EMBRYOPSIDA Pirani & Prado (crown group)

Gametophyte dominant, independent, multicellular, thalloid, with single-celled apical meristem, showing gravitropism; flavonoids + [absorbtion of UV radiation]; protoplasm dessication tolerant [plant poikilohydric]; cuticle +; cell walls with (1->4)-ß-D-glucans [xyloglucans], lignin +; rhizoids unicellular; several chloroplasts per cell; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles in vegetative cells 0, metaphase spindle anastral, predictive preprophase band of microtubules, phragmoplast + [cell wall deposition spreading from around the spindle fibres], plasmodesmata +; antheridia and archegonia jacketed, stalked; spermatogenous cells monoplastidic, centrioles develop de novo, associated with basal bodies of flagellae, multilayered structure +, proximal end of basal bodies lacking symmetry, stellate pattern associated with doublet tubules of transition zone; spermatozoids with a left-handed coil; male gametes with 2 lateral flagellae; oogamy; diploid embryo initially surrounded by haploid gametophytic tissue, plane of first division horizontal [with respect to long axis of archegonium/embryo sac], suspensor/foot +, cell walls with nacreous thickenings; sporophyte multicellular, sporangium +, single, with polar transport of auxin, dehiscence longitudinal; meiosis sporic, monoplastidic, microtubule organizing centre associated with plastid, cytokinesis simultaneous, preceding nuclear division, sporocytes 4-lobed, with a quadripolar microtubule system; spores in tetrads, sporopollenin in the spore wall, wall with several trilamellar layers [white-line centred layers, i.e. walls multilamellate]; spores trilete; close association between the trnLUAA and trnFGAA genes on the chloroplast genome.

Note that many of the bolded characters in the characterization above are apomorphies in the streptophyte clade along the lineage leading to the embryophytes rather than being apomorphies of the crown embryophytes.

STOMATOPHYTES

Abscisic acid, ?D-methionine +; sporangium with seta, seta developing from basal meristem [between epibasal and hypobasal cells], sporangial columella + [developing from endothecial cells]; stomata +, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and in rhizoids/root hairs; polar transport of auxins and class 1 KNOX genes expressed in the sporangium alone; MIKC, MI*K*C* and class 1 and 2 KNOX genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns.

[Hornworts + Polysporangiophyta]: archegonia embedded/sunken in the gametophyte; sporophyte long-lived, chlorophyllous, nutritionally largely independent of the gametophyte; sporophyte-gametophyte junction interdigitate, sporophyte cells showing rhizoid-like behaviour.

POLYSPORANGIOPHYTA

Sporophyte well developed, branched, free living, sporangia several; spore walls not multilamellate [?here]; apical meristem +.

EXTANT TRACHEOPHYTA / VASCULAR PLANTS

Photosynthetic red light response; water content of protoplasm relatively stable [plant homoiohydric]; control of leaf hydration passive; (condensed or nonhydrolyzable tannins/proanthocyanidins +); vascular tissue +, sieve cells + [nucleus degenerating], tracheids +, in both protoxylem and metaxylem; endodermis +; root xylem exarch [development centripetal]; stem with an apical cell; branching dichotomous; leaves spirally arranged, blades with mean venation density 1.8 mm/mm2 [to 5 mm/mm2]; sporangia adaxial on the sporophyll, sporangia derived from periclinal divisions of several epidermal cells, wall multilayered [eusporangium]; columella 0; tapetum glandular; stellate pattern split between doublet and triplet regions of transition zone; placenta with single layer of transfer cells in both sporophytic and gametophytic generations, embryo with roots arising lateral to the main axis [plant homorhizic].

[MONILOPHYTA + LIGNOPHYTA]

Branching ± monopodial; lateral roots +, endogenous, root apex multicellular, root cap +; tracheids with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangia borne in pairs and grouped in terminal trusses, dehiscence longitudinal, a single slit; cells polyplastidic, microtubule organizing centres not associated with plastids, diffuse, perinuclear; male gametes multiflagellate, basal bodies staggered, blepharoplasts paired; chloroplast long single copy ca 30kb inversion [from psbM to ycf2].

