation in the GC content of the genome (34.0-45.1%), the lower values being found in some taxa with smaller genomes - yet coding DNA tends to have a high GC content (Veleba et al. 2014).
Silva et al. (2016) discuss the evolution of the chloroplast genome in Utriculariaceae. Mutation rates in the matK gene in Genlisea in particular, and also Utricularia, are about the highest in all angiosperms (K. Müller et al. 2004), and that of other genes is also high (Jobson et al. 2003). Interestingly, genes in the plastid ndh gene complex (NAD(P)H-dehydrogenase) show complex patterns of presence and absence, being mostly absent from/truncated in the terrestrial members of the family examined (from all three genera), but present in the aquatic members (Silva et al. (2016); simple parsimony suggests that functionality is regained... Reduction in size of the small single copy portion of the genome shows a similar pattern.
Chemistry, Morphology, etc. In Pinguicula a single antipodal cell may persist, enlarge, and divide (Kopczynska 1964). The integument may be multiplicative in Genlisea (see Merl 1915); testa morphology in Utricularia is very variable.
For early corolla tube formation in Utricularia, see Degtjareva and Sokoloff (2012); the stamens are initiated before the corolla. "Nutritive tissue" is described from the chalazal end of the ovule, the funicle, and the placenta, i.e., at both ends of the developing embryo, but it is not recorded from Pinguicula. In some taxa of Utricularia, at least, the embryo sac more or less escapes from the ovule and apparently takes nutrients from the placenta, and nuclei from the placenta have been found in the aggressive micropylar endosperm haustorium (Farooq 1966; Khan 1970 and references). I know of no recent work on this system, and it is not mentioned by Fischer et al. (2004b).
For additional general information, see Goebel (1891, ), McPherson (2008: Pinguicula, 2010), the papers in Ellison and Adamec (2018), esp. Jobson et al (2018: Utricularia), Fleischmann and Roccia (2018: Pinguicula) and Fleischmann (2018: Genislea) and the Carnivorous Plants Database, for some chemistry, see Damtoft et al. (1994), for growth and vegetative morphology, see Brugger and Rutishauser (1989), Rutishauser and Isler (2001) and Grob et al. (2007a: Pinguicula sympodial), for floral morphology see Gross et al. (2007a) and in particular Degtjareva and Sokoloff (2012), for pollen, see Rodondi et al. (2010: Pinguicula), and for seeds and embryos, see Stolt (1936), Kausik (1938), Farooq (1965), Farooq and Bilquis (1966 and references), Degtjareva et al. (2004a), and Takhtajan (2013: also seedling and young plant). For an account of Genlisea, see Fleischmann (2012), and for a magnificent classic revision of Utricularia, see Taylor (1989).
Phylogeny. For the phylogeny of Lentibulariaceae, see Jobson et al. (2003), K. Müller et al. (2004, 2006b) and K. Müller and Borsch (2005a); Pinguicula is on a long branch (Refulio-Rodriguez & Olmstead 2014). Cieslak et al. (2005) and Degtjareva et al. (2006) discuss the phylogeny and evolution of Pinguicula. Reut and Jobson (2010) and Jobson et al. (2017) focussed on the phylogeny of Utricularia subgenus Polypompholyx in particular; this is sister to the rest of the genus (Silva et al. 2017). For more about relationships in the genus, see Silva et al. (2017) and Rodrigues et al. (2017). Note that Westermeier et al. (2017) found that the relationships between the subgenera in particular that depended on the particular analysis being carried out. Fleischmann et al. (2010) looked at relationship in Genislea.
Classification. Taylor's (1989) groupings are holding up quite well, although very distinctive species like U. resupinata, U. pubescens and U. nana, all placed in monotypic sections by Taylor, are likely to be derived from within other sections. For the sectional classification of subgenus Polypompholyx, see Jobson et al. (2017).
Synonymy: Pinguiculaceae Dumortier, Utriculariaceae Hoffmannsegg & Link
[Thomandersiaceae + Verbenaceae]: inflorescence racemose; staminode +; 3³ ovules/carpel; endosperm 0.
Age. This node is ca 39.8 m.y.o. (Magallón et al. 2015).
THOMANDERSIACEAE Sreemadhavan Back to Lamiales
Shrub or small tree; 2-indolinone alkaloids +; phloem stratified; pericyclic fibres massively thickened, ?short; nodes 1:3; petiole bundles forming a ring or incurved C-shaped; stomata anisocytic; leaves ± heterophyllous, lamina with flat glands abaxially, (margins deeply lobed), petiole swollen at apex and base; K with nectaries on the outside; pollen 5-6-colpate; nectary vascularized by carpellary traces; gynoecial vasculature 8-shaped; ovules 1-3/carpel, hemianatropous; capsule loculicidal, K accrescent; seed with cup-shaped expansion of funicle, hilum rather large; testa with ascending-imbricate scales or warts, exotesta palisade, not lignified, (to 6 layers of cells in the warts); embryo strongly curved, cotyledons complexly folded, thin-foliaceous; n = ?
1 [list]/6. W. and C. Africa (map: from Wortley et al. 2007a).
Chemistry, Morphology, etc. The flat glands mentioned above are dark-drying and up to 3 mm across, and are quite different from the lamialean glandular hairs with their radially-segmented heads which also often occur on the abaxial surface of the lamina here.
Despite the presence of structures sometimes described as jaculators, fruit dehiscence is not explosive, unlike Acanthaceae. The seed, with its prominent hilum, sits in a thin, cup-like expansion of the funicle. Inside the seed coat described above is a layer of much crushed cells, in turn above a layer of a few less crushed cells; the outer layer of the endosperm has a distinct outer periclinal cell wall. I am not sure exactly how the cotyledons are folded.
Study of the development of the ovule, embryo, and endosperm and of seed anatomy might well be profitable.
For alkaloids, see Ngadjul et al. (1995), and for general details, see Wortley et al. (2005a and especially 2007a). Thomandersia hensii: de Wilde & Jongkind 9400, seed, stem; Ngok Bamak et al. 1263, leaf; T. laurifolia: Dibata 30, seed; Thomandersia sp.: Reitsma et al. 1819, leaf, stem.
Previous Relationships. Thomandersia was previously usually included in Acanthaceae; aside from its rather different fruits, it does not have swollen nodes, cystoliths, etc.
VERBENACEAE Jaume Saint-Hilaire, nom. cons. Back to Lamiales
Vines, shrubs, or trees (perennial to annual herbs), often aromatic; 4-carboxy-iridoids +; (pits vestured); petiole bundles arcuate (also medullary, associated with median bundle); needle crystals common; stomata diacytic, (anomocytic); stems often square; eglandular hairs unicellular; (flowers sessile); flower often rather weakly monosymmetric; space between K and C [water calyx]; (A of two lengths, but free), ± sessile [so usu. included], (filaments +), (staminode 0); tapetal cells 2-4-nucleate; pollen (colpate, por[or]ate), exine thickened near apertures; G also 1 (4), collateral, placenta on the margin of the carpel, style short [to 1/2 length of corolla tube], (long), stigma capitate (bilobed, oblique), with conspicuous stigmatoid tissue, wet; ovules 2/carpel, apotropous, integument 5-9 cells across, obturator +; (antipodal cells multinuclear); K persistent, enclosing fruit; seeds not dispersed separately; testa thin-walled; cotyledons spatulate; n = 5-12+.
31 [list]/918: ten groups below. Pantropical (to warm temperate), but mostly New World, esp. S. South America. In Europe, Verbena officinalis may be native only from S. Europe and eastwards (map: from van Steenis & van Balgooy 1966; Hultén 1971; Lebrun 1977; Meusel et al. 1978; Brummitt 2007; Australia's Virtual herbarium 12.2012).
Age. Crown-group Verbenaceae are some (55-)42.6(-23.4) m.y.o. (Tank & Olmstead pers. comm.).
1. Petreeae Briquet
Shrubs and vines; lamina entire; flowers ± polysymmetric; K much enlarged, petal-like (not Petrea brevicalyx); G 1; fruit indehiscent, fleshy; n = 17.
1/12. Mexico to the Amazon Basin.
Synonymy: Petreaceae J. Agardh
[Duranteae [[Casselieae + Citharexyleae] [Priveae [Rhaphithamnus [Neospartoneae [Verbeneae + Lantaneae]]]]]]: fruit loculicidal, two-partite.
Age. The age for this node may be at least 42 m.y. (Nie et al. 2006).
2. Duranteae Bentham
Trees to herbs; eglandular hairs multicellular; (flowers sessile), (± polysymmetric); (A 2 + 2 staminodes); G 1(); n = 17.
6/192: Stachytarpheta (130). S. U.S.A. to Argentina, (Africa to India).
Synonymy: Durantaceae J. Agardh
[[Casselieae + Citharexyleae] [Priveae [Rhaphithamnus [Neospartoneae [Verbeneae + Lantaneae]]]]]: ?
[Casselieae + Citharexyleae]: ?
3. Casselieae Troncoso
Inflorescences axillary; (staminode 0); (G 1 [adaxial carpel]).
3/14. Mexico and the Caribbean to Argentina.
4. Citharexyleae Briquet
n = 38.
3/135: Citharexylum (130). S. U.S.A. to Argentina. [Photo - Flower.]
[Priveae, Rhaphithamnus [Neospartoneae [Dipyrena [Verbeneae + Lantaneae]]]]: flowers ± sessile; stigma bilobed (oblique, capitate).
5. Priveae Briquet
?1/21. Pantropical-warm Temperate.
6. Rhaphithamnus Miers
Inflorescences axillary; fruit indehiscent, fleshy.
1/2. Chile, Argentina.
[Neospartoneae [Dipyrena [Verbeneae + Lantaneae]]]: flowers sessile.
7. Neospartoneae Olmstead & O'Leary
(Ephedroid shrubs); plant glabrous; inflorescences axillary (terminal) inflorescences 0); (staminode +); G 1.
3/6. Argentina, Chile, S. to Patagonia.
[Dipyrena [Verbeneae + Lantaneae]]: staminode 0.
8. Dipyrena Hooker
Fruit of two bilocular pyrenes.
1/1: Dipyrena juncea (Gillies & Hooker) Ravenna. Temperate Chile, Argentina.
[Verbeneae + Lantaneae]: staminode 0.
Age. An estimate of the age of this node is (40-)30, 29(-18) m.y. (Bell et al. 2010); another is (31-)28, 20(-17) m.y. (Wikström et al. 2001).
9. Verbeneae Dumortier
(Iridoids from deoxyloganic acid); lamina margin often serrate; (inflorescence unbranched); (A 5 - Verbena, 2, staminodes 0); fruits also septicidal [four pyrenes]; n = 5, 7, 10.
3/260: Verbena (200), Junellia (48). Mostly American, Eurasia to Africa.
10. Lantaneae Endlicher
Ethereal oils +; stomata anisocytic; (inflorescence often ± capitate), rarely terminal; G 1 [Coelocarpum, with [G 2], probably sister to rest], "style short", stigma entire; (ovule 1/carpel - Lantana); (endosperm + - Lantana); n = 11.
9/275: Lippia (120), Lantana (100). Mostly New World
Synonymy: Lantanaceae Martynov
Evolution: Divergence & Distribution. The family appears to be of tropical South American origin (Olmstead 2013). A number of species grow in arid conditions in North America, and some have arrived from South America, but in various ways, while others (Citharexylum) seem to have come from mesic habitats in Central America (Frost et al. 2017).
O'Leary et al. (2012; Thode et al. 2013: characters useful below tribal level) reconstructed the evolution of characters and fruit. Both the tritomy [Lantaneae + Dipyrena + Verbeneae] and the uncertainty where Rhaphithamnus and Coelocarpum will end up on the tree affect our understanding of character evolution.
Ecology & Physiology. Junellia and other Verbeneae andAloysia (Lantaneae) often are dominants in communities in arid habitats in South America (Frost et al. 2017).
Pollination Biology & Seed Dispersal. Lu-Irving and Olmstead (2013) estimated that fleshy fruits had been derived from dry fruits at least five times in Lantaneae alone.
