EMBRYOPSIDA Pirani & Prado

Gametophyte dominant, independent, multicellular, not motile, initially ±globular; showing gravitropism; acquisition of phenylalanine lysase [PAL], phenylpropanoid metabolism [lignans +, flavonoids + (absorbtion of UV radiation)], xyloglucans in primary cell wall, side chains charged; plant poikilohydrous [protoplasm dessication tolerant], ectohydrous [free water outside plant physiologically important]; thalloid, leafy, with single-celled apical meristem, tissues little differentiated, rhizoids +, unicellular; chloroplasts several per cell, pyrenoids 0; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles/centrosomes in vegetative cells 0, microtubules with γ-tubulin along its length [?here], interphase microtubules form hoop-like system; metaphase spindle anastral, predictive preprophase band of microtubules [where cell plate will join parental cell wall], phragmoplast + [cell wall deposition spreading from around the spindle fibres], plasmodesmata +; antheridia and archegonia jacketed, surficial; blepharoplast +, centrioles develop de novo, bicentriole pair coaxial, separate at midpoint, centrioles rotate, associated with basal bodies of cilia, multilayered structure + [4 layers: L1, L4, tubules; L2, L3, short vertical lamellae] (0), spline + [tubules from L1 encircling spermatid], basal body 200-250 nm long, associated with amorphous electron-dense material, microtubules in basal end lacking symmetry, stellate array of filaments in transition zone extended, axonemal cap 0 [microtubules disorganized at apex of cilium]; male gametes [spermatozoids] with a left-handed coil, cilia 2, lateral; oogamy; sporophyte multicellular, cuticle +, plane of first cell division transverse [with respect to long axis of archegonium/embryo sac], sporangium and upper part of seta developing from epibasal cell [towards the archegonial neck, exoscopic], with at least transient apical cell [?level], initially surrounded by and dependent on gametophyte, placental transfer cells +, in both sporophyte and gametophyte, wall ingrowths develop early; suspensor/foot +, cells at foot tip somewhat haustorial; sporangium +, single, terminal, dehiscence longitudinal; meiosis sporic, monoplastidic, MTOC [MTOC = microtubule organizing centre] associated with plastid, sporocytes 4-lobed, cytokinesis simultaneous, preceding nuclear division, quadripolar microtubule system +; wall development both centripetal and centrifugal, sporopollenin + laid down in association with trilamellar layers [white-line centred lamellae; tripartite lamellae], >1000 spores/sporangium; nuclear genome size <1.4 pg, main telomere sequence motif TTTAGGG, LEAFY and KNOX1 and KNOX2 genes present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes [precursors for starch synthesis], tufA gene moved to nucleus.

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.

STOMATOPHYTES

Abscisic acid, L- and D-methionine distinguished metabolically; sporophyte with polar transport of auxins, class 1 KNOX genes expressed in sporangium alone; sporangium wall 4≤ cells across [≡ eusporangium], tapetum +, secreting sporopollenin, which obscures outer white-line centred lamellae, columella +, developing from endothecial cells; stomata +, on sporangium, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and of rhizoids/root hairs; spores trilete; shoot meristem patterning gene families expressed; MIKC, MI*K*C* genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns, mitochondrial trnS(gcu) and trnN(guu) genes 0.

[Anthocerophyta + Polysporangiophyta]: gametophyte leafless; archegonia embedded/sunken [on;y neck protruding]; sporophyte long-lived, chlorophyllous; cell walls with xylans.

POLYSPORANGIOPHYTA†

Sporophyte well developed, branched, branching apical, dichotomous, potentially indeterminate; hydroids +; stomata on stem; sporangia several, terminal; spore walls not multilamellate [?here].

TRACHEOPHYTA†

Vascular tissue + [tracheids, walls with bars of secondary thickening].

EXTANT TRACHEOPHYTA / VASCULAR PLANTS

Sporophyte with photosynthetic red light response, stomata open in response to blue light; plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; plant endohydrous [physiologically important free water inside plant]; (condensed or nonhydrolyzable tannins/proanthocyanidins +); xyloglucans with side chains uncharged [?level], in secondary walls of vascular and mechanical tissue; lignins +; stem apex multicellular, with cytohistochemical zonation, plasmodesmata formation based on cell lineage; tracheids +, in both protoxylem and metaxylem, G- and S-types; sieve cells + [nucleus degenerating]; endodermis +; leaves/sporophylls spirally arranged, blades with mean venation density ca 1.8 mm/mm2 [to 5 mm/mm2], all epidermal cells with chloroplasts; sporangia adaxial, columella 0; tapetum glandular; ?position of transfer cells; MTOCs not associated with plastids, basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; suspensor +, shoot apex developing away from micropyle/archegonial neck [from hypobasal cell, endoscopic], root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].

[MONILOPHYTA + LIGNOPHYTA]

Sporophyte endomycorrhizal [with Glomeromycota]; growth ± monopodial, branching spiral; roots +, endogenous, positively geotropic, root hairs and root cap +, protoxylem exarch, lateral roots +, endogenous; G-type tracheids +, with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangium dehiscence by a single longitudinal slit; cells polyplastidic, MTOCs diffuse, perinuclear, migratory; blepharoplasts +, paired, with electron-dense material, centrioles on periphery, male gametes multiciliate; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; LITTLE ZIPPER proteins.