LIGNOPHYTA

Plant woody; lateral root origin from the pericycle; branching lateral, meristems axillary; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].

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 derived from (some) sinapyl and particularly coniferyl alcohols [hence with p-hydroxyphenyl and guaiacyl lignin units, so no Maüle reaction]; root with xylem and phloem originating on alternate radii, vascular tissue not medullated, cork cambium deep seated; arbuscular mycorrhizae +; shoot apical meristem interface specific plasmodesmatal network; stem with vascular cylinder around central pith [eustele], phloem abaxial [ectophloic], endodermis 0, xylem endarch [development centrifugal]; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; stem cork cambium superficial; branches exogenous; leaves with single trace from vascular sympodium [nodes 1:1]; stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; leaves with petiole and lamina, 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 linear, functional megaspore single, chalazal, lacking sporopollenin, megasporangium indehiscent; pollen grains landing on ovule; male gametophyte development first endo- then exosporic, tube developing from distal end of grain, gametes two, developing after pollination, with cell walls; 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 with roots arising at the end of the main axis [plant allorhizic, shoot and root at opposite ends], white, cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, whole nuclear genome duplication [zeta duplication], two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], nrDNA with 5.8S and 5S rDNA in separate clusters; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.

MAGNOLIOPHYTA

Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, 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 1:?; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance to increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, venation hierarchical-reticulate, secondary veins pinnate, 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 +, 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], ± 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; 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 thin, compact, lamellate only in the apertural regions; nectary 0; carpels present, superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, 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, functional megaspore lacking cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; supra-stylar extra-gynoecial compitum +; ovule not increasing in size between pollination and fertilization; pollen grains landing on stigma, bicellular at dispersal, mature male gametophyte tricellular, 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; dark reversal Pfr -> Pr; Arabidopsis-type telomeres [(TTTAGGG)n]; 2C genome size 1-8.2 pg [1 pg = 109 base pairs], whole nuclear genome duplication [epsilon duplication]; protoplasm dessication tolerant [plant poikilohydric]; ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, 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]]]]]: 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 +; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; carpels plicate; nucellar cap + [character lost where in eudicots?]; 12BP [4 amino acids] deletion in P1 gene.

[[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]] / MESANGIOSPERMAE: benzylisoquinoline alkaloids +; sesquiterpene synthase subfamily a [TPS-a] [?level], polyacetate derived anthraquinones + [?level]; outer epidermal walls of root elongation zone with cellulose fibrils oriented transverse to root axis; P more or less whorled, 3-merous [possible position]; pollen tube growth intra-gynoecial; 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?; root epidermis developed from outer layer of cortex; trichoblasts in atrichoblast [larger cell]/trichoblast cell pairs, the former further from apical meristem, in vertical files, or hypodermal cells dimorphic; endodermal cells with U-shaped thickenings; cork cambium in root [uncommon] superficial; root vascular tissue oligo- to polyarch, medullated, lateral roots arise opposite phloem poles; primary thickening meristem +; vascular bundles in stem scattered, (amphivasal), closed, vascular cambium 0; tension wood 0; vessel elements in root 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 base ensheathing the stem, sheath open, petiole 0, blade linear, main venation parallel, main veins joining successively from the outside at the apex, transverse veinlets +, unbranched, vein/veinlet endings not free, margins entire, Vorläuferspitze +, colleters + ["intravaginal squamules"]; inflorescence terminal, racemose; flowers 3-merous [6-merous 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; G [3], 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 testal; endosperm with distinct nuclear and chalazal chambers, 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 [?level]; epidermis with bulliform cellls [?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).

[ASPARAGALES + COMMELINIDS]: style long.

COMMELINIDS

Unlignified cell walls fluorescing blue under UV, green with NH3 [ferulic acid ester-linked]; (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 or amoeboid.

ZINGIBERALES Grisebach  Main Tree.