Plant-Animal Interactions. Gall-forming fruit flies of the Tephretidae-Tephrellini are found here (and on Acanthaceae and Lamiaceae: Korneyev 2005).
Chemistry, Morphology, etc. Petraea (and Nashia) have polysymmetric flowers (Jabbour et al. 2008). An endothelium is only poorly developed (Johri et al. 1992). For the position of the carpels, see Sattler (1973). The ovules are described as being attached to the margins of the carpel (Junell 1934); two-chambered mericarps or stones may contain an ovule/seed from both carpels (Sanders 2001); indehiscent fruits are fleshy (O'Leary et al. 2012). Pericarp anatomy is more complex (Ryding 1995). The testa of at least some Verbenaceae has the hypodermal layer(s) thickened (Rohwer 1994a).
For general information, see Sanders (2001), Atkins (2004) and Brummitt (2007), for iridoids, see von Poser et al. (1997 - also Soltis et al. 2005b), for hairs and stomata, see Cantino (1990), for the megagametophyte, see Rudall and Clark (1992), and for exine thickening, see Chadwell et al. (1992).
Phylogeny. Marx and Olmstead (2007) found that Petraea and Duranta, both woody, were successively sister to the rest of the family. Marx et al. (2010) present a comprehensive phylogeny of the family, although, as they noted, sampling within the big genera needed to be improved. A couple of genera remained unplaced: Dipyrena may be close to Verbeneae while Rhaphithamnus may be close to Priveae, although branches within the latter are rather long; the position within Lantaneae of Coelocarpum, morphologically plesiomorphic, was also uncertain (Marx et al. 2010). The topology above was also recovered by Yuan et al. (2010b), but the position of Rhaphithamnus was unclear, Dipyrena, however, was consistently sister to the [Verbeneae + Lantaneae] clade, while in Thode et al. (2013) it was sister to Verbeneae.
For relationships around Verbena, see Yuan and Olmstead (2008), however, chloroplast and nuclear markers give substantially different topologies (Frost et al. 2017). Within the Lantana-Lippia complex, Aloysia formed a basal grade and members of the animal-dispersed Lantana with their pyrene-type fruits were polyphyletic (Lu-Irving et al. 2009, esp. 2014; Lu-Irving & Olmstead 2013).
Classification. For the circumscription of the family, see especially Cantino (1992a, b), and for a tribal classification, see Marx et al. (2010).
The whole Lantana-Lippia complex, speciose although it may be, could perhaps be reduced to a single genus, the larger genera currently recognised being para- or polyphyletic (Lu-Irving et al. 2009, see also 2014). Marx et al. (2010) suggested that nine genera could be recognised in the complex, but whatever taxonomic solution is adopted major generic adjustments in this area will be needed. Earlier taxonomists had used fruit characteristics to delimit genera, and fruit evolution has turned out to be highly homoplasious (Lu-Irving & Olmstead 2013). I provisionally include Glandularia, with about 100 species, within Verbena; Junellia is also part of this complex. The limits of genera around Junellia have been redrawn (O'Leary et al. 2009); for a revision of Junellia in the old sense, see Peralta et al. (2008).
Previous Relationships. Verbenaceae have often been considered very close to Lamiaceae, q.v. for differences. For Avicennia, also once included in Verbenaceae, see Acanthaceae; Phryma (Phrymaceae) is also separate.
[Lamiaceae [Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]]]: ?
Age. The crown-group age of this clade is about 40.3 m.y.o. (Magallón et al. 2015) or (62.4-)55.7, 52.1(-45) m.y.o. (Cusimano & Wicke 2016).
LAMIACEAE Martynov, nom. cons. // LABIATAE Jussieu, nom. cons. et nom alt. Back to Lamiales
Herbs (trees, vines); diterpenoids, betaines, C4-decarboxylated iridoids +, (β-hydroxy-(3,4-dihyroxyphenyl)-ethanoid glycoside +); cork also deep-seated; (pits vestured); (nodes 1:2); petiole bundles arcuate (annular); stomata diacytic (anomocytic); stem often square; (eglandular hairs unicellular; stellate); lamina vernation variable, margins toothed; inflorescence branches cymose; staminode 0 (+); tapetal cells multinucleate; pollen tricolpate, exine not thickened near apertures; style (unequally) bifid, stigma inconspicuous, not expanded, dry (wet); ovules 2/carpel, borne on inner side of carpel margin, apotropous, subbasal, ascending, integument 5-9 cells across; fruit indehiscent, all 4 seeds separating, K persistent; testa usu. thin, exotestal cells elongated or not, thickened on radial and often inner walls, (hypodermal cells sclerenchymatous); nuclear genome [1C] (269-1189(-6098) Mb [?level].
236 [list: subfamilies]/7,203 - 12 groups below. World-wide (map: from Vester 1940; Hultén 1971; Van Balgooy 1975; Lebrun 1979; Frankenberg & Klaus 1980). [Photos - Collection, Fleshy fruit.]
Age. That of a [Viticoideae [Ajugioideae [Prostantheroideae [Nepetoideae [Scutellarioideae + Lamioideae]]]]] clade may be (54.6-)43.1(-28.3) m.y. (Tank & Olmstead pers. comm.: note topology), and for an [Ajugioideae [Prostantheroideae [Nepetoideae [Scutellarioideae + Lamioideae]]] clade is (30-)28, 17(-15) m.y. (Wikström et al. 2001) or ca 23.8 m.y. (Salmaki et al. 2016: c.f. topology).
1. Prostantheroideae Luersson
(Plant aromatic); hairs branched; (leaves small - microphyllous); flowers polysymmetric (monosymmetric), (4-)5(-8) merous; (staminodes 2), (anthers with appendages); (nectary ± 0); ovary ±un-, 2- or 4-lobed; fruit a schizocarp, mericarps 4, (indehiscent); endosperm +; n = ?
17/317: Prostanthera (100), Hemigenia (50), Pityrodia (45). Australia.
Synonymy: Chloanthaceae Hutchinson
2. Callicarpoideae Bo Li & Olmstead
Shrubs to trees (lianes); hairs branched/stellate (simple); inflorescences axillary; flowers polysymmetric, 4(-5) merous; (A 5-7), (anthers porose); stigma peltate or capitate; fruit a drupe; endosperm 0; n = 8, 9.
1/170. Tropical to subtropical.
[[Viticoideae + Symphorematoideae], Nepetoideae, Tectonoideae, Premnoideae, Ajugoideae [Peronematoideae [Scutellarioideae [Cymaroideae + Lamioideae]]]]: ovary with false septum.
Age. There are fossils from the Deccan Traps that show similarities with Vitex (Viticoideae) and Gmelina (Premnoideae) (Wheeler et al. 2017).
[Viticoideae + Symphorematoideae]: ?
3. Viticoideae Briquet
Often woody; chlorogenic acid +, verbascoside 0, (protocatechuic acid, a-tocopherolhydroquione +); (hairs branched); leaves palmately compound (unifoliate); flowers ± poly- or bisymmetric; nectary 0 or poorly developed; fruit a drupe, (1-seeded); ?endosperm; n = 6, 8, ... 16, 17.
3/283: Vitex (250). Tropical (subtropical).
Synonymy: Viticaceae Jussieu
4. Symphorematoideae Briquet
Lianes; ?chemistry; hairs branched; inflorescences capitate, of 3-7-flowered cymes, involucrate; flowers polysymmetric, 5-16-merous, (monosymmetric, 5-merous - Congea), ± sessile; nectary 0; G imperfectly 2-locular; ovules apical, pendulous, straight, funicle 0; embryo sac ± on surface of ovule; fruit dry or subdrupaceous, seeds 1(-2); endosperm ?0; n = 12, 14, 17, 18.
3/27. India, Sri Lanka, South East Asia, West Malesia.
Synonymy: Symphoremataceae Wight
5. Nepetoideae (Dumortier) Luersson
Plant commonly aromatic [volatile terpenoids], rosmarinic acid [caffeic acid ester], nepetoidin A and B [caffeic acid esters], verbascoside 0; (distinctive seed fatty acids) +, betaine concentration low, iridoid glycosides; stem endodermis +; K with epidermal prismatic calcium oxalate crystals; (A 2 [abaxial pair], unithecate - Salvia); pollen tricellular, hexacolpate; style gynobasic; exocarp with mucilaginous cells producing hygroscopic spiral fibrils [i.e. myxospermy]; endosperm development highly asymmetric, the two haustoria lying close to each other, 1-layered [0?], cotyledons investing embryo; n = 6+; frequently attacked by Puccinia menthae.
105/3,675. World-wide, but esp. (warm) temperate.
Age. Diversification in the Nepetoideae is estimated to have begun (63.7-)57.6, 52.3(-42.3) m.y.a. (Drew & Systma 2012a) or ca 63.4 m.y.a. (P. Li et al. 2017).
5a. Mentheae Dumortier
: Salvia (900+), Thymus (220), Nepeta (200+), Clinopodium (100), Micromeria (55), Hedeoma (40), Lepechinia (40), Origanum (40), Satureja (38).
Age. The clade [Prunella + Salvia] is ca 41.4 m.y.o. (P. Li et al. 2017).
Synonymy: Glechomaceae Martynov, Melissaceae Berchtold & J. Presl, Menthaceae Burnett, Monardaceae Döll, Nepetaceae Berchtold & J. Presl, Salviaceae Berchtold & J. Presl, Saturejaceae Döll
[Elsholtzieae + Ocimeae]: ?
Age. This node is ca 61.8 m.y.o. (P. Li et al. 2017).
5b. Elsholtzieae Burnett
(Plant woody); n = (7)8(9)10...
Age. Crown-group Elsholtzieae are ca 50.1 m.y.o. (P. Li et al. 2017).
7/71: Elsholtzia (43). Central Asia to India, W. Malesia and Japan, E. North America (Collinsonia).
5c. Ocimeae Dumortier
A declinate, anthers synthecous, dorsifixed.
: Plectranthus (inc. Coleus: 300), Hyptis (280), Isodon (100), Ocimum (65), Platostoma (45), Aeollanthus (40), Pycnostachys (40), Lavandula (39).
Age. Crown-group [Lavandula + Hyptis] is ca 48.2 m.y.o. (P. Li et al. 2017).
6. Tectonoideae Bo Li & Olmstead
Large trees, deciduous; ?chemistry; hairs branched; inflorescences terminal and/or axillary; flowers polysymmetric, 5-7-merous; C infundibular, tube short; style terminal; fruit a drupe, ± surrounded by inflated calyx; stone 4-celled, with central cavity; endosperm 0; n = 12, 18.
1/4. India, Southeast Asia.
7. Premnoideae Bo Li, Olmstead & Cantino
Shrubs to trees (lianes), (herbs), aromatic; (leaves palmately compound); (flowers polysymmetric); (A 2); (nectary 0; fruit a drupe, stone 4-celled; ?endosperm; n = 19.
3/ca 168: Premna (50-200) Tropical, West Pacific.
8. Ajugoideae Kosteletzky
Annual herbs to shrubs, (aromatic); flowers (4 [Aegiphila] merous), also polysymmetric or 1-lipped [lobes 0:5 - Teucrium]; pollen exine with branched (simple, granular, etc.) columellae; nectary slight-0 (+); (antipodal cells numerous); nutlets reticulate, (fruit a drupe, K coloured, accrescent); endosperm several-layered/0, cotyledons investing embryo [?common]; n = 7, 10, ?12, 13-16+.
26/750, 1,115?: Teucrium (250), Clerodendrum (150), Aegiphila (120), Rotheca (50-60), Ajuga (40-50). Cosmopolitan, esp. South East Asia to Australia.
Age. The clade [Teu. Clero. Ajug.] is very approximately 16.3. m.y.o. (Salmaki et al. 2016).
Synonymy: Aegiphilaceae Rafinesque, Ajugaceae Döll, Siphonanthaceae Rafinesque
[Peronematoideae [Scutellarioideae [Cymaroideae + Lamioideae]]]: ?
