EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, initially ±globular; showing gravitropism; acquisition of phenylalanine lysase [PAL], phenylpropanoid metabolism [lignans +, flavonoids + (absorbtion of UV radiation)], xyloglucans in primary cell wall with distinctive side chains; 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, precursor for starch synthesis in plastid.
Many of the bolded characters in the characterization above are apomorphies of subsets of streptophytes along the lineage leading to the embryophytes, not apomorphies of crown-group embryophytes per se.
All groups below are crown groups, nearly all are extant. Characters mentioned are those of the immediate common ancestor of the group,  contains explanatory material, () features common in clade, exact status unclear.
Abscisic acid, L- and D-methionine distinguished metabolically; 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]: xyloglucans in the primary cell wall with fucosylated subunits; gametophyte leafless; archegonia embedded/sunken [on;y neck protruding]; sporophyte long-lived, chlorophyllous; cell walls with xylans.
Sporophyte dominant, branched, branching apical, dichotomous, potentially indeterminate; vascular tissue +; stomata on stem; sporangia several, each opening independently; spore walls not multilamellate [?here].
EXTANT TRACHEOPHYTA / VASCULAR PLANTS
Sporophyte with photosynthetic red light response; (condensed or nonhydrolyzable tannins/proanthocyanidins +); 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 +); xylans 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.
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].
Plants heterosporous; megasporangium surrounded by cupule [i.e. = unitegmic ovule, cupule = integument]; pollen lands on ovule; megaspore germination endosporic [female gametophyte initially retained on the plant].
EXTANT SEED PLANTS / SPERMATOPHYTA
Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins particularly with guaiacyl and p-hydroxyphenyl [G + H] units [sinapyl units uncommon, no Maüle reaction]; root stele with xylem and phloem originating on alternate radii, cork cambium deep seated; 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; seeds "large" [ca 8 mm3], but not much bigger than ovule, with morphological dormancy; embryo cellular ab initio, suspensor short-minute, embryo with roots arising at the end of the main axis [plant allorhizic, shoot and root at opposite ends], white, 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; stele di- to pentarch [oligarch], pith relatively inconspicuous, lateral roots arise opposite or immediately to the side of [when diarch] xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0, hypodermis suberised and with Casparian strip [= exodermis]; shoot apex with tunica-corpus construction, tunica 2-layered; 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; sugar transport in phloem passive; 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, 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, 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]]]]: 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).
MONOCOTYLEDONS / MONOCOTYLEDONEAE / LILIANAE Takhtajan
Plant herbaceous, perennial, rhizomatous, growth sympodial; non-hydrolyzable tannins [(ent-)epicatechin-4] +, neolignans, benzylisoquinoline alkaloids 0, hemicelluloses as xylans; root apical meristem?; epidermis developed from outer layer of cortex; trichoblasts in atrichoblast [larger cell]/trichoblast cell pairs, the former further from apical meristem, in vertical files; endodermal cells with U-shaped thickenings; cork cambium [uncommon] superficial; stele oligo- to polyarch, medullated [with prominent pith], lateral roots arise opposite phloem poles; stem primary thickening meristem +; vascular bundles scattered, (amphivasal), vascular cambium 0 [bundles closed]; tension wood 0; vessel elements in roots with scalariform and/or simple perforations; tracheids only in stems and leaves; sieve tube plastids with cuneate protein crystals alone; stomata parallel to the long axis of the leaf, in lines; prophyll single, adaxial; leaf blade linear, main venation parallel, the veins joining successively from the outside at the apex and forming a fimbrial vein, transverse veinlets +, unbranched [leaf blade characters: ?level], vein/veinlet endings not free, margins entire, Vorläuferspitze +, base broad, ensheathing the stem, sheath open, petiole 0; inflorescence terminal, racemose; flowers 3-merous [6-radiate to the pollinator], polysymmetric, pentacyclic; P = T, each with three traces, median T of outer whorl abaxial, aestivation open, members of whorls alternating, [pseudomonocyclic, each T member forming a sector of any tube]; stamens = and opposite each T member [primordia often associated, and/or A vascularized from tepal trace], anther and filament more or less sharply distinguished, anthers subbasifixed, endothecium from outer secondary parietal cell layer, inner secondary parietal cell layer dividing; pollen reticulations coarse in the middle, finer at ends of grain, infratectal layer granular; G , with congenital intercarpellary fusion, opposite outer tepals [thus median member abaxial], placentation axile; ovule with outer integument often largely dermal in origin, parietal tissue 1 cell across; antipodal cells persistent, proliferating; fruit a loculicidal capsule; seed small to medium sized [mean = 1.5 mg], testal; embryo long, cylindrical, cotyledon 1, apparently terminal, with a closed sheath, unifacial [hyperphyllar], both assimilating and haustorial, plumule apparently lateral; primary root unbranched, not very well developed, stem-borne roots numerous, hypocotyl short, (collar rhizoids +); no dark reversion Pfr → Pr; duplication producing monocot LOFSEP and FUL3 genes [latter duplication of AP1/FUL gene], PHYE gene lost.
[ALISMATALES [PETROSAVIALES [[DIOSCOREALES + PANDANALES] [LILIALES [ASPARAGALES + COMMELINIDS]]]]]: ethereal oils 0; raphides + (druses 0); leaf blade vernation supervolute-curved or variants, (margins with teeth, teeth spiny); endothecium develops directly from undivided outer secondary parietal cells; tectum reticulate with finer sculpture at the ends of the grain, endexine 0; (septal nectaries +) [intercarpellary fusion postgenital].
[PETROSAVIALES [[DIOSCOREALES + PANDANALES] [LILIALES [ASPARAGALES + COMMELINIDS]]]]]: cyanogenic glycosides uncommon; starch grains simple, amylophobic; leaf blade developing basipetally from hyperphyll/hypophyll junction; epidermis with bulliform cells [?level]; stomata anomocytic, (cuticular waxes as parallel platelets); colleters 0.
[[DIOSCOREALES + PANDANALES] [LILIALES [ASPARAGALES + COMMELINIDS]]]: nucellar cap 0; endosperm nuclear [but variation in most orders].
[LILIALES [ASPARAGALES + COMMELINIDS]]: (inflorescence branches cymose); protandry common.
[ASPARAGALES + COMMELINIDS]: style long; whole nuclear genome duplication [τ/tau event].
Unlignified cell walls fluorescing blue under UV, green with NH3 [ferulic acid ester-linked]; exodermal cells monomorphic; (vessels in stem and leaves); SiO2 bodies +, in leaf bundle sheaths; stomata para- or tetracytic, (cuticular waxes as aggregated rodlets [looking like a scallop of butter]); inflorescence branches determinate, peduncle bracteate; P = K + C, bicyclic [stamens adnate to/inside corolla/inner whorl only]; pollen starchy; embryo short, broad.
[POALES [COMMELINALES + ZINGIBERALES]]: primary cell wall mostly with glucurono-arabinoxylans; stomata subsidiary cells with parallel cell divisions; endosperm reserves starchy.
[COMMELINALES + ZINGIBERALES]: inflorescences with many-flowered cincinnal branches [helicoid cymes]; P = T; A opposite individual T members; tapetum invasive/amoeboid.
ZINGIBERALES Grisebach Main Tree.
Giant herbs; no aerial stem except when flowering; sieve tube plastids also with starch grains; petiole bundles in arcs; guard cells symmetric [inner and outer ledges of stomatal chamber equal] cuticular waxes as aggregated rodlets; leaf with petiole and blade, midrib +, lateral veins S-shaped , more than a single order, fine transverse venation; inflorescence branches spirally arranged; inflorescence bracts large, persistent; flowers large [>2 cm long], monosymmetric; A 5 [but different stamens fertile in different clades]; orbicules 0; anthers long [>5 mm long]; pollen inaperturate, exine at most thin, spinulose, to 0, outer intine thick, channeled; G inferior, (septal nectaries labyrinthine), style long, stigma large, elongate-clavate, wet; ovule with outer integument >5 cells across, epidermal cells of nucellus apex radially elongated [nucellar pad], suprachalazal tissue well developed; fruit opening laterally, loculicidal; seeds arillate, with germination valves, [operculate testa], micropylar collar + [developing from outer integument, forming annular inpushing in perisperm surrounding operculum], endotesta sclerotised and silicified, thickening often U-shaped in t.s.; endosperm nuclear, perisperm s.l. +, reserves starchy, embryo plug-like; cotyledon not photosynthetic, ligulate, collar roots +; 12-base insertion at 3' end of matK, six nucleotide deletion in atpA, whole nuclear genome duplication [γ/gamma event]. - 8 families, 92 genera, 2,185 species.
