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.
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.
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, embryonic axis not straight [root lateral with respect to the longitudinal 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].
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, embryonic axis straight [shoot and root at opposite ends; plant allorhizic], 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.
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; (tapetum glandular), cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine 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-)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, 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, heteropolar [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; endodermal cells with U-shaped thickenings; cork cambium in root [uncommon] superficial; root vascular tissue oligo- to polyarch, with prominent pith [medullated], lateral roots arise opposite phloem poles; primary thickening meristem +; vascular bundles in stem scattered, (amphivasal), vascular cambium 0 [bundles closed]; 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 blade linear, main venation parallel, the veins joining successively from the outside at the apex, transverse veinlets +, unbranched [leaf blade characters: ?level], vein/veinlet endings not free, margins entire, Vorläuferspitze +, base broad, ensheathing the stem, sheath open, petiole 0, colleters + ["intravaginal squamules"]; 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; 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 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 +); cotyledon with a closed sheath, unifacial [hyperphyllar], both assimilating and haustorial; 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 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.
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.
Age. The age of this node is ca 89 m.y. (Janssen & Bremer 2004) and a similar ca 86.8 m.y. in Naumann et al. (2013); Magallón and Castillo (2009) suggest an age of 123 to 111 m.y. and Wikström et al. (2001) again a much younger age of (91-)87, 83(-79) m.y.. The figures in Bremer (2000b: largely fossil calibrations) are ca 108 m.y., while estimates are ca 98.6 m.y. in Givnish et al. (2000), (120-)109(-89) m.y.o. in Merckx et al. (2008a), 105-84 m.y. in Mennes et al. (2013), and around 142 m.y. in Paterson et al. (2004).
Evolution. Plant-Animal Interactions. Sap-eating chinch bugs of the Hemiptera-Lygaeidae-Blissinae have been recorded from taxa throughout this clade, although they occur on Poales and especially Poaceae most frequently (Slater 1976).
Chemistry, Morphology, etc. For primary cell wall composition, see literature in Harris (2005); Arecaceae sampled are somewhat intermediate between this clade and other monocots. For stomatal development, see Tomlinson (1974) and Rudall (2000); development in Dasypogonaceae is apparently unknown.
Previous Relationships. Engler (1892) recognised a group, Farinosae, distinguished by its starchy endosperm, which included many of the taxa now in this clade. Engler thought that Farinosae were close to his Liliflorae, perhaps partly because he included Juncaceae (Poales here) in the latter.
POALES Small Main Tree.
Mycorrhizae absent; vessel elements in roots often with simple perforation plates, vessels also in stem and leaf, also with simple perforation plates; SiO2 epidermal; raphides 0; inflorescence indeterminate; style well developed, stigmas small, dry; micropyle bistomal, both integuments ca 2 cells across; embryo size?; cotyledon hyperphyllar, haustorial [?level]; mitochondrial sdh3 gene lost. - 17 families, 997 genera, 18325 species.
Age. Crown-group Poales are ca 83 m.y. old (Janssen & Bremer 2004: c.f. topology); Leebens-Mack et al. (2005) suggested an age of 109-106 m.y.a. and Wikström et al. (2001) a younger age of 72-69 m.y. ago. Magallón and Castillo (2009) suggested ages of ca 109 and 99.2 m.y., and Bell et al. (2010) ages of (103-)93, 85(-73) m.y.; estimates are (116-)106(-88) m.y. in Merckx et al. (2008a), only ca 52.3 or 51.6 m.y. in Xue et al. (2012), and 98-78 m.y. in Mennes et al. (2013).
However, there are problems. Poinar (2004, 2011) proposed that Programinis laminatus, found fossil in deposits from the Early Cretaceous of Myanmar some 110-100 m.y.a., can be placed in Poaceae-Poöideae, i.e. a clade rather highly embedded in Poaceae. Similarly, if the identity of the putative stem Bromeliaceae Protoananas lucenae, 114-112 m.y. old and from Brazil (Leme & Brown 2011), is confirmed, older dates for the clade are again suggested.
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. Magallón and Castillo (2009) suggest that Poales in the broad sense have the highest diversification rate in the monocots, about the same as Asparagales, but in both the rate is little over half that of Lamiales.
Linder and Rudall (2005) provide a detailed discussion of morphological evolution and diversification in Poales. Subsequently, Bouchenak-Khelladi et al. (2014: tree rather distinctive) looked at correlations of various ecological parameters and diversification; much diversification in major lineages was Late Cretaceous, even if the origins of those clades was substantially earlier; Bromeliaceae were a particularly good example of a yet more recent radiation with an extremely long fuse, i.e. a much older stem group.
Ecology & Physiology. Cornwell et al. (2008) found that litter decomposition of forbs was faster than that of graminoids - presumably mostly grasses and sedges - indeed, litter decomposition of monocots (sic) was slower that that of other angiosperms; such differences affect the rate of nutrient cycling in the environment.
Recently it has been emphasized that within commelinid monocots, and especially Poales, some sieve tubes lack companion cells, are notably thick-walled, and are close to the tracheary elements; they seem to be involved in short distance transport of not very concentrated sugars. Aphids do not probe such cells, rather, they prefer the thinner walled "normal" sieve tubes which have more concentrated sugars (Botha 2013). The distribution of these distinctive sieve tubes is unclear.
Plant-Animal Interactions. Many host-plants of reed beetles, Chrysomelidae-Donaciinae, are scattered in Poales, especially in Typhaceae, Juncaceae, and Cyperaceae (Kölsch & Pedersen 2008: much discussion on the age and evolution of the group). They show close co-speciation with endosymbiotic bacteria (gamma proteobacteria-Enterobacteriaceae - near Buchnera), which are believed to produce the material that makes up the cocoon that characterises this beetle clade, which is also noted for the larvae being able to grow under water (Kölsch & Pedersen 2010).
Pollination Biology & Seed Dispersal. For the repeated evolution of wind pollination in Poales, see Givnish et al. (2010a, b).
Genes & Genomes. For the general pattern of movement of genes from the mitochondrion to the nucleus, see Adams and Palmer (2003). J. J. Doyle et al. (1991) discussed chloroplast inversions and Ong and Palmer (2006) the rps14 nuclear gene/mitochondrial pseudogene system.
Chemistry, Morphology, etc. Eriocaulaceae, Poaceae, Cyperaceae and Juncaceae at least have lateral roots originating opposite the phloem of the vascular tissue, in Restionaceae and Bromeliaceae they originate opposite the xylem (ref.?). Note that at least some members of the Poaceae and Cyperaceae groups have distinctive cellulose orientation in the outer epidermal walls of their roots, but that some Typhaceae and Bromeliaceae do not (Kerstens & Verbelen 2002); one wonders what improved sampling will show.
There is variation in the way pollen is arranged in the pollen loculi. The plesiomorphous condition is likely to be central, i.e., some pollen grains are not in contact with the tapetum, but in some taxa it is peripheral, and here all grains are in contact with the tapetum (Kirpes et al. 1996), however, sampling is again poor.
See Prychid et al. (2004) for SiO2 bodies (phytoliths) and Tillich (2007) for seedling morphology and evolution.
Phylogeny. Poales do not always have very strong support, but c.f. e.g. Givnish et al. (2010b) and Barrett et al. (2012b). The topology of the tree in early versions of this site was based on the work of K. Bremer (2002) in particular, and also that of Harborne et al. (2000), but Janssen and Bremer (2004) suggested a rather different set of relationships, albeit some had little support, and relationships in Givnish et al. (2010b) are somewhat different again. It will become clear from the discussion below that the topology of the tree above is probably incorrect in detail, but I await further studies with better sampling and support before changing it.
The general pattern of movement of genes from the mitochondrion to the nucleus suggests that Bromeliaceae and Typhaceae (of the taxa sampled) are sister to other Poales (Adams & Palmer 2003), and of course Bromeliaceae, along with Rapateaceae, alone have septal nectaries in this clade. A three-nucleotide deletion in the atpA gene was found to characterise Typhaceae and Bromeliaceae (Davis et al. 2004), although there was little bootstrap support for this group (but see also Givnish et al. 2005, 2007; c.f. Givnish et al. 2006b). Similarly, Typhaceae are placed sister to Bromeliaceae with weak jacknife support but strong Bayesian posterior probabilities (Bremer 2002). Other work also suggests that Typhaceae and Bromeliaceae form a clade sister to other Poales, and Rapateaceae are in turn sister to the remainder (Givnish et al. 2005; Chase et al. 2006; also Rudall & Linder 2005; Givnish et al. 2005, 2007: ?rooting; Graham et al. 2006: see Rapateaceae; Soltis et al. 2011: strong support, but sampling; Ruhfel et al. 2014; Bouchenak-Khelladi et al. 2014b), although these relationships are not always obtained (Givnish et al. 2010a). Bromeliaceae and Typhaceae are also often placed as basal branches with respect to other clades in Poales (Givnish et al. 2005, 2008 [but rooting]; also Graham et al. 2006), while Rapateaceae appear to be sister to remaining Poales in some analyses (e.g. Davis et al. 2004), albeit with little support. Indeed, Givnish et al. (2010b) found quite strong support in both maximum parsimony and maximum likelihood plastome analyses for the topology [Bromeliaceae [Typhaceae s.l. [Rapateaceae + rest of Poales]]] (see also Barrett & Davis 2011; Barrett et al. 2013; Davis et al. 2013: again, both ML and MP trees; Ruhfel et al. 2014).