Giant herbs; no aerial stem except when flowering; SiO2 in bundle sheath; sieve tube plastids also with starch grains; petiole bundles in arcs; guard cells symmetric [with inner and outer ledges equal] cuticular waxes as aggregated rodlets; leaves with distinct petiole, and 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 [different stamens fertile in different clades]; 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, wet; ovule with outer integument >5 cells across, epidermal cells of nucellus apex radially elongated [nucellar pad], suprachalazal tissue well developed; seeds operculate, [operculum testal], 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 +; six nucleotide deletion in atpA. - 8 families, 92 genera, 2151 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: relaxed and constrained penalized likelihood datings) estimated 87 and 79.5 m.y. and Bell et al. (2010) (89-)84 m.y.; figures are (96-)67(-52) m.y. in Merckx et al. (2008a). However, Kress and Specht (2005, 2006) estimated crown group ages of ca 97 m.y. and 110-106 m.y. respectively.

The distinctive seeds of the unplaced (other than to order) Spirematospermum are known from the Late Cretaceous; they have in the past often been placed with Musaceae or Zingiberaceae (Collinson & van Bergen 2004; Benedict 2011: Smith et al. 2013b).

Note: Possible apomorphies are in bold. However, the actual level at which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is partly because many characters show considerable homoplasy, in addition, basic information for all too many is very incomplete, frequently coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there is the not-so-trivial issue of how ancestral states are reconstructed...

Evolution. Divergence & Distribution. It is suggested that there was a rapid radiation of Zingiberales in the early Tertiary 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. (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.

Polarization of some of the features in the ordinal characterization depends 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 - the former topology is a reasonable bet (see also Barrett et al. 2013).

Understanding floral evolution in Zingiberales is difficult, especially given the absence of a well-supported phylogeny for the group. Rudall and Bateman (2004) thought that there was a progressive change in symmetry and staminode evolution, the basic condition for the order being the suppression of the adaxial median stamen (of the inner whorl), and the abaxial median stamen (of the outer whorl) being similarly suppressed in the [Heliconiaceae [[Cannaceae + Marantaceae] [Costaceae + Zingiberaceae]]] clade, their Pattern 1 -> Pattern 2 zygomorphy transition; the former tends to be linked with labellum formation - see Lowiaceae! At the same time the adaxial median stamen would need to regain its fertility, not mentioned by Rudall and Bateman (2004). In any event, the topology used had no strong support, and the flowers of Heliconiaceae are inverted compared with those of the [[Cannaceae + Marantaceae] [Costaceae + Zingiberaceae]] clade. Yockteng et al. (2013) discussed floral evolution in Zingiberales in the context of the topology [Musaceae [[Strelitziaceae + Lowiaceae] [Heliconiaceae + The Rest]]]. They emphasized the role of the duplication of SEP-like genes, two copies of SEP3 showing balancing selection, two LOFSEP copies whowing balancing selection, while AGL6 genes - only a single copy, and not expressed in staminodes of the [[Cannaceae + Marantaceae] [Costaceae + Zingiberaceae]] clade - were involved in stamen development. However, if the relationships [Heliconiaceae [[Musaceae [Strelitziaceae + Lowiaceae]] [[Cannaceae + Marantaceae] [Costaceae + Zingiberaceae]]]] hold up, there will be important consequences when thinking about floral evolution (see esp. Barrett et al. 2013).

When the two whorls of tepals are differentiated, both are more or less petal-like, although the inner is larger and sometimes differently coloured. However, in Phenakospermum (Strelitziaceae), Lowia, as well as Heliconiaceae and Musaceae, the tepals are largely undifferentiated (see also Payer 1857), and stamens are individually opposite members of both whorls in all four families. Although practically all Zingiberales are monosymmetric, in terms of stamen morphology there are three different patterns of monosymmetry. Interestingly, the short, broad, concave staminodes of Heliconia and inner adaxial tepal of Musa and Strelitzia look quite similar. However, polarization of characters is not easy, given the variation in important features like symmetry and perianth within Commelinales - both oblique monosymmetry and a tepaloid perianth with stamens individually opposite perianth members are found there, too.

Endress (2011a) thought that an inferior ovary might be a key innovation for the clade.