9. Peronematoideae Bo Li, Olmstead & Cantino
Shrubs to large trees (lianes); (verbascoside 0); (A 2); nectary 0 or slight; fruit dry, indehiscent or with 2 or 4 nutlets, abcsission scar as long as mericarp; endosperm 0; n =
4/17. India to Malesia and Melanesia.
[Scutellarioideae [Cymaroideae + Lamioideae]]]: stem endodermis +; calyx ribbed, fibrous [large amounts of fibrous tissue associated with the veins]; pollen suprareticulate; ovary 4-lobed; fruit a schizocarp.
10. Scutellarioideae (Dumortier) Caruel
Annual herbs to shrubs, (aromatic); (leaves spiral); (inflorescence racemose); K strongly two-lipped, (rotate, coloured - Holmskioldia), lobes rounded; (C 0:5); style gynobasic (± terminal - Wenchengia); seeds tuberculate; endosperm various; n = 12+.
5/380: Scutellaria (360). ± Cosmopolitan.
Synonymy: Salazariaceae F. A. Barkley, Scutellariaceae Döll
[Cymaroideae + Lamioideae]: endosperm +.
11. Cymaroideae Bo Li, Olmstead & Cantino
Shrubs to subshrubs; ?chemistry; cymes long-pedunculate, branches monochasial; anther thecae divaricate, becoming confluent; nectary 0; abscission scar ca 1/2 length of mericarp; n = ?
2/3-4. Hainan to Malesia.
12. Lamioideae Harley
(Plant aromatic); laballenic fatty acid and related compounds [l. acid = CH3(CH2)10CH=C=CH(CH2)3COOH], 3,4-dihydroxyphenylethanoid glycosides and related compounds; (calyx mesophyll with narrow prismatic calcium oxalate crystals); (stamens about the same length - Pogostemon and relatives), (anther thecae divaricate, becoming confluent); style gynobasic; (ovule with glandular hairs - Leonurus); embryo sac with micropylar lobe longer and broader than chalazal lobe; nutlets hardly reticulate; embryo spatulate; n = 6+.
62/1260: Stachys (300), Phlomoides (150-170), Sideritis (140), Leucas (100), Phlomis (50-90), Pogostemon (80), Eremostachys (5-60), Lamium (40). Esp. Europe and Africa to Asia, some cosmopolitan, but v. few Antipodean.
Age. Diversification in the crown-group Lamioideae is estimated to have begun (26.1-)23.9(-19.9) m.y.a. (Roy & Lindqvist 2015: both analyses, see below)).
Synonymy: Mellitidaceae Martynov, Stachydaceae Döll
Evolution: Divergence & Distribution. The oldest fossils identified as Lamiaceae are ca 28.4 m.y.o. (Martínez-Millán 2010).
Diversification within Mentheae (Nepetoideae; ca 2,300 species, about a third of the family) is estimated to have begun ca 46 m.y.a., perhaps in the Europe/Mediterranean area (Drew & Systma 2012a). Menthineae are probably West Asian/Mediterranean in origin but are diverse in the New World, moving there perhaps via the North Atlantic land bridge ca 10 m.y.a. and with subsequent dispersal events onwards to South America (Drew et al. 2017b). Mentheae also include Salvia, the limits of which are becoming clear (see Drew et al. 2017a), and the genus is very speciose in the New World. There have been several independent movements to Africa and the Old World, and the genus probably began diversifying somewhat over 30 m.y.a. in the earlier part of the Oligocene (Will & Claßssen-Bockhoff 2014, 2017). There was some diversitication within Elscholtzieae ca 43-41 m.y.a. (5 clades then), but there was only one more clade 10 m.y. later, indeed, the clades resulting from this early burst had stems 8-49 m.y. in age - the latter is the stem of the [Ombrocharis + Perillula] clade (P. Li et al. 2017).
For divergence times and biogeographic scenarios in Lamioideae, see Roy and Lindqvist (2015). The ca 60 species of Lamiaceae endemic to Hawaii represent a major radiation there. They are currently placed in three separate genera, Stenogyne, Haplostachys and Phyllostegia, and they are all polyploids with fleshy fruits and are derived from within Stachys (Lamioideae), in particular, they may be the descendants of a hybrid between temperate North American and Meso/South America taxa. They probably represent but a single introduction to the islands that happened (7.4-)5(-3.6) m.y.a. (Lindqvist & Albert 2002; Lindqvist et al. 2003; Roy et al. 2013, esp. 2015 and references; Lim & Marshall 2017; see also the silversword alliance - Asteraceae). Sideritis subgenus Marrubiastrum has diversified extensively in Macaronesia within the last ca 4.2-3.3 m.y. (S.-C. Kim et al. 2008). Indeed, Lamiaceae shows a relatively high proportion of single-island endemics on the oceanic islands on which they are found (Lenzner et al. 2017).
Fragoso-Martínez et al. (2017) found ca 12 moves of Salvia> subgenus Calosphace from Mexico-Central America, its home, into South America, and perhaps one move from the Andes to the Antilles. Fruits in the genus do not have particularly distinctive dispersal mechanisms (Zona 2017).
Zhong et al. (2017) showed that radial symmetry in the corolla of Callicarpa and in two cases in Menthoideae was caused by different expression patterns of the genes. For a useful discussion of apomorphies within Lamiaceae, see B. Li et al. (2016). However, the position of several apomorphies on the tree remains unclear because of problems with character state delimitation, phylogeny, and/or variation within the terminals.
Ecology & Physiology. A number of Lamiaceae are gypsophiles, growing on soils high in gypsum, hydrous calcium sulphate (Escudero et al. 2014; Palacio et al. 2014). Prostantheroideae are an Australian radiation of often shrubby and small-leaved plants growing in dry conditions.
Pollination Biology & Seed Dispersal. Species in the very big, primarily New World-Mediterranean genus Salvia often have only two unithecate anthers. The connective is expanded and forms a lever arm which, when hit, makes the other end, with the single theca, pivot and comes down on the head, back or side of the pollinator (for androecial development, see Claßen-Bockhoff et al. 2004a). The genus as a whole has an expanded connective, and the fully-developed lever-arm pollination mechanism may have evolved three times in the genus via a bithecate condition with the thecae at opposite ends of an extended connective - which is interesting, since no other angiosperm has such a lever-arm pollination mechanism (Walker & Sytsma 2007; Drew et al. 2017a). As in other members of the family, pollination is predominantly by large insects and birds (Claßen-Bockhoff et al. 2003: summary of early literature, 2004b). The common ancestor of all unithecate clades had two more "ordinary" stamens (see also Walker et al. 2015; Drew et al. 2017a). Taxa like the 4-stamened Melissa and Lepechinia are at the base of the part of the tree that includes Salvia, and there are other taxa with two stamens immediately below the clades containing Salvia (Walker & Sytsma 2007); a number of other Mentheae, mostly New World, also have two stamens (Drew & Sytsma 2012a). Reith et al. (2007) described details of pollination in Salvia pratensis, and Wester and Claßen-Bockhoff (2006, 2007, 2011) focus on pollination by birds. There are over 300 bird-pollinated species of Salvia, and these are largely restricted to the New World; flowers with an ornithophilous syndrome encompass a remarkable amount of variation (Wester & Claßen-Bockhoff 2011). Fragoso-Martínez et al. (2017) focussed on subgenus Calosphace in which melittophily is plesiomorphic, but there are ca 20 subsequent shifts to ornithophily and one back to melittophily.
Wilson et al. (2017) looked at pollination in Prostanthera (Prostantheroideae), which have a variety of pollinators. The anthers may have appendages functionally rather similar to the lever arms of Salvia. In low Mediterranean shrublands, megachilid bees are important pollinators of Lamiaceae (Petanidou & Ellis 1996).
Drew and Sytsma (2012b) discussed the evolution of dioecy within the New World genus Lepechinia; it seems to have evolved at least three times there.
The calyx is an integral part of the dispersal mechanism of the propagules, whether being brightly coloured and helping to attract frugivores, as in Clerodendrum, having hooked hairs or being itself hooked (Priva and some species of Salvia respectively), or forming a kind of catapult mechanism (Scutellaria) or a wing. Various kinds of calcium oxalate crystals are found in the sepals, perhaps protecting the nutlets against insect predators (Ryding 2010b). Myxocarpy, the nutlets producing mucilage and so adhering to their disperser or anchoring the nutlet in the ground, is common in Nepetoideae (Pammel 1892; Ryding 1992, 2001; Western 2011; see also Yang et al. 2012); moreover, sand sticking to the nutlets may prevent their being eaten, granivores being fastidious about dirty food (Western 2011 and references). Genera like Lamium (Lamioideae) and Teucrium (Ajugoideae) have myrmecochorous nutlets (Lengyel et al. 2010) while myxospermy is common in Nepetoideae, including some species of Salvia (Zona 2017 for dispersal mechanisms here - quite a variety).
Plant-Animal Interactions. The leaf beetle Phyllobrotica (Chrysomelidae) eats plants from Scutellarioideae, Lamioideae and Viticoideae, but not members of Nepetoideae - or Verbenaceae (Farrell & Mitter 1990). Larvae eat the roots, adults the above-ground parts, which they can decimate. Gall-forming midges of the Tephretidae-Tephrellini are found on Lamiaceae (and on Acanthaceae and Verbenaceae: Korneyev 2005), as are gall-forming wasps of the Cynipidae-Cynipinae (Redfern 2011) and agromyzid dipteran leaf miners (Winkler et al. 2009).
A number of Lamiaceae are quite densely and viscidly hairy (Glas et al. 2012), and mirid bugs - often sap-suckers, but some carnivores - of subtribe Dicyphini in particular are able to walk easily in such conditions (Wheeler & Krimmel 2015; LoPresti et al. 2015); nitrogen from the excreta of the bugs may be taken up by the leaf (Spomer 1999).
Bacterial/Fungal Associations. Thymol, the essential oil 2-isopropyl-5-methylphenol and known from some Nepetoideae, at least, not only is bactericidal but it also seems to encourage nodulation of legume seedlings, which has implications for communty development (McKenna et al. 2013).
Genes & Genomes.
See Gill et al. (1983) for chromosome numbers of woody Lamiaceae.
Economic Importance. Chia, Salvia hispanica, has nutritious seeds very high in alpha-linolenic acid; it was a major crop in the Aztec empire (Ayerza & Coates 2005).
Chemistry, Morphology, etc. Trisaccharide esters of verbascoside are found in Lamiaceae alone, and disaccharides are also found there, as well as in Verbenaceae, Oleaceae and Orobanchaceae in particular (Mølgaard & Ravn 1988). For the distinctive allenic fatty acids, see Aitzetmüller et al. (1997). Some Labiatae have tanning compounds, Labiatengerbstoffe, and rosmarinic acid, a polyphenol ester of caffeic acid and 3,4-dihydroxyphenyllactic acid, seems to be restricted to Nepetoideae, and although it is scattered in land plants, it is common elsewhere only in Boraginales (Petersen et al. 2009).
Bailey (1956) and Balfour and Philipson (1962: variant of an Ascarina-type node) noted the vegetative nodes of Lamiaceae and "Verbenaceae" might be one gap, two trace. The distribution of such nodes needs to be clarified; Marsden and Bailey (1955) described 1:2 nodes in Clerodendron trichotomum in considerable detail. Species of Lamioideae and Scutellarioideae, but not Nepetoideae, tend to have relatively massive amounts of fibrous tissue associated with the veins in the calyx (Ryding 2007, 2010b).
Naghiloo et al. (2014b) discuss floral development in four genera of Nepetoideae. They noted substantial variation in patterns of initiation of corolla and androecium in particular, degree of gynobasy of the style, corolla aestivation, etc., and although all showed late corolla tube development, how early in development monosymmetry became evident varied considerably (Salvia - very early; Nepeta - late). There is further discussion of other asterids with polymerous flowers like those of Symphorematoideae elsewhere (see euasterids).