Age. Crown-group Zingiberales are dated to ca 88 m.y. (Janssen & Bremer 2004). Comparable figures are 62 m.y. in Bremer (2000b) and (66-)62, 57(-54) and (42-)38(-34) m.y. in Wikström et al. (2001). Magallón and Castillo (2009) estimated ages of 87 and 79.5 m.y. and Bell et al. (2010) (89-)84 m.y.; figures are around 83.5 m.y. (Tank et al. 2015: Table S2, Strel. 86.2 m.y.), (96-)67(-52) m.y. (Merckx et al. 2008a) and 75-30 and 66-26 m.y. (Mennes et al. 2013, 2015 respectively). However, Kress and Specht (2005, 2006) gave rather older crown group ages of ca 96.6 m.y. and 110-106 m.y. respectively and late Jurassic/early Cretaceous around 150 m.y.a. is the age in Fleming and Kress (2013, but c.f. their Fig 7.3), however, (85-)76(-65) and (60-)56(-54) m.y. are ages in Hertweck et al. (2015). - These dates all need checking in the context of the topology suggested by Sass et al. (2016).
The distinctive seeds of Spirematospermum are known from the Late Cretaceous; they have in the past often been placed with Musaceae or Zingiberaceae or unplaced other than to order (Collinson & van Bergen 2004; Benedict 2011; Friis et al. 2011: also other fossils; Smith et al. 2013b). Recent suggestions are that a place in stem Zingiberaceae is appropriate (Isles et al. 2015).
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. It is suggested that there was a rapid radiation of Zingiberales in the early Caenozoic some 65 m.y.a. (see also Christelova et al. 2011); families other than Cannaceae and Marantaceae had all diverged by ca 60 m.y. (Kress & Specht 2005), or all families had diverged by 86-74 m.y.a. (Kress & Specht 2006). However, Janssen and Bremer (2004) found divergence dates within Zingiberales to show a wide spread; those estimated under the DELTRAN optimisation were notably younger than under the two other regimes used.
A nice Zingiberales "tree" at the website of the Smithsonian Institution - Zingiberales Research - has for a decade or so depicted relationships in Zingiberales as [Musaceae [[Strelitziaceae + Lowiaceae] [Heliconiaceae + the Zingiberaceae group]]]. Such a tree allowed Rudall and Bateman (2004) to suggest that there had been a change in symmetry in the order. The basic condition for the order was the suppression of the adaxial median stamen of the inner whorl, Pattern 1 monosymmetry, which tended to be linked with labellum formation (see Lowiaceae). The abaxial median stamen of the outer whorl was similarly suppressed in the [Heliconiaceae + the Zingiberaceae group] clade, Pattern 2 monosymmetry (see also Kirchoff et al. 2009), and there had been a transition between the two (1 → 2). Of course, the adaxial median stamen would need to regain its fertility, not mentioned by Rudall and Bateman (2004), and the flowers of Heliconiaceae are inverted compared with those of the Zingiberaceae group. Using the same tree, Yockteng et al. (2013) emphasized the role of the duplication of SEP-like genes, two copies of SEP3 showing balancing selection, two LOFSEP copies showing balancing selection, while AGL6 genes - only a single copy, and not expressed in staminodes of the Zingiberaceae group - were involved in stamen development.
Given the extensive floral variation (in particular) in Zingiberales, they are certainly an order in which a well-supported phylogeny is needed before we can think much about morphological evolution. If the topology suggested by Sass ert al. (2016: see below) holds up, the features in common between Musaceae, Strelitziaceae, and Lowiaceae - the median inner tepal ± reduced, free, and hooded, and the median stamen of the inner androecial whorl being staminodial or absent, and the tapetum, will have evolved in parallel and/or have been lost and regained. Given the variation in features like symmetry and perianth type within Commelinales (see also Rudall & Bateman 2004) - both oblique monosymmetry and a tepaloid perianth with stamens individually opposite perianth members are found there, too - things get still trickier. Polarization of some of the features in the ordinal characterization above has depended on the [[Cannaceae + Marantaceae] [Costaceae + Zingiberaceae]] clade being embedded in the ordinal tree, not sister to a clade made up of the other four families, and this has been confirmed (see also Barrett et al. 2013; Sass et al. 2016).
When the two whorls of tepals are differentiated, both are still more or less petal-like, the inner usually being larger and sometimes differently coloured. In Phenakospermum (Strelitziaceae), and both Heliconiaceae and Musaceae, the tepals are largely undifferentiated (see also Payer 1857). Stamens are individually opposite members of both whorls in these families in particular. However, the recently-described Musa nanensis, with its more or less polysymmetric flowers, six tepals in two distinct whorls (the inner tepals are much smaller) and all connate, and six basally connate stamens (Swangpol et al. 2015) is decidedly odd. In the Marantaceae-Costaceae clade the two perianth whorls individually encircle the floral apex as is common in the commelinids. Interestingly, the short, broad, concave staminode of Heliconia and inner adaxial tepal of Strelitzia and most species of Musa look quite similar; at one level the flowers are similar, at another, rather different. For further discussion on monosymmetry see especially the Marantaceae-Costaceae clade below.
Variation in stamen number and morphology is very great (Fleming & Kress 2013 for a summary). More or less flattened and petal-like filaments are common, and this is associated with balanced ad/abaxial expression of polarity genes, as in many leaves (Almeida et al. 2014).
Endress (2011a) thought that an inferior ovary might be a key innovation for the clade.
For a still interesting general discussion on the evolutionary morphology of the order, focusing primarily on vegetative morphology, see Tomlinson (1962a).
Ecology & Physiology. In plants of Musaceae, Heliconiaceae and Strelitziaceae growing in more or less open conditions, the leaves tear along the veins producing a kind of compound leaf (c.f. Arecaceae). They can be conspicuous members of this vegetation, Phenakospermum, for example, being notably common in Amazonian rainforest (Fauet et al. 2015).
Givnish et al. (2005, 2006b) noted that net venation, animal-dispersed propagules and tolerance of shady habitats are linked in this group, as elsewhere in monocots.
Pollination Biology. Animal pollination pervades the order, and bird pollination in particular is perhaps notably common (Cronk & Ojeda 2008). In humming birds, much involved in the pollination of Heliconiaceae, crown-group diversification in lowland South America is (24.7-)22.4(-20.3) m.y.a. (Bleiweiss 1998a; McGuire et al. 2007, 2014) or (29.9-)28.8(-28.4) m.y.a. (Tripp & McDade 2014). Euglossine bees are also important pollinators of neotropical Zingiberales (Zucchi et al. 1969; Williams 1982), and the bees began diversifying some 42-27 m.y.a. (Ramírez et al. 2010). However, Fleming and Kress (2013) suggested that understanding the evolution of pollination was difficult, given a crown-group age in the late Jurassic/early Cretaceous around 150 m.y.a.; they thought that vertebrate pollination was ancestral (but c.f. their Fig. 7.3, where the crown-group age of Zingiberales is less than 100 m.y.).
Plant-Animal Interactions. McKenna and Farrell (2005, 2006) discuss the diversification of the chrysomelid beetle Cephaloleia on Zingiberales; they also occur on some other commelinids and on Cyclanthaceae and Orchidaceae (see also Staines 2004; García-Robledo et al. 2013). Both feeding on Zingiberales and specialisation of the larvae and particularly adults on the young, rolled leaves may each have evolved once; the association between the beetles and Zingiberales may date from the very late Cretaceous (Wilf et al. 2000; McKenna & Farrell 2006). However, ascribing feeding patterns in fossil material to the particular activities of hispine beetles may not be possible (García-Robledo & Staines 2008), so dating this association is complicated (see also Gómez-Zurita et al. 2007). Food plants of the Hesperiinae-Calopodini skippers are quite common here - caterpillars of most other skippers eat Poaceae (Warren et al. 2009).
