EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, thalloid, with single-celled apical meristem, showing gravitropism; rhizoids +, unicellular; acquisition of phenylalanine lysase [PAL], phenylpropanoid metabolism [lignans +, flavonoids + (absorbtion of UV radiation)], xyloglucans +; plant poikilohydrous [protoplasm dessication tolerant], ectohydrous [free water outside plant physiologically important]; cuticle +; cell wall also with (1->3),(1->4)-ß-D-MLGs [Mixed-Linkage Glucans]; chloroplasts per cell, lacking pyrenoids; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles in vegetative cells 0, metaphase spindle anastral, predictive preprophase band of microtubules, phragmoplast + [cell wall deposition spreading from around the spindle fibres], plasmodesmata +; antheridia and archegonia jacketed, stalked; spermatogenous cells monoplastidic; blepharoplast, bicentriole pair develops de novo in spermatogenous cell, associated with basal bodies of cilia [= flagellum], multilayered structure [4 layers: L1, L4, tubules; L2, L3, short vertical lamellae] + 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 dependent on gametophyte, multicellular, embryo initially surrounded by haploid gametophytic tissue, plane of first division horizontal [with respect to long axis of archegonium/embryo sac], early embryo spherical, developing towards the archegonial neck [from epibasal cell, exoscopic], with at least transient apical cell [?level], suspensor/foot +, cell walls with nacreous thickenings; sporangium +, single, terminal, dehiscence longitudinal; meiosis sporic, monoplastidic, microtubule organizing centre associated with plastid, cytokinesis simultaneous, preceding nuclear division, sporocytes 4-lobed, with a quadripolar microtubule system; spores in tetrads, sporopollenin in the spore wall laid down in association with trilamellar layers [white-line centred lamellae], white-line centred lamellae increase in numbers; nuclear genome size <1.4 pg, main telomere sequence motif TTTAGGG, LEAFY and KNOX1 and KNOX2 genes present, precursor for starch synthesis in plastid, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes.
Many of the bolded characters in the characterization above are apomorphies of subsets of streptophytes along the lineage leading to the embryophytes, not apomorphies of crown-group embryophytes per se.
All groups below are crown groups, nearly all are extant. Characters mentioned are those of the immediate common ancestor of the group,  contains explanatory material, () features common in clade, exact status unclear.
Abscisic acid, ?D-methionine +; sporangium tapetum +, secreting sporopollenin, outer white-line centred lamellae obscured by sporopollenin, columella + [developing from endothecial cells], seta developing from basal meristem [between epibasal and hypobasal cells]; stomata +, on sporangium, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and in rhizoids/root hairs; spores trilete; polar transport of auxins and class 1 KNOX genes expressed in the sporangium alone; shoot meristem patterning gene families expressed; MIKC, MI*K*C* and class 1 and 2 KNOX genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns.
[Anthocerophyta + Polysporangiophyta]: archegonia embedded/sunken in the gametophyte; sporophyte long-lived, chlorophyllous; sporophyte-gametophyte junction interdigitate, sporophyte cells showing rhizoid-like behaviour.
Sporophyte branched, branching apical, dichotomous; vascular tissue +; stomata on stem; sporangia several, each opening independently; spore walls not multilamellate [?here].
EXTANT TRACHEOPHYTA / VASCULAR PLANTS
Photosynthetic red light response; plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; (condensed or nonhydrolyzable tannins/proanthocyanidins +); sporophyte soon independent, dominant, with basipetal polar auxin transport; lignins +; G- and S-type tracheids, sieve cells + [nucleus degenerating], tracheids +, in both protoxylem and metaxylem, plant endohydrous [physiologically important free water inside plant]; endodermis +; leaves spirally arranged, blades with mean venation density 1.8 mm/mm2 [to 5 mm/mm2]; sporangia not terminating the main axis, adaxial on sporophylls, derived from periclinal divisions of several epidermal cells, wall multilayered [eusporangium], lacking sporagia; columella 0; tapetum glandular; gametophytes exosporic, green, photosynthetic; basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; placenta with single layer of transfer cells in both sporophytic and gametophytic generations, root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Sporophyte branching ± indeterminate; endomycorrhizal associations + [with Glomeromycota]; root apex multicellular, root cap +, lateral roots +, endogenous; G-type tracheids +, with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangia borne in pairs and grouped in terminal trusses, dehiscence longitudinal, a single slit; cells polyplastidic, microtubule organizing centres not associated with plastids, diffuse, perinuclear; blepharoplasts +, paired, with electron-dense material, centrioles on periphery, male gametes multiciliate; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; LITTLE ZIPPER proteins.
Sporophyte woody; lateral root origin from the pericycle; branching lateral, meristems axillary; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].
Plants heterosporous; megasporangium surrounded by cupule [i.e. = unitegmic ovule, cupule = integument]; pollen lands on ovule; megaspore germination endosporic [female gametophyte initially retained on the plant].
EXTANT SEED PLANTS / SPERMATOPHYTA
Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins particularly with guaiacyl and p-hydroxyphenyl [G + H] units [sinapyl units uncommon, no Maüle reaction]; root stele with xylem and phloem originating on alternate radii, cork cambium deep seated; mitochondrial density in whole SAM 1.6-6.2[mean]/μm2 [interface-specific mitochondrial network]; stem with vascular cylinder around central pith [eustele], phloem abaxial [ectophloic], endodermis 0, xylem endarch [development centrifugal]; 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; 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, blade simple; plant heterosporous, sporangia borne on sporophylls, sporophylls spiral; 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; megasporangium indehiscent; ovules with parietal tissue 2+ cells across, megaspore tetrad linear, functional megaspore single, chalazal, sporopollenin 0; gametophyte development initially endosporic, dependent on sporophyte, apical cell 0, rhizoids 0, development continuing outside the spore; 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, plane of first cleavage of zygote transverse, shoot apex developing away from micropyle [i.e. away from archegonial neck; from hypobasal cell, endoscopic], suspensor +, short-minute, embryonic axis straight [shoot and root at opposite ends; plant allorhizic], cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, whole nuclear genome duplication [ζ - zeta - duplication], two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], nrDNA with 5.8S and 5S rDNA in separate clusters; mitochondrial trans- nad2i542g2 and coxIIi3 introns present.