The pollen grains of at least some Lamiaceae become very much flattened as they dry out (Halbritter & Hesse 2004). The ovules are described as being attached (just) to the false septae (Junell 1934); there is variation in ovule attachment within the family. Many Lamiaceae have a single layer of sclerenchymatous, bone-shaped cells on the inside of the mesocarp, others have thicker pericarp walls, and the cells are often crystalliferous (Ryding 1995). The exotestal cells of the seed are thickened, particularly on their inner periclinal and anticlinal walls (Rohwer 1994a). Some Lamiaceae have asymmetric development of the endosperm such that the two haustoria come to lie very close to each other (Ram & Wadhi 1964 for references). This distinctive development may be restricted to Nepetoideae (further studies are needed), but it is also to be found in many Acanthaceae. Wunderlich (1967b) suggests that there is no endosperm in mature seeds of Nepetoideae.
For a comprehensive treatment of Lamiaceae, see Harley et al. (2004), for phenolics, see Pedersen (2000: more to add, not unidentified compounds), fatty acids in the seed, see Badami and Patil (1981), for betaine distribution, see Blunden et al. (1996: widespread, but Verbenaceae and other Lamiales?), for rosmarinic acid, see Petersen and Simmonds (2003) and Petersen et al. (2009), for secondary metabolite evolution, see Grayer et al (2003) and Wink (2003), for hairs and stomata, see Cantino (1990), for leaf anatomy in Mentheae, see Moon et al. (2009a), for some floral development, see Endress (1999) and Naghiloo et al. (2014a), for ovules, which have a vascular supply, see Guignard (1893), for gynoecial morphology and embryology, see Junell (1934), for seedlings, see Vassilczenko (1947: cotyledons in Lamiaceae s. str. usu. cordate to hastate), for pollen, ovules and seeds, see Wunderlich (1967b), for the megagametophyte, see Rudall and Clark (1992), for nutlet micromorphology, see Moon et al. (2009b: Mentheae) and especially Ryding (2010a and references), for nutlets in Stachys, see Salmaki et al. (2009), and for proteinaceous inclusions in the nucleus, see Speta (1979). Moon et al. (2008a, b) surveyed pollen morphology especially of Salviinae and other Mentheae.
Phylogeny. Bootstrap support for the family is 100% (Wagstaff et al. 1998). However, major relationships within the family remain unclear. Bendiksby et al. (2011) recovered the relationships [Callicarpa [Prostantheroideae [[Symphorematoideae + Viticoideae] [[Premnoideae, Gmelina, Tectona] [Nepetoideae [Garrettia (= Peronematoideae below) [Scutellarioideae + Lamioideae]]]]]]], mostly with strong support, although sampling was mediocre and analyses of individual markers gave different topologies. These relationships differ little from those in the treatment above (see B. Li et al. 2016; c.f. Bramley et al. 2009). Relationships along the spine of the family are largely unresolved in the two-gene analysis of Y.-P. Chen et al. (2016), indeed, a [Nepetoideae [Scutellarioideae + Lamioideae]] clade was not recovered, while in the study of Chinese taxa by Z.-D. Chen et al. (2016) there was some support for the relationships [Nepetoideae [Callicarpa [Viticoideae [Tectona [Premna + The Rest]]]]]. In the five-gene (chloroplast) anaysis of B. Li et al. although individual genes might provide little support, overall resolution was considerably improved. I have perhaps been overly cautious, and relationships may end up being [[Prostantheroideae + Callicarpa] [[Viticoideae + Symphorematoideae], Nepetoideae [Tectona [Premnoideae, Ajugoideae [Peronematoideae [Scutellarioideae [Cymaroideae + Lamioideae]]]]]]] (B. Li et al. 2016: Fig. 1).
B. Li et al. (2016 and references) discuss previous ideas of relationships within the subfamilies in some detail. For the phylogeny of the Australian-centered Chloantheae (Prostantheroideae), see Conn et al. (2009) and for that of Prostanthera itself, with the classical (Bentham!) morphologically-circumscribed infrageneric taxa not standing up too well, see Wilson et al. (2012).
For relationships in Viticoideae, see Bramley et al. (2009); Vitex itself is paraphyletic. Nakashima et al. (2016) looked at relationships in Bornean Callicarpa with a focus on species thought to be myrmecophilous.
Within Nepetoideae, basal relationships were explored by Y.-P. Chen et al. (2016) in the course of their placement of Ombrocharis. Moon et al. (2010) and Drew and Systma (2012a) have begun to circumscribe major clades within the huge Mentheae. Mentheae-Salviinae include the large New World-centred Salvia, with over 900 species, and Rosmarinus and some other mostly quite small genera are also involved (Walker et al. 2004, but c.f. Walker & Sytsma 2007; Moon et al. 2010; Drew et al. 2017a) - alas for "Scarborough fair". Jenks et al. (2013) looked at relationships within the speciose (500+ species) New World Salvia subg. Calosphace and found that many sections were not monophyletic, relationships following geography rather than morphology (there is substantial geographical signal in the Salvia area - see also Will & Claßssen-Bockhoff 2017) - hence much parallel evolution. The study by Fragoso-Martínez et al. (2017) extended that by Jenks et al. (2013); they found that only 12/42 of Carl Epling's sections for which they had data were monophyletic, and of these monophyly of 7 was apparent only in nuclear ribosomal analyses. Major changes in our ideas of relationships in Menthineae (for which, see Drew et al. 2017b) and in the limits of the subtribe are needed; species of Clinopodium, for example, are scattered through much of the tree (Bräuchler et al. 2010; Drew & Sytsma 2011; Drew et al. 2017b). Nepetinae are monophyletic, although Nepeta itself is polyphyletic (Serpooshan et al. 2018). For relationships in Micromeria, from the Canary Islands, see Puppo et al. (2015). Drew and Sytsma (2011, 2012b) explored the limits and relationships of Lepechinia. Nepetoideae also include the large tribe Ocimeae (see Paton et al. 2004 for relationships) which in turn include the large genus Hyptis; the other genera of Hyptinae are embedded in a paraphyletic Hyptis (Pastore et al. 2011), however, with little resolution along the backbone of the tree, so clade limits are unclear. In Elsholtzieae [Perillula + Ombrocharis] (both monotypic; congeneric?) are sister to the rest of the tribe and Elscholtzia is polyphyletic (P. Li et al. 2017).
Steane et al. (1999, 2004) looked at the relationships around the para/polyphyletic Clerodendrum (Ajugoideae). The limits of Teucrium were slightly expanded by Salmaki et al. (2016), who also looked at the extensive variation in chromosome numbers there.
Wenchengia has spiral leaves and a more or less terminal style, and it was initially unclear where it should be placed (Cantino & Abu-Asab 1993). However, a position sister to all other Scutellarioideae is strongly supported (B. Li et al. 2012) or, rather poorly supported, after Hymenopyramis (Z.-D. Chen et al. 2016).
Wagstaff et al. (1995) discussed phylogenetic relationships in Lamioideae. Scheen et al. (2010) found that Cymaria might be sister to the rest of the subfamily and Bendiksby et al. (2011) added Acrymia to Cymaria, although support for the sister group position of the combined clade was low, while Chen et al. (2014) preferred to exclude the two from the subfamily on morphological grounds (see also B. Li et al. 2016), although they included the odd genus Holocheila (see also Z.-D. Chen et al. 2016: Chinese taxa). A poorly-supported [Acrymia + Cymaria] clade was sister to the rest of the subfamily and Holocheila was in a strongly-supported Pogostemoneae in the chloroplast analyses of Roy and Lindqvist (2015). These odd genera were not included in their analyses using the nuclear pentatricopeptide repeat, and although many tribes in the two analyses were recovered in both, there were differences in their immediate relationships, and some tribes, like Pogostemoneae themselves, were paraphyletic in the second analysis, even if both the clades in which they appeared there had substantial morphological support, too (Roy & Lindqvist 2015). For relationships of the ca 60 species of lamioid mints endemic to Hawaii, see Lindqvist and Albert (2002) and Lindqvist et al. (2003); recognition of the three genera in which they are placed makes Stachys paraphyletic (see also Roy & Lindqvist 2012; Roy et al. 2013), but this aside, the limits of Stachys are difficult to determine (see also Scheen et al. 2010; Bendiksby et al. 2011), and there may have been ancient hybridization in Stachydeae (Salmaki et al. (2013). Leucas is also highly paraphyletic (e.g. Scheen & Albert 2009), while relationships within Phlomidae have been evaluated by Mathiesen et al. (2011) and Salmaki et al. (2012). See Scheen et al. (2007) for relationships around Physostegia. Isodon, diverse on the Hengduan mountains, also has two species in Africa, and their relationships were clarified by Yu et al. (2014), while there is a similar pattern of relationships in Pogostemon (Yao et al. 2016).
Classification. The subfamilial classification here is based on that of B. Li et al. (2016) and Li and Omstead (2017); see Cantino and Sanders (1986) for the distinctions between the two biggest subfamilies, Lamioideae and Nepetoideae. Some details of the subfamilial phylogeny above are still suspect, but one can now begin to get an idea of character variation in the whole family. Note that the circumscription of Viticoideae is more narrowly drawn than in Cantino et al. (1992). For tribal, etc., limits, see also Harley et al. (2004), for those in Lamioideae, see Scheen et al. (2010) and Bendiksby et al. (2011).
In general, generic limits need attention (e.g. Kadereit 2016). In both Stachys and Leucas characters associated with pollination prove unreliable indicators of clades (Scheen et al. 2010); the former genus in particular may have to be considerably expanded or pulverised (Salmaki et al. 2013). Clerodendrum has been dismembered (Steane & Mabberley 1998; Yuan et al. 2010a); Harley and Pastore (2012) reworked generic limits in Hyptidinae, and Coleus is to be included in Plectranthus. How Salvia is to be treated presents a challenge - perhaps Rosmarinus, Thymus, Mentha, and Origanum are to be included (Walker et al. 2004, 2006; Walker & Sytsma 2007), however, some of these genera turned out to have been misplaced, and a monophyletic somewhat expanded Salvia can now be attained with minimum pain and subgenera recognized (Drew et al. 2017a, but c.f. Will & Claßssen-Bockhoff 2017, 7 or more genera...). Mentheae are large and sampling will have to be improved to evaluate generic limits, but clearly there are major problems (e.g. Bräuchler et al. 2010; Drew & Sytsma 2011; Drew et al. 2017b; Serpooshan et al. 2018). There are many other places where generic/clade rearrangements are to be expected, as in Chloantheae (Prostantheroideae: Conn et al. 2009). All the floral characters used to distinguish genera in Menthineae turn out to be homoplastic, and Clinopodium in particular is polyphyletic (Bräuchler et al. 2010).
Previous Relationships. Lamiaceae and Boraginaceae have always been considered distinct, but their similar gynobasic styles and fruits with four separate nutlets (and also some chemistry) have invited comparisons between the two, and they were often placed fairly close to each other in the system, as by Cronquist (1981) where both are in Lamiales. However, there are numerous differences (chemistry, leaf insertion, floral symmetry, ovule morphology, etc.) between the two, and the radicle in Boraginaceae points upwards in fruit while in Lamiaceae it points downwards.
As their alternative name Labiatae implies, Lamiaceae have always been considered as an "eminently natural" family, being immediately recognisable because of their herbaceous habit, paired, serrate leaves, square stems, monosymmetric flowers, gynobasic style, and four nutlets. However, the gynobasic style and the four nutlets may have evolved more than once (Cantino 1992a), and a considerable number of ex-Verbenaceae must now be included in Lamiaceae (see Junell 1934 for important early work on the gynoecium; Cantino et al. 1992a, b). Those two families, previously considered close but separate, are now more easily distinguishable morphologically than before.
[Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]]: inflorescence racemose; (protein crystal stacks in nucleus).
Age. The age of this node is estimated to be (60.9-)50.5(-37.6) m.y. (Tank & Olmstead pers. comm.).
Chemistry, Morphology, etc. Note that there may be chemical differences within Phrymaceae s.l., thus Mazus has iridoids while Mimulus does not (Hegnauer & Kooiman 1978). However, sampling is poor - and needs to be expanded. For nuclear protein crystals, see Albach et al. (2009).