Genes & Genomes. There has been a triplication of the CYC-like gene in the clade (Bartlett & Specht 2009, 2011) as well as duplications of GLOBOSA-like genes (Bartlett & Specht 2010) that are perhaps involved in floral diversification and the evolution of monosymmetry; for the γ genome duplication, see D'Hont et al. (2012). A genome duplication in Musa has been dated to (68.9-)66.1(-62.8) m.y.a. (Vanneste et al. 2014a). For the atpA deletion, see Davis et al. (2004). Mahanty (1970) and Song et al. (2004) suggest that the base chromosome number for the order is 11.
Chemistry, Morphology, etc. The phenol zingerone (C11H14O3) has apparently been isolated from Eocene fossils of Spirematospermum (see above); is its presence a synapomorphy for the order (van Bergen & Collinson 1999)? The roots tend to have V-shaped aggregations of xylem, with an especially large metaxylem element at the angle (von Guttenberg 1968), and although the central stele of Strelitziaceae and Musaceae, with intermingled xylem and phloem occupying more of less the entire central part of the stem, seems very distinctive, careful reading of Tomlinson (1969) shows that other taxa commonly tend to do this. Arber (1925) suggests that the cauline vascular bundles are not amphivasal, but I have not checked this against recent anatomical literature. Korn (2006) noted that Musa and Calathea ornata were unusual in that in all the individuals that he examined the foliar genetic spiral proceeded in the same direction, although in plants of other species clockwise and counter-clockwise spirals occurred in equal frequencies, and asymmetry of the base of the leaf blade is notable in this order (see also Martinez et al. 2016). For a summary of leaf venation, see Salvi et al. (2014).
Musaceae have various kinds of determinate inflorescences (Kunze 1985). Bracteoles are more or less lateral in Canna, Costus, Heliconia, etc., and flowers of the first seem to have inverted orientation (see also Heliconia below), while the flowers of Marantaceae may have an oblique plane of symmetry - at one level, not very different. There is variation in the stage at which monosymmetry is evident in the flower (see also Kirchoff 2003; Kunze et al. 2005c). Endress (1994b) noted that there may be massive development of endothecial/and/or lignified tissue on the connective side of the anther. Although pollen grains of the order are apparently inaperturate, they range from functionally monoaperturate or omniaperturate (Kress 1986; Furness & Rudall 2000b). How widely distributed stamens supplied by several vascular traces are in the order is unclear (see Rao et al. 1954 for some records).
For sieve tube inclusions, etc., see Behnke (1994), for phenylphenalenones, see Otálvaro et al. (2002), for vegetative anatomy, see Tomlinson (1969), for phytoliths, see Piperno (2006) and Benvenuto et al. (2015), and for vessel and tracheid micromorphology, see Carlquist and Schneider (2010); for information on floral anatomy, see Rao et al. (1954), on nectary and nectary duct morphology and position, see Kirchoff (1992) and Stauffer et al. (2009), on the tapetum, see Furness and Rudall (2001), on ovules, see Mauritzon (1936d), on seed morphology and anatomy, Humphrey (1896), Mauritzon (1936d), Grootjen and Bouman (1981), Manchester and Kress (1993), and Liao et al. (2004), and on cytology, see Satô (1960: primitive karyotype established by comparison with Takakia, a moss) and Mahanty (1970).
Phylogeny. For discussion of the relationships of Zingiberales, see the Arecales page.
Phylogenetic relationships within the order have been much studied, but they some still remain unclear - see especially Kress (1990b, 1995) and Andersson and Chase (2001: Costaceae and Zingiberaceae not obviously sister taxa). Musaceae were weakly (barely over 50%) supported as sister to the rest of the order in Kress et al. (2001: 2 genes + morphology, successive approximation weighting, see also Janssen & Bremer 2004), and slightly better, but still not that well (78%) supported as member of a clade [Heliconiaceae, Musaceae, [Lowiaceae + Strelitziaceae]] in Givnish et al. (2006b: one gene), while Wikström et al. (2001: three genes) found the relationships [Musaceae [Heliconiacaeae [[Lowiaceae + Strelitziaceae] [the Zingiberaceae group]]]] and in Magallón et al. (2015) Strelitziaceae are sister to the rest of the order. Even the Zingiberaceae group, [[Costaceae + Zingiberaceae] [Marantaceae + Cannaceae]], was not not found in some analyses (e.g. Davis et al. 2004: support values very low; Soltis et al. 2007a), or relationships within this group were scrambled (Wikström et al. 2001). Johansen (2005), looking at six DNA regions (plastid, nuclear), suggested that Lowiaceae and Strelitziaceae were successively sister to remaining Zingiberales, which would make reconstruction of character evolution of the flowers in particular ambiguous; however, support was not strong and sampling other than in Orchidantha, the focus of the paper, was poor. Bell et al. (2010) found the relationships [Musaceae [[Cannaceae + Heliconiacaeae] [Lowiaceae + Strelitziaceae] [Zingiberaceae [Costaceae + Marantaceae]]]. Yockteng et al. (2013) prefered the relationships [Musaceae [[Strelitziaceae + Lowiaceae] [Heliconiaceae + the Zingiberaceae group]]], although they obtained other relationships as well as between Zingiberales and other monocots in separate analyses of the SEPALLATA, AGL6 and LOFSEP genes.
Barrett et al. (2012b) found the relationships [Heliconiaceae [Musaceae + Zingiberaceae]] among the four taxa whose complete chloroplast genomes they analyzed; support was not strong. After adding plastid genomes from nine other members of the order (Barrett et al. 2013: codon-based likelihood analyses), the relationships *[Heliconiaceae [*[Musaceae [Strelitziaceae + Lowiaceae]] [[Cannaceae + Marantaceae] [Costaceae + Zingiberaceae]]]] were obtained, although support for the clades with asterisks was slight. Most recently, Sass et al. (2016) analyzed 308 nuclear gene exons and 68 plastid genes for 53 Zingiberales, and in most analyses they retrieved the relationships [Musaceae [[Heliconiacaeae [Lowiaceae + Strelitziaceae]] [[Zingiberaceae + Costaceae] [Cannaceae + Marantaceae]]]], however, in perhaps suspect coalescent analyses, support for the basal position of Musaceae dropped below 50%, the most dramatic drop in the whole tree.
Classification. For a detailed classification of the order, see Kress et al. (2001), c.f. the phylogeny here.
Includes Cannaceae, Costaceae, Heliconiaceae, Lowiaceae, Marantaceae, Musaceae, Strelitziaceae, Zingiberaceae.
Synonymy: Amomales Lindley, Cannales Berchtold & J. Presl, Lowiales Reveal & Doweld, Marantales Martius, Musales Berchtold & J. Presl
MUSACEAE Jussieu, nom. cons. Back to Zingiberales
Plant cormose; (phenylphenalenones +); SiO2 bodies ± trough-shaped; roots not medullated, centre portion occupied by scattered wide vessels and strands of phloem; rhizome with endodermis; sieve tube plastids also with peripheral protein fibres; laticifers +, articulated; mucilage cells +; petiole with 1 series of ± abaxial air canals; plant glabrous; prophylls lateral; leaves spiral, petiole short, buds not axillary [leaf-opposed]; plant monoecious; inflorescence bracts deciduous, cincinni at right angles to the main axis, floral bracts and bracteoles 0; T connate [?position], connation congenital, median inner T ± reduced, hooded [cucullate], free, (all 6 T connate, whorls strongly differentiated); septal nectary labyrinthine; staminate flowers: median [adaxial] A of inner whorl absent, (A 6; basally connate), with several vascular bundles; anther wall formation of the basic type [Musella s. str.], tapetum glandular, exothecium +, endothecium poorly developed; pistillode +; carpellate flowers: staminodes +, G with intra-ovarian trichomes, loculi mucilaginous, stigma capitate; ovules (micropyle exostomal), outer integument "massive", inner integument 2-3 cells acoss, cells anticlinally elongated, hypostase +; fruit a berry; seed with chalazal chamber, micropylar collar well developed, aril?, the inner periclinal exotestal wall siliceous, crystals exposed by exfoliation of the outer part of the testa, mesotesta 20-25 cells across, sclerotised; n = 9(-11), chromosomes 1.2-2.9 µm long; collar at right angles to cotyledon.