Within remaining Poales there are some well-supported clades, the Xyridaceae, Juncaceae, and Poaceae groups, although the exact composition of the first clade in particular remains somewhat unclear. Thus in the complete plastome analysis of Ruhfel et al. (2014), for example a clade [[Eriocaulaceae + Mayacaceae] [Xyridaceae + Poaceae, Restionaceae, etc.]] was obtained - only a single species of each of the first three families was included - while Bouchenak-Khelladi et al. (2014b) recovered the clades [[Rapateaceae + Mayacaeae] [Thurniaceae [Juncaceae + Cyperaceae]]] and [[Eriocaulaceae + Xyridaceae] [Restionaceae et al. + Poaceae et al.]]. There is support for these three groups forming a larger clade (e.g. Givnish et al. 2005, 2010b; Chase et al. 2006), perhaps compatible with the distribution of deletions in the chloroplast inverted repeat ORF 2280 region and absence of a full accD gene (Hahn et al. 1995; Katayama & Ogihara 1996).
Xyridales of Kubitzki (1998c) included Mayacaceae, Xyridaceae, Eriocaulaceae and Rapateaceae. However, there was some evidence for a group made up of the first three families, perhaps, but not very probably, also including Rapateaceae (see above). Bremer (2002) noted that Mayacaceae and Hydatellaceae might be weakly associated with Xyridaceae or Eriocaulaceae, depending on what taxa were included in the analysis, but there were a number of long branches in this area and he excluded the first two families from his final analysis (Chase et al. 2006 also found the position of Hydatellaceae to be problematic; for the association of Mayacaceae with Eriocaulaceae and Xyridaceae, see also Campbell et al. 2001). Davis et al. (2004) found a more complex set of relationships, although with very little support. Members of this group of families were in adjacent branches along the spine of the tree, with one including Flagellariaceae, the Juncaceae group, some Xyridaceae, Mayacaceae, and perhaps Hydatellaceae. Both Xyridaceae and Mayacaceae have more or less clawed petals and anthers with an exothecium. Finally, some Mayacaceae have been linked with Rapateaceae (e.g. Bouchenak-Khelladi et al. 2014b, see above), and both have poricidal anthers. Although there are several distinctive characters in this group of families, but relationships remain unclear.
The situation may, however, be becoming a little tidier. Saarela et al. (2006, esp. 2007) showed that Hydatellaceae are completely misplaced and belong to Nymphaeales, being sister to other members of that clade, and this new position has very strong molecular and morphological support. The three members of the old Xyridales that remain here may form a grade as follows: [Mayacaceae [[Xyridaceae + Eriocaulaceae] [Thurniaceae [Juncaceae + Cyperaceae]]]] (Givnish et al. 2006b; Chase et al. 2006); the topology of the tree in Graham et al. (2006) although with poor sampling, is consistent with such relationships. Givnish et al. (2010b) found that Abolboda, the only member of Xyridaceae examined, did not link with the Eriocaulaceae-Mayacaceae clade in maximum likelihood analyses, while in maximum parsimony analyses there was some support for the clade [Juncaceae etc. + Xyridaceae etc.] (the latter grouping was also recovered by Davis et al. 2013). In maximum likelihood analyses the general relationships were [[Juncaceae, etc.] [[Xyridaceae etc.] [Abolboda [Poaceae, etc.]]]] (Givnish et al. 2010b). Generally similar relationships were found by Barrett and Davis (2011), while Davis et al. (2013) found the grouping [Eriocaulaceae/Mayacaceae [Xyridaceae + Restionaceae/Poaceae area]], but there Abolboda stayed with other Xyridaceae).
Poaceae and their immediate relatives consistently form a clade, although details of relationships within it are still somewhat unclear (see below). Note that in versions 6 [before November] and earlier of this site, Eriocaulaceae and their relatives were weakly associated with the Poaceae group.
Includes Anarthriaceae, Bromeliaceae, Cyperaceae, Ecdeiocoleaceae, Eriocaulaceae, Flagellariaceae, Joinvilleaceae, Juncaceae, Mayacaceae, Poaceae, Rapateaceae, Restionaceae, Thurniaceae, Typhaceae, Xyridaceae.
Synonymy: Eriocaulineae Thorne & Reveal, Xyridineae Thorne & Reveal - Avenales Bromhead, Bromeliales Link, Centrolepidales Takhtajan, Cyperales Berchtold & J. Presl, Eriocaulales Nakai, Flagellariales Reveal & Doweld, Juncales Berchtold & J. Presl, Mayacales Nakai, Rapateales Reveal & Doweld, Restionales Berchtold & J. Presl, Typhales Berchtold & J. Presl, Xyridales Lindley
[Typhaceae + Bromeliaceae]: stomatal subsidiary cells with oblique divisions; leaf without distinct sheath; endosperm helobial, cell wall formation in small chalazal chamber before that in large micropylar chamber; three-nucleotide deletion in the atpA gene.
Age. The divergence of these two families - or, if they are not sister taxa, the crown-group age for Poales as a whole - is estimated at around (105-)100(-95) m.y.a. (Givnish et al. 2011a; Sulman et al. 2013).
TYPHACEAE Jussieu, nom. cons. Back to Poales
Marsh plants or aquatics; flavonoids +; SiO2 bodies 0; starch grains pteridophyte-type, amylophilic; leaves two-ranked; plant monoecious; inflorescences dense, complex, staminate and carpellate flowers in separate groups but on the same inflorescence, carpellate below the staminate; flowers very small [<3 mm across], monosymmetric by reduction; P chaffy; nectary 0; staminate flowers: A 1-8; tapetum amoeboid, 8 nuclei/cell; pollen grains trinucleate, monoulcerate; carpellate flowers: G 1 [but see below], style single, stigma rather elongated, on one side, dry; ovule 1/carpel, pendulous, apotropous, nucellar cap ca 2 cells across, obturator +; fruit indehiscent; seed coat ± obliterated; endosperm +, perisperm +, thin, embryo long, slender; x = 15; ORF 2280 deletion; seedling with hypocotyl and collar hairs.
2/ca 25. More or less world-wide.
Age. The two genera separated ca 89 m.y.a. (Janssen & Bremer 2004), (76-)72(-70) m.y.a. (Sulman et al. 2013) or (87-)80.9(-74) m.y.a. (Bouchenak-Khelladi et al. 2014b).
For the rich fossil record of the family - although Cretaceous occurrences need re-evaluating - see Smith et al. (2010); fossil Sparganium may have up to 7-locular fruits (Cook & Nicholls 1986). Collinson and van Bergen (2004) found similar chemical signatures in fruits of extant and fossil representatives of both genera.
Emergent (floating) aquatic; stomatal subsidiary cells with intersecting oblique divisions; inflorescence as globose heads; P 1-6, when 3, median member adaxial; staminate flowers: anthers extrorse-latrorse; pollen mixed with raphides; carpellate flowers: G (-3), stigma papillate; antipodal cells multiply after fertilization; fruit a spongy drupe, with micropylar plug, P persistent; testa membranous; perisperm with oil; phanomer + [unifacial, ± assimilating], hypophyll quite well developed.
1/14. Temperate and Arctic, little in S. hemisphere, but to New Zealand (map: see Hultén 1958, 1962; Meusel et al 1965; Hultén & Fries 1986).
Age. Crown-group Sparganium has been dated to (17-)13(-8.9) m.y.a. (Sulman et al. 2013).
Synonymy: Sparganiaceae Hanin, nom. cons.
Stems lacking vessels; (styloids +); cuticular waxes as aggregated rodlets; leaf with distinct sheath; inflorescence densely spicate, (staminate and carpellate part adjacent); P 0; staminate flowers: A connate; (pollen in tetrads); carpellate flowers: long hairs on pedicels; G stipitate, fruit an achene with a little operculum; endosperm also with oil.
1/8-13. Temperate and tropical regions worldwide (map: see Hultén 1962; Meusel et al. 1965; Hultén & Fries 1986; Flora Base 2005 - somewhat notional: the map in Knobloch & Mai 1986 differs very considerably from its source, Meusel et al. 1965). [Photos - Collection.]
Age. Crown-group Typha may be (10-)7.1(-4.1) m.y.o. (Sulman et al. 2013: see sampling).
Evolution. Divergence & Distribution. Sulman et al. (2013) discussed the biogeography and evolution of Sparganium, not easy to work out partly because of the very long evolutionary "fuse" of the genus, perhaps 80 m.y. or more.
Pollination Biology & Seed Dispersal. Typha has a sort of unofficial extragynoecial compitum; the carpellate flowers are so close that tubes from each of the four grains of a tetrad may reach the stigmas of four different flowers (Nicholls & Cook 1986).
Bacterial/Fungal Associations. Similar rusts are shared by the two genera (Savile 1979).