Phylogeny. There is still doubt as to details of relationships in this clade, in particular, whether genera like Mazus are to be included in a broadly-circumscribed Phrymaceae, or not (Oxelman et al. 2005; Tank et al. 2006). However, Xia et al. (2009), Albach et al. (2009), Schäferhoff et al. (2010) and Fischer et al. (2012) have all found support for the paraphyly of Phrymaceae s.l., with Mazus and Lancea forming a clade separate from that containing the rest of the family (see also Nie et al. 2006), so dismemberment is in order.
The woody Paulownia, Brandisia and Wightia have been associated with Bignoniaceae and/or Scrophulariaceae in the past, but they are to be placed in this clade. Brandisia is best included in Orobanchaceae (Bennett & Mathews 2006; esp. McNeal et al. 2013; Q.-M. Zhou et al. 2014). There is some support for the placement of Paulownia as sister to Lamiaceae (Olmstead et al. 2000) or with Phrymaceae interpolated between it and Orobanchaceae (some analyses in Albach et al. 2009), but a position sister to Orobanchaceae is on balance more likely (Olmstead et al. 2001; Mueller et al. 2001; Hilu et al. 2003; K. Müller et al. 2004; Wortley et al. 2005a [80% bootstrap]). Although chloroplast data did not link Wightia with Paulownia, ITS and combined analyses did, and other relationships were labile (Q.-M. Zhou et al. 2014). Thus Phrymaceae were sister to Orobanchaceae and Mazaceae were part of a large polytomy (ITS), or all were members of polytomies (chloroplast), or relationships were [Mazaceae [[Rehmannia, etc. [Phrymaceae + Paulownia etc.]] remaining Orobanchaceae]] (combined). Zhou et al. (2014) also drew attention to the fact that Paulownia and Hemichaena (Phrymaceae) both had the iridoid tomentoside, known from nowhere alse (other Phrymaceae did not have this iridoid).
MAZACEAE Reveal Back to Lamiales
Annual or perennial herbs; iridoids +; cork?; vessel elements?; pericyclic fibres 0; leaves opposite (spiral), margins toothed; flowers with very well developed lower lip; anther thecae divergent, staminode 0; stigma lobes sensitive; integument 5-6 cells across; (fruit indehiscent); n = 19; nuclear genome [1C] ca 362 Mb.
3 [list]/33: Mazus (30). Central Asia and North China to the Antipodes, rather scattered, but esp. China (map: from Barker 1991; AgroAtlas viii.2012 - India, Malesia esp. vague).
Chemistry, Morphology, etc. Mazus has 1:1 nodes and lacks a pericyclic sheath. For more information, see under Phrymaceae, but little is known about this clade.
Phylogeny. Fischer et al. (2012) found that the monotypic Central Asian Dodartia, usually included in Phrymaceae, was sister to Mazus (support good).
Genes & Genomes. There are gene duplications in common between Mimulus and Orobanchaceae (Z. Wang et al. 2014).
[Phrymaceae [Paulowniaceae + Orobanchaceae]]: ?
Age. The age of this node is around 67 m.y. (Wikström et al. 2001), (61.9-)54.2, 51.9(-43) m.y. (Cusimano & Wicke 2016), (56-)45.4(-33.9) m.y. (Tank & Olmstead pers. comm.), (54-)44(-33) m.y. (Wikström et al. 2015), or ca 32.2 m.y. (Tank et al. 2015: Table S2, Paulowniaceae outside this clade and slightly older).
PHRYMACEAE Schauer, nom. cons. Back to Lamiales
Annual or perennial herbs (woody); (iridoids 0); cork?; vessel elements?; lamina (punctate), margins toothed (entire); (inflorescence fasciculate), (inflorescence branches cymose), (flowers single); K tubular, toothed, subplicate-ribbed (4-, 3-lobed), (C polysymmetric; 2 + 0 - Mimulus douglasii); A (2), anthers subreniform, thecae confluent; pollen (tricellular), 6-8-colpate (each colpus with 2 orae), spiraperturate, or tricolpate; nectary +/0; (fertile carpel 1), (placentation parietal, near-basal), stigma broadly 2-lobed (1-lobed; shortly 2-fid), sensitive (not); ovules (1, basal-)many/carpel, straight, integument 3-7 cells across; (fruit indehiscent), K persistent; (seeds with pedestals); endosperm +/almost 0, cotyledons convolute; n = 7-12, 14-16, 22, etc.
13 [list]/188: Erythranthe (111), Diplacus (46). ± World-wide, esp. temperate and W. North America and Australia, but few humid tropics (map: from Meusel et al. 1978; Barker 1982; Hong 1983, 1993; India-Southeast Asia-Antipodes very inaccurate.). [Photos - Collection, Mimulus Flower.]
Age. The crown age may be ca 40 m.y. (Nie et al. 2006: Fig. 2, probably low end of range); Phryma separated from most of the rest of the family (the divergence of Peplidium is older) some 49.4-32.3 m.y. ago; (43.9-)29.5(-14.6) m.y. is the estimate in Tank and Olmstead (2017: [Mimulus + Phryma])
Evolution: Divergence & Distribution. Although Phryma represents an old clade, its well-known East Asian - E. North American disjunction was established a mere ca 6-2 m.y.a. (Nie et al. 2006, q.v. for other estimates). Mimulus s. str., although a small genus, has species in (i.a.) east North America, Madagascar, and Australia.
Ecology & Physiology. Members of the family are common in more or less permanently inundated habitats, indeed, species like the Erythranthe guttatus complex is noted for its tolerance of a variety of extreme conditions (Selby et al. 2016 for literature, as Mimulus guttatus, etc.).
Pollination Biology & Seed Dispersal. Friedman et al. (2017) discuss sensitive stigmas and their loss in inbreeding taxa.
Genes & Genomes. There is extensive polyploidy and aneuploidy (both happening 10+ times) in North American Mimulus (= Erythranthe), but neither is associated with the evolution of major clades (Beardsley et al. 2004).
Chemistry, Morphology, etc. Whipple (1972) described the nodes of Phryma as having three traces coming from a single gap; the ovules were described as being apotropous and hemitropous.
For general information about other genera included here, see Fischer (2004b: Scrophulariaceae p. pte), for some chemistry, see Q.-M. Zhou et al. (2014), for pollen, see Argue (1980, 1981) and Chadwell et al. (1992); for Phryma, see Whipple (1972), Venkata Ramana et al. (2000: embryology), and Cantino (2004: general). For floral development in Mazus, see Rawat et al. (1988).
Phylogeny. Phryma and Mimulus and its relatives make up this unexpected clade. There are four clades within Phrymaceae, Phryma, the North American [Erythranthe + Leucarpon] clade, the largely Australian [Mimulus s. str., Glossorhyncha, Peplidium] clade, all with blue flowers, and the North American Diplacus clade, but their interrelationships are unclear ((Beardsley & Olmstead 2000, esp. 2002; Beardsley et al. 2001, 2004; Beardsley & Barker 2004; Barker et al. 2012). Does Cyrtandromoea belong here (see discussion in Gesneriaceae under Phylogeny)?
Classification. For a conspectus of the family, see Barker et al. (2012); Mimulus has had to be dismembered, many species now being found under Erythranthe and Diplacus. For a monograph of Mimulus old style, species of which are the subjects of many evolutionary studies, see Grant (1924) and Thompson (2005).
Previous Relationships. Phryma was previously placed in a monotypic family on account of its distinctive morphology, or allied with Verbenaceae. Mimulus and other genera were included in Scrophulariaceae s.l.
Botanical Trivia. The mostly Australian Glossostigma is scarcely bigger than Lemna, while small plants of Mimulus jepsonii may consist only of cotyledons, a pair of foliage leaves, and a flower (T. Livschultz, pers. comm.).
[Paulowniaceae + Orobanchaceae]: ?
Age. An estimate of the age of this node (Paulownia sister to Buddleja!) is (58-)48, 38(-26) m.y. (Bell et al. 2010); Bremer et al. (2004) suggest an age of ca. 64 m.y., while m.y. is the age in Wikström et al. (2001), (51-)40(-28) m.y. in Wikström et al. (2015) and (50.9-)39.8(-27.6) m.y. in Tank and Olmstead (2017).
PAULOWNIACEAE Nakai Back to Lamiales
Woody*, trees, woody epiphytes turning stranglers, deciduous; iridoids +, (cornosides + - Wightia); cork cambium outer cortical; nodes 1:1; hairs uniseriate-branched to stellate*; petiolar bundle annular; lamina margins entire*; inflorescence branched, ultimate units cymose; flowers large; K ± valvate, leathery*, deeply lobed, space between K and C [water calyx], C with adaxial-lateral lobes outside others [quincuncial, ascending cochlear] in bud, hairs uniseriate with tapering terminal cell; anther thecae head-to-head or parallel and apically confluent, endothecium massive, extending across connective, staminode 0; pollen tricolpate; nectary vascularized; placentae massive, style hollow, head expanded or not, stigma punctate, hollow; seed pedestals +, seeds winged (several sinuous wings - Paulownia); exotesta cells broad, with complex reticulate thickenings; endosperm +; n = 19, 20, nuclear genome size [1C] ca 0.6 pg.
2 [list]/8 or more. South East Asia to E. Malesia (map: from Hu 1959, Paulownia alone). [Photo - Flower.]
Evolution: Divergence & Distribution. In the characterization above, possible apomorphies that refer to both genera have an asterisk, the rest refer to Paulownia alone; Wightia is very poorly known.
Chemistry, Morphology, etc. The combination of cornoside with iridoids is unusual in Lamiales (Q.-M. Zhou et al. 2014); Zhou et al. (2014: p. 2010) also show seedlings of Wightia as having "inflated tubers".
Erbar and Gülden (2011) noted that the terminal flowers in an inflorescence of Paulownia might have five stamens - peloria. The ad- → abaxial direction of development of members of the calyx and the corolla whorls is unusual in Lamiales (Erbar & Gülden 2011), although observations are limited.
For additional information, see Fischer (2004b: as Scrophulariaceae, general), Schilling et al (1982: verbascoside, etc.), and Dos Santos and Miller (1993: wood anatomy).
Phylogeny. For a discussion on the relationships of Paulownia and Wightia, see above; the latter genus is only provisionally included here.
Previous Relationships. Paulownia is superficially like Catalpa (Bignoniaceae) and both have been shuttled back and forth between "Scrophulariaceae" and Bignoniaceae. Paulownia has endosperm and lacks the distinctive ovary and seed anatomy of Bignoniaceae (Armstrong 1985; Manning 2000; Lersten et al. 2002); on the other hand, Catalpa is definitely to be included in Bignoniaceae. Wightia has often been associated with Paulownia in the past (Q.-M. Zhou et al. 2014 and references).
OROBANCHACEAE Ventenat, nom. cons. Back to Lamiales
Plant turning black on drying (not); cork?; head of glandular hairs lacking vertical partitions; lamina margins often toothed to deeply lobed; C with abaxial-median or abaxial-lateral lobes outside others [quincuncial, descending cochlear] in bud; placentae paired-stipitate; seed with exotestal cells variously thickened on the inner walls.
99 [list]/2,060. World wide, but especially North (warm) Temperate and Africa-Madagascar.
Age. Crown-group Orobanchaceae are estimated to be (47.1-)35.7(-24.3) m.y.o. by Tank and Olmstead (2017) and (36-)30.2(-25.6) m.y. by Schneider and Moore (2017: ?too young, but c.f. topology used as a calibration in Magallón et al. 2015).
1. Rehmannieae Rouy
Plant rhizomatous; leaves spiral; bracts ± foliaceous, (bracteoles 0); (staminode +); stigma lobes sensitive; n = ?
2/7. China (map: from Flora of China vol. 18. 1998; green = R. glutinosa, also cultivated).
Synonymy: Rehmanniaceae Reveal
[Lindenbergieae [Cymbarieae [Orobancheae [Brandisia [Rhinantheae [Buchnereae + Pedicularidae]]]]]]: stomata do not close (usually...); placentation parietal.