LIGNOPHYTA†

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].

SEED PLANTS†

Plants heterosporous; megasporangium surrounded by cupule [i.e. = unitegmic ovule, cupule = integument]; pollen lands on ovule; megaspore germination endosporic [female gametophyte initially retained on the plant].

EXTANT SEED PLANTS / SPERMATOPHYTA

Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignin chains started by monolignol dimerization [resinols common], particularly with guaiacyl and p-hydroxyphenyl [G + H] units [sinapyl units uncommon, no Maüle reaction]; root stele diarch to pentarch, xylem and phloem originating on alternating radii, cork cambium deep seated; stem apical meristem complex [with quiescent centre, etc.], plasmodesma density in SAM 1.6-6.2[mean]/μm2 [interface-specific plasmodesmatal network]; eustele +, protoxylem endarch, endodermis 0; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; cork cambium superficial; leaf nodes 1:1, a single trace leaving the vascular sympodium; leaf vascular bundles amphicribral; guard cells the only epidermal cells with chloroplasts, stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; axillary buds +, exogenous; prophylls two, lateral; leaves with petiole and lamina, development basipetal, lamina simple; sporangia borne on sporophylls; spores not dormant; microsporophylls aggregated in indeterminate cones/strobili; grains monosulcate, aperture in ana- position [distal], primexine + [involved in exine pattern formation with deposition of sporopollenin from tapetum there], exine and intine homogeneous, exine alveolar/honeycomb; ovules with parietal tissue [= crassinucellate], megaspore tetrad linear, functional megaspore single, chalazal, sporopollenin 0; gametophyte ± wholly dependent on sporophyte, development initially endosporic [apical cell 0, rhizoids 0, etc.]; male gametophyte with tube developing from distal end of grain, male gametes two, developing after pollination, with cell walls; female gametophyte initially syncytial, walls then surrounding individual nuclei; embryo cellular ab initio, suspensor short-minute, embryonic axis straight [shoot and root at opposite ends; plant allorhizic], cotyledons 2; embryo ± dormant; ycf2 gene in inverted repeat, mitochondrial trans- nad2i542g2 and coxIIi3 introns present; whole nuclear genome duplication [ζ - zeta - duplication], two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], 5.8S and 5S rDNA in separate clusters.

ANGIOSPERMAE / MAGNOLIOPHYTA

Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANA grade?], lignin also with syringyl units common [G + S lignin, positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], hemicelluloses as xyloglucans; root apical meristem intermediate-open, pith relatively inconspicuous, lateral roots initiated immediately to the side of [when diarch] or opposite xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0, hypodermis suberised and with Casparian strip [= exodermis]; shoot apex with tunica-corpus construction, tunica 2-layered; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, not occluding pores of plate, companion cell and sieve tube from same mother cell; ?phloem loading/sugar transport; nodes 1:?; dark reversal Pfr → Pr; protoplasm dessication tolerant [plant poikilohydric]; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance with increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, secondary veins pinnate, fine venation hierarchical-reticulate, (1.7-)4.1(-5.7) mm/mm2, vein endings free; flowers perfect, pedicellate, ± haplomorphic, protogynous; parts free, numbers variable, development centripetal; P +, ?insertion, members each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], each theca dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, endothecium +, cells elongated at right angles to long axis of anther; tapetal cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine lamellate only in the apertural regions, thin, compact, intine in apertural areas thick, pollenkitt +; nectary 0; carpels present, superior, free, several, ascidiate [postgenital occlusion by secretion], stylulus at most short [shorter than ovary], hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry; suprastylar extragynoecial compitum +; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across, nucellar cap?; megasporocyte single, hypodermal, functional megaspore lacking cuticle; female gametophyte lacking chlorophyll, not photosynthesising, four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; ovule not increasing in size between pollination and fertilization; pollen grains land on stigma, bicellular at dispersal, mature male gametophyte tricellular, germinating in less than 3 hours, pollen tube elongated, unbranched, growing between cells, growth rate (20-)80-20,000 µm/hour, apex of pectins, wall with callose, lumen with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametes lacking cell walls, ciliae 0, siphonogamy; double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; mature seed much larger than fertilized ovule, small [], dry [no sarcotesta], exotestal; endosperm +, cellular, development heteropolar [first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous, embryo short [<¼ length of seed]; plastid and mitochondrial transmission maternal; Arabidopsis-type telomeres [(TTTAGGG)n]; nuclear genome very small [1C = <1.4 pg, mean 1C = 18.1 pg, 1 pg = 109 base pairs], whole nuclear genome duplication [ε/epsilon event]; ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, palaeo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]]; chloroplast chlB, -L, -N, trnP-GGG genes 0.

[NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]]: wood fibres +; axial parenchyma diffuse or diffuse-in-aggregates; pollen monosulcate [anasulcate], tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.

[AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: phloem loading passive, via symplast, plasmodesmata numerous; vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood + [reaction wood: with gelatinous fibres, g-fibres, on adaxial side of branch/stem junction]; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; nucellar cap + [character lost where in eudicots?]; 12BP [4 amino acids] deletion in P1 gene.

[[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]] / MESANGIOSPERMAE: benzylisoquinoline alkaloids +; sesquiterpene synthase subfamily a [TPS-a] [?level], polyacetate derived anthraquinones + [?level]; outer epidermal walls of root elongation zone with cellulose fibrils oriented transverse to root axis; P more or less whorled, 3-merous [?here]; pollen tube growth intra-gynoecial; extragynoecial compitum 0; carpels plicate [?here]; embryo sac bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid.

[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (extra-floral nectaries +); (veins in lamina often 7-17 mm/mm2 or more [mean for eudicots 8.0]); (stamens opposite [two whorls of] P); (pollen tube growth fast).

[CERATOPHYLLALES + EUDICOTS]: ethereal oils 0.

EUDICOTS: (Myricetin, delphinidin +), asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; (vessel elements with simple perforation plates in primary xylem); nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; protandry common; K/outer P members with three traces, ("C" +, with a single trace); A ?, filaments fairly slender, anthers basifixed; microsporogenesis simultaneous, pollen tricolpate, apertures in pairs at six points of the young tetrad [Fischer's rule], cleavage centripetal, wall with endexine; G with complete postgenital fusion, stylulus/style solid [?here]; seed coat?

[PROTEALES [TROCHODENDRALES [BUXALES + CORE EUDICOTS]]]: (axial/receptacular nectary +).

[TROCHODENDRALES [BUXALES + CORE EUDICOTS]]: benzylisoquinoline alkaloids 0; euAP3 + TM6 genes [duplication of paleoAP3 gene: B class], mitochondrial rps2 gene lost.

[BUXALES + CORE EUDICOTS]: ?

CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one position]; micropyle?; γ whole nuclear genome duplication [palaeohexaploidy, gamma triplication], PI-dB motif +, small deletion in the 18S ribosomal DNA common.

[ROSIDS ET AL. + ASTERIDS ET AL.] / PENTAPETALAE: root apical meristem closed; (cyanogenesis also via [iso]leucine, valine and phenylalanine pathways); flowers rather stereotyped: 5-merous, parts whorled; P = calyx + corolla, the calyx enclosing the flower in bud, sepals with three or more traces, petals with a single trace; stamens = 2x K/C, in two whorls, internal/adaxial to the corolla whorl, alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G [5], G [3] also common, when [G 2], carpels superposed, placentation axile, style +, stigma not decurrent; compitum +; endosperm nuclear; fruit dry, dehiscent, loculicidal [when a capsule]; RNase-based gametophytic incompatibility system present; floral nectaries with CRABSCLAW expression; (monosymmetric flowers with adaxial/dorsal CYC expression).

[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?; if nectary +, gynoecial; G [2], style single, long; ovules unitegmic, integument thick, endothelium +, nucellar epidermis does not persist; exotestal [!: even when a single integument] cells lignified, esp. on anticlinal and/or inner periclinal walls; endosperm cellular.

[ERICALES [ASTERID I + ASTERID II]]: (ovules lacking parietal tissue) [tenuinucellate].

[ASTERID I + ASTERID II] / CORE ASTERIDS / EUASTERIDS: plants woody, evergreen; ellagic acid 0, non-hydrolysable tannins not common; vessel elements long, with scalariform perforation plates; nodes 3:3; sugar transport in phloem active; inflorescence usu. basically cymose; flowers rather small [<8 mm across]; C free or basally connate, valvate, petals often with median adaxial ridge and inflexed apex; A = and opposite sepals or P, (numerous [usu. associated with increased numbers of C or G]), free to basally adnate to C; G #?; ovules 2/carpel, apical, pendulous; fruit a drupe, drupe ± flattened, surface ornamented; seed single; duplication of the PI gene.

ASTERID I / LAMIIDAE: ?

[METTENIUSALES [GARRYALES [GENTIANALES, VAHLIALES, SOLANALES, BORAGINALES, LAMIALES]]]: ?

[GARRYALES [GENTIANALES, VAHLIALES, SOLANALES, BORAGINALES, LAMIALES]]: G [2], 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 Boraginales, see discussion under Gentianales.

BORAGINALES Berchtold & J. Presl, nom. cons.   Main Tree.

Plant ± herbaceous; (pyrrolizidine alkaloids +), rosmarinic acid + [caffeic acid ester]; root lacking hypodermis [2 records]; (nuclear crystalloids in sieve tubes); (cork mid-cortical to pericyclic); (silicon concentration high [?level; see hairs]); axial parenchyma (±) 0; 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) [= heterocolpate]; nectary +, not vascularized; placentation intrusive parietal, stigma dry; ovules many/carpel; fruit a loculicidal capsule, K ± accrescent; testa with single layer of transfer cells [cells with labyrinthine ingrowths of the wall]; chalazal endosperm haustorium +, cotyledons accumbent[?]. - 6 families, 150 genera, 3,095 species. [Photos - Collection.]