Chemistry, Morphology, etc. Some flowers of Sparganium may have a second, empty loculus, or there may even be three fertile loculi (Dahlgren et al. 1985). Given the fossils with multilocular fruits placed in the genus (see above), it seems likely that the pseudomonomerous gynoecium in the two genera evolved independently.
Much information is taken from Kubitzki (1998d: general); see also D. Müller-Doblies (1970: inflorescence and flower) and Grayum (1992) and Albert et al. (2011), both pollen - the two genera are palynologically almost identical. For general information on Typha, see Thieret and Luken (1996: southeast U.S.A.). See U. Müller-Doblies (1970) for flower and embryology and Carlquist (2012a) for vessels in Sparganium.
Phylogeny. For phylogenetic relationships in Typha, see Kim and Choi (2011).
Classification. See Cook and Nicholls (1986, 1987) for a monograph of Sparganium, Sulman et al. (2013) for an infrageneric classification.
BROMELIACEAE Jussieu, nom. cons. Back to Poales
Plants rosette-forming; (C-glycosylated/6-oxygenated) flavones, flavonols +; vessel elements with scalariform perforation plates; mucilage +; cuticular waxes as aggregated rodlets; water storage tissue in mesophyll, fibrous bundle sheaths + [?higher level]; indumentum lepidote; leaves spiral, blade vernation curved, thick, horny, (margins serrate), base dilated; (A basally connate), (adnate to C); septal nectaries +, style +, long, apically ± 3-branched, branches conduplicate-spiral, stigmas also wet; micropyle endostomal, nucellar epidermis cells anticlinally elongated, (nucellar cap ca 2 cells across), chalazal appendage +, micropylar appendage +; fruit a septicidal capsule, K persistent; seeds caudate, testal-tegmic, testa 3-7 cells across, cells variously thickened and lignified, tegmen ca 2 cells across, (exotegmen thickened), endotegmen tanniniferous; embryo (long), cylindrical, often lateral; hypocotyl and hypophyll common; n = 25, x = 8, chromosomes 2.75> µm long.
57[list]/1770 - eight groups below. (Sub)tropical America; W. tropical Africa. [Photo - Flower.]
Age. From estimates in Janssen and Bremer (2004) the age of crown-group Bromeliaceae must be in excess of 112-96 m.y. ago. However, other estimates are much more recent, thus Givnish et al. (2004a, 2008a) suggest a crown age of a mere 24.9-18.4 m.y., Givnish et al. (2011a) an age of ca 19.1 m.y. and Bouchenak-Khelladi et al. (2014b) an age of (32.3-)19.5(-17.4) m.y. ago.
The situation is yet more confused. Protoananas lucenae, from the Crato limestone of Brazil and some 114-112 m.y. old, has been assigned to a "putative ancestral stem-lineage of Bromeliaceae" (Leme & Brown 2011: p. 217), but in the discussion it is also referred to as if it were in a separate family, Protoananaceae. It appears to have an inferior ovary, presumably of independent origin from that found in other Bromeliaceae (but see below: superior ovaries in some Bromeliaceae are thought by some to be secondarily so).
1. Brocchinioideae Givnish
(Tank epiphytes), (plant carnivorous); (stem erect and with intracauline adventitious roots); leaves with stellate chlorenchyma; (leaf blade deciduous); (K ±= C); G ± inferior, septal nectary above the insertion of the ovules; ovules 2 (3+?)/carpel; (seeds with basal tuft of hairs); n = ?9, 23.
1/21. South America, the Guyana Highlands (map: from Smith & Downs 1974).
Age. Divergence within Brocchinia may have begun some 14 m.y.a. (Givnish et al. (2004a, 2008a) or 14.3-13.1 m.y. (Givnish et al. 2011a).
[Lindmanioideae [Tillandsioideae [Hechtioideae [Navioideae [Pitcairnioideae [Puyoideae + Bromelioideae]]]]]]: cap cells of trichomes dead; septal nectaries below the insertion of the ovules; parietal tissue ca 1 cell across (map: from Givnish 2004a).
Age. The age for this node was estimated to be between 112 m.y. and 96 m.y. (Janssen & Bremer 2004), while ca 15.6 m.y. is the age suggested by Givnish et al. (2011a).
2. Lindmanioideae Givnish
Stellate chlorenchyma 0; leaf margin entire/serrate; K contorted; stigmas straight; ?ovule number; cotyledonary hypophyll blade-like.
1-2/43. South America, the Guyana Highlands.
Age. The origin of crown-group Lindmanioideae can be dated to 16.3-8.9 m.y. (Givnish et al. 2011a).
[Tillandsioideae [Hechtioideae [Navioideae [Pitcairnioideae [Puyoideae + Bromelioideae]]]]]: (inflorescence axis, bracts, floral bracts coloured); (C often with subbasal scales and/or longitudinal callosities); ovules 6-many/carpel.
Age. The age for this node has been estimated as ca 96 m.y. (Janssen & Bremer 2004) and 15.4-14 m.y. (Givnish et al. 2011a).
3. Tillandsioideae Burnett
Air epiphytes, (also tank-forming), roots often for attachment only (0); scales radially symmetric; leaf margins entire; (flowers in inflorescence 2-ranked); (pollen with raphides); (micropyle also bistomal), (outer integument to 5 cells across), hypostase +, ovules with long chalazal projection; apical and/or basal tufts of hair usu. derived from longitudinal splitting of the outer integument; embryo short to long; (n = 17, 21), karyotype bimodal; (primary root none or soon aborting); (n = 16, 18, 20, 22).
9/1015: Tillandsia (620: polyphyletic), Vriesia (195: poly/paraphyletic), Guzmania (170), Werauhia (70), Racinaea (60). Almost the range of the family in America. [Photo - Flower.]
Age. Divergence within Tillandsioideae may have begun some 14.2-11.8 m.y.a. (Givnish et al. 2011a).
Synonymy: Tillandsiaceae Wilbread
[Hechtioideae [Navioideae [Pitcairnioideae [Puyoideae + Bromelioideae]]]]: seeds not caudate.
Age. This node can be dated to 15.2-14 m.y.a. (Givnish et al. 2011a).
4. Hechtioideae Givnish
Plant xeromorphic; (CAM photosynthesis +); hypodermal sclerenchyma +, internal water storage tissue +, chlorenchyma undifferentiated; trichomes in parallel rows; leaf margin serrate (entire); plants dioecious; (G subinferior), stigma simple-erect; seeds circumferentially winged (not); cotyledonary hypophyll blade-like.
1/51. Texas, Mexico, N. Central America.
Age. The age of crown-group Hechtioideae is 12.1-10.3 m.y. (Givnish et al. 2011).
[Navioideae [Pitcairnioideae [Puyoideae + Bromelioideae]]]: ?
Age. This node is some 12.1-10.3 m.y. old (Givnish et al. 2011a).
5. Navioideae Harms
Plant xeromorphic; peripheral water storage tissue +, stellate chlorenchyma 0; leaf margin serrate/entire; C minute; seeds circumferentially winged or not.
5/105: Navia (98). Guyana Highlands, N.E. Brasil.
Age. Crown-group Navioideae are 10.4-9.4 m.y. old (Givnish et al. 2011a).
[Pitcairnioideae [Puyoideae + Bromelioideae]]: ?
Age. This node was dated to ca 15 or 13.4-13.3 m.y.a. (Givnish et al. 2004a, 2011a respectively).
6. Pitcairnioideae Harms
Scales ± divided, or hairs stellate; leaf margin?; (flowers monosymmetric), G to inferior; ovules with (outer integument ca 5 cells across), (parietal tissue several cell layers across), antipodal cells multiply after fertilization - - Dyckia, (micropylar appendage 0); seeds tailed, body cells differing from tails (winged), (no appendages); embryo lateral or not; (karyotype bimodal); hypocotyl quite long, cotyledonary hypophyll blade-like, (collar rhizoids - Pitcairnia).
5/515: Pitcairnia (405), Dyckia (150), Forsterella (30). Mexico to Chile, Pitcairnia feliciana W. Africa.
Age. Crown-group Pitcairnioideae are around 11.8-9.4 m.y. old (Givnish et al. 2011a).
[Puyoideae + Bromelioideae]: micropylar appendage 0.
Age. This node is around 10 m.y. old (Givnish et al. 2011a).
7. Puyoideae Givnish
Plant rather xeromorphic; hypodermal sclerenchyma +, internal water storage tissue +, chlorenchyma undifferentiated; trichomes in parallel rows, foliar trichomes ± well developed scales; leaf margin serrate; flowers monosymmetric, K contorted, C clawed, tightly spiralled after anthesis; parietal tissue several cell layers across [?all]; seeds circumferentially winged; cotyledonary hypophyll blade-like; (n = 24).
1/195. Mountains, etc., Costa Rica and Guyana to Chile and Argentina. [Photos - Puya Flower, Puya Habit, Puya Habit.]
Age. Divergence within Puyoideae may have begun some 10-8.7m.y.a. (Givnish et al. 2011a).