ANGIOSPERMAE / MAGNOLIOPHYTA
Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANA grade?], lignin also with syringyl units common [G + S lignin, positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], hemicelluloses as xyloglucans; root apical meristem intermediate-open; root vascular tissue oligarch [di- to pentarch], lateral roots arise opposite or immediately to the side of [when diarch] xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0, hypodermis suberised and with Casparian strip [= exodermis +]; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, associated gelatinous fibres [g-fibres] with innermost layer of secondary cell wall rich in cellulose and poor in lignin; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, cytoplasm not occluding pores of sieve plate, companion cell and sieve tube from same mother cell; sugar transport in phloem passive; nodes 1:?; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance to 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 spiral [esp. the A], free, numbers unstable, development in general centripetal; P +, members each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], sporangium pairs dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, endothecium +, endothecial cells elongated at right angles to long axis of anther; (tapetum glandular), cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine lamellate only in the apertural regions, thin, compact, intine in apertural areas thick, pollenkitt +; nectary 0; carpels present, superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus at most short [shorter than ovary], hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry, 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 [crassinucellate], nucellar cap?; megasporocyte single, hypodermal, functional megaspore lacking cuticle; female gametophyte lacking chlorophyll, not photsynthesising, four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; ovule not increasing in size between pollination and fertilization; pollen grains land on stigma, bicellular at dispersal, mature male gametophyte tricellular, germinating in less than 3 hours, pollen tube elongated, unbranched, growing between cells, growth rate (20-)80-20,000 µm/hour, apex of pectins, wall with callose, lumen with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametes lacking cell walls, cilia 0, siphonogamy; double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; mature seed much larger than ovule when fertilized, small , dry [no sarcotesta], exotestal; endosperm +, cellular, development heteropolar [first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous; dark reversal Pfr → Pr; Arabidopsis-type telomeres [(TTTAGGG)n]; nuclear genome very small [1C = <1.4 pg, 1 pg = 109 base pairs], whole nuclear genome duplication [ε - epsilon - duplication]; protoplasm dessication tolerant [plant poikilohydric]; 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]]]]: vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood + [with gelatinous fibres: lignified primary cell wall + thick gelatinous wall]; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; carpels plicate; 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 [possible position]; pollen tube growth intra-gynoecial [extragynoecial compitum 0]; embryo sac bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid.
[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (extra-floral nectaries +); (veins in lamina often 7-17 mm/mm2 or more [mean for eudicots 8.0]); (stamens opposite [two whorls of] P); (pollen tube growth fast).
[CERATOPHYLLALES + EUDICOTS]: ethereal oils 0.
EUDICOTS: (Myricetin, delphinidin +), asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; (vessel elements with simple perforation plates in primary xylem); nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; protandry common; K/outer P members with three traces, ("C" +, with a single trace); A ?, filaments fairly slender, anthers basifixed; microsporogenesis simultaneous, pollen tricolpate, apertures in pairs at six points of the young tetrad [Fischer's rule], cleavage centripetal, wall with endexine; G with complete postgenital fusion, stylulus/style solid [?here]; seed coat?
[PROTEALES [TROCHODENDRALES [BUXALES + CORE EUDICOTS]]]: (axial/receptacular nectary +).
[TROCHODENDRALES [BUXALES + CORE EUDICOTS]]: benzylisoquinoline alkaloids 0; euAP3 + TM6 genes [duplication of paleoAP3 gene: B class], mitochondrial rps2 gene lost.
[BUXALES + CORE EUDICOTS]: ?
CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one place]; micropyle?; γ whole nuclear genome duplication [palaeohexaploidy, gamma triplication], PI-dB motif +, small deletion in the 18S ribosomal DNA common.
[ROSIDS ET AL. + ASTERIDS ET AL.] / PENTAPETALAE: root apical meristem closed; (cyanogenesis also via [iso]leucine, valine and phenylalanine pathways); flowers rather stereotyped: 5-merous, parts whorled; P = calyx + corolla, the calyx enclosing the flower in bud, sepals with three or more traces, petals with a single trace; stamens = 2x K/C, in two whorls, internal/adaxial to the corolla whorl, alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G , G  also common, when [G 2], carpels superposed, compitum +, placentation axile, style +, stigma not decurrent; 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).
[SANTALALES [BERBERIDOPSIDALES [CARYOPHYLLALES + ASTERIDS]]] / ASTERIDS ET AL. / SUPERASTERIDS : ?
[BERBERIDOPSIDALES [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?; (nectary gynoecial); G , style single, long; ovules unitegmic, integument thick, endothelium +, nucellar epidermis does not persist; exotestal [!: even when a single integument] cells lignified, esp. on anticlinal and/or inner periclinal walls; endosperm cellular.
[ERICALES [ASTERID I + ASTERID II]]: (ovules lacking parietal tissue) [tenuinucellate].
[ASTERID I + ASTERID II] / CORE ASTERIDS: ellagic acid 0, non-hydrolysable tannins not common; sugar transport in phloem active; inflorescence basically cymose; A = and opposite sepals or P, (numerous, usu. associated with increased numbers of C or G); style short[?]; duplication of the PI gene.
ASTERID I / LAMIIDAE: loss of introns 18-23 in d copy of RPB2 gene.
[METTENIUSALES [GARRYALES [GENTIANALES, VAHLIACEAE, SOLANALES, BORAGINALES, LAMIALES]]]: ?
[GARRYALES [GENTIANALES, VAHLIACEAE, SOLANALES, BORAGINALES, LAMIALES]]: G , superposed; loss of introns 18-23 in RPB2 d copy.
[GENTIANALES, VAHLIACEAE, SOLANALES, BORAGINALES, LAMIALES]: (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.
[[VAHLIACEAE + SOLANALES] [BORAGINALES + LAMIALES]]: chalazal endosperm haustorium +.
[BORAGINALES + LAMIALES]]: iridoids 0; inflorescence cymose; placentation parietal.
Age. The age of this node is estimated to be around 88.2 m.y. by Magallón et al. (2015) or (105-)97(-88) m.y. (Wikström et al. 2015).
Evolution. Divergence & Distribution. How characters are going to be optimised along this part of the tree is unclear. Lack of bracteoles, deeply divided styles, etc., could all be placed somewhere around here. For the complex pattern of variation in a number of other characters in this part of the tree, see the Gentianales page.
Chemistry, Morphology, etc. For other characters of potential phylogenetic interest, see above.
Phylogeny. For the relationships of Boraginales, see Refulio-Rodriguez and Olmstead (2014), and discussion under Gentianales.
BORAGINALES Berchtold & J. Presl, nom. cons. Main Tree.
Plant ± herbaceous; (pyrrolizidine alkaloids +); root lacking hypodermis [2 records]; (nuclear crystalloids in sieve tubes); (cork mid-cortical to pericyclic); (silicon concentration high [?level; see hairs]); (vessel elements with scalariform perforation plates); sieve tubes with nuclear non-dispersive protein bodies; petiole bundle(s) arcuate; plant ± roughly hairy, hairs with a basal cystolith or cystolith-like body, walls calcified or silicified; leaves spiral; inflorescences terminal, cyme scorpioid, ± circinate, (bracteoles 0); K free, C tube formation late; anther placentoid 0; (pollen with pseudocolpi), colporate; nectary not vascularized; placentation intrusive parietal, (heterostyly +), stigma dry; ovules many/carpel; K persistent; chalazal endosperm haustorium +, cotyledons accumbent[?]. 6 families, 148 genera, 2755 species. [Photos - Collection.]