Age. Wikström et al. (2001) estimate crown-group Boraginales as being (63-)59, 56(-52) m.y.o.; the age is (73-)57, 54(-39) m.y. in Bell et al. (2010) and rather older, (92.8-)76.4(-62) m.y. in Tank and Olmstead (2017), (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: 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. 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. 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, some Boraginaceae and Heliotropaceae are visited by adult moths, especially tiger moths (Arctiidae), that use the pyrrolizidine alkaloids they contain as a basis for their pheromones (see Heliotropaceae), and these alkaloids may be an apomorphy for the order (see Reimann et al. 2004). Arctiid catepillars also eat the plants (Hartmann 2009; other articles in Conner et al. 2009), and pyrrolizidine alkaloids and pentacyclic triterpene saponins variously sequestered and modified are also 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 Boraginaceae 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). All Boraginales sampled (three families) have rosmarinic acid, no other lamiids do except Lamiaceae themselves, although the related chlorogenic acid (both are esters of caffeic acid) is reported from Boraginales and is scattered in lamiids (Petersen 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 discussion under the euasterids). 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. Boraginaceae are well known to have a gynobasic style, and it has 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).The style in at least some Boraginaceae and Hydrophyllaceae apears to be hollow (Guéguen 1901). This group has a variety of septal structures in the ovary (see Gottschling 2004). 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).

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 of the families 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 Cave and Constance (1959 and references) and Constance (1963) for 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. For the most recent classification, see Luebert et al. (2016).

Previous Relationships. 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 (but lack alkannin and pyrrolizidine alkaloids), 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 placed 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.

Boraginaceae tree

Includes Boraginaceae, Codonaceae, Cordiaceae, Ehretiaceae, Heliotropiaceae, Hydrophyllaceae, Namaceae", Wellstediaceae.

Synonymy: Cordiales Martius, Echiales Lindley, Ehretiales Martius, Hydrophyllales Martius - Boraginanae Doweld

[Codonaceae [Wellstediaceae + Boraginaceae]]: ?

Evolution. Ecology & Physiology. Members of the first three pectinations live in semi desert/desert areas (see also Bittrich & Kadereit 2016).

Codonaceae

CODONACEAE Weigend & Hilger  Back to Boraginales

Subshrubs; ?chemistry; plant spiny-hairy, unicellular hairs with cystolithic epidermal/foot cells; flowers (10-)12(-20)-merous; K deeply linear-lobed, open, broad and narrow lobwes alternating; C broadly campanulate; septae at filament bases form lateral walls of nectar compartments, (lateral filament scales); pollen tricolp(or)ate, pseudocolpi 0; placentae T-shaped, style deeply bilobed, stigmas papillate, punctate; integument ca 12 cella across; testa reticulate-papillate; endosperm copious; n = 17.

1[list]/2. S.W. Africa (map: see Retief et al. 2005).

Chemistry, Morphology, etc. Codon is unique in Boraginales in having a kind of revolver flower, with basal nectar chambers, variously protected, alternating with the stamens (Jeiter et al. 2016).

For additional information, see Retief and van Wyk (2005), and Weigend and Hilger (2010, 2016).

[Wellstediaceae + Boraginaceae]: ovules 2/carpel, apical, pendulous; testa transfer cells 0.

WELLSTEDIACEAE Novák  Back to Boraginales

Wellstediaceae

Small shrubs; ?chemistry; indumentum ± scabrid, glands multicellular, peltate; leaves 2-ranked; inflorescences along the branches; flowers four-merous; C lobes three-veined, C tube eight veined, (faucal scales +); pollen 12-25 x 8-15 µm, exine perforate to reticulate, tricolporate, pseudocolpi +, mesocolpium coarse-reticulate; nectary ?0; style (slightly) bifid, wet; ovule one/carpel, apical, epitropous, chalazal end pointed; fruit flattened, septae may separate from the walls; seed with fringe of 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, Hunt (1969) and 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 and Hunt (1969) described it as being both, but in different places in the text. The ovule has a distinctive shape apparently caused by a chalazal projection (e.g. Reteif & van Wyk 2008).

See Hilger and Weigend (2016) for general information.

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

Boraginaceae

Annual herbs to shrubs; cork cambium deep seated [?sampling]; leaves with midvein alone obvious; corolla often funneliform, lobes spreading; anther connective produced or not; tapetal cells multinucleate, or nucleus polyploid; pollen grains tricellular, prolate or dumbbell-shaped; pollen tube with callose; G median, ovary deeply lobed, with secondary septae, style gynobasic, hollow; ovules basal, integument 7-20 cells across, vascularized, (nucellar cap +), placental obturator +, (hypostase +); fruit a schizocarp, with central column/gynobase, nutlets 4, exocarp sclerified; testa (vascularized), exotestal cells with outer walls thickened and lignified (other patterns of thickening, or unthickened), most other cells disappear; endosperm (nuclear), slight, haustoria 0, oily [oils omega 6 gammalinoleic acid GLA, omega 3 stearidonic acid SDA], suspensor short [1-2 cells] or 0; (protein inclusions in nucleus).