2[list]/41. Africa, Himalayas to South East Asia, Philippines and N. Australia (map: J. Kress, pers. comm.). [Photos - Collection.]
Age. Crown-group Musaceae are dated to ca 61 m.y.a. (Janssen & Bremer 2004), and ages suggested by Christelova et al. (2011) are similar, being (80.5-)69.1(-57.8) m.y.; those in Bell et al. (2010) are younger, (51-)36, 34(-20) m.y.a., as are those in in Wikström et al. (2001) - (55-)50, 48(-43) or (35-)39(-25) m.y. ago. Kress and Specht (2005, 2006) offered crown group ages of around 47.5 and ca 87 or 51 m.y.a. respectively.
Evolution. Divergence & Distribution. Musaceae - Ensete oregonense - are known fossil in Eocene deposits some 43 m.y. old from west North America (Manchester & Kress 1993) - quite a range extension when compared with the distributions of extant taxa.
Pollination Biology. As with Heliconiaceae, the inflorescence may be erect or pendent, and insects, birds, bats and tree shrews are all known pollinators (Nur 1976; Liu et al. 2002; Xue et al. 2005 and references).
Genes & Genomes. There may have been one (or more) duplications in the genome (polyploidization) of this clade some 60 m.y.a. (Lescot et al. 2008; see also D'Hont et al. 2012; McKain et al. 2016).
The mitochondria, but not the chloroplasts, are paternally inherited in Musa (Fauré et al. 1994).
Economic Importance. For general information on the domestication of the banana (Musa spp. and hybrids), see Heslop-Harrison and Schwarzacher (2007) and for breeding, etc., see Pillay and Tenkouano (2011); see Piperno (2006) for phytoliths and domestication.
Chemistry, Morphology, etc. For the remarkable polysymmetric flowers of Musa nanensis, see Swangpol et al. (2015). Does the endosperm have a small chalazal chamber?
Some information is taken from Andersson (1998: general), Tomlinson (1959, 1969: anatomy), Fahn (1983: inflorescence), Xue et al. (2005: microsporogenesis, etc., 2007: embryology of Musella), Fahn et al. (1961: nectary), Kirchoff (1992: ovary), and Graven et al. (1996: seed).
Phylogeny. Liu et al. (2010) and Li et al. (2010) discuss the phylogeny of the family, in which there are two main clades; the suckering Musella is derived from the non-suckering Ensete in the former, but in some analyses in the latter the two were sister taxa.
[[Heliconiaceae [Strelitziaceae + Lowiaceae]] [[Cannaceae + Marantaceae] [Costaceae + Zingiberaceae]]]: ?
Age.Suggested ages for this node are (61-)52, 50(-43) m.y.a. (Bell et al. 2010), (61-)57, 53(-49), (37-)33(-29) m.y. (Wikström et al. 2001), around 96.6 and 109.3 m.y.a. (Kress & Specht 2006, 2006 respectively), and 75-30 m.y.a. (Mennes et al. 2013).
[Heliconiaceae [Strelitziaceae + Lowiaceae]]: ?
HELICONIACEAE Vines Back to Zingiberales
Rhizome with endodermoid layer; SiO2 bodies decorated and trough-shaped; anticlinal walls of epidermal cells sinuous, stomata polycytic, neighbouring cells with oblique divisions; petiole long; inflorescence branches often 2-ranked; flowers obliquely monosymmetric; 5 T connate, connation postgenital, median [adaxial] member of outer whorl ± free, recurved; A 5, basally adnate to T, staminode = median adaxial member of outer whorl, ± hooded; tapetum at least initially non-syncytial; pollen asymmetric, heteropolar [± hat-shaped], functionally monoaperturate; ovule 1/carpel, basal, apotropous, micropyle bistomal; fruit fleshy, schizocarp or drupe, endocarp well developed, operculate, operculum derived from funicle; testa and tegmen thin, undifferentiated; n = (11) 12, chromosomes 1.4-4.5 µm long; coleoptile 0, but sheath lobed, collar at right angles to cotyledon.
1[list]/100-200. Mostly tropical America, a few Celebes to the Pacific (map: Old World from Kress 1990a; New World, J. Kress, pers. comm.). [Photo - Flower, Flower.]
Age. Estimates of the age of divergence of crown group Heliconia are ca 87 or 32-28 m.y., depending on the method used (Kress & Specht 2006), or ca 32 m.y.a. (McKenna & Farrell 2006).
Evolution. Pollination Biology & Seed Dispersal. Variation in floral and inflorescence morphology is considerable (Berry and Kress 1991), as in Musaceae, the inflorescences being erect or pendant. Humming bird pollination is prevalent, and Heliconia is a major nectar resource for sickle-bill humming birds (Eutoxeres) and other hermits, trap-lining pollinators, at lower altitudes in the New World (they may also nest underneath the leaves); at higher altitudes, as in the Andes, the birds take nectar from Centropogon (Campanulaceae-Lobelioideae) (Stiles 1975; Stein 1992; Kress & Beach 1994; Pedersen & Kress 1999; Fleming et al. 2005).
Water collects in the inflorescence bracts of species with erect inflorescences. The corolla is held just above the surface of the water for the pollinator, although the ovary may be under water; later the thick and fleshy pedicel elongates raising the fruits above the water and making them accessible for the seed disperser.
Plant-Animal Interactions. The herbivorous Cephaloleia beetles (Cassidinae+Hispinae, Chrysomelidae) seem to have diversified in the Oligocene coincident with crown Heliconia diversification (McKenna & Farrell 2006).
Chemistry, Morphology, etc. Kirchoff et al. (2009) suggest that the flower of Heliconia is obliquely monosymmetric (the characterization above follows this interpretation), the floral diagram in Eichler (1875) shows an inverted orientation; clarification is in order. There are pollen-connecting threads derived from the break-down of cell walls (Rose & Barthlott 1995; Simão et al. 2007). The parietal tissue soon disintegrates.
Additional information is taken from Andersson (1998; general), Tomlinson (1959, 1969: anatomy), and Kirchoff (1992: ovary); see Stone et al. (1979), Prakash et al. (2000), Kress (1986b) and Simão et al. (2007) for pollen and anther and Simão et al. (2006) for ovule and seed.
[Strelitziaceae + Lowiaceae]: growth monopodial; petiole with adaxial and abaxial series of air canals; inflorescences axillary; T whorls differentiated, 2 abaxial members of inner whorl enclosing stamens, median member of inner whorl ± reduced, hooded [cucullate], free; staminode = median [adaxial] A of inner whorl; tapetum glandular; apex of ovary prolonged, sterile [= "floral column"], stigma 3-lobed; outer integument 14-20 cells across; aril of long hairs; both exo- and endo-testa developed.
Age. Suggested ages for this node are (52-)48, 45(-41) or (30-)26(-22) m.y. (Wikström et al. 2001), (53-)42, 40(-30) m.y. (Bell et al. 2010), and ca 78 m.y. (Janssen & Bremer 2004); ages in Kress and Specht (2005, 2006) are around 49.1 and 96-80 m.y.a. respectively.
Chemistry, Morphology, etc. The exostomal aril is lobed or fimbriate. For details of anatomy, see Tomlinson (1959), and of the floral column, the result of intercalary growth at the top of the ovary, see Kirchoff and Kunze (1995).