Age. Wikström et al. (2001) estimate the age for Boraginales as (63-)59, 56(-52) m.y.; the age is (73-)57, 54(-39) m.y. in Bell et al. (2010) and rather older, (87.7-)72.6(-54.3) m.y., in Nazaire et al. (2014) and (88.4-)67.9(-46.4) m.y. in Naumann et al. (2013).
Note: (....) denotes a feature common in the clade, exact status uncertain, [....] includes explanatory material. Possible apomorphies are in bold. However, the actual level at which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is partly because many characters show considerable homoplasy, in addition, basic information for all too many 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. The diversification of primarily woody boraginalean taxa may have taken place in the mid-Cretaceous, some 90 m.y.a., in South America (Gottschling et al. 2004), however, many ages estimates there seem overly high. Moore and Jansen (2006) suggest rather later dates, with the very end Cretaceous at 67-63 m.y. being a date for the diversification of the woody taxa.
The removal of Codon from Hydrophyllaceae makes biogeographical sense; it was the only genus endemic to Africa in that family under its old circumscription, and Wellstedia, the next branch of that part of the tree where it now resides, is also African.
Pollination Biology. Pseudocolpi and other features of the pollen appear to be involved in harmomegathic movements of the walls of the pollen grains (Volkova et al. 2013).
Plant-Animal Interactions. Boraginales are not often eaten by caterpillars (Ehrlich & Raven 1964). However, Boraginaceae and Heliotropaceae are visited by adult lepidoptera that use the pyrrolizidine alkaloids they contain as a basis for their pheromones (see Heliotropaceae). Pyrrolizidine alkaloids and pentacyclic triterpene saponins variously sequestered and modified are found in the secretions of the defensive glands of some Chrysolina and Platyophora beetles (Chrysomelidae, both very speciose genera: Pasteels et al. 2001; Termonia et al. 2002; Hartmann et al. 2003).
Bacterial/Fungal Associations. Holm (1979) noted that some Boraginoideae and Hydrophyllaceae have similar rusts.
Chemistry, Morphology, etc. The homospermidine synthase gene, the first gene in the pathway that leads to pyrrolizidine alkaloids, has diverged considerably from the deoxyhypusine gene, from which it is derived, and this suggests an ancient separation of the two (Nurhayati et al. 2009). Taxa with root trichoblasts in radial files are quite common in Boraginales.
Floral evolution shows much of interest in this group, although lacking both a well-supported phylogeny as well as developmental studies of the more distinctive flowers, details remain poorly known. Three unrelated clades have flowers that are not the normal 5-merous asterid flower. These include Codon (10-12-merous), Hoplestigma, and Lennoa and relatives (see also the euasterid). The first two of these have many more stamens and petals than normal, but a simple bicarpellate gynoecium; Lennoa and relatives also show an increase in carpel number. Both the petals and stamens of Hoplestigma are described as being in several series (Goldberg 1986), and its floral morphology and development would clearly repay investigation.
There are usually many veins diverging in the corolla lobes of Boraginales, but not in Wellstedia. A variety of septal structures are produced in this group (see Gottschling 2004). The style in at least some Boraginaceae and Hydrophyllaceae apears to be hollow (Guéguen 1901). There is considerable variation in ovule and endosperm development in Boraginales, conveniently summarized by Khaleel (1985). The extent of development of parietal tissue in the ovules is unclear - Boraginaceae, for example are tenuinucellate, while Ehretiaceae and Heliotropaceae show development of parietal tissue, Hydrophyllaceae s. str. may have both conditions (e.g. Di Fulvio 1981, 1987; c.f. Gottschling 2004; Berg 2009). Suspensor size in the embryo varies considerably, and it may be haustorial (e.g. Lloyd 1899, 1902).
Boraginaceae are well known to have a gynobasic style, and it has also been suggested that the terminal style of Heliotropaceae, at least, may be derived from the gynobasic condition: In the latter the pollen transmitting tissue proceeds to the base of the gynoecium (e.g. Hanf 1935).
Since Boraginaceae often included Heliotropaceae, etc., and Hydrophyllaceae included an even greater variety of taxa, much literature on Boraginaceae and Hydrophyllaceae in particular refers to more than one family as circumscribed below. For additional literature, see Al-Shehbaz (1991) and Gürke (1891), both general, Aniszewski (2007: alkaloids), Hartmann and Witte (1995) and Reimann et al. (2004), both pyrrolizidine alkaloids, Gunstone (1992) and Velasco and Goffman (1999), fatty acids, esp. gamma linolenic acid, but not restricted to Boraginoideae, Fisher et al. (1989), sieve tubes with massive nuclear ?protein bodies, not always present in families other than Boraginaceae, Buys and Hilger (2003: inflorescence morphology), Prósperi and Cocucci (1979: callose in pollen tube variable in Hydrophyllaceae s.s., sampling needs to be extended), Diane et al. (2002b: transfer cells in seeds), Guignard (1893) and Svensson (1925), both embryology, and di Fulvio (1991: protein inclusions in nucleus). For Hydrophyllaceae s.l., see Brand (1913) and K. A. Wilson (1960), both general, di Fulvio 1997 (floral vasculature), Constance and Chuang (1982: pollen), and Constance (1963: chromosome numbers).
Phylogeny. Wellstedia and Codon (ex Hydrophyllaceae), both African, are clades successively sister to Boraginaceae. Thus the latter linked with Boraginaceae in Moore and Jansen (2006) and both linked with Boraginoideae in Ferguson (1999), Luebert and Wen (2008), and in the comprehensive studes of Weigend et al. (2013a, see also 2013b) and Nazaire et al. (2014: Suppl. Fig. 4B).
Two groups of ex Hydrophyllaceae are successive sister taxa within the other major clade in some reconstructions; Nameae in particular may be sister to the [Cordioideae + Heliotropoideae + Ehretioideae] clade (Olmstead & Ferguson 2001; Moore & Jansen 2006: low bootstrap but high p.p. values; Luebert & Wen 2008). Nameae include the only woody and tropical members of Hydrophyllaceae s. str. (i.e., excluding Hydrolea, see below). The relationships of Hydrophyllaceae were unclear in Weigend et al. (2013a), although this was not the focus of their study; there was weak support for their polyphyly in Weigend et al. (2013b). Gottschling et al. (2001), looking at the secondary structure of the ITS1 transcript, found Hydrophyllaceae s. l. to be monophyletic (within these, Nameae were paraphyletic) and sister to a clade [Heliotropiaceae [Cordiaceae + Ehretiaceae]], all with some support. Nazaire and Hufford (2012) sampled the whole Boraginales in the course of placing Mertensia. [[Boraginaceae + Codonaceae] [Hydrophyllaceae mono- or paraphyletic + the rest]], but support was not strong (see also Nazaire et al. 2014: Suppl. Fig. 4A). Within a monophyletic Hydrophyllaceae s.l., again Nameae might be paraphyletic. Heliotropoideae were sometimes polyphyletic (see also Weigend et al. 2013b), while the grouping [Cordiaceae + Ehretiaceae] had some support in Weigend et al. (2013b). Refulio-Rodriguez and Olmstead (2014) found moderate support for the relationships [Hydrophyllaceae [Nameae [Heliotropaceae [Cordiaceae + Ehretiaceae]]]]; see also (Cohen 2014: sampling slight, but general relationships not the focus) and Nazaire et al. (2014: Suppl. Fig. 4A) for the final threesome. Boraginaceae and Hydrophyllaceae also have meroterpenoids, rusts (see above) and very variable endosperm development in common - all plesiomorphic?? See also Ferguson (1999) for relationships of Hydrophyllaceae s.l..