Ca 94[list]/1,793 - eleven 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, by Weigend et al. (2009), or substantially older, around (76.9-)63.5(-46.5) m.y., by Nazaire et al. (2014).

1. Echiochiloideae Weigend

Echiochileae

(Annual) herbs, subshrubs; ?chemistry; indumentum ± sericeous; leaves ± opposite; (flowers monosymmetric); corolla throat densely hairy or with cilia, (with ± obscure invaginations; pollen 2-3 colpate/colporate, not heterocolpate, (oblate-square in equatorial view); stigma punctate, (subterminal, tip sterile, bilobed to notched); gynobase flat or shortly pyramidal, nutlets (laterally compressed), (with non-basal attachment), (scar triangular, with a rim), thickened pericarp several-layered, ± ovoid, surface verrucose; n = ?

3/28. Mexico, S. Brazil to N.E Argentina, Canary Isles, North and Northeast Africa to W. India (Map: from Lönn 1999; Långström & Chase 2002).

Age. Fossil nutlets of Boraginocarpus from northwest Africa that were confidently placed in Echiochileae (= Echiochiloideae: ?crown-group) are dated to 56-41 m.y.a. (Hammouda et al. 2015).

[Boraginoideae + Cyngolossoideae]: rosmarinic (and lithospermic) acid + [caffeic acid esters], (pyrrolizidine alkaloids), (meroterpenoids) +, D-bornesitol + [cyclitol], isokestose oligosaccharides [= fructans], (with starch), (none in annuals); indumentum often ± hispid/scabrid, mineralized with Ca or Si, hairs with basal tubercule [usu. whitish], cystoliths +; (flowers heterostylous); corolla salverform, with faucal invaginations [fornices, faucal scales]; pollen grains 2-5-colporate; nutlet scar lacking a rim.

2. Boraginoideae Arnott

Perennial (annual) herbs; flowers (monosymmetric), also with basal scales; gynobase flat, nutlets with basal attachment scar.

42/610. Mostly Mediterranean, East Asia, also Africa, South America.

2A. Boragineae Reichenbach

Basal leaves + (0); (floral bracts 0); (pollen to 15-zonocolporate); (style hollow); embryo sac with lateral outgrowth towards the funicle; nutlets also 1, with thickened pericarp, usu. laterally compressed, ventrally keeled, surface tessellate and papillate, often with elaiosome [gynobase tissue]; n = (6) 7, 8, 9 (-11<).

17/146: Anchusa (35), Symphytum (35). Mediterranean, also South America

Synonymy: Anchusaceae Vest

2b. Lithospermeae Dumortier

Annual herbs to shrubs; (naphthoquinones + [e.g. alkannin, reddish or purple dye]); corolla often urceolate or funnelform, (faucal appendages 0, but pubescent/glandular patches +), tube commonly with abaxial trichomes, ("glands" inside); (pollen porate), heteropolar (apertures closer to one pole]); style with/without sterile tips, stigma lobes (2), 4; nutlet with several-layered thickened pericarp, walls encrusted with calcium carbonate, surface often smooth, shiny; n = (4-)6, 7 (8<).

25/460: Onosma (150), Lithospermum (80), Echium (60), Arnebia (30). Mainly N. Africa and Eurasia, not tropical or Antipodean, America (esp. Lithospermum.

Synonymy: Buglossaceae Hoffmannsegg & Link nom. illeg., Cerinthaceae Berchtold & Presl, Echiaceae Rafinesque, Onosmaceae Martynov

3. Cynoglossoideae Weigend

(Basal leaves +); vestured pits +; lamins with evident secondary venation; floral bracts 0 (+); flowers polysymmetric; anther epidermis with fibrous thickening [Mertensia]; tapetal cells uninucleate; (pollen grains 6-8 porate); (G lacking secondary/false septum); gynobase broadly pyramidal to subulate (flat), nutlets often dorsiventrally compressed, dorsally concave, ventrally attached, (with large, triangular scar), (glochids, marginal wings or other ornamentation +), thickened pericarp single-layered.

Ca 48/1,070. ±World-wide.

Age. Crown-group Cynoglosseae are estimated to be (38.3-)31.1(-23.2) m.y.o. (Nazaire et al. 2014).

[Lasiocaryeae + Trichodesmeae]: inflorescence bracteate; stigma capitate.

3A. Lasiocaryeae Weigend

Small, annual to perennial herbs; indumentum sericeous; anthers included; nutlets very small, erect, ovoid to subcylindrical, often hairy; n = ?

3/5. Himalayas.

3B. Trichodesmeae Riedl

Biennial herbs with rosette to (tall) shrubs; indumentum hispid to sericeous (0); anthers exserted; pollen tricolporate; nutlets 1(-4), usu. winged, glochidiate or not; n = 7, 11, 12.

2/ca 50: Trichodesma (45). Iran, southern, central and southeast Asia, Australia.

[Asperugeae, Omphalodeae, Rochelieae [Craniospermeae, Myosotideae, Cynoglosseae]]:

3C. Asperugeae Ovczinnikova

Annual to perennial herbs; indumentum often 0, leaves glaucous; (faucal invaginations 0); style capitate [?all]; nutlets somooth to rugose; n = 12.