8. Bromelioideae Burnett
Epiphytes, (often tank-forming), roots often for attachment only; (CAM photosynthesis common); scales irregularly peltate; leaf margin entire/serrate; (perianth tube/hypanthium +), (K asymmetric), (C with adaxial subbasal petal appendages); (pollen 2-4-porate), (with raphides); G inferior, ovules with appendage at chalazal end [= funicular], (micropyle also bistomal), (outer integument to 4 cells across), (nucellar epidermal cells not elongated anticlinally), (chalazal appendage 0); fruit baccate; seed without an appendage; sarcotesta [gelatinous] common; embryo lateral; (n = 17, 21); (cotyledon not photosynthetic), collar rhizoids +, primary root prominent, short hypocotyl present; (n = 17).
31/722: Aechmea (185), Neoregelia (100), Billbergia (65), Bromelia (50), Hohenbergia (50), Nidularium (50). Mexico and the West Indies to Chile, esp. Brazil. [Photo - Flower, Fruit, Flower, Flower.]
Age. Crown-group Bromelioideae are 9.5-8.9 m.y. old (Givnish et al. 2011a).
Evolution. Divergence & Distribution. Estimates of diversification within the family suggest that much has occurred very recently. Givnish et al. (2004a, 2008) suggested that there was radiation from an ancestral home on the Guayana Shield (see also Givnish et al. 1997, 2011a: much detail, b); divergence within the Guayanan Brocchinia may have begun only some 14 m.y.a. (Givnish et al. (2004a, 2008). Indeed, Givnish et al. (2011a, b) proposed that there was a ca 80 million year hiatus between the origin of stem and crown Bromeliaceae (stem ca 100 m.y., crown ca 19 m.y.); so presumably there was much extinction. Much of the diversity in the family is in the Andean core tillandsioids, which began to radiate ca 14.2 m.y.a., and the Brazilian Shield bromelioids, which starting speciating only around 9.1 m.y.a. (Givnish et al. 2011a). The speciose clade made up of Aechmea and relatives seems to have diverged from Ananas about seven m.y.a. and diversified within the last four m.y. (Givnish et al. 2004a; Sass & Specht 2010). For diversification rates in the family, particularly high in tank epiphytes, see also Givnish et al. (2011b).
The ancestor of Pitcairnia feliciana seems to have moved to Africa by long distance dispersal perhaps 12-9.3 m.y.a. (Givnish et al. 2008, 2011). For the diversification of Puya, which seems to have begun in Peru (along with other early branches of Bromelioideae), and then following the Andean orogeny north, see Schmidt Jabaily and Sytsma (2010; esp. 2013); it seems to have occurred within the last ten m.y. (Givnish et al. 2010).
Givnish et al. (2008, 2013) discuss the evolution of CAM, bird pollination, epiphytism and xeromorphic traits, and how all these features interact (see also Smith et al. 2005; Nyffeler & Eggli 2010b). Givnish et al. (2013) thought that extsensive speciation followed from functional divergence, like evolution into the epiphytic habitat, CAM in arid environments, and adaptations to understory life in forests, and then geographic spread and radiation into different areas and environments. Features like bird pollination per se were probably not the major drivers of speciation here.
Ecology & Physiology. The diversity of growth form in Bromeliaceae is well known. Many taxa are terrestrial and have a well-developed root system. However, about 1,700 species - and so just over half the family - are epiphytic, and are especially common in montane habitats (Benzing 1990 for much discussion; Luther & Norton 2008: epilithic species not included). Tillandsioideae predominate here, and some are air epiphytes, any roots being for attachment only (see below). A major clade in Bromelioideae, some Brocchinia, a few Tillandsioideae, etc., are tank epiphytes, the tanks being formed by the closely appressed overlapping bases of the leaves.
Roots of tank bromeliads may grow into the tank where they absorb the contents, the rotted detritus made by their inhabitants (see above); Pittendrigh (1948) noted that such roots were mycorrhizal, while roots growing into the soil were not obviously mycorrhizal. Leroy et al. (2013) propose that association of tank bromeliads in particular with mutualistic ants enhances nitrogen uptake of the former, nitrogen moving from ants and their debris into the plant via its roots; Bromeliaceae in general have extremely low leaf nirogen concentrations. Blue-green algae may fix nitrogen in some bromeliads, although there are perhaps more algae in seepage areas from the tank than in the tank itself (Bermudes & Benzing 1991). Within Bromelioideae, the evolution of tanks may be a key innovation, increasing diversification rates by decreasing extinctions in the epiphytic habitat frequented by these plants compared to the harsh, dry and open conditions of more ancestral Bromelioideae; tank Bromelioideae also have CAM photosynthesis (Silvestro et al. 2014 - see below).
The multicellular hairs on the leaf surface are integral to the ecology of the different growth forms. Perhaps somewhat paradoxically, adaxial leaf surfaces in Bromelioideae and some other subfamilies are hydrophilic while abaxial surfaces are hydrophobic (Reuter & Brown 2009). Dense scales or a powdery epicuticular wax make the abaxial leaf surface water-repellent so the stomata there remain functional even in wet conditions, and it has even been suggested that repelling water was an ancestral function of bromeliaceous scales (Pierce et al. 2001). The less dense scales on the adaxial surfaces of the leaves are involved in nutrient uptake (Benzing et al. 1985; Pierce et al. 2001) for which water is essential. Phosphate is taken up very efficiently by the hairs on the adaxial surfaces of the leaves in tank epiphytes like Aechmea fasciculata and either moved elsewhere in the plant or stored as phosphorus-containing phytin (Winkler & Zotz 2009; Gonsiska & Givnish 2009). Leaves of Bromeliaceae also do not seem to lose metabolites easily (Benzing & Burt 1970; McWilliams 1974).
The rather elegant multicellular peltate trichomes of Tillandsioideae, subjects of detailed early studies by Mez (1904), take in water and nutrients; they flex as they dry and so pull away from the leaf surface, but when it rains they readily take up water and come to lie flat on the surface (Benzing 1976; Pierce et al. 2001); water and nutrient absorbtion takes place then. It has also been suggested that the dry, white scales in Tillandsia may reflect light and so provide photoprotection (Pierce 2008). Roots in epiphytic Tillandsioideae may be for attachment only. Adult plants of Tillandsia usneoides (Spanish moss) lack roots entirely, the plants growing readily on any available support - branches, telegraph wires, etc. (Wester & Zotz 2010 and references); the leaves take over the nutritional function of roots. The rootless T. latifolia and T. purpurea are quite happy lying in the full sun in Peruvian deserts (McWilliams 1974). In at least some species that do develop roots, the radicle of the embryo aborts (Fiordi Cecchi et al. 1996; Magalhães & Mariath 2012).
Some two thirds of Bromelioideae have some form of CAM metabolism and ca 44% have strong CAM, and although details of the evolution of this feature remain somewhat unclear (Crayn et al. 2000, 2004; Reinert et al. 2003; Schulte et al. 2005). Quezada and Gianoli (2011) consider the acquisition of CAM photosynthesis to consist of a series of key innovations; in five sister group comparisons the CAM clade was significantly more diverse than the non-CAM clade. Silvestro et al. (2014) also noticed an increase in speciation rates in CAM Bromelioideae (see above for tank Bromeilioideae), and they suggested that there had been multiple origins of CAM there (see their Fig. 1; reconstruction of ancestral states?). CAM evolution may have occurred initially in the context of moving in to dry/arid terrestrial habitats, rather than as an adaptation facilitating epiphytism (Quezada & Gianoli 2011). There is considerable plasticity in the development of the CAM syndrome within genera like Puya (Schulte et al. 2011).
Carnivory may have evolved more than once in Bromeliaceae. The tillandsioid Catopsis berteroniana traps terrestrial arthropods and is possibly carnivorous; interestingly, it also harbours larvae of the mosquito Wyeomyia, which also live in the pitchers of Sarracenia (Frank & O'Meara 1984; Gonsiska & Givnish 2009). For possible carnivory in Brocchinia reducta, see Givnish et al. (1984) and Plachno and Jankun (2005). Brocchinia reducta does not produce nectar, only a sweet scent, but lives in the same area as the rather similar-looking and nectar-producing Heliamphora (Sarraceniaceae), and it has been suggested that the former is a Müllerian mimic of the latter (Joel 1988).
Brocchinia, a small genus restricted to the Roraima region, nevertheless includes different growth forms and takes up nirogen in different ways. Some species are tank plants, and of these B. reducta may acquire nitrogen through carnivory (see above). Brocchinia acuminata is an ant plant. Givnish et al. (1997) discussed the diversification of the genus, which seems to have begun only ca 14 m.y.a. (Givnish et al. 2004a, 2008, 2011a).
Pollination Biology & Seed Dispersal. Perhaps 1,060-1,300 species of Bromeliaceae are pollinated by humming birds. Bird-pollinated species are commonest at higher altitudes in the Andes, less common in bromeliads of drier habitats or in terrestrial lowland forest habitats (Snow & Snow 1980; Stiles 1981; Benzing et al. 2000a; Kessler & Krömer 2000; Krömer et al. 2006; Givnish et al. 2008, 2014). It is odd that there appears to be no prezygotic reproductive isolation between species of Bromeliaceae growing together in southeastern Brazil; the flowers are not notably different morphologically and flowering times overlap extensively, yet hybrids are very uncommon there (Wendt et al. 2008) as they are in the family as a whole. Furthermore, only a few species of humming birds are the major pollinators in southeastern Brazil (Snow & Snow 1986; Sazima et al. 1996; Placentini & Varassin 2007). Benzing et al. (2000a) summarize many aspects of the reproductive biology of the family.