The holoparasitic Lennooideae/Lennoaceae are often associated with Boraginaceae and/or Hydrophyllaceae (Cronquist 1981; Takhtajan 1997; esp. Yatskievych et al. 1986), and a position within Ehretiaceae seems likely, although they have very long branches. Both Ehretia + Lennoaceae have a shared intron in the mitochondrial gene cox1, and Tiquilia in particular has been placed as sister to Pholisma by Smith and dePamphilis (1998; see also Smith et al. 2000; Olmstead & Ferguson 2001; Hardy & Cook 2012; Nazaire & Hufford 2012: some analyses; Weigend et al. 2013b), although support values are often rather low, and a position sister to the rest of the family is possible (see also Nazaire et al. 2014: Suppl. Fig. 4A).
Classification. Given the suggested position of Boraginaceae s.l. as sister to Lamiales (Refulio-Rodriguez & Olmstead 2014), and the quite distinctive morphology of the group, ordinal status seems appropriate, with the major clades given family status. Family names have been given to clades in this part of the tree (e.g. Weigend & Hilger 2010), and Weigend et al. (2013b) and others provide a phylogeny on which to hang them; Cohen (2014) discusses the neeed to recognize Codonaceae and Wellstediaceae if Boraginaceae are to have featurees characterising them.
Previous Relationships. No putative relative of Boraginaceae s. l. has alkannin or pyrrolizidine alkaloids. Boraginaceae/Boraginales have sometimes been associated with Lamiaceae (Lamiales) because both often have gynobasic styles and fruits with four separate nutlets, but the latter have iridoids, opposite leaves, square (not rounded) stems, monosymmetric flowers usually with 4 stamens, endosperm with haustoria and embryo with a long suspensor - the two are not close. Furthermore, the radicle in Boraginaceae points upwards in fruit, while in Lamiaceae it points downwards. In previous classifications the woody Verbenaceae with a terminal style were separated from a more or less herbacous Lamiaceae with a gynobasic stye, almost a parallel between a herbaceous Boraginaceae s. str with a gynobasic style and the rest, more often woody and with a terminal style.
Pteleocarpa, with vestured pits, was usually included in Boraginaceae s.l., but it is here placed in Gelsemiaceae (Gentianales). Hydrolea, ex Hydrophyllaceae but with axile placentation, is here to be found in Solanales as Hydroleaceae.
Although members of this group were previously thought to be related, the main division within them was thought to be between a Hydrophyllaceae s.l., with parietal placentation and capsular fruits, and Boraginaceae s.l., with ovaries that usually had four ovules and fruits that were usually indehiscent.
Thanks. I am grateful to Mark Gottschling for discussion, and also the tree used here.
Includes Boraginaceae, Codonaceae, Cordiaceae, Ehretiaceae, Heliotropiaceae, Hydrophyllaceae, Nama, etc., Wellstediaceae.
Synonymy: Cordiales Martius, Echiales Lindley, Ehretiales Martius, Hydrophyllales Martius - Boraginanae Doweld
[Codonaceae [Wellstediaceae + Boraginaceae]]: ?
CODONACEAE Weigend & Hilger Back to Boraginales
Subshrubs; ?chemistry; plant prickly-hairy; flowers 10-12-merous; K deeply linear-lobed, C broadly campanulate, with flaps near filament bases; pollen tricolpate, without pseudocolpi; style deeply bilobed; testa reticulate-papillate; endosperm copious; n = 17.
1[list]/2. S.W. Africa (map: see Retief et al. 2005).
Chemistry, Morphology, etc. For additional information, see Retief and van Wyk (2005), and Weigend and Hilger (2010).
[Wellstediaceae + Boraginaceae]: ovules 2/carpel, apical, pendulous.
WELLSTEDIACEAE Novák Back to Boraginales
Small shrubs; ?chemistry; inflorescences in two ranks along the branches; flowers four-merous; C lobes three-veined, C tube eight veined; pollen 12-25 x 8-15 µm, exine perforate to reticulate, tricolporate, pseudocolpi +, mesocolpium coarse-reticulate; style bifid, wet; ovule one/carpel, ?epitropous; fruit septae may separate from the walls; seed with fringe of downwardly-pointing hairs from near the apex; embryo curved, cotyledons accumbent, endosperm 0; n = ?
1[list]/5. S.W. and N.E. Africa (map: see Thulin & Johansson 1996; Reteif & van Wyk 2008).
Evolution. Pollination Biology & Seed Dispersal. Wellstedia is a tumbleweed (?all species), and its capsules open only when wetted (Thulin & Johansson 1996).
Chemistry, Morphology, etc. The field notes of Goldblatt & Manning 8763 describe the flowers as being "filled with nectar", however, Retief and van Wyk (2008) noted that there was no disc; where is the nectar secreted? Thulin and Johansson (1996) described the capsule of Wellstedia as being septifragal, Reteif and van Wyk (2008) as being loculicidal; the latter appear to be correct. The ovule has a distinctive shape caused by a chalazal projection (e.g. Reteif & van Wyk 2008). It would be interesting to know details of embryology and seed development.
Previous Relationships. Wellstedia was often associated with Coldenia (now Cordiaceae), largely, it seems, because both have 4-merous flowers.
BORAGINACEAE Jussieu, nom. cons. Back to Boraginales
Annual to perennial herbs (shrubs); prenylated (naphthoquinones [e.g. alkannin, reddish or purple dye] +), gamma-linolenic acid, (pyrrolizidine alkaloids), (meroterpenoids) +, stem storage polysaccharides isokestose and higher inulin oligosaccharides [fructans] (with starch; none in annuals); leaves with midvein alone obvious; one (or both) bracteoles 0; (flowers monosymmetric); corolla funneliform, lobes spreading, mouth with inpushings of corolla tube [faucal appendages or fornices, morphology variable] (0); anther connective produced or not; tapetal cells multinucleate, or nucleus polyploid; pollen grains tricellular, 2-5-porate; ovary with secondary septae, style gynobasic, hollow, (branched), stigma punctate to capitate; ovule with integument 7-12 cells across, integument vascularized, (nucellar cap +), placental obturator +, (hypostase +); fruit a schizocarp, nutlets (1-)4, with basal attachment, exocarp sclerified, (elaiosomes +); testa (vascularized), exotestal cells with outer walls thickened and lignified (other patterns of thickening, or unthickened), most other cells disappear; endosperm oily or 0, also nuclear, haustoria 0, suspensor short or 0 [?level]; n = (4-)12(-13), (protein inclusions in nucleus).