STRELITZIACEAE Hutchinson, nom. cons. Back to Zingiberales
(Plant arborescent), (stem dichotomizing), (growth sympodial - Pheonakospermum; phenylphenalenones +; roots not medullated, centre portion with scattered wide vessels and strands of phloem; vessels also in stem (not Ravenala); SiO2 bodies ± druse-like; stems often lacking endodermis; petiole with several arcs of air canals; anticlinal walls of epidermal cells sinuous, hypodermis 3-6-seriate; inflorescence branches 2-ranked; (T whorls not differentiated), 2 lateral members of inner whorl basally connate, large; (A 6 - Ravenala), stamen with three or more vascular bundles, staminode 0; tapetal cells to 32-ploid; stigma long-turbinate; ovules with bistomal micropyle, outer integument ca 17 cells across, suprachalazal area massive; capsule woody; micropylar collar 0, operculum rudimentary, seed coat sclerenchymatous, tegmen only a cuticle; (perisperm 0); n = (7, 9) 11, chromosome length?; primary root well developed.
3[list]/7. Tropical South America, E. southern Africa, Madagascar (map: J. Kress, pers. comm.). [Photo - Flower]
Age. Crown-group Strelitziaceae are dated to (33-)29(-25) or (22-)18(-14) m.y. (Wikström et al. 2001), ca 59 m.y. (Janssen & Bremer 2004), or (36-)25, 23(-14) m.y. (Bell et al. 2010); ages in Kress and Specht (2005, 2006) are around 25.3 and ca 74 or 58-55 m.y. (depends on the methods used) respectively.
Evolution. Pollination Biology. Pollination in the group has been much studied, although it is unclear what the plesiomorphic condition might be (c.f. Kress et al. 1994).
Chemistry, Morphology, etc. The rhizomes of Strelitzia reginae branch dichotomously (Fisher 1976). Stomatal morphology may vary depending on where in the plant the stomata are; the basic morphology seems to be brachyparacytic, with cells at the two ends of the stomata often being shorter than other epidermal cells, and there may be other associated and more or less thick-walled cells (Tomlinson 1960).
Thread-like structures are found in the anthers of Strelitzia; these are formed from rows of epidermal cells (Kronestedt & Bystedt 1981).Some information is taken from Andersson (1998: general); he suggested that staminodes were absent; for anatomy, see Tomlinson (1969), for floral morphology of Strelitzia, see Kronestedt & Walles (1986), for the remarkable arils of Strelitzia, see Pfeiffer (1891), Serrato-Valenti et al. (1991), and Pirone et al. (2010) and references.
Phylogeny. Relationships are [Ravenala [Heliconia + Phenakospermum]] (e.g. Kress & Specht 2006).
LOWIACEAE Ridley, nom. cons. Back to Zingiberales
SiO2 bodies ± conical; starch grains angular; endodermoid layer in rhizome; fiber cells or bundles of fibers in leaf; stomata paracytic, guard cells asymmetric [inner and outer ledges of the chamber unequal]; cross veins +, in abaxial part of blade; inflorescence of repeating 1-flowered units, branching from bracts below the flower, the flower axillary; prophyll 0 [?all]; flowers resupinate or not; outer T unequal, basally connate or not, inner median T large [= labellum when resupinate], inner abaxial pair small; A basally adnate to inner T, grouped around style, (inner median staminode +); ?tapetum; septal nectary 0/non-functional; ovary prolongation several times the length of the ovary, stigma complex, monosymmetric, apex tubular, expanded, unequally three-lobed, lobes ± fimbriate, secretory tissue on adaxial side at base [= viscidium]; ovule with outer integument 14-16 cells across, inner integument ca 4 cells across; aril of few hairs; seed shortly hairy to smooth, micropylar collar?, testa vascularized, exotesta and next two layers lignified, endotesta of radially elongated sclereids; perisperm slight; n = 9, chromosomes 4.3-6.6 µm long; seedling?
1[list]/20. S. China to Borneo (map: J. Kress, pers. comm.; Sakai & Inoue 1999).
Age. Crown-group Lowiaceae may be around 3 or 19-13 m.y.o. (Kress & Specht 2005, 2006 respectively: ?sampling).
Evolution. Pollination Biology. The flowers last one day. They may be held in an inverted position, the adaxial median petal then forming a labellum. The flowers smell foul, and the apparently nectarless Orchidantha inouei is pollinated by scarabeid dung beetles (Sakai & Inoue 1999).
Chemistry, Morphology, etc. The longitudinal and horizontal vascular bundle systems of the leaf blades appear independent of one another in cross section. The stamens are opposite both calyx and corolla separately (Kirchoff & Kunze 1995). Extra-floral nectaries, when present, may be non-functional and the apical prolongation of the ovary is traversed by the stylar canal (Kirchoff & Kunze 1995, c.f. Larsen 1998)). It is not clear if the endotesta is silicified.
Much information is taken from Larsen (1998); see also Tomlinson (1969: anatomy), Kunze (1986: esp. inflorescence), Pedersen (2001) and Pedersen and Johansen (2004) both flowers, and Wen et al. (1997: seed).
The family is very poorly known.
Phylogeny. Johansen (2005) provides a phylogeny of the family.
[[Cannaceae + Marantaceae] [Costaceae + Zingiberaceae]]: SiO2 bodies ± spherical/druse-shaped; raphides 0; petiole with one series of air canals; stomata paracytic, guard cells asymmetric in transverse section [inner and outer ledges unequal]; petiole short, poorly differentiated; inflorescence branches spiral; P fully bicyclic, inner whorl connate, A not opposite all T members; A 1 [= median (adaxial) member of inner whorl], 2 A of both whorls staminodial, ± petal-like, median [abaxial] member of outer A whorl 0/staminodial; (tapetum multilayered), non-syncytial; micropyle endostomal; cells of exotesta longitudinally elongated, endotestal cells large, sclerified; chalazosperm + [= perisperm of some authors], endosperm slight.
Age. Ages suggested for this node are (51-)47(-43) and (32-)28(-24) m.y. (Wikström et al. 2001: note topology), ca 47.7 m.y.o. (Magallón et al. 2015) or ca 84 m.y.a. (Janssen & Bremer 2004). Similar, if rather older, ages are suggested by Kress and Specht (2005, 2006), the crown group being estimated at ca 88.5 and 106-100.5 m.y. old respectively.
Chemistry, Morphology, etc. Costus, Canna and Kaempferia and at least some other genera have more or less lateral floral prophylls (e.g. Rüter 1918). Zingiberaceae and Cannaceae have anther placentoids (Weberling 1989).
Some information on seed anatomy is taken from Tang et al. (2005); there is no mention of starch in the endosperm; for some floral morphology, see Endress (1995b). Judd et al. (2007) provide useful information.
[Cannaceae + Marantaceae]: vessels in stem; oblique cells at apex of petiole [in longitudinal view]; flowers asymmetric; A bisporangiate, monothecal, staminodes free; stigma not notably expanded; endosperm absent or almost so, cells of chalazal intrusion into nucellus degenerate forming chalazal channel; embryo long; x = 9.
Age. The Cannaceae and Marantaceae clades diverged 101-91 m.y.a. (Kress & Specht 2006), ca 68 m.y.a. (Janssen & Bremer 2004), (54-)45, 43(-36) m.y.a. (Bell et al. 2010: note position of Cannaceae) or as little as 38.2 m.y.a. (Magallón et al. 2015); ages in Kress and Specht (2005, 2006) are around 80.1 and 96-91 m.y. respectively.
Evolution. Pollination Biology. Although both Cannaceae and Marantaceae have asymmetric flowers and secondary pollen presentation, details of both are quite different in the two families.
Chemistry, Morphology, etc. CiGLO, a B-class MADS-box gene, is, rather surprisingly, expressed in the petals, stamens, and also gynoecium (Yu et al. 2014).
For flowers, see Kirchoff (1983: table of equivalencies of different parts of flowers of Cannaceae and Marantaceae) and Kunze (1984), for ovules, etc., see Johri et al. (1992), for the micropylar collar, see Boesewinkel and Bouman (1984).