Dispersal is primarily by ingestion of fruits by animals or movement of the seeds by wind. However, the coma on the seeds of Catopsis (Tillandsioideae) may also assist materially in germination and seedling establishment as well as dispersal by taking up water which can be used by the plantlet; this could be critical in allowing the establishment of the plant in the epiphytic habitat where Catopsis grows and where water may be at a premium (Wester & Zotz 2011). Seed hairs in Tillandsioideae develop in a variety of ways, including the almost complete separation of series of exotestal cells from the rest of the seed (Rohweder 1956; Palací et al. 2004; Barfuss et al. 2005; Magalhães & Mariath 2012).
In tank bromeliads the apical meristem is submerged and at the bottom of the tank. In some species the flower buds develop under water and open above; after flowering, the perianth rots, and the fruits, which also initially develop under water, are raised above the surface by the elongation of their pedicels.
Plant-Animal Interactions. Nymphalinae-Riodininae larvae may be found on Bromeliaceae (and Orchidaceae: Hall 2003 and references). Some epiphytic Bromeliaceae are more or less closely associated with ants (Benzing 1990); see also below.
A diverse fauna showing considerable endemism is associated with the tanks; the animals include frogs, insects, land crabs, earthworms, ostracod crustaceans, protists and the like, while a few carnivorous Utricularia (Lentibulariaceae) also live in the tanks (Thienemann 1934; Benzing 1990; Kitching 2000; Greeney 2001: bibliography). Indeed, the evolution of a group of specialised diving beetles (Dystiscidae) may be almost contemporaneous with the appearance of the tank habitat (Balke et al. 2008). In Trinidad, at least, mosquitoes that breed in bromeliad tanks help spread malaria (Pittendrigh 1948).
Genes & Genomes. The rate of molecular evolution in Bromeliaceae is very low, ca 0.00059 substitutions/site/m.y.; although the family is not particularly woody, its members have a long generation time, which seems to be connected with this low rate of molecular evolution (Smith & Donoghue 2008).
There is curious variation in diploid chromosome numbers in the vegetative parts of the plants in some species (Brown & Gilmartin 1986). Brown and Gilmartin (1989) suggested that the base chromosome number in the family was the result of sequential polyploidy: n = 8 x n = 9 -> n = 17 x n = 8 -> n = 25.
Chemistry, Morphology, etc. The flowers of Tillandsia are shown as being inverted, but those of Bilbergia have the normal position with an abaxial median sepal (Spichiger et al. 2004); the former position is incorrect (W. Till, pers. comm.). Tapetum development is described as being intermediate, the cells initially being secretory, but tending to become invasive later (Sajo et al. 2005); the pollen of Tillandia leiboldiana is described as having a proximal sulcus (Albert et al. 2010). The superior ovary of Bromeliaceae such as Tillandsioideae may be secondarily so (Böhme 1988; Sajo et al. 2004b), although I find it difficult to understand why the vascular traces to the various floral organs should then often depart independently in these taxa; they are fused when the ovary is clearly inferior. Ovule number in Brocchinioideae is unclear; L. B. Smith (in Smith and Downs 1974) seems not to have recorded this, but illustrations suggest there can be three ovules per carpel. Variation in stigma morphology in Tillandsioideae is great (Brown & Gilmartin 1989), and that in ovule morphology is extreme (e.g. Gross 1988a). Fagundes and Mariath (2014) note the variation in the chalazal appendage.
For additional information on phytoliths, see Piperno (2006), on rhizome and root anatomy, see Proença and Sajo (2008), on leaf anatomy of Pitairnioideae, see Santos-Silva et al. (2013), on petal appendages, see Brown and Terry (1992), on stigma morphology, see Brown and Gilmartin (1989), on the ovule, Sajo et al. (2004a) and Fagundes and Mariath (2014: summary table), on fruit anatomy, see Fagundes and Mariath (2010), on seed anatomy, Szidat (1922), Rohweder (1956), Gross (1988a) and Varadarajan and Gilmartin (1988a), on germination, Gross (1988b), on chromosomal evolution, see Gitaí et al. (2005), on tetraporate pollen of Hohenbergia, see Albert et al. (2011), on cultivated bromeliads, Rauh (1990), etc., and for general information, Varadarajan and Gilmartin (1988b), Smith and Till (1998) and Benzing (2000).
Phylogeny. For the phylogeny of the family, I largely follow Givnish et al. (2008: 1 gene, good generic sampling, few species, but note rooting of Fig. 1, also 2009b, 2011a, b), which is rather similar to that in Schulte et al. (2005: focus on Bromelioideae). In earlier studies, Bromelioideae were monophyletic, even when Pitcairnioideae were included (Crayn et al. 2004: matK + rps16), however, in some studies (Horres et al. 2000) Puya did not link with them (see also Jabaily & Sytsma 2010). Hechtia and Navia were of uncertain position in the study by Horres et al. (2000: trnL), but were weakly linked with Tillandsioideae in Crayn et al (2004); in that study Navia was polyphyletic. Support for Pitcairnioideae is weak (55% - Terry et al. 1997: ndhF), and the subfamily was not apparent in Horres et al. (2000), although a group of Pitcairnioideae genera was apparent, albeit with <50% bootstrap. See also Crayn et al. (2004) for phylogenetic problems with Pitcairnioideae; it has of course turned out to be eminently paraphyletic (see e.g. Givnish et al. 2007, 2011a). Givnish et al. (2011a) found strong support for most elements of the topology used here, support for the monophyly of Pitcairnioideae s. str. and for the position of Navioideae improving over earlier studies, but the monophyly of Puyoideae was still not well supported; Puya may be paraphyletic. For other phylogenetic studies, see Crayn et al. (2000), and Givnish et al. (2004b: ndhF).
For the association of Ayensua with Brocchinia and the phylogeny of Brocchinioideae, see Givnish et al. (1997) and Horres et al. (2000).
For phylogenetic relationships in Tillandsioideae, see Barfuss et al. (2004, 2005: extensive discussion on morphology), and relationships within the Tillandsia group are being realigned (Barfuss et al. 2011); Alcantarea is close to or embedded within Vriesia (Versieux et al. 2012).
Weising et al. (2011) outline phylogenetic relationships within Pitcairnioideae.
There is little phylogenetic structure along the backbone of Puya (Jabaily & Sytsma 2010: morphological study of Puya subgenus Puya; Hornung-Leoni & Sosa 2008: somewhat different relationships; Schulte et al. 2011).
For relationships within Bromelioideae, see Horres et al. (2008), Schulte and Zizka (2008) and especially Schulte et al. (2009); Bromelia serra alone may be sister to the rest of the subfamily, although support for this position is weak, and there is a large clade including it and other taxa that are all tank epiphytes. For relationships within Forsterella, see Rex et al. (2009 and references). Bromelioideae with tanks also often have flowers with asymmetric sepals and porate pollen (Schulte & Zizka 2008; Schulte et al. 2009).
Classification. The family was monographed quite recently by Smith and Downs (1974, 1977, 1979) although the supraspecific groups that they recognized are now dated. The subfamilial classification of Givnish et al. (2008) is followed here; see also the World Checklist of Monocots. Barfuss et al. (2005) provide a tribal classification of Tillandsioideae.
Generic limits need attention in much of the family. Thus within Bromelioideae, Aechmea is hopelessly poly/paraphyletic (Schulte et al. 2009; Sass & Specht 2010) and generic limits in the subfamily are generally unclear (Horres et al. 2008).
[Rapateaceae [[[Eriocaulaceae + Xyridaceae] [Mayacaceae [Thurniaceae [Juncaceae + Cyperaceae]]]] [[Anarthriaceae + Restionaceae] [Flagellariaceae [[Joinvilleaceae + Ecdeiocoleaceae] Poaceae]]]]]: little oxalate accumulation; endosperm nuclear, embryo ± undifferentiated.
Age. Givnish et al. (2004a) suggested that the age of this node is ca 87 m.y.; the age in Givnish et al. (2000) was 62 m.y..
Chemistry, Morphology, etc. For oxalate accumulation, see Zindler-Frank (1976); I do not know about accumulation in Xyridaceae and Eriocaulaceae (the latter has calcium oxalate crystals, at least) and the small families in the Poacaeae-Restionaceae clade.
Whatever the state of differentiation of the embryo, the embryo is small and rather broad (but c.f. Poaceae). Malcomber et al. (2006) described the embryo of Joinvilleaceae and Ecdeicoleaceae as being undifferentiated, embryos of Centrolepidoideae also seem to be undifferentiated (Hamann 1975), those of Restionaceae, largely undifferentiated (Linder et al. 1998), of Mayacaceae, undifferentiated (Stevenson 1998), and those of Eriocaulaceae, "poorly differentiated", or with "no exomorphological differentiation" (Stützel 1998). Embryos of the Cyperaceae group are described as being small, but they are more or less differentiated (e.g., see van der Veken 1965).
