Huerteales

LIGNOPHYTA

Plant a shrub or tree; true roots +, origin endogeneous, root cap +, apex multicellular; endodermis +; shoot apical meristem multicellular; lateral meristems +, cork cambium producing cork abaxially, vascular cambium producing phloem abaxially and xylem adaxially; lamina with mean venation density 1.8 mm/mm² (to 5 mm/mm²).

EXTANT SEED PLANTS/SPERMATOPHYTA

Plant woody, 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 derived from (some) sinapyl and particularly coniferyl alcohols, thus containing p-hydroxyphenyl and guaiacyl lignin units, so no Maüle reaction; root xylem exarch, cork cambium deep seated; arbuscular mycorrhizae +; shoot apical meristem interface specific plasmodesmatal network; stem with vascular tissue around central pith [eustele], vascular bundles with interfascicular tissue, ectophloic, endodermis 0, xylem endarch; 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 +; stem cork cambium superficial; branches exogenous; leaves with single trace from vascular sympodium ["nodes 1:1"]; vascular bundles collateral [stem: phloem external; leaf: phloem abaxial]; stomata morphology?, pore opening controlled by abscisic acid; leaves with petiole and lamina, spiral, development basipetal, blade simple; axillary buds +, not associated with all leaves; prophylls two, lateral; plant heterosporous, sporangia borne on sporophylls; microsporophylls aggregated in indeterminate cones/strobili; true pollen +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, parietal tissue 2+ cells across, megaspore tetrad tetrahedral, only one megaspore develops, megasporangium indehiscent; male gametophyte development first endo- then exosporic, tube developing from distal end of grain, to ca 2 mm from receptive surface to egg, gametes two, developing after pollination, with cell walls, flagellae numerous; ovules increasing considerably in size between pollination and fertilization, female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large" [ca 8 mm³], but not much bigger than ovule, with morphological dormancy; embryo cellular ab initio, endoscopic, plane of first cleavage of zygote transverse, suspensor +, short-minute, embryo straight, shoot and root at opposite ends [allorrhizic], white, cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, 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 nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.

MAGNOLIOPHYTA

Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, non-hydrolysable tannins, quercetin and/or kaempferol +, apigenin and/or luteolin scattered, [cyanogenesis in ANITA grade?], S [syringyl] lignin units common, positive Maüle reaction [syringyl:guaiacyl ratio more than 2-2.5:1], and 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, 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 unilacunar [1:?]; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, secondary veins pinnate, overall growth ± diffuse, venation hierarchical, fine venation reticulate, veins (1.7-)4.1(-5.7) mm/mm², endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, ± haplomorphic, parts spiral [esp. the A], free, numbers unstable, development in general centripetal; P not sharply differentiated, with a single trace, outer members not enclosing the rest of the bud, often smaller than inner members; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], ± embedded in the filament, with at least outer secondary parietal cells dividing, each theca dehiscing longitudinally, 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 columellar, endexine thin, compact, lamellate only in the apertural regions; nectary 0; G superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, dry [not secretory]; 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, megaspore tetrad linear, functional megaspore chalazal, lacking sporopollenin and cuticle; female gametophyte 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 binucleate at dispersal, male gametophyte trinucleate, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing between cells, growth rate 20-20,000 µm/hour, outer wall pectic, inner wall callose, 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, flagellae 0, double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; seed exotestal, becoming much larger than ovule at time of fertilization; endosperm diploid, cellular [micropylar and chalazal domains develop differently, 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; embryogenesis cellular; germination hypogeal, seedlings/young plants sympodial; Arabidopsis-type telomeres [(TTTAGGG)_n]; whole genome duplication, 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, paleo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]].

[NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]]: vessels +, elements with elongated scalariform perforation plates; 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]]]]: essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood 0; 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 +; 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 positiion]; embryo sac bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid; ?germination.

[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (veins in lamina often 7-17mm/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 scattered, asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; K/outer P members with three traces, "C" with a single trace; A few, (polyandry widespread, initial primordia 5, 10, or ring, ± centrifugal), 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?; 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 developing internally/adaxially to the corolla whorl and successively alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G [5], G [3] 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.

[DILLENIALES [SAXIFRAGALES [VITALES + ROSIDS s. str.]]]: nodes 3:3; stipules + [usually apparently inserted on the stem].