CANNACEAE Jussieu, nom. cons. Back to Zingiberales
Chelidonic acid, aromatic resin +; mucilage canals in stem; (leaves spiral); inflorescence branched; flower short-lived; fertile ½ stamen with petaloid appendage, staminodes 1-4(-5); tapetal cells 2-6-nucleate; microsporogenesis also successive; G muricate, style flattened, secondary pollen presentation [pollen deposited on abaxial surface of style], stigma on one edge; outer integument ca 10 cells across; capsule glandular-muricate; seed pachychalazal, funicle hairy, aril 0, imbibition lid on raphe, micropylar collar 0, operculum 0, malpighian layer formed by exotesta and also epidermis of chalaza, mesotesta sclereidal, endotesta 0; n = 9, chromosomes 2.1-3.4 µm long; primary root well developed, collar roots +.
1[list]/10. New World (sub)tropics (map: Maas-van de Kamer & Maas 2008). [Photo - Flower]
Age. Crown group Cannaceae may be around 32-24 m.y.o. (Kress & Specht 2005, 2006).
Evolution. Divergence & Distribution. Diversification in Cannaceae has slowed down (Hertweck et al. 2015).
Pollination Biology & Seed Dispersal. Pollen is deposited on the abaxial surface of the flattened style whence it is picked up by the pollinator.
The seeds may retain their ability to germinate for some 600 years (references in Grootjen & Bouman 1988).
Chemistry, Morphology, etc. Floral diagrams in Eichler (1875) suggest that the prophyll is lateral and the plane of symmetry of the flower inverted. The nature of tha androecium is unclear. Miao et al. (2014a, b) suggested that in Canna indica the fertile ½ stamen represents two primordia, one member of the outer whorl (the fertile bit) and one member of the inner whorl (the petaloid bit); the labellum there consists of another member of the outer whorl and another member of the inner whorl. On the other hand, Almeida et al. (2013) thought that both the fertile and petaloid parts were produced by a single half anther. ABC-type floral genes have very broad expression patterns across the various floral organs (Almeida et al. 2013).
The micropyle becomes zig-zag after fertilization of the flower. Grootjen and Bouman (1988) described a pachychalaza in Cannaceae, with mitosis occurring during ovule development in the chalaza and basal part of the nucellus. This is unlike the pachychalaza in other zingiberalean families. An aril appears to be absent (e.g. Grootjen & Bouman 1981), and the hairy funicle (see above) is unique in Zingiberales.
Additional information is taken from Tomlinson (1961b, 1969: anatomy), Kubitzki (1998d: general), Tanaka (2001: revision), Maas-van de Kamer and Maas (2008: monograph), and Tanaka et al. (2009: cytology).
Phylogeny. For phylogenetic relationships in the genus, see Prince (2010); the North American Canna flaccida is sister to the rest of the clade, whose origin is perhaps to be sought in South America.
MARANTACEAE R. Brown, nom. cons. Back to Zingiberales
(Aerial stem +); (mucilage canals - Thalia); SiO2 bodies also hat-like; (stomata anomocytic); leaf sheath closed; petiole often long, pulvinate at the apex [oblique cells]; (inflorescence bracts deciduous); flowers in mirror image pairs [2-flowered units], of moderate size, median member of the outer whort adaxial; inner whorl T and A develop before outer whorl T and A; C, A and style all basally fused, (outer staminodes 0), one inner staminode hooded [= staminodium cucullatum], another ± fleshy and with callosities [= staminodium callosum], fertile half stamen often with a petal-like lateral appendage; (only 1 G fertile), style under tension, becoming curved, secondary pollen presentation [pollen deposited on secretory area on adaxial surface of style, the "stamp"]; ovule 1/carpel, basal, becoming amphitropous, (micropyle bistomal - Phrynium), outer integument 6-8(-12) cells across, (nucellar cap ca 2 cells across), lateral epidermal cells dividing periclinally; (fruit a berry); mesotesta tanniniferous, operculum endotestal, (tegmen with thin elongated sclereids); embryo curved; n = ?4, (9-13), chromosomes "very small"; (mesocotyl +), collar at right angles to cotyledon.
31[list]/550: Goeppertea (250). Tropics, esp. American, not in Australia (map: from Heywood 1978; Andrew Ford, pers. comm.; Fl. N. Am. 4: 2003; ; Trop. Afr. Fl. Pl. Ecol. Distr. 7. 2012). [Photo - Leaf, Flower.]
Age. Divergence within the crown group is dated to ca 56.7 or 71.5-61 m.y. (Kress & Specht 2005, 2006: Marantochloa + Mar.) or ca 57 m.y. (Janssen & Bremer 2004); ages of (26-)23(-20) and (17-)14(-11) m.y. (Wikström et al. 2001: Cal. + Mar.) have also been suggested, but note sampling in all these studies.
Evolution. Divergence & Distribution. Marantaceae may have originated in Africa, with subsequent dispersal to South East Asia and the New World ((Andersson & Chase 2001; Ley & Claßen-Bockhoff 2011b). Marantaceae are considerably more speciose than Cannaceae, perhaps because of their distinctive explosive pollen transfer mechanism (Ley & Claßen-Bockhoff 2009), although it is likely that a variety of factors have shaped diversification (Ley & Claßen-Bockhoff 2011b). There is considerable asymmetry of clade size within the family; the oligospecific Thalia and Haumania are both sister to far more speciose clades.
Pollination Biology & Seed Dispersal. Marantaceae have complex, highly integrated, enantiostylous, asymmetric flowers. Pollination is explosive. The style is held under tension by the hooded inner staminode (the staminodium cucullatum) that has various lobes and appendages (Pischtschan et al. 2010), while the other inner staminode (the staminodium callosum) is firm and fleshy, with knobs, etc., on its adaxial surface. Sticky pollen is deposited on the flattened stamp on the adaxial surface of the style by the early-maturing anther while the flower is still in bud, and there is an adjacent secretory area. The progress of the pollinator in the flower is guided by the knobs, etc., of the firm staminode, and the flower is tripped by the pollinator when it comes into contact with an appendage on the hooded staminode. The style then abruptly curves and pollen from the stamp of that flower, aided by the secretions of the adjacent secretory area, is deposited on the pollinator, and pollen from another flower deposited on the stigma itself, which is depressed (Ley & Claßen-Bockhoff 2011b, 2012).
During pollination, the sensitive style can move across the flower in 0.33 seconds, most of the movement occurring within about 0.0033 seconds (Claßen-Bockhoff 1991b). The anatomy of the style is distinctive, with a combination of collenchymatous cells, large intercellular spaces, extensive elliptical openings on the walls, and separation of the cells by breakdown of the primary wall starting before the flower opens. As the style moves, there is extensive redistribution of water between the cells (Pischtschan & Claßen-Bockhoff 2010).
In the New World in particular, long-tongued, trap-lining euglossine bees are the main pollinating agents, and the floral tube lengths of New World Marantaceae are appreciably longer than their Old World representatives, ca 17.6 mm long versus ca 4.6 mm long. Interestingly, there are no intrinsic barriers to selfing (see Claßen-Bockhoff 1991b for floral morphology and function and Kennedy 2000 for general information, also Andersson 1998; Classen-Bockhoff & Heller 2008 for a developmental study on the diversity of form of some New World Marantaceae). African Marantaceae are pollinated by large and small bees and sunbirds, and there has been parallel evolution of the various morphologies involved when compared with New World taxa also with bee and bird pollination (Ley & Claßen-Bockhoff 2010, 2011a, esp. 2009 for details). The main floral types have evolved in the context of adaptation to different pollinators, but variation in tube length alone may allow effective pollination by very different kinds of pollinator within the one floral type (Ley & Claßen-Bockhoff 2010, 2011b). Hooded staminodes with a rather simplified morphology may be derived (Pischtschan et al. 2010; Ley & Claßen-Bockhoff 2011b).
For seed dispersal in some New World Marantaceae, dispersed by birds or ants, see Horvitz et al. (2002 and references).