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).

Givnish et al. (2005, 2006b) noted that acquisition of net venation, animal-dispersed propagules and tolerance of shady habitats are linked in this group.

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, it has been shown that ascribing feeding patterns on fossil material to the activities of hispine beetles in particular is not possible (García-Robledo & Staines 2008), so dating this association is complicated (see also Gómez-Zurita et al. 2007).

Pollination Biology. Animal pollination pervades the order, and bird pollination in particular is perhaps notably common (Cronk & Ojeda 2008). 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).

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 atpA deletion, see Davis et al. (2004). Mahanty (1970) and Song et al. (2004) suggest that the base chromosome number for the order (x) = 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. Koen (2006) noted that Musa and Calathea ornata were unusual in that in all the individuals of these two species that he examined the genetic spiral proceeded in the same direction, although in other plants clockwise and counter-clockwise spirals occurred in equal frequencies.

As in Commelinales, variation in floral morphology is considerable (see above). 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). The flowers of Marantaceae may have an oblique plane of symmetry. There is variation in the stage at which monosymmetry is evident in the flower (see also Kunze 1985; Kirchoff 2003; Kunze et al. 2005c). There are several vascular bundles in the massive stamens of Musaceae and Zingiberaceae, at least. 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).

For an early but still interesting general discussion on evolutionary morphology of the order, see Tomlinson (1962a). 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 for vessel and tracheid micromorphology, see Carlquist and Schneider (2010); for information on floral anatomy, see Rao et al. (1954), on cytology, see Mahanty (1970), on ovules, see Mauritzon (1936d), on seed morphology, Humphrey (1896), Mauritzon (1936d), Grootjen and Bouman (1981), Manchester and Kress (1993), and Liao et al. (2004); on nectary and nectary duct morphology and position, see Kirchoff (1992) and Stauffer et al. (2009), and on tapetum, see Furness and Rudall (2001).

Phylogeny. Phylogenetic relationships in the order have been much studied, but they are still 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 approximations, see also Janssen & Bremer 2004), and slightly better, but still not that well (78%) supported as member of a clade [[Lowiaceae + Strelitziaceae], Heliconiaceae, Musaceae] in Givnish et al. (2006b: one gene), while Wikström et al. (2001: three genes) found the relationships [Musaceae [Heliconiacaeae [[Lowiaceae + Strelitziaceae] [The Rest]]]] Even the 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 the relationships in this group are scrambled (Wikström et al. (2001). Johansen (2005), looking at six DNA regions (plastid, nuclear), recently 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 Rest]]], although they obtained other relationships within the order and between the order 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. Hence the conservative and rather minimal resolution of relationships in the tree here.

Classification. For a detailed classification of the order, see Kress et al. (2001); pending stabilization of the phylogeny of the clade, I have been conservative.



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

HELICONIACEAE Vines   Back to Zingiberales

Heliconiaceae

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 [functionally inverted]; 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 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 4.7 m.y. and ca 87 or 32-27 m.y. (Kress & Specht 2006), or ca 32 m.y.a. (McKenna & Farrell 2006).

Evolution. Divergence & Distribution. Rudall and Bateman (2004, see also Kirchoff et al. 2009) note that flowers in which the abaxial stamen of the outer whorl is sterile is a feature of a [Heliconiaceae [[Marantaceae + Cannaceae] [Zingiberaceae + Costaceae]]] clade. Heliconiaceae diverged from other Zingiberales 114-104 m.y. before present (Kress & Specht 2006) or ca 88 m.y. before present (Janssen & Bremer 2004)

Plant-Animal Interactions. The herbivorous Cephaloleia beetles (Cassidinae+Hispinae, Chrysomelidae) seem to have diversified in the Oligocene coincident with crown Heliconia diversification (McKenna & Farrel 2006).

Pollination Biology & Seed Dispersal. Variation in floral and especially inflorescence morphology is considerable (Berry and Kress 1991), and, as in Musaceae, the inflorescences may be 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 just above the surface of the water and later the thick and fleshy pedicel elongates raising the fruits above the water and making them accessible for the seed disperser.