110[list]/1595 - four groups below. Largely (north (warm) temperate, some on mountains in the tropics (map: see Wickens 1976; Meusel et al. 1978; Hultén & Fries 1986; Böhle et al. 1996; Långström & Chase 2002; FloraBase 2005; Wiegend et al. 2010: still incomplete).
Age. The age of this node is estimated at some 43 m.y. (56-30 m.y.) ago (Weigend et al. 2009), or substantiallyolder, (76.9-)63.5(-46.5) m.y., by Nazaire et al. (2014).
1. Echiochileae Långström & M. W. Chase
Corolla with abaxial trichomes; pollen not ellipsoid [oblate-square, triangular-prism]; (nutlets with non-basal attachment).
[Cyngolosseae [Boragineae + Lithospermeae]]: (flowers heterostylous); corolla salverform, with "glands" inside.
2. Cynoglosseae W. D. J. Koch
(Basal leaves +); vestured pits +; lamins with evident secondary venation; floral bracts 0 (+); flowers polysymmetric; corolla with faucal appendages; anther epidermis with fibrous thickening [Mertensia]; tapetal cells uninucleate; (pollen grains 6-8 porate), (pseudocolpate [heterocolpate]); (G lacking secondary/false septum); nutlets with non-basal attachment, (glochids, marginal wings or other ornamentation +).
Cryptantha (160), Myosotis (90), Cynoglossum (75), Paracaryum (70), Plagiobothrys (70), Amsinckia (50), Mertensia (50), Trigonotis (50).
Synonymy: Cynoglossaceae Döll
Age. Crown-group Cynoglosseae are estimated to be (38.3-)31.1(-23.2) m.y.o. (Nazaire et al. 2014).
[Boragineae + Lithospermeae]: ?
3. Boragineae Reichenbach
Basal leaves + (0); (floral bracts 0); corolla with faucal appendages.
Synonymy: Anchusaceae Vest
4. Lithospermeae Dumortier
Corolla often urceolate or funnelform, faucal appendages usu. 0, commonly with abaxial trichomes, rarely with "glands" inside; n = 6+.
Onosma (150), Lithospermum (70), Echium (60).
Synonymy: Buglossaceae Hoffmannsegg & Link nom. illeg., Cerinthaceae Berchtold & Presl, Echiaceae Rafinesque, Onosmaceae Martynov
Evolution. Divergence & Distribution. Weigend et al. (2013a) suggested that Boraginaceae are likely to have originated in the Africa-West/Central Asia area, where its immediate outgroups and Echiochileae, sister to the rest of the subfamily, are to be found. As Weigend et al. (2013a) emphasized, extant members of the subfamily are predominantly Asian(-European), including eastern Asia; taxa elsewhere are clearly derived. Thus the South American Moritzia and Thaumatocaryon, the only Boragineae in the New World, are sister taxa, and are in turn sister to all other Boragineae, which are largely Eurasian; interestingly, there are fossils from North America of late Miocene age that are assignable to this clade, so filling the distributional gap (Weigend et al. 2010).
Nazaire et al. (2014, q.v. for dates) discussed biogeographical relationships within the Asian-North America Mertensia. There have been a number of New World intercontinental dispersal events within Cryptantha s.l., nearly all in the north → south direction (Hasenstab-Lehman & Simpson 2012, see also Guilliams & Baldwin 2011). There are other distributions like this in Boraginales, and the lopsided directionality of such events seems to be connected with the behaviour of the migrating birds that are likely to have dispersed the fruits. the 40-plus species of Myosotis in New Zealand are morphologically very diverse - caespitose, rosette-forming, etc., flowers yellow, white, or blue, stamens exserted or not - yet there is very little resolution between them in molecular studies (Meudt et al. 2015a; see also Winkworth et al. 2002).
Weigend et al. (2013a) give further details of the evolution and diversification of Boraginaceae, especially Cynoglosseae s.l., while Cohen (2014) discusses the evolution of numerous morphological characters in the context of the phylogeny of the family.
Echium is a good example of "island woodiness", and here woody, more or less tree-like (up to 3 m tall) and sometimes monocarpic species have evolved on Macaronesia from herbaceous ancestors. Divergence within Echium may have begun some 20.6 m.y.a., but the Macaronesian diversification - there seem to have been two reversions to the herbaceous habit, and the majority of the species are on the Canary Islands - can be dated to a mere (6.3-)3.9(-1.5) m.y.a. (Böhle et al. 1996; Stöcklin 2011; García-Maroto et al. 2009: see Mansion et al. 2009 for other Mediterranean insular endemic Boraginaceae).
Pollination Biology & Seed Dispersal. Pollination is predominantly by insects, although bumble bees seem to avoid collecting pollen from Boraginaceae in the U. K., at least (Goulson 2010). North temperate megachilid osmiine bees like Hoplitis species of the Annonosmia-Hoplitis group collect pollen from concealed-pollen flowers of this family and/or members of Fabaceae-Faboideae. This odd pairing is perhaps because both groups of plants have pyrrolizidine alkaloids and/or nutrients that are essential for larval development of the bees (Sedivy et al. 2013). Basal Halictidae pollinate Boraginaceae (and Hydrophyllaceae: Patiny et al. 2008).
In Boraginaceae the corolla often changes colour as it ages, pink to blue, yellow to pink to blue, yellow to white, and so on; p.H. changes of the cell sap are involved in the shift pink to blue, and perhaps cell turgor changes in the shift of the colour of the "eye" of the flower from yellow to white (Weiss 1995; Nuttman & Wilmer 2008). Such changes seem to affect pollinator behaviour (Casper & La Pine 1984; Nuttman & Wilmer 2008 and references). In a number of taxa buzz pollination occurs; nectar is also produced by these flowers (Teppner 2011). Heterostyly also occurs in some Boraginaceae, and it has evolved at least 12 times here (Cohen et al. 2012; Cohen 2014). Lithospermum, one of the heterostylous genera, has undergone large increases and decreases in corolla tube length (Cohen 2012). Finally, in Echium pollen is displayed in hairs that develop from tissue between the sporangia (Hesse et al. 2000).
Nutlets of Boragineae may have elaiosomes and are then dispersed by ants, while in taxa like Cynoglossum the nutlets have glochids and are dispersed in the fur of larger animals (Selvi et al. 2011). Some species of the large genus Cryptantha, especially diverse in western North and South America, have inflorescences with basal, cleistogamous flowers and non-dispersing fruits (Grau 1983).
Chemistry, Morphology, etc. Fructans are absent in annual species but also in the perennial Alkanna; starch may sometimes also be present (Bourdu 1957; Meier & Reid 1982).