Age. Bremer et al. (2004) suggested that the age of this node can be put at around 48 m.y., the age in Wolfe et al. (2005) was ca 52.2 m.y. and in Wikström et al. (2015) (38-)26(-13) m.y.; (56.5-)50, 44(-38.3) m.y. (Cusimano & Wicke 2016) and (38.5-)27.8(-17.3) m.y. (Tank & Olmstead pers. comm.) are other estimates.
2. Lindenbergieae T. Yamazaki
Bracts ± leaf-like, bracteoles usu. 0; A thecae on connective arms; testa usu. with hook-shaped thickenings adnate to surface; n = 16.
1/12. N.E. Africa to N. Philipines (map: see Hjertson 1995).
Synonymy: Lindenbergiaceae Doweld
[Cymbarieae [Orobancheae [Brandisia [Rhinantheae [Buchnereae + Pedicularidae]]]]]: herbs, root hemiparasites, haustoria from lateral roots; orobanchin +, little oxalate accumulation, 6- and/or 8-hydroxylated flavone glycosides 0; leaves spiral to opposite; (K ± free), C (tube development intermediate), (aestivation imbricate); staminode 0, anther thecae parallel or ± synthecous, sagittate to inverted U-shaped, often hairy, with tails or basal awns, (tapetum amoeboid); pollen often starchy, commonly tricolpate, surface retipilate, (polyporate); ([G 5]), (placentation axile), (placentae [2, bilobed] 4 [-6], [much divided]), stigma clavate to capitate; ovule (>1/carpel), unvascularized or not, variants of anatropous, integument (2-)4-7(-12 )cells across, (embryo sac protrudes beyond the micropyle); (antipodal cells persistent); capsule loculicidal to septicidal, (indehiscent); (seed pedestals +); (seed with elaiosomes), (cells of seed wings with reticulate thickenings on anticlinal walls), (cells of layers other than the exotesta thickened and lignified); endosperm +, (walls thickened; reserves starch; mannose-rich polysaccharides; 0); (perisperm +, 1-layered), embryo often small (minute, undifferentiated); (germination via germination tube); nuclear genome [1C] (553-)3374(-8729) Mb.
96/2040. Worldwide, but especially N. (warm) temperate and Africa-Madagascar (map: from van Steenis & van Balgooy 1966; Hultén 1971; Meusel et al. 1978; Hong 1983). [Photo - Plant, Collection.]
Age. The age of the hemiparasitic clade is estimated at (55.2-)49.5, 41.3(-35.7) m.y. (Cusimano & Wicke 2016), ca 47.7 m.y. (Wolfe et al. 2005) or (33.1-)27.7(-23.5) m.y. (Schneider & Moore 2017: ?too young) - all include Schwalbea.
3. Cymbarieae D. Don
6/14. E. North America (1 sp.), Eurasia. n= 8.
[Orobancheae [Brandisia [Rhinantheae [Buchnereae + Pedicularidae]]]]: mannitol + [?all]; endodermis 0.
Age. This clade is ca 44.4 m.y.o. (Woolfe et al. 2005) or (31.9-)26.6(-22.6) m.y.o. (Schneider & Moore 2017).
4. Orobancheae Lamarck & de Candolle
Holoparasites, haustoria from radicle/primary root; (bracteoles 0); (A free from C - Eremitilla); microsporogenesis successive [?level], pollen variable, inc. inaperturate, (heteromorphic); n = 12, 19.
12/180: Orobanche (150)/Orobanche (), Phelipanche (), Aphyllon (25<). North temperate, North Africa, Arabian Peninsula.
Age. The age of the holoparasitic clade [Epifagus + Orobanche] is (56.4-)49.1, 39.7(-33.3) m.y. (Cusimano & Wicke 2016), ca 39.4 m.y. (Wolfe et al. 2005) or (19.7-)16.5(-13.7) m.y. (Schneider & Moore 2017).
Synonymy: Aeginetiaceae Livera, Phelypaeaceae Horaninow
[Brandisia [Rhinantheae [Buchnereae + Pedicularidae]]]: ?
5. Brandisia J. D. Hooker & Thomson
Shrubs to lianas; hairs stellate; anther thecae long-ciliate; n = ?
1/13. Burma to China.
[Rhinantheae [Buchnereae + Pedicularidae]]: ?
Age. This clade is estimated to be ca 33.9 m.y.o. (Wolfe et al. 2005) or a little over 24 m.y.o. (Schneider & Moore 2017).
6. Rhinantheae Lamarck & de Candolle
(Plants annual), (holoparasitic); n = 9-14.
18/540: Euphrasia (170-350), Bartsia (50), Rhinanthus (45). ± Worldwide, but esp. Eurasian.
Age. The age of this clade is (38.8-)30.8(-25.5) m.y. (Uribe-Convers & Tank 2015).
Synonymy: Euphrasiaceae Martynov, Melampyraceae Hooker & Lindley, Rhinanthaceae Ventenat
[Buchnereae + Pedicularidae]: seeds minute, dust-like [?level].
7. Buchnereae Bentham
(Plants holoparasitic); (axillary 3-flowered cymes); n = 12, 14, 19+.
16/350: Buchnera (100), Alectra (40), Harveya (40), Sopubia (40), Striga (33). Tropics, inc. Australia.
Synonymy: Buchneraceae Lilja, Cyclocheilaceae Marais, Nesogenaceae Marais
8. Pedicularidae Duby
(Plants annual); (wood rayless); (flower asymmetrical); (anther thecae unequal or single); n = 8, 11-15, etc.
16/857: Pedicularis (600-?800), Castilleja (160-200), Agalinis (45). Mostly northern hemisphere, some to South America and the Caribbean.
Age. This clade is about 33.3 m.y.o. (Wolfe et al. 2005).
Synonymy: Pedicularidaceae Jussieu
Evolution: Divergence & Distribution. Orobanchaceae may have diversified north of the Tethys Sea, perhaps in eastern Asia (Wolfe et al. 2005). The evolution of holoparasites with minute dust seeds - which may have happened three times or so - may have been driven by the expansion of grasslands in the middle of the Caenozoic (Eriksson & Kainulainen 2011; see also McNeal et al. 2013). The age of around 31.5 m.y. for the adoption of the holoparasitic habit in Epifagus may not be too terribly far off the mark (see Naum,ann et al. 2013), but the sister taxon used in the estimation (Digitalis) is a very distant outgroup so the agreement of 31.5 m.y. with anything is likely to be coincidental.
Orobanchaceae are unusual in that the non-parasitic Lindenbergia is much less diverse than its sister group, which is parasitic, the reverse of the size imbalance common when comparing non-parasitic and parasitic sister clades, however, most Orobanchaceae are only hemiparasitic (Hardy & Cook 2012); see also Santalales which also includes substantial diversity (its sister taxon is uncertain). Although phylogenetic relationships at the base of Orobanchaceae are not entirely clear, all clades potentially sister to the (hemi)parasitic clade are small.
Pedicularis is particularly common in montane-alpine areas in the Northern Hemisphere although actual species numbers are uncertain (Mill 2001); there are about 600 species in the Sino-Himalayan region, 217 from the Hengduan region alone (Boufford 2014). There may have been two movements of Pedicularis from somewhere in eastern Asia to North America, the few European species being independently derived from within the North American clades; patterns of movement in the genus are complex (Robart et al. 2015). The around 25 species of Pedicularis in the Arctic represent around 13 colonizations from mountainous regions at lower latitudes; they include the only polyploid species in the genus (Tkach et al. 2014). Pedicularis, as well as three of the other six orobanchaceous genera growing at high latitiudes, include annual species (Tkach et al. 2014).
Euphrasia has a North Temperate - circum-Pacific distribution and is basically bipolar; much dispersal seems to have been involved in attaining this range (Gussarova et al. 2008). Diversification within the large genus Castilleja is becoming better understood. There is a speciose West North American/Central/South American perennial clade - some 160 species in North America alone - derived apparently quite recently from an annual ancestor; polyploidy is common in the perennials, but not in the annuals (Tank & Olmstead 2008, 2009; see also Hughes & Atchison 2015). Annuals have dispersed more than once to South America (Tank & Olmstead 2009).
Neobartsia showed increased diversification when it moved to South America (4.1-)2.6(-1.5) m.y.a., although exactly how it got there from Europe is unclear (Uribe-Convers & Tank 2015, 2016). Several stems of speciose clades in holoparasitic Orobancheae are long, up to ca 7 m.y. (the whole clade is only ca 16.5 m.y.o.), perhaps because extinction has been very common (Schneider & Moore 2017).
There are three amphitropical disjunctions in the family, all involving holoparasitic taxa - which might seem a little odd given the at least moderate host specificity shown by some of these plants. Aphyllon has moved to South America twice within the last 1.9 m.y., and both North American taxa close to the South American migrants and the South American species are parasitic on Grindelia (Asteraceae-Asteroideae-Astereae), while other species of Aphyllon also parasitize Asteraceae (Schneider & Moore 2017, q.v. for dates of both parties involved). Relatives of Orobanche cernua var. australiana from South Australia, are also from the Northern Hemisphere, and the move happened within the last 0.46 m.y. (Schneider & Moore 2017).
Ecology & Physiology. Hemiparasitism appears to have evolved once (McNeal et al. 2013) in Orobanchaceae, while holoparasites have evolved from hemiparasites perhaps three times (dePamphilis et al. 1997; Nickrent et al. 1998; Young et al. 1999; Schneeweiss et al. 2004a; Bennett & Mathews 2006; esp. McNeal et al. 2013), and ca 12 times in angiosperms as a whole (Westwood et al. 2010). The hemiparasitic Harveya obtusifolia is well embedded in a holoparasitic clade of the genus; whether there has been reversion in life style here or there have been yet more independent acquisitions of the holoparasitic habit in that part of the family is unclear (Morawetz & Randle 2009; species not included by McNeal et al. 2013); Morawetz et al. (2014) incline to the latter position. Indeed, the distinction between hemi- and holoparasitism is not sharp. Species like Striga linearifolia and Alectra sessiliflora are close to being holoparasitic, while Tozzia alpina may live underground for a decade or so as a holoparasite before producing photosynthetic, fertile above-ground shoots (McNeal et al. 2013).
Strigolactones stimulate germination of seeds of holoparasitic Orobanchaceae in particular (Tsuchiya & McCourt 2009; Akiyama et al. 2010; Westwood et al. 2010; Conn et al. 2015). The mechanism involved is similar to some specific germination responses in Arabidopsis thaliana mediated by the KAI2 gene, but evolved after an ancient - as old as the common ancestor of [Solanales + Lamiales] - duplication of that gene. The KAI gene controls the response to karrikin, a substance found in smoke that is responsible for the positive germination response of some species to fires (e.g. Flematti et al. 2013), although karrikin receptors are found throughout embryophytes and are involved in the establishment of arbuscular mycorrhizal associations (Gutjahr et al. 2015 and references). (Both karrikin and strigolactones have a distinctive butenolide element.) Orobanchaceae, including the hemiparasitic species, usually have more copies of the KAI2 paralogs than other Lamiales, and the orobanchaceous KAI2d genes respond to strigolactones. Strigolactones are commonly exuded from plant roots and are important in the plant/fungus signalling involved in the establishment of vesicular-arbuscular mycorrhizae, and they are also related to plant hormones that control branching; they are essential for the host. Surprisingly, although both Striga and Phelipanche/Orobanche require strigolactones to germinate, they also synthesize them themselves (Das et al. 2015); endogenous production may be essential for the growth of the parasite. Finally, the parasite does not respond to all strigolactones produced by the host. Thus Sorgum resistant to Striga produces the strigolactone orobanchol rather than the strigolactone 5-deoxystrigol which has the opposite stereochemistry and to which the parasite does respond (Gobena et al. 2017). There are also suggestions that germination is in part controlled by maternal genes in persistent maternal (nucellar) tissue in the seed of the parasite (Plakhine et al. 2012).