4/50: Mertensia (40). North temperate.

3D. Omphalodeae Weigend

Annual to perennial herbs; style short, stigma capitate; nutlets compression?, glochidiate or not; n = 10, 11, 12..., also 2n = 19.

6/35: Omphalodes (25). Northern Hemispere, one sp. on Juan Fernandes and another on the Chatham Islands(!)

3E. Rochelieae A. de Candolle

Annual to perennial herbs; indumentum often hispid; anthers included; stigma capitate; nutlets ?compression, glochidiate; n = 10, 11, 12...

7/210: Lappula (55), Eritrichium (50), Hackelia (45). Esp. Eurasia, also America, Australia, North Africa.

[Craniospermeae, Myosotideae, Cynoglosseae]: inflorescence usu. at least apically ebracteate;.

3F. Craniospermeae Meisner

Biennial to perennial herbs; indumentum hirsute to floccose; faucal invaginations 0, (scales between C lobes); anthers exserted; stigma depressed capitate to disciform; nutlets erect, ovoid, rugose, dentate-winged; n = ?

1/6. Central and East Asia.

3G. Myosotideae Reichenbach f.

Annual to perennial herbs; indumentum various; (C contorted); stigma subcapitate (obscurely bilobed); nutlets (→10), lenticellate to tetrahedral, not much dorsally compressed, with lateral (ventral) keels, smooth to papillate; n = 6≤.

5/160: Myosotis (80-100), Trigonotis (60). ± Cosmopolitan.

3H. Cynoglosseae W. D. J. Koch

Annual to perennial herbs; (naphthoquinones + [e.g. alkannin, reddish or purple dye]); indumentum sericeous to hispid; (inflorescence bracteate); corolla with basal scales; (style deeply divided), stigma capitate [?all]; nutlets glochidiate (surface granular); n = (6, 7, 10, 11) 12...

Ca 20/553: Cynoglossum (180-200), Cryptantha (160), Plagiobothrys (70). America (Amsinckiinae), Eurasia, Australia (few).

Synonymy: Cynoglossaceae Döll

Evolution. Divergence & Distribution. Weigend et al. (2013a) and Hammouda et al. (2015) 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 family, are to be found; they all grow in rather arid conditions. As Weigend et al. (2013a) emphasized, extant Boraginoideae 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 Boragineae, 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. (Cynoglossoideae-Cynoglosseae, nearly all in the north → south direction (Hasenstab-Lehman & Simpson 2012); all told, there are between 17 ans 19 such events, all occuring within the last ca 5 m.y., in Amsinckiinae alone (Guilliams & Baldwin 2011; Guilliams et al. 2016). 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 in the protoplasm are involved in the shift of 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 occurs in some Boraginaceae and 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; Weigend et al. 2016).

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 Weigend et al. (2016: general), Lönn (1999: Echiochileae), 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. In the detailed study of Weigend et al. (2013a) and especially Cohen (2014) and Chacón et al. (2016) the same general relationships, including the position of Echiochileae, were recovered.

Support for the monophyly of Boraginoideae is quite good, but relationships within the two tribes it contains are not well supported (Chacón et al. 2016: sampling rather poor). 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).

The monophyly of Cynoglossoideae is well supported, and although its tribes also have good support, relationships between them are unclear (Chacón et al. 2016). Cynoglossoideae include 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 have arisen independently. Asperugeae. 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. Myosotidae. 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). Rochelieae. Huang et al. (2013) discuss relationships within Lappula. Cynoglosseae. The subtribes are well supported, but relationships within them for the most part need more support (see Chacón et al. 2016). Hasenstab-Lehman and Simpson (2012) looked at relationships within the large North American genus Cryptantha, either highly para- or polyphyletic.

Classification. See Chacón et al. (2016) for the classification above; they also recognize subtribes.

Generic limits need much attention - see Weigend (in Kadereit et al. 2016) for generic limits in European taxa. Hasenstab-Lehman and Simpson (2012) adjusted the limits of Cryptantha, but broader limits were adopted by Chacón et al. (2016). Genera like Lithospermum, 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). Cohen (2014) found that genera like Myosotis, Anchusa and Cynoglossum were not monophyletic, indeed, the findings of Weigend et al. (2013a) point out the need for a generic reclassification of Cynoglossoideae s.l. (see also Chacón et al. 2016).

Botanical Trivia. At ca 4 x 2 mm, the pollen of Cryptantha clevelandii is about the smallest of all angiosperms (Hargrove & Simpson 2003).

[Hydrophyllaceae [Namaceae [Heliotropiaceae [Cordiaceae + Ehretiaceae]]]]: (plant smells unpleasantly); tapetal cell nucleus number?; endosperm with both chalazal and micropylar haustoria; suspensor long.