[SAXIFRAGALES [VITALES + ROSIDS]] / ROSANAE Takhtajan / SUPERROSIDAE: ??

[VITALES + ROSIDS] / ROSIDAE: anthers articulated [± dorsifixed, transition to filament narrow, connective thin].

ROSIDS: (mucilage cells with thickened inner periclinal walls and distinct cytoplasm); embryo long; genome duplication; chloroplast infA gene defunct, mitochondrial coxII.i3 intron 0.

ROSID II / MALVIDAE / [[GERANIALES + MYRTALES] [CROSSOSOMATALES [PICRAMNIALES [SAPINDALES [HUERTEALES [MALVALES + BRASSICALES]]]]]]: ?

[CROSSOSOMATALES [PICRAMNIALES [SAPINDALES [HUERTEALES [MALVALES + BRASSICALES]]]]]: ?

[PICRAMNIALES [SAPINDALES [HUERTEALES [MALVALES + BRASSICALES]]]]: ovules 2/carpel, apical.

[SAPINDALES [HUERTEALES [MALVALES + BRASSICALES]]]: flavonols +; vessel elements with simple perforation plates; (cambium storied); petiole bundle(s) annular; style +; inner integument thicker than outer; endosperm scanty.

[HUERTEALES [MALVALES + BRASSICALES]]: ?

Evolution. Divergence & Distribution. The age of the stem of this clade was estimated as (102-)96(-90) and (80-)76(-72) m.y. (two penalized likelihood dates); Bayesian relaxed clock estimates were similar to the first estimate (Wang et al. 2009), while Magallón and Castillo (2009) estimated ages of ca 98.1 and 98.4 m.y. for relaxed and constrained penalized likelihood datings.

HUERTEALES Doweld Main Tree, Synapomorphies.

Vessel elements with scalariform perforation plates; mucilage cells +; lamina margins toothed, stipules cauline; inflorescence cymose; flowers small, short hypanthium +, stamens = and opposite sepals; G [2], ovary unilocular; fruit a berry; exotegmen rather massive, of more or less strongly laterally-compressed fibres; endosperm +, embryo at most medium. - 4 families, 6 genera, 24 species.

Note: Possible apomorphies are now being added throughout the site; they 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 because there is very considerable homoplasy, with variation within and between clades, for most characters. Furthermore, the basic information for all too many characters is very incomplete, often coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there is the not-so-trivial issue of how ancestral states are reconstructed...

Evolution. Divergence & Distribution. For some comments on the biogeography of the groups, see Christenhusz and; Chase (2013)>

Chemistry, Morphology, etc. The morphology, anatomy, and secondary chemistry of the whole group are badly in need of detailed investigation. Overall, the flowers of Huerteales seem to be rather similar, although there is variation in androecial position in particular. The mechanical (lignified) layer of the seed may differ in its origin within the order, but I have tentatively suggested that exotegmic seeds are a synapomorphy for the clade, however, developmental studies of seeds of taxa like Gerrardina and Petenaea are much needed. Worberg et al. (2009) summarize what is known about this group, and information in their summary is slightly emended below; see also Yang et al. (2009) for chromosome numbers.

Phylogeny. For the association of the Tapisciaceae and Dipentodontaceae, see Peng et al. (2003), also James Horn (pers. comm.). Perrottetia was previously in Celastraceae, if only rather uneasily so; molecular data suggest that it is to be placed near Tapiscia (M. Simmons, in Matthews & Endress 2005b), a placement with which its morphology is in general agreement. Alford, when describing his Gerrardinaceae, found that Huerteales (Perrottetia not included), Brassicales and Malvales formed a polytomy, the combined group being rather poorly supported as sister to Sapindales. Gerrardina eylesiana shows a possibly superficial but still striking similarity to Perrottetia in particular, and perhaps there is a similarity in seed coat anatomy between the two genera, despite this they do not appear to be sister taxa (Worberg et al. 2009). Petenaea has recently been found to be rather weakly (bootstrap) associated with Gerrardina, and in general bootstrap values for relationships are low, even if posterior probabilities are higher (Christenhusz et al. 2010). Relationships within the order seem to be [[Gerrardinaceae + Petenaeaceae] [Tapisciaceae + Dipentodontaceae]], although Dipentodon is sister to Tapisciaceae in some analyses (Worberg et al. 2009).