Haustoria are produced by both hemi- and holoparasitic Orobanchaceae, and may have but a single origin within Orobanchaceae (Fischer 2004b for a summary). Their development - and also control by the host - is detailed in Musselman and Dickison (1975), Thorogood and Hiscock (2010), Joel et al. (2013), and elsewhere. The host produces a variety of haustorium-inducing metabolites (Westwood et al. 2010 and references). Haustoria develop quickly in holoparasitic Orobanchaceae, most of which have tiny seeds with no reserves, and they terminate the radicle, but in hemiparasites, and later in some/?many holoparasites, too, they develop on lateral roots (Westwood et al. 2010; Joel 2013). Seeds may be relatively larger in hemiparasitic species, and for more on germination there, see Tesitel et al. (2011 and references). A number of upregulated genes that may be involved in the evolution of the parasitic habit have been identified. Many are derived from genes that act in the root, but also in pollen, the latter perhaps because pollen tube growth is intrusive and also involves interactions between the tube and stylar tissue, similar to interactions between host and haustoria (Thorogood & Hiscock 2010; Z. Wang et al. 2014: Lindenbergia the outgroup - a little too close?).
Haustoria function in different ways. Hemiparasitic taxa in the [Rhinantheae [Buchnereae + Pedicularidae]] clade have chlorophyll and take up largely water, nitrogen, etc., from their hosts, their haustoria tapping the xylem. The lumina of the xylem cells in the host and parasite are in direct contact as haustorial cells punch through the walls of host xylem and form tubular openings of various shapes before themselves differentiating into water-conducting cells (Dörr 1997; Cameron et al. 2006). In these hemiparasites, carbon may also be obtained from the host - indeed, sometimes most of the parasite's needs may be supplied this way - and it moves through the xylem of the parasite (Tesitel et al. 2010b, 2011 and references). The holoparasite Orobanche also takes up organic materials, but here the haustoria tap the phloem (Irving & Cameron 2009; Joel 2013; Tesitel 2016). Ordinary-looking sieve plates form between host and parasite phloem elements, although the latter are not associated with companion cells (Dörr & Kollmann 1995). The holoparasite Lathraea lacks haustorial phloem connections, but host sap is taken up by the xylem of the parasite (Ziegler 1955; Dörr 1990). The perennial haustorium of Boschniaka hookeri also has only xylem connections, and its host (Gaultheria) forms a wood rose rather like those in the hosts of some hemiparasitic Santalaceae and Loranthaceae (Kuijt & Toth 1985). Iridoid glucosides, pyrrolizidine and quinolizidine alkaloids, etc., may also move from host to parasite (e.g. Adler & Wink 2001; Hibberd & Jaeschke 2001; Shen et al. 2005 [also host selection]; Rasmussen et al. 2006 and references). (Secondary) metabolites may also move from parasite to host. Thus some of the severe effects on the host caused by the parasite may be due in part to the breakdown of the iridoid glucoside of the parasite and the release of the cytotoxic iridoid aglucone, perhaps caused by the host's ß-glucosidases, themselves common because they are involved in the host's cyanogenic defence pathway (Rank et al. 2004). For other information on parasitism in the family, see Irving and Cameron (2009) and Tesitel (2016) and references.
Xylem flow from host to parasite is also aided by active mechanisms. Thus mannitol may be high in the parasite, mannitol synthesis being massively increased as paratism is established, so increasing the osmotic gradient between the host and parasite (Jiang et al. 2005; Cameron et al. 2006). Tesitel and Tesarová (2013) described two kinds of glandular hairs that actively secrete water in Rhinantheae, including those that live below ground for most of their life cycle, that also help pull water through the plant; these hairs may occur in the entire [Rhinantheae [Buchnereae + Pedicularidae]] clade.
Adler (2000, 2002, 2003; Adler & Wink 2001) found a complex relationship between hosts and parasite, the annual Castilleja indivisa. Association with Lupinus in particular led to fewer herbivores eating the parasite (sometimes), more visitors by pollinators, increased seed set, etc., when compared with other hosts. These effects were mediated by the movement both of alkaloids and nitrogenous compounds (increase in growth s.l.) from the lupin to the parasite; alkaloids acted as a deterrent to herbivores and indirectly increased visits by aesthetically sensitive pollinators who were no longer put off by half-eaten inflorescences (Adler 2000). Iridoid glycosides can move from hemiparasite to caterpillar eating it, the amount of a particular iridoid in the caterpillar not necessarily reflecting that in the hemiparasite (Haan et al. 2018).
Host specificity, and the formation of races specific to particular hosts, is well-known in Orobanche in particular (see Westwood et al. 2010). Incompatability between the host and parasite is first evident in the endodermal region, at least in Orobanche (Thorogood & Hiscock 2010).
Stomata in Orobanchaceae are often, but not always, perpetually open (Stewart & Press 1990; Smith & Stewart 1990), even in the apparently autotrophic Lindenbergia, sister to most other Orobanchaceae; the situation in Rehmannia and relatives (see below) is unknown. The stomata remain open despite the presence of large amounts of abscisic acid, which normally would be expected to result in their closure (e.g. Jiang et al. 2010). Perpetually-open stomata are common in hemiparasitic plants in general because they increase the transpiration flow in the parasite so facilitating movement of water, nutrients, etc., from the host (e.g. Phoenix & Press 2005).
The effects of hemiparasitic Orobanchaceae on the general community can be considerable. They may increase overall diversity if, like Rhinanthus minor, they parasitize dominant species like grasses in grasslands, the growth of associated legumes and forbs then tending to increase (Bardgett et al. 2006; Cameron et al. 2007; Irving & Cameron 2009). Indeed, it has even been suggested that they be used to help restore diverse grassland (Bullock & Pywell 2005). The hemiparasites, especially the annuals, increase the rate of community cycling of nutrients such as nitrogen, perhaps particularly in the Arctic. Their litter can be relatively rich in nutrients, nutrients not being resorbed by the plant as it senesces, and it often decomposes more rapidly than that of other species in the community; overall, the positive ecological effects of the litter can counteract the negative effects of parasitism (Quested et al. 2003; Phoenix & Press 2005; Bardgett et al. 2006; Watson 2009; Fisher et al. 2013).
Pollination Biology & Seed Dispersal. The remarkable flowers of Pedicularis show considerable variation, especially in corolla tube length and in galea (the hood-shaped structure formed by the apex of the two adaxial petals) morphology (e.g. Li 1951 and references; W.-B. Yu 2013 for its development). W.-B. Yu et al. (2015) discuss aspects of floral evolution. Some species have a corolla tube ca 10 cm long or more, or there may be an asymmetric, proboscis-like extension of the galea (e.g. Li 1951 and references). The around 600 species of Pedicularis in the Sino-Himalayan region are likely to be pollinated by bumble bees - over fifty species of the bees, almost a quarter of the genus (Williams et al. 2009), and 217 species of Pedicularis (Boufford 2014) are known from the Hengduan region. Species with red, long-tubed flowers and growing at higher elevations may lack nectar and be pollinated by pollen-collecting bumble bees, which raises the question of the function of these very long tubes - effectively they are pedicels, the plants not having long inflorescence axes (Huang & Fenster 2007). Character displacement, in which sympatric taxa differ more than would be expected, so reducing the chances of pollen being deposited on the wrong stigma (pollen interference), seems to be one component in the generation of the exceptional diversity of the genus in the Hengduan Mountains (Eaton et al. 2012). Sympatric species sharing the same pollinating bee tend to deposit and pick up pollen from different parts of the bee's body, but if one species of Pedicularis is particularly common, this will help ensure pollinator constancy (Huang & Shi 2013), however, other studies suggest reproductive isolation caused by strongly differing floral morphologies is not that great (Armbruster et al. 2013a). For comments on the floral evolution of the genus, see also Macior (1984) and Ree (2005a); pollen morphology - there is quite extensive variation - is linked with corolla morphology and pollinator type (H. Wang et al. 2009a); buzz pollination is reported, as also in Melampyrum (Teppner 2018 and references)..
Hairs are common on the anthers in Orobanchaceae, and in Esterhazya in particular they form a pollination basket in which the pollen is held (Hesse et al. 2000). For other literature on pollination, see Kampny (1995: as Scrophulariaceae).
Melampyrum and Pedicularis in particular have myrmecochorus seeds (Lengyel et al. 2009, 2010). Eriksson and Kainulainen (2011) discuss the distinctive dust seeds of many parasitic Orobanchaceae (also in Ericaceae-Monotropoideae and mycoheterotrophic taxa in general). Lathraea squamaria, parasitic on Corylus, has few and relatively large seeds (its fruits are capsules), perhaps connected with the need of the seedling to reach the relatively deep roots of their future host, while the fleshy fruits of Phacellanthus tubiflorus, borne at ground level, are dispersed by camel crickets (Rhaphidophoridae: e.g. Tachycines elegantissima), another "strategy" of mycoheterotrophs (Suestsugu 2017).
Tesitel et al. (2011), Tesitel (2016 and references) discuss germination of hemiparasitic Orobanchaceae.
Plant-Animal Interactions. Agromyzid dipteran leaf miners have diversified on hemiparasitic Orobanchaceae (Winkler et al. 2009), and larvae of Nymphalinae-Melitaeini butterflies are also commonly found on the plants (also on Plantaginaceae, but not on Scrophulariaceae: Wahlberg 2001).
Bacterial/Fungal Associations. Striga hermonthica and Orobanche aegyptiaca, at least, but not Pedicularis, are unable to form endomycorrhizal associations since they have lost their symbiosis-specific genes, interestingly, Lindenbergia also does not have/has lost some of these genes (see Delaux et al. 2014: Fig. 3).
Genes & Genomes. Wicke et al. (2016) discuss the evolution of the chloroplast genome in the hemi/holoparasitic members of the family. The genome in holoparasites may as small as 45 kb in taxa like Conopholis americana (Wicke et al. 2013) and become extensively rearranged. However, a few chlorophyll synthesis genes often remain functional, even in holoparasitic taxa, although they are much more affected by the adoption of parasitism than housekeeping genes (Wicke et al. 2016), and rbcL genes are also often conserved (Wickett et al. 2011; Wicke et al. 2013); Cistanche deserticola retains all its 30 tRNA genes (X. Li et al. 2013). The IR has been lost more than once (Wolfe et al. 1992; Jansen & Ruhlman 2012). As the chloroplast genome changes, the rate at which it evolves changes, both speeding up and slowing down (Wicke et al. 2016), but there is no correlation of rate of change with generation time (Cusimano & Wicke 2016). Genes or gene fragments have moved (several times each) from the chloroplast to the mitochondrion and in particular the nucleus (Cusimano & Wicke 2016).
Horizontal nuclear gene transfer from Sorghum bicolor to Striga hermonthica (but not Orobanche) has been demonstrated, the transferred host gene functioning in the nucleus of the parasite (Yoshida et al. 2010). Similarly, the nuclear-encoded SSL gene has moved from Brassicales to Orobanche aegyptica (D. Zhang et al. 2014) and the distinctive albumen-1 gene moved from Fabaceae-Faboideae (a species close to Onobrychis may be the source) to Orobanche s.l. ca 16 m.y.a. (Y. Zhang et al. 2013). The cprpoC2 gene has moved from Haloxylon ammodendron (Amaranthaceae-chenopod) to Cistanche deserticola (X. Li et al. 2013, q.v. for HGT of chloroplast genes in other Orobanchaceae). The mitochondrial atp6 gene has moved to Orobanche coerulescens probably from its host, Artemisia (Asteraceae) (Kwolek et al. 2017). For more possible horizontal gene transfer, see Cusimano and Wicke (2016).