Chemistry, Morphology, etc. The plant body is made up of repeating units consisting of a prophyll, a reduced leaf (both with short internodes), and then expanded leaves. These latter vary in number and internode length (although the first is often longest) and also orientation, since the plane of distichy of a unit may be at right angles to that of its parent axis.
The inflorescence is almost mind-bogglingly complex (Tomlinson 1961a; Andersson 1976; Kunze 1985); the latter suggests that the apparently indeterminate units that bear the paired flowers are modified from determinate structures. There has been much recent work on floral morphology and development. The basic orientation of the flower is inverted, the adaxial sepal being median (Pischtschan & Claßen-Bockhoff 2008; Ley & Claßen-Bockhoff 2011b, 2012).
Some information is taken from Andersson (1981, 1998: general), who questioned the chromosome numbers reported for the family because of the small size of the chromosomes, problems with the identity of the material counted, etc. For morphology and anatomy, see Tomlinson (1961a, 1969), and for seed morphology, see Grootjen (1983).
Phylogeny. Prince and Kress (2006a) suggest that five informal groups be recognized, the Sarcophrynium, Stachyphrynium, Maranta, Donax and Calathea clades. Relationships between these clades is for the most part unclear (very low bootstrap vales, mostly high posterior probabilities alone), and support for the five informal groups themselves other than the Stachyphrynium and Maranta groups (also well supported as sister taxa) is little better (Prince & Kress 2006b: eight genes, all three compartments). For relationships among Asian members of the Stachyphrynium and Donax clades, see Suksathan et al. (2009).
Classification. See Andersson and Chase (2001) for a phylogenetic classification of the family. However, this now hardly reflects what is known about phylogeny, and Prince and Kress (2006a) suggest that five informal groups be recognized (see above). Studies on Asian members of the Stachyphrynium and Donax clades has led to generic realignments - Phrynium was paraphyletic (Suksathan et al. 2009), while Calathea is polyphyletic, most of its species being placed in Goeppertea (Borchsenius et al. 2012).
[Costaceae + Zingiberaceae]: fibrous sheath in stem; leaf ligulate; bracteole lateral; outer T connate; stamen with three or more vascular bundles [?sampling]; filament flattened, connective prolonged, abaxial member of outer A whorl staminodial, all 5 staminodes connate ["lateral staminodes fused to labellum"], forming labellum, with narrow tube and distinct open limb; exine + [so pollen resistant to acetolysis]; nectary +, vascularized, not septal; style slender, running between two half anthers, stigma cup- or funnel-shaped, ± bilobed; ovule with hypostase; endotesta well developed; endosperm helobial, persistent, not that copious; seedling with well developed hypocotyl.
Age. Estimates for the time of divergence of these two families are ca 83 or 105-99 m.y.a. (Kress & Specht 2005, 2006 respectively) and ca 79 m.y.a. (Janssen & Bremer 2004).
The seed fossil Spirematospermum chandlerae 83.6-72.1 m.y.o. has been placed as stem-node Zingiberaceae (Isles et al. 2015).
Evolution. Divergence & Distribution. For possible additional floral synapomorphies, see Specht et al. (2001).
Chemistry, Morphology, etc. The fibrous sheath in the stem may be outside the vascular bundles, or somwhat more interior (Tomlinson 1969). For floral development, see Rao et al. (1954) and Kirchoff (1988a). The massive stamens of Costus and some Zingiberaceae, at least, have several vascular bundles (Rao et al. 1954). Van Heel (1988) described the gynoecium of Costus as having septal nectaries, that of Zingiberaceae as lacking them; what the nectaries of Costaceae "are" morphologically is still unclear (see also Rao et al. 1954; Newman & Kirchoff 1992).
COSTACEAE Nakai Back to Zingiberales
(Plant epiphytic); aerial stem +, (branched); benzoquinones, steroidal saponins +; sheath with 1 series of adaxial air canals, no canals in petiole and blade, vascular bundles adaxial; hypodermis ³1 layered; (hairs multicellular); leaves spiromonostichous, sheath closed; inflorescence spicate-capitate, (axillary), unbranched, (flowers single); floral bracts often with abaxial nectaries; anthers with several vascular bundles, filaments medium; pollen aperturate; nectary branched, tubular, ± above ovary loculi; (G ), stigma with adaxial projection, fimbriate; outer integument 5-6 cells across; chalaza sunken in the mature seed, chalazal chamber +; endosperm without starch; n = 9 (14); cotyledon blade-like, photosynthetic, with apical backwardly-directed process; n = 9, chromosomes 2.3-3.7 µm long.
6[list]/110: Costus (90). Pantropical, esp. America and Papuasia-Australia (map: Maas 1972; Trop. Afr. Fl. Pl. Ecol. Distr. 7. 2012). [Photo - Costus © L. Brothers, Dimerocostus © L. Brothers.]
Age. Divergence within crown group Costaceae can be dated to (30-)27, 26(-23) and (18-)15(-12) m.y.a. (Wikström et al. 2001), ca 47 m.y. (Janssen & Bremer 2004), or 23.2 m.y.a. and 74 or 52-47 m.y.a. (Specht 2005, 2006 respectively).
Evolution. Divergence & Distribution. Specht (2006) discussed the diversification and biogeography of the family in detail.
Pollination Biology & Seed Dispersal. For floral evolution and pollination, see Specht (2005; also Kay et al. 2005; Kay & Schemske 2003). Humming bird pollination seems to have been particularly important in facilitating diversification of neotropical Costus, but euglossine bees are also effective pollinators (Salzman et al. 2015). There are often extrafloral nectaries on the inflorescence bracts that are visited by ants.
Species with seeds that are dispersed by ants are common here (Lengyel et al. 2010).
Chemistry, Morphology, etc. How the leaves become spiromonistichous in the course of development was detailed by von Veh (1931).
The bracteole is described as being lateral and consistently anodic by Kirchoff (1988b) and is drawn in an adaxial-oblique position by Ronse de Craene (2010). The pollen is particularly variable, being disulcate, porate, pantoporate or spiraperturate; the grains are resistant to acetolysis. There are two to four rows of ovules (Newman & Kirchoff 1992). The endosperm is oily.
Some information is taken from Tomlinson (1969: anatomy), Panchaksharappa (1963: embryology), Larsen (1998: general), Grootjen and Bouman (1981: ovule and seed development) and Kirchoff (1988b: floral morphology).
Phylogeny. Specht (2006) provides a detailed phylogeny of the family (see also Specht et al. 2001); the clade [Chamaecostus [Dimerocostos + Monocostus]] is sister to the rest, within which the distinctive Tapeinochilos is embedded.
Classification. A generic revision (Specht & Stevenson 2006) is based on an earlier phylogeny of the family in which Costus turned out to be polyphyletic (Specht 2006); the genera that they recognize can be characterized morphologically.
ZINGIBERACEAE Martinov, nom. cons. Back to Zingiberales
Phenylpropanoids and related curcumins, ethereal oils +; SiO2 usu. as sand; (vessels also in stem); sieve tubes with nuclear non-dispersive crystalline protein bodies; oil cells +; (hairs with sunken bases); plane of distichy of leaves of axillary bud at right angles to the main axis; (leaf sheath closed); vascular bundles in leaf axis abaxial; hypodermis 0-1-layered; (inflorescence bracts deciduous); anther crest petaloid, filament short, median A of outer whorl 0; nectaries 2, on top of ovary; ovules (1-)many/carpel, outer integument (5-)7-13 cells across; (nucellar cap +), lateral epidermal cells dividing periclinally, epistase +; (embryo sac with postament); fruit fleshy, opening loculically and laterally; (hairs on seed); seed testal, exotesta of fibriform cells, uniseriate, micropylar hilar rim [external tube or flange]; endotestal cells parenchymatous, chalazal pigment cells disciform; chalazosperm 0; embryo ± length of seed, (curved) [plumular end L- or J-shaped]; n = 8-14+; seedling collar not prominent.
46-52[list]/1075-1340 - four groups below. (Sub)tropical, esp. South East Asia-Malesia (map: from Maas 1977; Heywood 2007; Trop. Afr. Fl. Pl. Ecol. Distr. 7. 2012). [Photo - Fruit.]