Trichodesma has opposite leaves and the pendulous and campanulate flowers are borne in a congested inflorescence at the end of a rather long peduncle. Echium has obliquely monosymmetric flowers, while the flowers of some species of Nonea may be vertically monosymmetric, the abaxial stamen being much longer than the others (the flowers of Echiochilon are also monosymmetric - I would guess obliquely so); the flowers of Cerinthe have an oblique plane of symmetry (Selvi et al. 2009), although the flowers are functionally polysymmetric. With pollen grains at ca 4.1 µm long, Cryptantha clevelandii has about the smallest grains of any flowering plant (Hargrove & Simpson 2003). Amsinckia has very strongly bilobed cotyledons.
See Rabaey et al. (2010: vestured pits, ± correlations with clades), Carke (1977), Weigend et al. (2009) and Bigazzi and Selvi (1998: Boragineae) for pollen morphology, Y. Heslop-Harrison (1981) and Bigazzi and Selvi (2000) for the morphology of stigma papillae, Millsaps (1940) and Khaleel (1977a) for embryology, Hilger (1985, 2014: Cynoglosseae), Seibert (1978: Lithospermeae), Ovczinnikova (2007 and references) and Simpson and Hasenstab (2009: Cryptantha, see the cover photograph!) for fruit morphology and development, and Almasi and Ranjbar (2013: chromosomes in Onosma).
Phylogeny. Långström and Chase (2002) discussed tribal relationships within Boraginaceae. Nazaire and Hufford (2012; see also Cohen 2011a; Nazaire et al. 2014: Suppl. Fig. 4B) found quite good support for the relationships [Echiochileae [Cynoglossseae [Boragineae + Lithospermeae]]], the position of Echiochileae having the least support, and in the detailed study of Weigend et al. (2013a) and especially Cohen (2014) the same general relationships, including the position of Echiochileae, were recovered.
The monophyly of Cynoglosseae is quite well supported, yet it includes representatives of just about all tribes of Boraginaceae ever described (Nazaire & Hufford 2012). Weigend et al. (2013a, see also Selvi et al. 2011; Nazaire & Hufford 2012) found that Omphalodes and in particular Cynoglossum were highly para/polyphyletic, clades with species currently included in both Cynoglossum and Paracynoglossum may even have arisen independently. Nazaire et al. (2014), focusing on Mertensia, found a largely Asian and a largely North American clade; the Beringian M. rivularis was sister to the latter. Within Myosotis, the Antipodean species are derived; although morphologically and palynologically very diverse they show little divergence at the molecular level (Winkworth et al. 2002: sections not monophyletic; Meudt et al. 2015a). Huang et al. (2013) discuss relationships within Lappula.
Within Lithospermeae, the limits of Lithospermum itself are to be extended (Weigend et al. 2009; Cohen & Davis 2009a, esp. b, 2012), however, the tree was poorly supported and the addition of relatively few (22) morphological characters had a major effect on support values and some on topology (Cohen & Davis 2011). Vegetative and floral features are highly homoplastic when optimised on the tree (Cohen & Davis 2011). For the limits of Lithospermeae, see also Saadati et al. (2011); Lithodora is polyphyletic (Thomas et al. 2008). For the phylogeny of insular Echium, see García-Maroto et al. (2009).
Within Boragineae, Trigonotidae are to be completely dismembered, its two South American genera being sister to the Eurasian Boragineae (Weigend et al. 2010). For relastionships within Myosotis, see Winkworth et al. (2002) and Meudt et al. (2015a: New Zealand species).
Generic limits need much attention. Hasenstab-Lehman and Simpson (2012) adjusted the limits of Cryptantha; genera like Lithosperma, Trigonotis and Anchusa are polyphyletic (e.g. Nazaire & Hufford 2012). The limits of Lithospermum have been adjusted, but the relationships of names to clades around there is still unclear (Cohen & Davis 2009b; Cohen 2011b). The findings of Weigend et al. (2013a) point out the immediate need for a generic reclassification of Cynoglosseae s.l., while Cohen (2014) found that genera like Myosotis, Anchusa and Cynoglossum were not monophyletic.
Classification. Broad limits for Cynoglosseae are followed above; if a Trichodesmeae are recognised (as in Cohen 2014), the monophyly of remaining Cynoglosseae is unclear, and anyhow it is a very small clade with just a couple of genera.
[Hydrophyllaceae [Nameae [Heliotropiaceae [Cordiaceae + Ehretiaceae]]]]: (plant smells unpleasantly); tapetal cell nucleus number?; testa with single layer of transfer cells [cells with labyrinthine ingrowths of the wall]; endosperm with both chalazal and micropylar haustoria; suspensor long.
HYDROPHYLLACEAE R. Brown, nom. cons. Back to Boraginales
Annual to perennial herbs; (meroterpenoids), inulin?, alkaloids?; (mycorrhizae 0); ?cork; (vascular bundles separate); (stinging hairs - Phacelia); leaves (opposite; compound), margins lobed, toothed (entire), secondary veins pinnate (palmate); (flowers axillary); bracts and bracteoles usu. 0; (K free), (C contorted), (lobes serrate); A usu. with small (lobed) scales at each side of the filament base; pollen tricolpate, (pseudocolpi +), (tubes lacking callose); placentae swollen, style ± divided (to the base), stigma punctate (capitate); ovules (2-), (pleurotropous), integument ca 6 cells across, parietal tissue 0; (embryo sac with a chalazal haustorium - Nemophila); (fruit a loculicidal + septicidal capsule), (indehiscent); (seeds ruminate), (chalazal elaiosome +); exotestal cells thickened on inner and radial walls, (largely disappearing - Nemophila), endotestal cells persistent, walls esp. the inner periclinal ± thickened; endosperm also nuclear, copious to scanty, (chalazal haustoria 0), haustoria with lateral projections, (reserve hemicellulose), embryo (short), green or white; n = (5-)8-13, etc..
11[list]/240: Phacelia (210). Western North and South America, esp. drier areas of southwestern North America (map: see Brummitt 2007; Heckard 1963). [Photo - Undetermined Flower.]
Evolution. Seed Dispersal. Myxospermy is reported from Hydrophyllaceae (Grubert 1974).
Chemistry, Morphology, etc. Acicular protein bodies are found in the nuclear remnants in the sieve tubes of Hydrophyllaceae.
The mesocolpium is coarse-reticulate, as in some Boraginaceae (Wagenitz 1992). Cronquist (1981) suggested that Hydrophyllaceae lacks nectaries, but nectaries that are either raised and annular or are swellings at the base of the ovary wall are often described ((di Fulvio 1997; Hoffmann 1999; di Fulvio et al. 1999). The various structures so common in the corolla tube at about the level of stamen insertion presumably have something to do with guiding the pollinator to a nectar source! The tenuinucellate condition seems to be common for ovules here (e.g. Berg 2009)
For embryology, see di Fulvio (1989a, 1993), for seed morphology, see Chuang and Constance (1992), and for chromosomes in Phacelia, see Walden et al. (2014).