RAPATEACEAE Dumortier, nom. cons. Back to Poales
Growth monopodial, plants rosette-forming; Al-accumulators; (culm vascular bundles amphivasal); vessels in leaf?; (mucilage-producing canals +); cuticular wax with globules or wax 0, stomatal guard cells dumbbell-shaped; leaves (spirally) two-ranked, (petiole + blade), sheath open, or asymmetric and conduplicate, axillary uniseriate hairs + [slime-secreting]; inflorescence scapose, axillary, capitate, head subtended by ± spathaceous bracts (bracts 0), units cymose, flowers single, with several basal "bracteoles", large; C basally connate; A basally connate, adnate to C or not, wall with three layers [epidermis, endothecium, tapetum - Reduced type], anthers dehiscing by pores, endothecium at apex of anther only, cells with spiral thickenings (0); microsporogenesis simultaneous [tetrads tetrahedral]; (pollen grains with encircling aperture); placentation axile/parietal, style +, stigma capitate; ovules apotropous, (micropyle endostomal), outer integument 3-10 cells across, nucellar epidermal cells often radially elongated [check], suprachalazal area ± massive, funicular obturator +; (antipodal cells several); exo- (and endo)testa with SiO2, endotestal cells with U-shaped thickenings, cuticular layer between testa and tegmen, tegmen tanniniferous; hypophyll with median sheath lobe, no collar or rhizoids, primary root at most short.
16[list]/94. Tropical South America, West Africa (one species): three subfamilies below. (map: from Givnish 2004a.) [Photo - Epidryos Habit © A. Gentry, Stegolepis Flower © G. Davidse.]
Age. Crown-group Rapateaceae are dated to ca 79 m.y.a. (Janssen & Bremer 2004: note topology); ages in Givnish et al. (2000) and Givnish et al. (2004a) are substantially different, being ca 32 m.y. and (44.6-)40.8(-33.8) m.y. respectively; ages in Bouchenak-Khelladi et al. (2014b), at (55.7-)36.3(-28) m.y.a., are in line with the latter.
1. Rapateoideae Maguire
Involucral bracts long; middle layer of anther persistent; septal nectaries 0; ovule 1/carpel, ± basal; seeds ovoid-oblongoid, (with papillate apical appendage).
3/29. The Guianas to Bolivia and the Matto Grosso.
Age. Crown-group Rapateoideae can be dated to ca 38 m.y. (Givnish et al. 2004a).
[Monotremoideae + Saxofridericioideae]: ?
Age. The age of this node is around 29 m.y. (Givnish et al. 2004a).
2. Monotremoideae Givnish & P. E. Berry
Vessels with simple perforation plates; inflorescence axis determinate; ovule 1/carpel, ± basal; seeds white-granulate [muriculate], with flattened apical appendage, ovoid-oblongoid.
4/8. Guiana, upper Rio Negro in Colombia and Venezuela, Maschalocephalus dinklagei in Sierra Leone and Liberia.
Age. Crown Monotremoideae are only some 7.3 m.y. old (Givnish et al. 2004a).
3. Saxofridericioideae Maguire
(Leaves petiolate - Saxofridericieae), (sheath with auricles - Stegolepis); septal nectaries 0, intra-ovarian trichomes +; ovules few-many/carpel; seeds prismatic, pyramidal, lenticular or crescent-shaped.
9/54: Stegolepis (30+). N. South America, esp. the Guyana Highlands, Panama.
Age. The age of crown-group Saxofridericoideae is ca 15 m.y. (Givnish et al. 2004a).
Evolution. Divergence & Distribution. The ancestor of Maschalocephalus dinklagei, the only African representative of the family, probably arrived there by long distance dispersal 7.6-6.9 m.y. ago (Givnish et al. 2004a: much information on diversification).
Chemistry, Morphology, etc. Septal nectaries seem to occur in Rapateaceae only in Monotremoideae, but there are also reports of humming bird pollination in other genera (Stevenson et al. 1998a); Vogel (1981) was not sure if nectaries were to be found in the family, and Tiemann (1985) does not mention them. The ovules are described as being crassinucellate (e.g. Rudall 1997), but in some illustrations (e.g. Tiemann 1985) only the nucellar epidermis seems to cover the embryo sac.
Some information is taken from Stevenson et al. (1998a); for anatomy, see Carlquist (1966); for ovules and seeds, see Venturelli and Bouman (1988), and for some floral morphology, see Oriani and Scatena (2013).
Phylogeny. Subfamilies and tribes are all well supported at a level of >95% bootstrap, although the [Monotremoideae + Saxofridericioideae] clade has only 74% bootstrap support (Givnish et al. 2004a).
Classification. See Givnish et al. (2004a) for a infrafamilial classification; see also the World Checklist of Monocots.
[[[Eriocaulaceae + Xyridaceae] [Mayacaceae [Thurniaceae [Juncaceae + Cyperaceae]]]] [[Anarthriaceae + Restionaceae] [Flagellariaceae [[Joinvilleaceae + Ecdeiocoleaceae] Poaceae]]]]: cell wall also with (1->3),(1->4)-ß-D-glucans [Mixed-Linkage Glucans], (isoflavonoids +); cellulose fibrils in the outer epidermal walls of root elongation zone oriented parallel to root axis; trichoblast in atrichoblast/trichoblast cell pair closest to apical meristem; rhizodermal cells dimorphic; pollen grains tricellular; septal nectary 0; ovules lacking parietal tissue.
Age. This node has been dated to (96-)87, 79(-68) m.y. (Bell et al. 2010).
Evolution. Ecology & Physiology. This clade, along with core Caryophyllales, are the two major foci of the evolution of C4 photosynthesis (Ehleringer et al. 1997), although whether the origins in Poaceae and Cyperaceae are truly independent is not known (c.f. the N-fixing clade). 24/62 of the origins of this syndrome in angiosperms - and nearly all the origins in monocots - occur here (Sage et al. 2011).
Genes & Genomes. Graham et al. (2006) found an accelerated rate of change in the chloroplast genes they sequenced in the Poales - but not in the representatives of Bromeliaceae and Typhaceae (other genes also show accelerated evolution, see G. Petersen et al. 2006b); Smith and Donoghue (2009) found a similar pattern. Givnish et al. (2010b) confirmed that the rate of evolution of the whole plastome has markedly increased in this part of the tree compared to that of most other monocots, although Joinvillea and in particular Flagellaria seem to be exceptions (rate slow-down?).
Chemistry, Morphology, etc. For the distribution of the glucans in both lignified and unlignified cell walls, readily detectable by immunogold labeling, see Trethewey et al. (2005). They are sometimes present in only very small amounts and may be localized according to the thickening of the cell wall, and the family-level sampling is a bit exiguous (see also Smith & Harris 1999). Rapateaceae were not examined; these glucans are also found in Equisetum (Fry et al. 2009). For the orientation of cellulose fibrils in the root, see Kerstens and Verbelen (2002), sampling still poorer. Sampling for the distribution of trichoblast position is also poor...
[[Eriocaulaceae + Xyridaceae] [Mayacaceae [Thurniaceae [Juncaceae + Cyperaceae]]]]: flavonoids +; leaves spiral; A basifixed; fruit with persistent K/T; deletions in ORF 2280 region, full chloroplast accD and mitochondrial sdh4 genes lost.
Evolution. Genes & Genomes. Branch lengths of the ndhF and other genes are notably longer in this part of the monocot tree than anywhere else (e.g. Givnish et al. 2005, 2006b; Saarela et al. 2006).
The distribution of the sdh4 gene deletion (see Adams et al. 2002b) is consistent with the topology of the tree presented by Bremer (2002); for the accD gene and ORF 2280 region, etc., see especially Hahn et al. (1995) and Katayama and Ogihara (1996).
[Mayacaceae [Eriocaulaceae + Xyridaceae]]: root with protosylem elements in pericycle next to endodermis; vascular bundles in the stem in two rings on outside and inside of sclerified ring; SiO2 bodies 0; stomata brachyparacytic; leaf blade vernation ± flat; C clawed; ovules straight, micropyle endostomal; parietal tissue 0, hypostase +; seed operculate, operculum endotegmic in origin, tegmen tanniniferous/resiniferous.
Evolution. Divergence and Distribution. Oriani and Scatena (2014) evaluated variation in many floral character in the context of a clade [Mayacaceae [Eriocaulaceae + Xyridaceae]]. Characters are hard to place on the tree: is the absence of a leaf sheath an apomorphy for the clade, with a reversal, or two independent aquisitions, ditto colleter presence, etc.?
[Eriocaulaceae + Xyridaceae]: plants rosette-forming; root not medullated, vascular tissue with xylem and phloem mixed, or with single central vessel; vessel elements with simple perforation plates; leaves also two-ranked; inflorescence capitate, with involucral bracts, terminal (axillary), scapose; (flowers monosymmetric, 2-merous); C epidermal cells elongated, walls straight; endothecial cells with U-shaped band-like thickenings; pollen more or less spiny; carinal stylar appendages +, vascularized by the dorsal carpellary bundle, styles/stigmas commissural, not vascularized; micropylar obturator 0; seed surface ± ridged; cuticular layer between testa and tegmen.