HYDROPHYLLACEAE R. Brown, nom. cons.  Back to Boraginales

Hydrophyllaceae

Annual to perennial herbs; (meroterpenoids), inulin?, alkaloids?; (mycorrhizae 0); (wood rayless); ?cork; (vascular bundles separate); (stinging hairs - Phacelia); leaves (opposite; compound), margins lobed, toothed (entire), secondary veins pinnate (palmate); (flowers axillary); (bracts and bracteoles 0); (flowers 4-6-merous); ; (K free), (C contorted), (lobes serrate); A usu. with small (lobed) lateral scales at each side of the filament base; pollen (pseudocolpi +), tubes with callose (0); placentae swollen, enlarging after ovule initiation [Hydrophylleae], style ± divided (to the base), stigma punctate (capitate); ovules (2-), (pleurotropous), integument ca 6 cells across, parietal tissue 0; (embryo sac with chalazal haustorium - Nemophila); (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 (nuclear), copious to scanty, haustoria with large lateral projections, (micropylar 0), (reserve hemicellulose), embryo (short), green or white; n = (5-)8-13, etc..

12[list]/250: 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; Hofmann 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 general information, see Hofmann et al. (2016), for wood anatomy, see Carlquist and Eckhart (1984), 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

[Namaceae [Heliotropiaceae [Cordiaceae + Ehretiaceae]]]: ?

NAMACEAE Molinari  Back to Boraginales

Namaceae

Annual to perennial herbs and shrubs (rhizomatous) to small trees; inulin?, alkaloids?; (mycorrhizae 0); axial parenchyma diffuse; leaf margins toothed to entire, secondary veins pinnate; bracts and bracteoles usu. 0; (K free); A usu. without small lateral scales at the base; pollen tricolporate, ?pollen tube callose; tapetal cells 2-nucleate; G (semi-inferior), placentae ± narrow, (base of ovary 1 or falsely 4-locular), style divided to the base (ca 1/4]), stigma capitate-funneliform or punctate; ovules (2<), epi- and apotropous, integument 6-12 cells across, (parietal tissue ca 1 cell layer across), (nucellar cap ca 2 cells across); (embryo sac bisporic [the chalazal dyad], 8-nucleate [Allium

type]); (capsule loculicidal + septicidal); (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, 13, 14, 17, 19, (protein inclusions in nucleus).

4[list]/71: Nama (56). Southwest North America, Central America and western South America, Antilles, Hawaii (map: see Brummitt 2007; Heckard 1963). [Photo - Undetermined Flower.]

Chemistry, Morphology, etc. There are nectaries at the base of the ovary in the ovary wall, and the number (1, 3) of vascular bundles varies (di Fulvio et al. 1997). Di Fulvio (1989a) described the ovules of Nama as being crassinucellate, but there can only be a single cell layer below the nucellar epidermis.

For general information, see Hofmann et al. (2016), for wood anatomy, quite distinctive, see Carlquist and Eckhart (1984), 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 lack callose; ovary with secondary septae; ovules 2/carpel, epitropous [check], parietal tissue 1(2) cells across, (nucellar cap ca 2 cells across); transfer cells in funicle and placenta also; fruit a schizocarp, or indehiscent, endocarp multilayered; endosperm cellular.

Age. The age of this clade is ca 62 m.y. (Chomicki & Renner 2015: fig. S5).

HELIOTROPIACEAE Schrader, nom. cons.  Back to Boraginales

Heliotropiaceae

(Annual herbs, lianes); fructan sugars accumulated as isokestose oligosaccharides [inulin] [Heliotropium]; cambium not storied; pericyclic sheath 0 [?always]; pits not vestured (+); petiole bundles arcuate; (tetrahedral crystals +); leaves usu. conduplicate [Tournefortia]; bracts 0 (+); C imbricate, with involute margins, contorted, etc., mouth with scales [?all]; anthers basifixed, usu. connate at apex, connective produced or not; tapetal cells binucleate; pollen (4 colporate), (porate); ovary becoming deeply lobed, style (deeply) impressed, 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 anatropous and hemitropous [same ovary], integument (?3-)8 cells across, parietal tissue 0, nucellar cap +, (obturator +); fruit a schizocarp, stones one (two seeded, (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]/425: Heliotropium (300), Euploca (100). 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), but its age in Chomicki and Renner (2015: fig. S5) is ca 42.4 m. years.

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 of these insects or deter predation 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. Caterpillars of arctiid moths also eat alkaloid-containing members of these families (Hartmann 2009; other articles in Conner et al. 2009).

Chemistry, Morphology, etc. Tournefortia astrotricha lacks inulin.

For general information, see Förther (1998) and Diane et al. (2016); 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]: caffeic and rosmarinic acids +; cambium storied; epidermal cells calcified or silicified; lamina margins toothed to entire; anther connective usu. not produced; tapetal cells bi- to multinucleate; ovules with parietal tissue ca 1 cell across; micropylar and chalazal haustoria +; fruit often a drupe.

Age. The age of this clade is ca 60.7 m.y. (Chomicki & Renner 2015: fig. S5).