Age. The age of crown-group Zingiberaceae is somewhat more than 70 m.y. (Auvray et al. 2010, age of Zingiberopsis).
1. Siphonochiloideae W. J. Kress
Plants show dormancy; rhizome fleshy, ± vertical; inflorescence a raceme, bracteoles 0; filament of fertile stamen adnate to base of labellum, forming a tube above point of insertion of petals; raphe externally visible, aril solid, micropylar; (exotesta multiseriate), micropylar collar 0; n = 13, 14, 21.
1-2/20. Africa and Madagascar.
[Tamijioideae [Alpinioideae + Zingiberoideae]]: 12-base insertion at 3' end of matK absent.
2. Tamijioideae W. J. Kress
Plants evergreen; rhizome fibrous; inflorescence axes separate from vegetative axes; placentation parietal; fruit and seeds unknown.
1/1: Tamijia ciliaris. Borneo.
[Alpinioideae + Zingiberoideae]: (root ± not medullated, centre portion with phloem strands); (blade with extrafloral nectaries on adaxial midrib); (anther crest 0); aril usu. surrounding more than half the seed, adpressed; (chalazal chamber +); endosperm without starch.
Age. Divergence of these two subfamilies has been dated to ca 26 m.y. (Janssen & Bremer 2004); ages of (11-)10(-9) and (6-)5(-4) m.y. (Wikström et al. 2001) and ca 65 m.y. (calibration point) (Kress & Specht 2005, 2006) have also been suggested.
3. Alpinioideae Link
Plants evergreen; rhizome fibrous; filament medium; lateral staminodes of outer whorl very small or 0; micropylar hilar rim usu. 0; endotesta lignified, endotestal chalazal pigment cells non-disciform [trumpet-shaped, etc.]; perisperm with simple starch grains, endosperm lacking starch, (seed with chalazal chamber); embryo medium to long; n = 12, chromosomes 0.7-4.5 µm long.
20/920. Mainly Indo-Malesia, also tropical Australia and American and African tropics.
3A. Alpinieae A. Richard
(Styloids + - Aframomum); (placentation free-central); (fruit indehiscent); (raphe externally visible); (n = 11).
16/815Alpinia (200), Etlingera (110), Amomum (150), Renealmia (75), Aframomum (60), Hornstedia (50). Indo-Malesia, American and African tropics Renealmia only.
Synonymy: Alpiniaceae Link, Amomaceae Jaume Saint-Hilaire
3B. Riedelieae W. J. Kress
Blade with extrafloral nectaries on adaxial midrib; (placentation parietal); fruits elongated, opening to the base; aril micropylar, solid; n = 12.
4/105. Riedelia (75). Eastern Malesia, also Australia (Queensland) and Thailand, both one species.
4. Zingiberoideae Hasskarl
Plants show dormancy; rhizomes fleshy, (starchy roots or tubers); plane of distichy of leaves of axillary bud parallel to the main axis; filament short to long; (tapetum amoeboid); (placentation basal), style with 2 vascular bundles; (micropylar collar 0); hairs on seed; starch grains of perisperm compound, endosperm with starch [aleurone]; chromosomes 2.1-5.8 µm long.
29/680. Indo-Malesia, tropical Australia.
4A. Zingibereae Petersen
Pseudostem common; (steroidal saponins + - Hedychium); (pollen sulcate - Zingiber); (anther crest wrapped around style), lateral staminodes (adnate to C tube), (lateral staminodes and/or labellum reduced or 0); (placentation basal or free-central); fruits globose or ovoid, fleshy, (indehiscent); aril various, inc. carunculate, hairs on seed usu. 0, (seeds not operculate - Hedychium); starch grains of perisperm compound; n = ?
25/570. Curcuma (100), Zingiber (100), Boesenbergia (60), Hedychium (50). Indo-S. China-Malesia, tropical Australia.
Synonymy: Curcumaceae Dumortier
4B. Globbeae Petersen
(Anther crest spurred); lateral staminodes and/or labellum and filament connate (not); placentation parietal; (seeds carunculate); exotesta usu. multiseriate; starch grains of perisperm simple; n = (8, 10, 11, 12, 14) 16, 24 (etc.).
4/110: Globba (100). Indo-S. China-Malesia.
Evolution. Divergence & Distribution. Renealmia is the only genus of Zingiberaceae in South America, and it seems to have migrated from Africa to America within the last 16 m.y. (Särkinen et al. 2007). Aframomum is its sister taxon, and there diversification may have begun ca 34.3-25.2 m.y.a., although some other estimates are much younger (Auvray et al. 2010).
Some species of Curcuma may be of hybrid origin. In one of these, C. vamana, members of one putative parent group are currently ca 2,000 km distant, yet most of the features of C. vamana are of this group (Záveská et al. 2012).
Much "familial" information like sieve tube morphology is properly to be placed at the [Alpinioideae + Zingiberoideae] node, the situation in other two subfamilies being unknown. Benedict et al. (2015b) optimise a number of seed characters on the tree.
Pollination Biology. For a detailed study of floral morphology and pollination (pollinators: two kinds of bees and a nectariniid spiderhunter) in some Bornean gingers, see Sakai et al. (1999b, 2013). Ley and Harris (2014) looked at floral morphology in the African Aframomum; there most species had purple, trumpet-shaped flowers that were probably pollinated by bees. Flexistyly (the style changing its orientation during anthesis) is scattered through Alpinioideae (Kress et al. 2005 and references).
Economic Importance. For Zingiber, the spice ginger, etc., see Ravinandran and Babu (2005).
Chemistry, Morphology, etc. The plane of distichy of leaves of the axillary bud is commonly at right angles to the axis, so sequential branches have leaves at right angles to each other; the prophyll is, as usual for monocots, adaxial. In Zingiberoideae the plane is parallel to the axis, so the rhizomes, as of Zingiber itself, readily form a flat, branching-digitate complex.
Although Larsen et al. (1998) suggest that Hedychieae lack an operculum in the seed, Grootjen and Bouman (1981) report one from Hedychium itself. Globba and Hedychium and relatives (Zingiberoideae) lack U-shaped cells in the endotesta. Pommereschea has a parenchymatous endotesta (Liao & Wu 2000). Ellettaria has an embryo almost as long as the seed.
Some information is taken from Larsen et al. (1998) and Kress et al. (2002), both general, Tomlinson (1956, 1969: anatomy), Uma and Muthukumar (2014: root anatomy), Harling (1949: embryology), Liao and Wu (1996) and Benedict et al. (2015a: Alpinioideae, 2015b, whole family, X-ray tomographic microscopy), all seed anatomy, Beltran and Kiew (1984: cytology), Wood et al. (2000: Hedychium and relatives), Poulsen (2012: Etlingera) and Sakai and Nagamasu (2000: Tamija). For floral morphology and development, see Rao (1963: nectaries), Rao et al. (1954), Kirchoff (1997: Hedychium, i.a. distinctive floral orientation), Box and Rudall (2006: Globba) and Kong et al. (2007: Globba).
Phylogeny. Basic relationships in the family are [Siphonochiloideae [Tamijioideae [Alpinioideae + Zingiberoideae]]]; all clades have strong support (Kress et al. 2002: two genes; Harris et al. 2006).
For a phylogeny of part of Alpinioideae, see Pedersen (2004) and especially Kress et al. (2005); Alpinia, Etlingera, and Amomum are all more or less strongly para/polyphyletic. Särkinen et al. (2007) provide a phylogeny of the African-American Renealmia and Auvray et al. (2010) of the African Aframomum.
Ngamriabsakul et al. (2004) discuss relationships within Zingiberoideae-Zingibereae; for a phylogeny of Globbeae, see Williams (2003), while Záveská et al. (2012) clarify the limits of Curcuma.
Classification. Generic limits in Alpinioideae need attention (e.g. Xia et al. 2004; Kress et al. 2007). Záveská et al. (2012) include four small genera in Curcuma and provide a subgeneric classification.