Chemistry, Morphology, etc. Kirchoff et al. (2009) suggest that the flower of Heliconia is obliquely asymmetric (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 Tomlinson (1959, 1969: anatomy), Kress (1986b: pollen), Kirchoff (1992: ovary), Andersson (1998; general) and Kirchoff et al. (2009: floral development); Simão et al. (2006) provide information about ovule and seed.

[[Musaceae [Strelitziaceae + Lowiaceae]] [[Cannaceae + Marantaceae] [Costaceae + Zingiberaceae]]]: fruit opening laterally, loculicidal; seeds arillate.

[Musaceae [Strelitziaceae + Lowiaceae]]: adaxial inner T reduced and ± hooded; tapetum glandular; median [adaxial] A of inner whorl non-functional.

MUSACEAE Jussieu, nom. cons.   Back to Zingiberales

Musaceae

Plant cormose; (phenylphenalenones +); SiO2 bodies ± trough-shaped; roots with scattered wide vessels and strands of phloem in the pith; 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, connation congenital, adaxial inner T free; staminate flowers: median [adaxial] A of inner whorl absent, (A 6), anther wall formation of the basic type [Musella s. str.], exothecium +, endothecium poorly developed, staminode 0; pistillode +; carpellate flowers: G with intra-ovarian trichomes, loculi mucilaginous, stigma capitate; ovules (micropyle exostomal), outer integument "massive", inner integument ca 3 cells acoss, 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. (Janssen & Bremer 2004), and ages suggested by Christelova et al. (2011: hpd estimates) 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.a.. Kress and Specht (2005, 2006), however, offered crown group ages of around 47.5 and ca 87 or 51 m.y. (depending on the methods used) 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 a duplication in the genome (polyploidization) of this clade some 60 m.y.a. (Lescot et al. 2008).

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).

Chemistry, Morphology, etc. The tegmen is two cells layers across; the cells are elongate. Does the endosperm have a small chalazal chamber?

Some information is taken from Fahn (1983: inflorescence), Tomlinson (1959, 1969: anatomy), Kirchoff (1992: ovary), Andersson (1998: general), Graven et al. (1996: seed), Xue et al. (2005: microsporogenesis, etc., 2007: embryology of Musella); see Piperno (2006) for phytoliths and domestication.

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.

[Strelitziaceae + Lowiaceae]: petiole with adaxial and abaxial series of air canals; T whorls differentiated, but both petal-like, 2 abaxial members of inner whorl enclosing stamens, median [adaxial] A of inner whorl staminodial; apex of ovary sterile [= floral column], stigma 3-lobed; outer integument 14-20 cells across; aril hairy; 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 and ca 96-80 m.y. (depending on the methods used) 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

Strelitziaceae

(Plant arborescent), (growth monopodial); phenylphenalenones +; roots with scattered wide vessels and strands of phloem in the pith; 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), inner whorl basally connate (2 lateral connate), large, adaxial A of inner whorl cucullate; (A 6 - Ravenala), tapetal cells to 32-ploid; stigma long-turbinate; ovules with bistomal micropyle; capsule woody; micropylar collar 0, operculum rudimentary, 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 and ca 74 or 58-55 m.y. (depending 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. 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 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).

Phylogeny.

LOWIACEAE Ridley, nom. cons.   Back to Zingiberales

Lowiaceae

SiO2 bodies ± conical; endodermoid layer in rhizome; fiber cells or bundles of fibers in leaf; stomata paracytic, guard cells asymmetric [with inner and outer ledges unequal]; cross veins +, in abaxial part of blade; inflorescence of repeating 1-flowered units, branching from bracts below the flower, the flower axillary; flowers held upside down; outer T basally connate, adaxial T large [= labellum when resupinate], abaxial pair small; A basally adnate to C, (staminode +); ?tapetum; septal nectary 0; stigma monosymmetric, dorsiventrally flattened, secretory tissue on adaxial side at base [= viscidium], lobes ± fimbriate; ovule with outer integument 14-16 cells across, inner integument ca 4 cells across; seed hairy, 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]/15. S. China to Borneo (map: J. Kress, pers. comm.; Sakai & Inoue 1999).