CORDIACEAE Dumortier, nom. cons.  Back to Boraginales

Cordiaceae

(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/with clavate projections, (substriate, rugulose), pseudocolpi 0 (+), (3-porate - Varronia); styles once [Coldenia] or twice divided, stigmas punctate to capitate; ovules straight, integument 6-10 cells across, (parietal tissue 0), (obturator +); stones 1 or 4, if 1, then often 1-seeded, K often much accrescent [an anthocarp!]; testa vascularized [Cordia], 3-4 layers of transfer cells; endosperm haustoria?, 0, (cotyledons plicate, margins toothed); n = 7-9.

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., but ca 50.8 m.y. seems more plausible (see Chomicki & Renner 2015: fig. S5; Cordia s.l., ca 38.6 m.y.).

Evolution. Seed Dispersal. Myxospermy is reported from Cordia (Grubert 1974).

Plant-Animal Interactions. Cordia nodosa is a well-known myrmecophyte. An ant associated with it, Myrmelachista schumanni, forms so-called "devil's gardens" by poisoning the surrounding vegetation with formic acid, C. nodosa alone persisting; the gardens are known from western Amazonia and French Guiana (Salas-Lopez et al. 2016 and references). For its food bodies, see Solano et al. (2005), and for the evolution of myrmecophytism here see Chomicki and Renner (2015); see also Ruiz-González et al. (2011).

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 1977b for nodal anatomy of Cordia myxa - a similarly modified 1:3 node).

For information, see Gottschling et al. (2016: general), Heubl et al. (1990: esp. Cordia), Nowicke and Miller (1990: pollen), and 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, perhaps sister to Coldenia (Weigend et al. 2013b: support weak). The genus is little known, but there are three vascular traces in the base of the petiole, so its nodal anatomy may be similar to that of Cordia.

1/2. West Africa.

Studies of floral development would be very interesting.

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 (if separate, the former has adventitous roots and teramerous flowerrs as apomorphies, the latter, four stigmatic branches, an undivided endocarp, and plicate cotyledons (Luebert et al. 2016). Luebert and Wen (2008) suggest a narrow circumscription for Cordiaceae. For generic limits see Gottschling et al. (2003), Gottschling and Miller (2014) and Luebert et al. (2016). Miller and Gottschling (2007) segregated Varronia from Cordia; the latter has a rather lengthy synonymy...

Previous Relationships. Hoplestigmataceae were included in the Violales by Cronquist (1981), perhaps because of their parietal placentation.

Synonymy: Coldeniaceae, Hoplestigmataceae Gilg, Sebestenaceae Ventenat, nom. illeg.

EHRETIACEAE Martius, nom. cons.  Back to Boraginales

Ehretiaceae, Lennoaceae (green)

?Smell; (herbs); inulins?; (pits vestured - e.g. Ehretia, Rochefortia); petiole bundle arcuate; bracteoles?; (plant dioecious); flowers (4-)5-merous; K (5-15; valvate), C imbricate or inwards-folded, ± rotate; (tapetal cells uninucleate; polyploid); (pollen 3-porate), pseudocolpi common, tecta rugulose; (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); fruit a schizocarp (not), stone (1-)2-(4-)seeded, (sterile chambers +), K accrescent or not; endosperm copious to 0, micropylar haustorium esp. variable, embryo curved; n = 5, 7-11, 13, 16, etc.

9[list]/150: (7/160) Ehretia (ca 50), Bourreria (48), Tiquilia (28). Mostly &Jansen 2006).

Age. Gottschling et al. (2004: plausible ages) estimated the age for the [Ehretia + Bourreria] clade at (120-)107, 98(-86) m.y., while ca 51.9 m.y. is the estimate in Chomicki and Renner (2015: fig. S5).

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.

Chemistry, Morphology, etc. Ehretiaceae vary in their wood anatomy; Lepidocordia has 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).

For additional information, see Gottschling et al. (2016: general), 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.

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, 2016).

LENNOACEAE Solms-Laubach, nom. cons.

Plant echlorophyllous, root parasite, annual to perennial herbs; mycorrhizae 0; vascular stele with separate bundles; hairs glandular, uniseriate, leaves scales. margins entire; inflorescence ± capitate, (involucrate); flowers 4-10-merous; K long, narrow, C induplicate-valvate; (A in two series); tapetal cells 1-2-nucleate; nectary 0; G [5-16], placentation axile, style stout, (hollow), stigma capitate or lobed, wet; ovule epitropous, subcampylotropous, integument ca 2 cells across, parietal tissue 0; fruit with circumscissile outer pericarp, pyrenes 1-seeded, dispersed irregularly subsequently, K and C persistent; exotesta with fine reticulate thickening; endosperm starchy, with chalazal haustorium, embryo minute, undifferentiated; n = 9.

2/4. California and Arizona to Guatemala, N. South America (green area in Ehretiaceae, see Yatskievych & Mason 1986; Parasitic Plants.).

Age. The stem-group age of this clade is (88-)68(-46) m.y., the crown-group age is (66-)41(-16) m.y. (Naumann et al. 2013: Phol., Lenn. respectively).

For general information, see Suessenguth (1927), Yatskievych and Mason (1986) and Bittrich (2016), also The Parasitic Plant Collection. Yhe embryology of Lennoa and relatives is largely unknown.