Age. Eriocaulaceae and Xyridaceae may have diverged ca 105 m.y.a. (Janssen & Bremer 2004).
Evolution. Divergence & Distribution. The pattern of floral evolution in this clade is unclear. Some Eriocaulaceae and some Xyridaceae have very similar carinal nectariferous appendages at the base of or along the style, and unvascularised commissural stylar branches with stigmas (see below), a very unusual and distinctive arrangement; these are placed here as synapomorphies for the larger clade, with subsequent reductions, although independent origins are also possible. Similarly, an androecium consisting of three antepetalous stamens may have evolved independently; it is treated below as apomorphic for both Eriocaulaceae-Paepalanthoideae and Xyridaceae. See Oriani and Scatena (2012) for a comparison of reproductive features of the two families.
Chemistry, Morpology, etc. The scape of Eriocaulaceae lacks inflorescence bracts, i.e., it is a "true" scape, while that of Xyridaceae may have inflorescence bracts half way up. The various layers in the seed may be differently thickened, and Albolboda has been characterized as having an exotegmic seed, Mayacaceae an exotestal seed, and Eriocaulaceae and Xyris, endotestal seeds ().
ERIOCAULACEAE Martinov, nom. cons. Back to Poales
Root cortex aerenchymatous; (vessel elements with scalariform perforation plates); in leaves aerenchyma alternating with lignified strands, photosynthetic tissue in separate packets in t.s.; calcium oxalate crystals +; leaf bundle sheath cells large, without chloroplasts, palisade tissue 0; hairs common, various, on vegetative parts with foot cell and bulbous persistent usually dark colored basal cell; cuticle waxes as aggregated rodlets, stomata variable; leaf sheath not distinct; plant monoecious; receptacle ± flat, scape spirally twisted, bract at base with with closed sheath; flowers small [<6 mm across]; K with single trace, lacking stomata, aestivation open, median K adaxial, (± elongated internode between K and C), C with single trace, scarious, aestivation open; staminate flowers: (A dorsifixed), endothecial cells with complete base plate; tapetal cells uni(bi)nucleate; microsporocytes in a single row in each loculus, (microsporogenesis simultaneous); pollen spiraperturate; carpellate flowers: placentation axile; ovules 1/carpel, pendulous; antipodal cyst + [formed by fusion of antipodal cells]; fruit (indehiscent), K/C persistent; endotesta thickened on (anticlinal and) inner periclinal walls (Leiothrix exotestal); radicle 0; n = 9, 15, 20, 25; (ORF 2280 present).
6[list]/1160. Pantropical (to temperate), but esp. Guyana Highlands and S.E. Brasil (map: from Hamann 1961; Giulietti & Hensold 1990; Fl. N. Am. 22: 2000; Australia's Virtual Herbarium i.2014; Trop. Afr. Fl. Pl. Ecol. Distr. 7. 2012). 2 groups below.
Age. Crown-group Eriocaulaceae are ca 58 m.y.o. (Janssen & Bremer 2004) or(78-)64(-55.2) m.y. (Bouchenak-Khelladi et al. 2014b).
Plants usu. of aquatic habitats; roots and leaves with aerenchyma; plant dioecious; (K monosymmetric [connate, forming adaxial spathe-like structure]), C free or connate, with black glandular tips; staminate flowers: A 4-6, inner whorl ± adnate to C; pistillode +; carpellate flowers: staminodes inconspicuous; carinal stylar appendages 0 (+, very small), styles/stigmas carinal; testa poorly developed, tegmen tanniniferous.
1-2/420: Eriocaulon (400). Pantropical (to Temperate).
Plants usu. terrestrial; (aerenchyma +); (hairs T-shaped); (flowers perfect); K = to or longer than C, (C 0); staminate flowers: K and C basally fused, (C connate in the middle, free at base by schizogenous slits); C eglandular; A 3 (2), opposite C, (bisporangiate, dithecal; monothecal); pistillode +, nectariferous, (styluli separate); carpellate flowers: (K valvate), (C free); staminodes +; (carinal stylar appendages very small); seeds exo/endotestal, the anticlinal walls with prominent rib-type thickenings, the outer periclinal wall of the exotesta breaking down.
4/76: Paepalanthus (460), Syngonanthus (200), Comanthera (40). New World, esp. tropical South America, few Africa.
Evolution. Divergence & Distribution. Neotropical Paepalanthoideae show much local diversification, and early-divergent taxa are found in the Venezuela-Guayana higlands (Trovó et al. 2013).
Ecology & Physiology. In some submerged species of Eriocaulon, CO2 is taken up from the mud in which they grow via their very well developed root systems (Raven et al. 1998).
Pollination Biology & Seed Dispersal. Although the flowers of Eriocaulaceae are individually rather small and inconspicuous, pollination seems to be by insects, indeed, with their capitate inflorescences and tiny flowers that nevertheless show a great deal of variation, Eriocaulaceae are the Asteraceae of the monocots. The dark-colored glands on the petals of Eriocaulon may produce nectar. Rosa and Scatena (2003) suggest that in at least some Paepalanthoideae the pistillode (in staminate flowers) and carinal appendages on the gynoecium (carpellate flowers) are nectariferous (see also Rosa & Scatena 2007; c.f. Ramos et al. 2005); the nectary in both cases is made up of much elongated epidermal cells (Oriani et al. 2009).
For a summary of seed dispersal in the family, see Trovó and Stützel (2011).
Genes & Genome. There has been major movement of ribosomal protein and succinate dehydrogenase genes from the mitochondrion in Lachnocaulon (= Paepalanthus), at least (Adams & Palmer 2003).
Chemistry, Morphology, etc. In an anatomical survey of Brazilian Eriocaulaceae, secondary thickening was reported from species of Paepalanthus and Syngonanthus (Scatena et al. 2005). Malmanche (1919) draws phloem and xylem elements intermixed in the root stele of Paepalanthus weddellianus, but not in other taxa; this feature is common in Xyridaceae (Carlquist 1966). In Tonina (= Paepalanthus) the scape is not twisted, although it is also short; at the base is a sheathing adaxial prophyll that is shortly fused abaxially.
Inflorescence morphology shows considerable variation, even if the variation is on a single theme (Stützel & Trovó 2013: lovely shots of closed bract = branch prophyll associated with the young inflorescences). The flowers of Eriocaulaceae may be tiny, yet they show a great deal of variation in meristicity, tepal texture, connation of members of the two whorls (this may differ in staminate and carpellate flowers of the same species), sometimes being connate at the base and the apex, or apex only, and so with three apertures on the sides, the presence of perianth glands, etc. (e.g. Giulietti & Hensold 1990). Stützel (1985) found that the morphologically apical glands on the petals of Eriocaulon were displaced by an abaxial outgrowth of tissue and became adaxial-subapical. The tetratsporangate anthers are described as being extrorse (Coan et al. 2012), but they seem to be more or less latrorse; the two sporangia of bisporangiate anthers represent a single theca. When the style is commissural, as in Paepalanthoideae, it is unvascularized; the ovarian appendages of Syngonanthus, etc., are in the position of the style branches of Eriocaulon, and both are vascularized (Coan & Scatena 2004; Rosa & Scatena 2007). Rosa and Scatena (2007) describe staminodial scales opposite to the ovary septae or adnate to the base of the petals in Paepalanthoideae.
For much general information, see also Unwin (2004) and Stützel (1998), for anatomy, see Malmanche (1919), Tomlinson 1969, Stützel (1988) and Alves et al. (2013), for inflorescence and flower, Stützel (1984), for floral morphology, see Stützel (1990), and Stützel and Gansser (1995), for floral anatomy, Sajo et al. (1997: petals compound structures) and Rosa and Scatena (2003), for pollen morphology, see de Borges et al. (2009), for embryology and seed development, Arekal and Ramaswamy (1980), and Scatena and Bouman (2001), for seed and seedling of Paepalanthus, Kraus et al. (1996), finally, for seed morphology, see Giulietti et al. (1984) and Barreto et al. (2013).
Phylogeny. Support for the monophyly of Eriocauloideae and Paepalanthoideae sampled was good (Unwin 2004: three genes). The more detailed study by Gomes de Andrade et al. (2010: also three genes) provided considerable additional phylogenetic resolution; the basic phylogenetic structure is [[Mesanthemum + Eriocaulon] [Comanthera, Syngonanthus, The Rest]]. Within Paepalanthoideae, Giulietti et al. (2012) found the relationships [Syngonasnthus [Comanthera [[Rondonanthus + Leiothrix] [The Rest]]]], although not with particularly strong support. In the extensive study of Echternacht et al. (2014) there was good support for Rondonanthus being sister to the all other Paepalanthoideae, [Paepalanthus [Leiothrix [Syngonanthus + Comanthera]]] was the topology in the rest of the subfamily. Trovó et al. (2013) also discussed the phylogeny of Paepalanthoideae.