Classification. Like Crossosomatales, Huerteales are accumulating several small families; when the clade is better known, rationalization (= reduction in number) may be in order - we hardly know enough so say whether or not the families are similar other than in gross phenetic terms.

Includes Dipentodontaceae, Gerrardinaceae, Petenaeaceae, Tapisciaceae.

Synonymy: Dipentodontales C. Y. Wu et al.

[Gerrardinaceae + Petenaeaceae]: ?

GERRARDINACEAE M. H. Alford Back to Main Tree

Vessel elements with scalariform perforation plates; petiole bundle arcuate, or three in an arc; mucilage cells in epidermis; leaves spiral, margin toothed, with vein proceeding to glandular tooth and with a branch to the vein above; C clawed, thin, small; stamens equal and opposite petals; nectary cupular; placentae apical, stigma?; seed with a fleshy outer layer, lignified laterally-compressed cells inside; endosperm ?type, embryo minute; n = ?

1[list]/2. Eastern and southern Africa (map: data from Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; GBIF, vii.2009).

Chemistry, Morphology, etc. Gerrardina foliosa appears to have clawed petals and three sepals larger than the others (ToL, vii.2009). See Alford (2006) for what little is known about the family; the description of the venation is modified from that source. Christenhusz et al. (2010) describe the wood anatomy of young stems. In addition, see G. eylesiana: stem anatomy, J. D. & E. G. Chapman 9242; leaf anatomy, Brass 16641; seed anatomy, Iversen et al. 85748; G. foliosa: stem and seed anatomy, Strey 11052; leaf anatomy, Hilliard & Burtt 6751.

Previous Relationships. Gerrardina has previously been included in Flacourtiaceae.

PETENAEACEAE Christenhusz, M. F. Fay & M. W. Chase Back to Main Tree

Vessels in radial multiples; leaves spiral, lamina venation palmate, stipules +; P valvate, with adaxial moniliform hairs and basal glands; P +; A 8-12; nectary +; G [5], placentae pendent, style long; ovules many; berry lobed, with a persistent style; n = ?

1/1: Petenaea cordata. Central America (map: from Christenhusz et al. 2010).

Petenaea is a distinctive plant with its spirally-arranged and palmately-nerved closely serrate leaves; its flowers are borne in branched inflorescences and the adaxial surface of the single perianth whorl is densely covered by pink, beaded hairs.

Chemistry, Morphology, etc. For the wood anatomy of Petenaea, see also Kukachka (1962). The genus is described as having minute stipules (Bayer 2002). For some general information, see Christenhusz et al. (2010).

Previous Relationships. Petenaea has previously been linked with Tiliaceae and Elaeaocarpaceae (Mabberley 2009), Bayer et al. (1999, but sampling) had suggested on molecular data that it might be associated with Malvales, being tentatively associated with Muntingiaceae (see also A.P.G. 2003).

[Tapisciaceae + Dipentodontaceae]: wood parenchyma 0.

TAPISCIACEAE Takhtajan Back to Main Tree

Wood fluorescing; fibres with simple pits; nodes also 5:5; petiole bundle annular, fibrous sheath 0; mucilage cells +; stomata paracytic; leaves spiral, odd-pinnately compound or trifoliolate, glands or stipels at articulations; K connate or not; (anthers extrorse, inflexed - Huertea); pollen colpate; nectary not vascularized (0); G septate or not, style hollow, apically branched or styles ± separate, stigma?; ovule 1/carpel, basal, apotropous, hypostase +; (fruit a drupe); testa thin-walled, (mesotesta sclerotic), chalaza ballooning into endosperm; endosperm ?type, embryo medium, coyledons flat; n = 13, 15.

2[list]/5. China (Tapiscia sinensis), West Indies and N. South America (map: from Ying et al. 1993; GBIF and TROPICOS vii.2009; fossils [blue] from Manchester 1988). [Photo - Fruit]

Tapisciaceae can be recognised by their spirally arranged, stipulate, odd-pinnately compound or trifoliolate leaves with serrate margins and glands or even foliaceous stipels at the point of articulation of the petiolule with the rhachis; the rhachis collapses at the nodes when the leaf dries. The flowers are small.

Evolution. Divergence & Distribution. The distinctive fruits of Tapiscia are known from the Eocene onwards in Europe, and somewhat later in North America (Manchester 1988; Manchester et al. 2009 and references).