Evolution. Pollination Biology. The flowers last one day. They may be held in an inverted position, the adaxial median petal then forming a labellum. In some taxa the flowers are very odoriferous, and the apparently nectarless Orchidantha inouei is pollinated by scarabeid dung beetles (Sakai & Inoue 1999).

Chemistry, Morphology, etc. The family is very poorly known. The longitudinal and horizontal vascular bundle systems of the leaf blades appear as if they are independent in cross section. The stamens are opposite both calyx and corolla separately (Kirchoff & Kunze 1995). It is not clear if the endotesta is silicified.

Much information is taken from Larsen (1998); see also Tomlinson (11969: anatomy), Wen et al. (1997: seed), Pedersen (2001: general), and Pedersen and Johansen (2004: flowers).

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, both whorls ± petal-like, 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 amoeboid, non-syncytial; micropyle endostomal; micropylar collar well developed, cells of exotesta longitudinally elongated; 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) or ca 84 m.y.a. (Janssen & Bremer 2004). Similar, if rather older, ages are suggested by Kress and Specht (2005, 2006), with the crown group estimated as being ca 88 and 106-105 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, at least, 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 in pairs, 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; 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), or (54-)45, 43(-36) m.y.a. (Bell et al. 2010: note position of Cannaceae); ages in Kress and Specht (2005, 2006) are around 80 and 96-91 m.y. respectively.

Evolution. Pollination Biology. Although both Cannaceae and Marantaceae have asymmetric flowers and secondary pollen presentation, details are quite different in the two families.

Chemistry, Morphology, etc. 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

Cannaceae

Chelidonic acid, aromatic resin +; mucilage canals in stem; (leaves spiral); inflorescence branched; flower short-lived; 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/operculum 0, malpighian layer formed by exotesta and also epidermis of chalaza, mesotesta sclereidal, endotesta 0; embryo long; 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. Kress and Specht (2005, 2006).

Evolution. 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 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 other zingiberalean families. The aril is often described as being absent (e.g. Grootjen & Bouman 1981), and the funicular aril mentioned above is unlike that of other 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

Marantaceae

(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 cymules], 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 adaxial surface of style, on "stamp", with secretory area]; 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, long; n = (-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 57 or 72-60 m.y. (Kress & Specht 2005, 2006) 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). The 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 (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 pollinations 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).

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 may be at right angles to that of the parent axis. The inflorescence is almost mind-bogglingly complex (Tomlinson 1961a; Kunze 1985).

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 morpology and anatomy, see Tomlinson (1961a, 1969), for inflorescence structure, see Andersson (1976), 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 Stachyphryniumand Donax clades, see Suksathan et al. (2009).

Classification. See Andersson and Chase (2001) for a phylogenetic classification of the family. However, the current classification 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 species nopw being placed in Goeppertea (Borchsenius et al. 2012).

[Costaceae + Zingiberaceae]: fibrous sheath in stem; leaf ligulate; bracteole lateral; outer T connate; filament flattened, connective prolonged, abaxial member of outer A whorl staminodial, all 5 staminodes connate, forming labellum, with narrow tube and distinct open limb, connate; exine + [so pollen resistant to acetolysis]; nectary at base of tube, vascularized; 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 88 or 105-99 m.y.a. (Kress & Specht 2005, 2006 respectively) and ca 79 m.y.a. (Janssen & Bremer 2004).

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 Kirchoff (1988a). The massive stamens of Costus, at least, have several vascular bundles in the region of the anthers. Van Heel (1988) described the gynoecium of Costus as having septal nectaries, that of Zingiberaceae as lacking them.

COSTACEAE Nakai   Back to Zingiberales

Costaceae

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, unbranched, (flowers single); floral bracts often with abaxial nectaries; pollen aperturate; (G [2]), stigma with adaxial projection, fimbriate; outer integument 5-6 cells across; seed with 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. (Wikström et al. 2001), ca 47 m.y. (Janssen & Bremer 2004), or 23 m.y. and 74 or 52-47 m.y. (Specht 2005, 2006).