There may have been genome duplication in obligate hemiparasitic and holoparasitic taxa (Wickett et al. 2011). For the evolution of nuclear genome size in the family, see Weiss-Schneewiess et al. (2005); genome size is reduced after polyploidization (alsoLyo et al. 2017 for overall variation in the family). Unlike chloroplast genomes, nuclear genomes of holoparasitic taxa are much larger - to almost 10x - than that of the free-living Lindenbergia, although the nuclear genome of the hemiparasite Schwalbea is only slightly larger. Orobanche has many more repetitive DNA clusters contributing to genome size increase (Piednoël et al. 2012; see also Westwood et al. 2010). Gruner et al. (2010) suggested that a facilitating factor for this increase was rootlessness; root growth in taxa with large nuclear genomes is in general reduced, but of course root growth in holoparasitic taxa is minimal, and so this constraint is relaxed.
For chromosome numbers and karyotype evolution in Orobanche and relatives, see Schneeweiss et al. (2004c).
Economic Importance. A number of Orobanchaceae are very serious parasites primarily on legume and grain crops in warmer and drier areas, and especially in sub-Saharan Africa where they are still spreading. Striga is a particularly serious parasite that parasitizes mostly monocots (S. gesnerioides attacks eudicots). It affects ca 40% of the cereal-producing areas in Africa in particular and it causes average losses in yield of 30-90%, especially on poorer soils and so where farmers can least cope with the losses. A single plant of Striga produces up to 100,000 seeds which can remain viable for about 20 years (Scholes & Press 2008; see also Mohamed et al. 2001: African species; Ejeta & Gressel 2007; Yoshida & Shirasu 2009; Irving & Cameron 2009). Alectra vogelii may cause the complete loss of legume crops it infects (Morawetz & Wolfe 2009). Orobanche parasitizes eudicot crops (there is a fair degree of species specificity) in more or less temperate parts of the world, again with very serious results (Westwood et al. 2010 for references). However, although all told losses are in the billions of dollars, accurate information about the extent of the infestations is hard to obtain (Parker 2009).
Chemistry, Morphology, etc. Orobanchaceae have orobanchin, a phenylpropanoid ester of caffeic acid, and silicic acid, and their iridoids are produced via the aucubin pathway (Thieret 1971; Rank et al. 2004); c.f. Gesneriaceae. For fatty acids in the seeds of Orobanche, see Velasco et al. (2000). For haustorial anatomy, see Solms-Laubach (1867); Batashev et al. (2013) note that phloem companion cell morphology in Orobanchaceae is distinctive, but the variation patterns in minor vein phloem are complex.
A collar-like base of the corolla tube persists after the rest has fallen off (Fischer 2004b) - is this a family character? Corolla aestivation is interesting in this clade. The abaxial-lateral pair of corolla lobes commonly envelops the adaxial-lateral lobes, while in Euphrasia and its relatives the abaxial lobe also envelops this latter pair of lobes - both forms of quincuncial aestivation; in other Orobanchaceae, the abaxial lobe envelops all other lobes, i.e. ascending cochleate aestivation (Armstrong & Douglas 1989). For floral development, see Armstrong and Douglas (1989), Endress (1999). Greilhuber (1974) observed endomitotic polyploidization in the cells of the inner tapetum in some genera - but not in Pedicularis, Melampyrum, and Plantaginaceae. The chalazal haustorium of Melampyrum is massive and binucleate (Takhtajan 2013).
The recently-described Eremitilla is very distinctive morphologically, i.a. the stamens are free from the corolla tube and the anther thecae are more or less embedded in the expanded filament apex (Yatskievych & Jiménez 2009).
For general information, see Terekhin and Nikitcheva (1981), Fischer (2004b: Scrophulariaceae p. pte), Demissew (2004: Cyclocheilaceae), Harley (2004: Nesogenaceae), papers in Folia Geobot. 40(2-3). 2005, the Parasitic Plants website (Nickrent 1998 onwards), Heide-Jørgensen (2008) and Hjertsen (1995: Lindenbergia); for floral development, see Canne-Hilliker (1987), for corolla aestivation, see Eichler (1875) and Armstrong and Douglas (1989), for the development of the upper lip/galea of the corolla in Pedicularis, see W.-B. Yu et al. (2013), for pollen, see Minkin and Eshbaugh (1989), Lu et al. (2007), Zare et al. (2014: heteromorphism in Orobancheae) andPiwowarczyk et al. (2015: C. European Orobancheae), for ovules and seeds, see Takhtajan (2013), for ovules of Cyclocheilon, etc., see Junell (1934), for embryology, see Krishna Iyengar (1940b), Tiagi (1963) and Arekal (1963) and references, for embryo and endosperm, see Crété (1955), and for seed morphology, see Musselman and Mann (1976), Joel et al. (2012), M.-L. Liu et al. (2013: Pedicularis) and Dong et al. (2015: substantial variation).
Phylogeny. For the delimitation and composition of the family, see Young et al. (1999), Wolfe et al. (2005), Bennett and Mathews (2006), etc. In a rather restricted phylogenetic analysis, Rehmannia (previously in Gesneriaceae) was associated with Oreosolen (Albach et al. 2007), in Scrophulariaceae s. str. (Oxelman et al. 2005), but this may be a rooting problem. In a rather more extended study, Rehmannia was sister to Orobanchaceae, while Oreosolen indeed linked with Verbascum and relatives, forming part of a north temperate group in Scrophulariaceae (Jensen et al. 2008b). In a tree found by Oxelman et al. (2005), Rehmannia linked very weakly with Phryma, Paulownia, Mazus and Lancea, as well as with genera of Orobanchaceae. McNeal et al (2013: both nuclear and plastid genes) included ca 2/3 the genera of Orobanchaceae and obtained a rather strongly supported phylogeny that is the basis for the groupings above, although the position of Brandisia was unclear.
Recent work suggests that Rehmannia and Trianeophora, both East Asian, form a strongly supported clade that is sister to the rest of the family - i.e. Lindenbergia and the rest (Xia et al. 2009; see also Albach et al. 2009; Fischer et al. 2012). Albach et al. (2007) had recorded the presence of iridoids in Rehmannia, although these are at best very uncommon in Gesneriaceae, and also at least some mannitol, a polyol not occurring in Scrophulariaceae s. str. but found i.a. in some Orobanchaceae. However, [Rehmannia + Trianeophora] did not immediately link with other Orobanchaceae in some analyses in Q.-M. Zhou et al. (2014). Rehmannia is not known to be hemiparasitic; it has a racemose inflorescence, its flowers lack bracteoles, the two abaxial-lateral corolla lobes are outside the others (as is common in Orobanchaceae), and its stigma lobes are sensitive. Trianeophora has bracteoles, it may have a staminode, but its floral aestivation is similar, if quite variable (Wang & Wang 2005: close to Digitalis). Phytochemistry also links Triaenophora closely with Rehmannia (Jensen et al. 2008b). Rehmannia has 1:3 nodes and petioles with arcuate + wing bundles, both very common in Lamiales (pers. obs.).
Lindenbergia may be sister to the remainder of the family (e.g. Wolfe et al. 2005; Albach et al. 2009, but sampling limited; Fischer et al. 2012) or it may link more particularly with a small group of parasitic taxa (Bennett & Mathews 2006: support weak). Recent work places it sister to the rest of Orobanchaceae with overall rather strong support (McNeal et al. 2013: not basal in the PHYB + PHYA analyses; some analyses in Q.-M. Zhou et al. 2014).
For summary relationships, see Latvis et al. (2017). General relationships in the family may be [holoparasitic clade [[Castilleja, Pedicularis, etc.] [[Euphrasia, Rhinanthus, etc.] + [tropical clade]]]] (Bennett & Mathews 2006). R. G. Olmstead (pers. comm. 2003) noted that the inclusion in the tropical clade of Nesogenes (Nesogenaceae) and Cyclocheilon and Asepalum (Cyclocheilaceae), all poorly known, was likely (see also B. Bremer et al. 2002 for Cyclocheilon). There was strong support for Nesogenes (the only taxon of this group included) being sister to the shrubby Radamea (Bennett & Mathews 2006; McNeal et al. 2013), the two genera belonging to the strongly supported tropical clade (Bennett & Mathews 2006). In a comprehensive analysis, ex Cyclocheilaceae and Nesogenaceae are sister to this tropical clade, within which there was some resolution of relationships (Morawetz & Randle 2009, esp. Morawetz et al. 2010); Nesogenes was sister to Graderia and in a clade that includes Striga (Morawetz et al. 2010; see also Fischer et al. 2012). Relationships found by Z.-D. Chen et al. (2016) in Chinese Orobanchaceae largely are consistent with those above. In a study focussing on Acanthaceae, McDade et al. (2012) found a fascinating set of relationships, [Rehmannia [Lindenbergia [Cyclocheilon + the rest]]], although support for the position of Cyclocheilon was not that strong.
The position of the woody liane Brandisia is unstable and the genus is isolated (Bennett & Mathews 2006; esp. McNeal et al. 2013; see also Z.-D. Chen et al. 2016). Wightia, with which it has been linked, is not immediately related, but it does belong somewhere in the area [Mazaceae [Phrymaceae [Paulowniaceae + Orobanchaceae]]] - see above).
Inclusion of Nesogenes, and in particular Cyclocheilon and Asepalum considerably increases the morphological diversity of Orobanchaceae. Cyclocheilon and Asepalum lack much in the way of a calyx, it being at most a minute rim, but have large bracteoles enveloping the flower bud (c.f. Acanthaceae-Nelsonioideae). They are also shrubs with red roots [?always]; the flowers are single in the leaf axils; the exine is thickened near the apertures; the placentation is axile or parietal, with 1-5 apotropous ovules/carpel, endothelium?, the funicles are long and the stigma is lingulate. The fruit is a capsule or schizocarp; there is no endosperm. Although Harley (2004) notes similarities between the pollen of Cyclocheilaceae, Nesogenaceae (both have tricolpate pollen, that of Nesogenes is perhaps also pilate) and Orobanchaceae, I know nothing of stomatal closure and parasitism in these plants. Clarification of their relationships and their ecology is needed to help our understanding of the evolution of parasitism in Orobanchaceae.
For a re-evaluation of relationships of genera in the old Rhinantheae, see Tesitel et al. (2010a); Scheunert et al. (2012) suggest that Rhinanthus itself is not monophyletic (see also Bennett & Mathews 2006). Pinto-Carrasco et al. (2017) focussed on Odontites, and clearly the pattern of relationships within the tribe has been very fluid, depending in part on the compartment of the genus sampled. For a phylogeny of Pedicularis, see also Ree (2005), for that of Euphrasia, see Gussarova et al. (2008), and of Orobanche and relatives, see Schneeweiss et al. (2004a, c), Park et al. (2008) and X. Li et al. 2017. Scheunert et al (2012) and in particular Uribe-Convers and Tank (2015) and Uribe-Convers et al. (2016a) examined relationships around Bartsia, which has turned out to be polyphyletic. Z.-D. Chen et al. (2016) looked at relationships in ca 50 species of Chinese Pedicularis, and P. lachnoglossa was weakly supported as being sister to the others. For further details of relationships, see dePamphilis (1995) and Olmstead and Reeves (1995).
Schneider and Moore (2017) examined relationships in Orobancheae with a focus on Aphyllon
Classification. See McNeal et al. (2013) for the tribal classification that is followed here - Cyclocheilon and Asepalum were absentees. Although a number of genera were not sampled, they are small and will have only a marginal effect on species numbers of the clades. Thus 12 genera from the old Buchnereae (Fischer 2003) were not examined, but they include a mere 25 species.
Tank et al. (2009) provide a phylogenetic classification of Castillejinae; Uribe-Convers and Tank (2016) rearranged generic limits around Bartsia, and for genera in the Rhinantheae as a whole, see Pinto-Carrasco et al. (2017) - one hopes limits are now fixed.
Previous Relationships. Hemiparasitic genera like Euphrasia and Pedicularis used to be considered intermediates between holoparasitic Orobanchaceae and Scrophulariaceae s.l. (e.g. Boeshore 1920; Cronquist 1981). Rehmannia has often been linked with Titanotrichum and included in Gesneriaceae (Xia et al. 2009 for references).
Botanical Trivia. The purple-flowered Lathraea clandestina is one of the few parasitic plants cultivated for its horticultural merit.
Thanks. To David Tank for useful comments; Robert Mill also caught a number of mistakes around here.