Chemistry, Morphology, etc. Dickison (1987b) noted that small accessory traces from the central bundle also proceeded into the leaves. The pollen of Tapisciaceae is smaller than that of Staphyleaceae, being only some 13-18 µm long (Jin & Wei 2002). There is quite a prominent nectariferous disc in Huertea, but it is not vascularized (Dickison 1986a; Danilova 1996). The embryo is up to about half the length of the seed, and is embedded in copious endosperm. In Tapiscia sinensis, at least, the fruit takes about eighteen months to develop, the receptacle also becoming inflated and suberised (Liu et al. 2008; Teng & Liu 2009).

See also Corner (1976: seed anatomy), Carlquist and Hoekman (1985: wood anatomy), Dickison (1987a: pollen morphology) and Wei et al. (2002: pollen of Tapiscia), and for general information, see Kubitzki (2002d).

Previous Relationships. The two genera that make up the family were long included in Staphyleaceae (but see Corner 1976 for differences in seed coat and Dickison 1987b for a table of differences separating them from the rest of Staphyleaceae) and placed in Sapindales by Cronquist (1981), while a segregated Tapisciaceae were still included in Sapindales by Takhtajan (1997).

Synonymy: Huerteaceae Doweld

DIPENTODONTACEAE Merrill, nom. cons. Back to Main Tree

Trees; secondary veins pinnate; K and C similar, K ± valvate; micropyle endostomal [Perrottetia]; K + C persistent in fruit.

2/[list]16. Southeast Asia to Malesia, Mexico to Peru.

Dipentodon Dunn

Petiole bundle arcuate; ?stomata; hairs uniseriate; leaves two-ranked, stipules lobed; inflorescence umbellate; flowers 5(-7)-merous, hypanthium short, spreading; K and C valvate, basally connate; staminodial[?] nectaries opposite petals; G [3], placentation axile basally, ovules borne on top of placenta, with a free-central prolongation, stigma punctate; ?ovule morphology; fruit eventlaterally-compressedually ?septicidally dehiscent from the base upwards, ?funicle much enlarged; seed single; coat with obliquely-lying lignified ribbon cells, collapsed polygonal cells underneath; endosperm ?type, embryo ?very short; n = 17.

1/1: Dipentodon sinicus. S. China and adjacent Burma, India and Vietnam (map: from Yuan et al. 2008).

Perrottetia Kunth

(Vessel elements simple); paratracheal parenchyma +; sclereids +; petiole bundle depressed annular with an adaxial inverted bundle and wing bundles; stomata anomocytic (anisocytic); leaves distichous (spiral); inflorescence thyrsoid; (flowers 4-8-merous); ovary septate, style short, single; ovules basal, erect, epi-apotropous; seed arillate [Yang et al.]; testa thin-walled, ± fleshy, inner tangential walls of endotesta with rod-like structures, exotegmen ridged; endosperm ?type, embryo medium; n = 10.

1/ca 15. China to Malesia and N.E. Australia, Mexico to Peru (map: from Ding Hou 1962, New World rather approximate).

Chemistry, Morphology, etc. The flowers of Perrottetia may be imperfect. It has idioblasts in the sepals with thickened inner tangential walls, and the seeds lack an aril (Corner 1976; c.f. Ding Hou 1962).

Mabberley (1997) described the leaves of Dipentodon as being spiral. In the two flowers that I examined I could find only a single well-developed ovule in each.

For general information on Perrottetia, see Ding Hou (1962), for seed coat, see Corner (1976), for floral morphology, etc., see Matthews and Endress (2005b: also mucilage cells!), for mostly stomatal morphology, see den Hartog and Baas (1978), for vegetative anatomy, see P. sessiliflora - Cogollo et al. 7294. For general information on Dipentodon, see Merrill (1941), for pollen, see Lobreau-Callen (1982), and for floral morphology and a comparison with putatively related taxa, see Liu and Cheng (1991).

Previous relationships. Dipentodontaceae were included in Santalales by Cronquist (1981) because of apparent similarities in gynoecial structure, but the toothed lamina margin and large, lobed stipules suggested that this was incorrect. They were placed by Takhtajan (1997) in his Violales (= Malpighiales), while Wu et al. (2002, 2003) recognised a Dipentodontales C. Y. Wu et al. in Dilleniidae, where it was placed between Passiflorales (which included Caricaceae) and Violales (Cucurbitales were next).