Phylogeny. Walden et al. (2014: sampling quite good) outlined the phylogeny of Phacelia. Romanzoffia was sister to Phacelia, and within the latter subg. Pulchellae sensu restricto was sister to the rest, albeit with poor support.
Synonymy: Ellisiaceae Berchtold & J. S. Presl, Eutocaceae Horaninow
[Nameae [Heliotropiaceae [Cordiaceae + Ehretiaceae]]]: ?
Nama, etc. Back to Boraginales
Annual to perennial herbs and shrubs (rhizomatous) to small trees; inulin?, alkaloids?; (mycorrhizae 0); leaf margins toothed to entire, secondary veins pinnate; bracts and bracteoles usu. 0; (K free); A usu. without small scales at the base; pollen tricolporate, ?pollen tube callose; tapetal cells 2-nucleate; G (seminferior), placentae ± narrow, (base of g 1, falsely 4-locular), style divided to the base (ca half way), stigma capitate-funneliform or punctate; ovules (2-), epi- and apotropous, integument 6-12 cells across, parietal tissue ca 1 cell layer across; (embryo sac bisporic [the chalazal dyad], 8-nucleate [Allium type]); fruit a loculicidal (+ septicidal) capsule, (indehiscent); (seeds ruminate by inpushings of the exotestal cells), exotestal cells thickened on inner and radial walls, endotestal cells persistent, walls esp. the inner periclinal, ± thickened; endosperm also nuclear, chalazal and micropylar haustoria?, copious to scanty, (reserve hemicellulose), embryo (short), green or white; n = 7, 14 17-18, (protein inclusions in nucleus).
4[list]/58: Nama (60). Southwest North America, Central America and western South America, Antilles, Hawaii (map: see Brummitt 2007; Heckard 1963). [Photo - Undetermined Flower.]
Chemistry, Morphology, etc. Nectaries are to be found at the base of the ovary in the ovary wall, and the number (1, 3) or vascular bundles varies (di Fulvio et al. 1997). Di Fulvio (1989a) described the ovules of Nama as being crassinucellate, but from the information given there can only be a single cell layer below the epidermis there.
For floral morphology, see Hilger (1987), for embryology, see di Fulvio (1993), for seed coat morphology, see Chance and Bacon (1984) and Bacon et al. (1986).
[Heliotropiaceae [Cordiaceae + Ehretiaceae]]] / Primarily Woody Boraginaceae: trees or shrubs; bark oxidises; pollen tubes lacking callose; ovary with secondary septae, transfer cells in funicle and placenta also; ovules 2/carpel, epitropous [check], parietal tissue 1(2) cells across, (nucellar cap ca 2 cells across); fruit a schizocarp, or indehiscent, with a multilayered lignified endocarp; endosperm cellular.
HELIOTROPIACEAE Schrader, nom. cons. Back to Boraginales
(Herbs, lianes); (pyrrolizidine alkaloids +); cambium not storied; pericyclic sheath 0 [?always]; pits not vestured (+); petiole bundles arcuate; (tetrahedral crystals +); leaves usu. conduplicate [Tournefortia]; C imbricate or with involute margins, (contorted); A connate at apex via papillae, connective produced; tapetal cells binucleate; pollen (4 colporate), (porate); style much swollen apically (0), stigma receptive only basi-laterally, discoid, then conical and ± bilobed at sterile apex, or hemispherical, with a ring of hairs, stigma wet; ovules with integument (?3-)8 cells across, (obturator +); fruit a schizocarp, (drupe with 4, 1-seeded stones); seed exotestal; endosperm 0 (slight) at maturity, ?haustoria, embryo curved or straight, cotyledons large, suspensor long; n = 5, 7-9, 11-14, etc.
4[list]/405: Heliotropium (390). Tropical to warm temperate (map: see Frankenberg & Klaus 1980; Flora of China; Gottschling et al. 2004; Flora Base 2005). [Photo - Flower.]
Age. Most of the ages for this clade were over 122 m.y. (Gottschling et al. 2004).
Evolution. Divergence & Distribution. Luebert et al. (2011a) suggest that Heliotropaceae diversified in the Palaeocene or earlier, and within Heliotropium (inc. Tournefortia) diversification began about 45 m.y.a., stem node age is ca 60.7 m.y.a. in the Middle Eocene (see Luebert et al. 2011b for many more details). For the evolution of habit, etc., in neotropical Heliotropium, see Luebert et al. (2011b). Heliotropium sect. Cochranea is a notable endemic group of the Atacama Desert (Luebert & Wen 2008).
Ecology & Physiology. Heliotropium, especially section Orthostachys, contains perhaps ca 150 species with C4 photosynthesis, as well as intermediates between C3 and C4 photosynthetic pathways with C2 photosynthesis (Vogan et al. 2007; Sage et al. 2011) and proto-Kranz species (R. Sage et al. 2014).
Plant-Animal Interactions. Wilting plants and/or flowers of Boraginaceae and Heliotropaceae, especially the latter, are visted by adult butterflies (Danainae, Ithomiinae) and moths (Ctenuchidae, Arctiidae). The pyrrolizidine alkaloids the plants contain are used in their pheromones or are deterrents to feeding by other animals (see also Crotalaria, Apocynaceae and Asteraceae-Asteroideae: e.g. Edgar 1984; Edgar et al. 1974; Ackery & Vane-Wright 1984 [considerable detail for the danaines]; Boppré 1986; Brown 1987; Zaspel et al. 2014: evolution of pharmacophagy in Arctiinae). Cordia (Cordiaceae) is also sometimes visited, although it is not known to contain these alkaloids.
Chemistry, Morphology, etc. Tournefortia astrotricha lacks inulin.
For additional general information, see Förther (1998); details of embryology are taken from DiFulvio (1978).
Phylogeny. Hilger and Diane (2003) found a clade [Ixorhea [Myriopus + Euploca]] to be sister ot Heliotropium, but relationships of the first group were not very well supported. For relationships in neotropical Heliotropium, see Luebert et al. (2011b).
Classification. Generic limits in Heliotropiaceae need attention (Diane et al. 2002a; Hilger & Diane 2003; Luebert et al. 2011a, b); Craven (2005) suggested that the whole lot were best placed in Heliotropium s.l. - a suggestion not without merit. Certainly Tournefortia remains to be synonymised under Heliotropium.
[Cordiaceae + Ehretiaceae]: cambium storied; lamina margins toothed to entire; anther connective usu. not produced; tapetal cells bi- to multinucleate; micropylar and chalazal haustoria +; fruit often a drupe.