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. 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. here are two to four rows of ovules (Newman & Kirchoff 1992). The endosperm is oily. T

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); [Chamaecostus [Dimerocostos + Monocostus]] are 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

Zingiberaceae

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); (leaf sheath closed); vascular bundles in leaf axis abaxial; hypodermis 0-1-layered; (inflorescence bracts deciduous); labellum adnate to filament and forming tube, 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); capsule fleshy; exotesta of fibriform cells; chalazosperm 0; 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

Rhizome fleshy, ± vertical; ?plane of distichy; inflorescence a raceme, bracteoles 0; filament of fertile stamen adnate to base of labellum, forming a tube above point of insertion of petals; n = 13, 14, 21.

1-2/20. Africa and Madagascar.

[Tamijioideae [Alpinioideae + Zingiberoideae]]: ?

2. Tamijioideae W. J. Kress

Rhizome fibrous; plane of distichy parallel to the ground; inflorescence axes separate; placentation parietal.

1/1: Tamijia flagellaris. Borneo.

[Alpinioideae + Zingiberoideae]: (root with phloem strands in pith); 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

Rhizome fleshy, plane of distichy parallel to the ground; (styloids + - Aframomum); (leaf blade with nectary pits on abaxial midrib - Riedelieae); lateral staminodes of outer whorl very small or 0; (fruit indehiscent - some Alpinieae; opening by longitudinal slits - Riedelieae); seed operculate; endotesta with sclerotic U-shaped cells; perisperm with simple starch grains, endosperm lacking starch, (seed with chalazal chamber); n = (11) 12, chromosomes 0.7-4.5 µm long.

20/ Alpinia (200), Etlingera (110), Amomum (150), Renealmia (75), Riedelia (60), Aframomum (60), Hornstedia (50). Indo-Malesia, tropical Australia; Renealmia, American and African tropics.

Synonymy: Alpiniaceae Link, Amomaceae Jaume Saint-Hilaire

4. Zingiberoideae Hasskarl

Rhizomes fibrous, plane of distichy at right angles to the ground; (steroidal saponins + - Hedychium); (lateral staminodes of outer whorl free from labellum), (filament curved, style bow-string like - Globbeae), (tapetum amoeboid); (pollen sulcate - Zingiber); (placentation basal; parietal - Globbeae), style with 2 vascular bundles; (seed carunculate - Globba, Zingiber), operculate (not - Hedychieae]; (multilayered exotestal epidermis - Globbeae), endotesta parenchymatous or with sclerotic U-shaped cells; starch grains of perisperm compound (simple - Globbeae), endosperm with starch [aleurone], embryo long [Hedychium]; n = (8-)10-12(-14), etc., chromosomes 2.1-5.8 µm long.

29/: Globba (100), Zingiber (100), Boesenbergia (60), Hedychium (50). Indo-Malesia, tropical Australia.

Synonymy: Curcumaceae Dumortier

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).

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. (2013 and references). Ley and Harris (2014) looked at floral morphology in the African Aframomum, where most of the 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. Much "familial" information like sieve tube morphology is properly to be placed at the [Alpinioideae + Zingiberoideae] node. 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. Ellettaria has an embryo almost as long as the seed.

Some information is taken from Larsen et al. (1998: general), Tomlinson (1956, 1969: anatomy), Uma and Muthukumar (2014: root anatomy), Harling (1949: embryology), Beltran and Kiew (1984: cytology), Wood et al. (2000: Hedychium and relatives), Poulsen (2012: Etlingera and Sakai and Nagamasu (2000: Tamija). For floral development, see 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 is strongly para/polyphyletic, Amomum in polyphyletic. Särkinen et al. (2007) provide a phylogeny of the African-American Renealmia and Auvray et al. (2010) of the African Aframomum. Pommereschea has a parenchymatous endotesta (Liao & Wu 2000) and also a long style - it is somewhat odd in Alpinieae.

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.