CORDIACEAE Dumortier, nom. cons. Back to Boraginales
(Lianes); terpenoid-based quinones +; secondary phloem stratified; nodes 3:3 [Cordia, see below]; petiole bundles (invaginated) annular and with (cortical and) rib bundles; crystal sand and prismatic or columnar crystals +; bracteoles usu. 0; (cymes subdichasial); (flowers heterostylous), (4-merous - Coldenia); K valvate to open, persistent to accrescent, C contorted (imbricate); pollen often spiny, pseudocolpi 0, (3-porate - Varronia); styles twice divided (once divided), stigmas punctate to capitate; ovules straight, integument 6-10 cells across, (parietal tissue 0), (obturator +); stones 1 (2, 4), (K accrescent [an anthocarp!]); testa vascularized [Cordia], 3-4 layers of transfer cells; endosperm haustoria?, 0, cotyledons plicate, toothed; n = 9, 14-16, 19.
3[list]/330: Cordia (200+), Varronia (100). Tropical, especially South America (map: see Gottschling et al. 2004; Flora Base 2005; green, Hoplestigma, from Brummitt 2007). [Photo - Flower, Fruit.]
Age. Gottschling et al. (2004: plausible ages) estimated the age for Cordia alone at (107-)95, 92(-80) m.y..
Evolution. Seed Dispersal. Myxospermy is reported from Cordia (Grubert 1974).
Vegetative Variation. The growth pattern of some species of Cordia, including the myrmecophilous species, is distinctive: the apex of the stem aborts, some branches are plagiotropic, while one becomes orthotropic and forms the renewal shoot. The inflorescence can also be oddly placed.
Chemistry, Morphology, etc. The central foliar trace of Cordia is at least sometimes a striking inverted "C" when it joins the central stele, but I do not know how widespread this character is (see Neubauer 1977 for nodal anatomy of Cordia myxa - a similarly modified 1:3 node).
Heubl et al. (1990: general, esp. Cordia), Nowicke and Miller (1990: pollen), Khaleel (1975, 1982: embryology).
Phylogeny. For the phylogeny of Cordiaceae, see Gottschling et al. (2003); Coldenia is sister to the rest of the family. For relationships in Cordia s. str. and its immediate relatives, see Miller and Gottschling (2007) and Weeks et al. (2010).
The distinctive West African Hoplestigma belongs around here (see e.g. Hallier 1911). It has been placed near Boraginaceae s.l. because of its scorpioid cymose inflorescence, absence of bracts, pollen with pseudocolpi (as in Ehretiaceae: Nowicke & Miller 1989; see also Takhtajan 1997). Molecular data place it close to Cordia (K. Wurdack, pers. comm.), perhaps sister to Coldenia (Weigend et al. 2013b: support weak). The genus is little known, but there appear to be three vascular traces in the base of the petiole, so its nodal anatomy may be similar to that of Cordia.
Classification. Gottschling et al. (2005) equivocated as to whether Coldenia should be included in Cordiaceae - if it is, as here, the family has few apomorphies. Luebert and Wen (2008) suggest a narrow circumscription for Cordiaceae. For generic limits see Gottschling et al. (2003) and Gottschling and Miller (2014). Miller and Gottschling (2007) segregated Varronia from Cordia, although since the two are sister taxa, strictly speaking this is not necessary, even if the split is supported by morphology.
Previous Relationships. Hoplestigmataceae were included in the Violales by Cronquist (1981), perhaps because of their parietal placentation.
Synonymy: Hoplestigmataceae Gilg, Sebestenaceae Ventenat, nom. illeg.
EHRETIACEAE Martius, nom. cons. Back to Boraginales
?Smell; (herbs); inulins?; (pits vestured - e.g. Ehretia, Rochefortia); petiole bundle arcuate; bracteoles?; flowers (4-)5-merous; K (5-15; valvate), C imbricate or inwards-folded, ± rotate; (tapetal cells uninucleate; polyploid); (pollen 3-porate), mesocolpium coarse-reticulate; (G loculi divided), placentation apical to axile, (style impressed), stigmas capitate or elongate; ovules (1/carpel), apotropous, integument 6-12 cells across, epidermal cells anticlinally elongated or not, placental obturator +/0, (hypostase +); (embryo sac bisporic, [chalazal dyad], 8-nucleate [Allium type]), (-3 megaspores functional); stone (1-)2-(4-)seeded, K accrescent or not; endosperm copious to 0, micropylar haustorium esp. variable, embryo curved; n = 5, 7-11, 13, 16, etc.
9[list]/150: Bourreria (48), Ehretia (42), Tiquilia (28). Mostly tropical (map: see Gottschling et al. 2004; Australia's Virtual Herbarium iii.2014; Moore & Jansen 2006; green also = Pholisma and co.).
Age. Gottschling et al. (2004: plausible ages) estimated the age for the [Ehretia + Bourreria] clade at (120-)107, 98(-86) m.y..
Evolution. Divergence & Distribution. Initial diversification in the family may well have been New World (Gottschling et al. 2014b). Moore and Jansen (2006) and Moore et al. (2006) outline speciation and distribution in the amphitropical disjunct desert genus, Tiquilia, in some detail; it may have originated in the Palaeocene ca 58 m.y. before present but began to diversify only rather later, some 33-38 m.y.a., and with repeated dispersal from W. North America to W. South America. Species of Tiquilia are mostly plants of American deserts and are unusual within Ehretiaceae in being herbs, or shrubs that flower very quickly, and their inflorescences may be crowded. Their fruits are dry, and secondary veins in the leaves go to the sinuses (Richardson 1977).Tiquilia nuttallii is a wide disjunct that grows in the western U.S.A. and also western Argentina.
Ecology & Physiology. The holoparasitic Ehretiaceae may parasitize their close relatives (Smith et al. 2000), but their hosts are in fact various. More work is needed to clarify the evolution of this distinctive parasitic clade; Naumann et al. (2013) estimate a crown-group age of (65.7-)40.9(-16.2) m.y., but in the context of their study the stem age (Borago is the sister taxon) must be an overestimate.
Chemistry, Morphology, etc. Ehretiaceae vary in their wood anatomy; both Antrophora and Lepidocordia have vessels in radial groups, apotracheal parenchyma, and fibre tracheids with bordered pits (Gottwald 1982).
For a variety of septae in the gynoecium of Tiquilia, see Gottschling et al. (2014a). In embryology Ehretiaceae are perhaps closest to Heliotropiaceae (Diane et al. 2002a), but the embryology of Lennoa and relatives is largely unknown.
For additional information, see J.-X. Liu et al. (2003: pollen), and Johri and Vasil (1956), Nagaraj and Fathima (1967), Khaleel (1977b) and Hanumantha Rao and Prakana Rao (1984), all embryology; see also The Parasitic Plant Collection for general information about ex-Lennoaceae.
Phylogeny. For relationships within Ehretiaceae, see Gottschling and Hilger (2001) and Gottschling et al. (2014a, b); the exact relationships of the old Lennoaceae are unclear as basal nodes in the family and not strongly supported.
Classification. For genera in Ehretiaceae, see Gottschling et al. (2014b).
Synonymy: Lennoaceae Solms-Laubach, nom. cons.
Chemistry, Morphology, etc. Gottwald (1982: wood anatomy).