Classification. Generic limits in Paepalanthoideae are in part unclear, but Syngonanthus needs to be divided (Parra et al. 2010; Gomes de Andrade et al. 2010) and Paepalanthus, already large, expanded somewhat (Gomes de Andrade et al. 2010); see also Trovó et al. (2013). See the World Checklist of Monocots for a listing of species.
XYRIDACEAE C. Agardh, nom. cons. Back to Poales
(Plant caulescent; monopodial); anthraquinones +; root with stellate cortical cells; culm vascular bundles amphivasal; cuticle with insoluble [organic solvent] secretion; mucilage-producing multicellular hairs +; K monosymmetric, keeled, (2 keeled), the median [abaxial] membranous, (deciduous), C more or less clawed, ephemeral, connate or not: A 3, opposite C, extrorse or latrorse, (free), (sporangia connate), wall with three layers [epidermis, endothecium, tapetum - Reduced type: ?level]; stigma complex and lobed/infundibular; ovules many/carpel; seed coat testal and tegmic, tegmen mechanical; deletions in ORF 2280 region [?whole family].
5[list]/260. Pantropical to warm temperate. 2 groups below.
Age. Crown group Xyridaceae are ca 87 m.y. old (Janssen & Bremer 2004) or rather younger, (84.5-)63(-53.5) m.y.a. (Bouchenak-Khelladi et al. 2014b).
(Plant rhizomatous), (monopodial); stem vascular bundles in a single ring; leaves 2-ranked, isobifacial [oriented edge on to the stem], (terete), ligulate or not; K lacking stomata, (C enclosing stamen + two half staminodes from adjacent staminodes); (A 6), (endothecium lacking thickenings), staminodia 3, branched, with moniliform hairs on branch ends (hairs 0); tapetal cells binucleate; pollen often binucleate, elliptic (subspherical), surface reticulate and punctate or foveolate, (sulcus U-shaped), (bisulcate), 32-70µm; placentation (intrusive) parietal, basal, axile or free central, carinal stylar appendages 0, styles/stigmas commissural; ?micropyle, funicle long, hypostase 0; seeds with apical exotestal scales or fimbriae; starch grains compound; n = ?8, 9, 13, 14, 16, etc., extensive polyploidy; n = 9, 13, 17; cotyledonary hypophyll bifacial and photosynthetic, hypocotyl and collar rhizoids +.
1/225-300. Pantropical to warm temperate, 150 spp. in Brasil (map: from Hamann 1960; FloraBase 2004; Trop. Afr. Fl. Pl. Ecol. Distr. 7. 2012). [Photo - Xyris Flower, Infructescence © H. Wilson.]
Stem vascular bundles also scattered in center; leaves spiral (2-ranked), (isobifacial - Achlyphila); (inflorescence branched), (open - Achlyphila, some Abolboda), (with 1 or more pairs of opposite bracts along the scape - Achlyphila, Abolboda); P vasculature?, (K polysymmetric), (2 - Abolboda); (A introrse), staminodes 0 (filiform - some Abolboda); pollen spherical, inaperturate, surface spinose, large and small clavate, 49-250 µm (22-34 µm, clypeate - Achlyphila); placentation axile to parietal, (style solid), (carinal appendages 0 - Achlyphila); ovules anatropous (slightly campylotropous), micropyle bistomal, suprachalazal tissue massive, hypostase +; exotesta thick-walled, (of several layers, forming wing - Orectanthe), endotesta enlarged, exotegmen thick-walled; endosperm helobial [Abolboda; n = 8-10, 13, 17.
4/26: Abolboda (22). South America, Guyana Highlands in particular (map: from Campbell 2004).
Synonymy: Abolbodaceae Nakai
Evolution. Divergence & Distribution. If Achlyphila is sister to other Abolbodoideae, apomorphies for the latter may need to be adjusted.
Pollination Biology. Pollen grains may collect among the hairs on the bifid staminodes of Xyris, perhaps a form of secondary pollen presentation (Remizowa et al. 2012a).
Bacterial/Fungal Associations. The family apparently lacks mycorrhizae.
Chemistry, Morphology, etc. Cury et al. (2012) describe primary thickening in the rhizome of Xyris. Mucilage is secreted by hairs in the leaf axils of Xyris (c.f. Mayacaceae?).
The scape of Xyris is sometimes spirally twisted (c.f. Eriocaulaceae). Placentation is very variable in Xyris, but that of the whole family may be basically parietal. Sajo et al. (1997) show small swellings on the style of Xyris paradisiaca just below the stylar branches. Collar rhizoids are not drawn in Tillich (1994).
Additional information is taken from Carlquist (1960), Tiemann (1985), Kral (1988: Xyris, 1992: other than Xyris, 1998), Judd et al. (2002), Campbell (2004, especially 2008, all general. See also Malmanche (1918), Tomlinson (1969), Sajo and Rudall (1999), all anatomy, Tiemann (1985), Kral (1988: Xyris, 1992: other than Xyris), Rudall and Sajo (1999: flower and seed), Scatena and Bouman (2001: seed operculum), Benko-Iseppson and Wanderley (2002: cytology), Campbell (2012: pollen, Achlyphila perhaps multiaperturate), Stützel (1990), Campbell and Stevenson (2008: esp. Aratitiyopea), Remizowa et al. (2012a: Xyris), and Oriani and Scatena (2011: Abolboda, 2012: Xyris), all floral morphology, etc., and Winzieher (1914) and Govindappa (1955), both embryology of Xyris.
Phylogeny. There have been suggestions that Xyridaceae are be monophyletic (Michelangeli et al. 2003; Davis et al. 2004, support very weak), thus Abolboda was separate from Xyris (Givnish et al. 2010b), but sampling needs to be improved. Campbell (2004: q.v. for more information) carried out a detailed phylogenetic analysis of morphological variation.
Classification. For the above subfamilial classification, see Campbell (2004); see also the World Checklist of Monocots; for a revision of most Abolbodoideae, see Kral (1992).
[Mayacaceae [Thurniaceae [Juncaceae + Cyperaceae]]]: air canals [?= septate aerenchyma].
Evolution. Age. The age for this node is over 100 m.y.a. (Janssen & Bremer 2004: Hydatellaceae included; Besnard et al. 2009b).
MAYACACEAE Kunth Back to Poales
Marsh plants; lateral roots originate opposite the phloem; vessels in leaves 0; stem with endodermis, vascular bundles often 3; leaves amphistomatic, stomatal subsidiary cells with intersecting oblique divisions; leaves apically bidentate, univeined, lacking a distinct sheath, uniseriate colleters +; K with a single trace, C with a single trace, epidermal cells rounded, papillose; A 3, opposite sepals, dehiscing by pores, (sporangia 2), wall with three layers [epidermis, endothecium, tapetum - Reduced type], exothecium +, endothecium lacking thickenings; tapetal cells uninucleate; ?pollen morphology; placentation parietal, style with dorsal and ventral carpellary bundles, stigmatic lobes small; ovules 2-30/carpel, obturator +; exotegmic cells with massive U-shaped lignifications; primary root and cotyledonary hypophyllar sheath 0; n = 8.
1[list]/4-10. Mostly tropical and American (inc. S.E. U.S.A.), 1 sp. from Africa (map: from Hamann 1961; Boutique 1971; Fl. N. Am. 22: 2000; Trop. Afr. Fl. Pl. Ecol. Distr. 7. 2012).
Age. An estimate of the age of crown-group Mayacaceae is (109-)82.4(-68.8) m.y.a. (Bouchenak-Khelladi et al. 2014b).
Chemistry, Morphology, etc. Mayacaceae are vegetatively rather different from many other Poales. There are no vessels in stems and leaves, perhaps associated with the aquatic habitat of the plant (Carlquist 2012a). The vascular bundles on the outside of the endodermal ring are well separated from it (c.f. Eriocaulaceae: Malmanche 1919).
The flowers are sometimes described as being terminal, but the flowers seem to be axillary and associated with a broad, adaxial prophyll-like structure. Tomlinson (1969) described the flowers as being terminal, although evicted into an exillary position by the growth of an axillary shoot. Given the association of Mayacaceae with families that have scapose inflorescence with involucral bracts, the inflorescence of Mayacaceae bears re-examination. Sajo (in Sajo & Rudall 2012) noted that all perianth members had a single trace, but that to the petals divided into six. Anthers in some species are monothecal, and the stamens may be basically extrorse (Silveira de Carvalho et al. 2009). The nucellar epidermis is thick basally.
Some information is taken from Thieret (1975), Stevenson (1998) and Oriani and Scatena (2012), all general, Tomlinson (1969, 1974: anatomy), Venturelli and Bouman (1986: ovule and seed), and Endress (2008c: ovule), but the family is poorly known.
Classification. See the World Checklist of Monocots.
[Thurniaceae [Juncaceae + Cyperaceae]]: 3-desoxyanthocyanins [1 + 2], luteolin 5-methyl ether +; starch grains pteridophyte-type, amylophilic; leaves 3-ranked, margins serr(ul)ate; inflorescence racemose; flowers small [<1 cm across]; P = T, scarious; microsporogenesis simultaneous [tetrads tetrahedral], pollen in tetrads; style short, branches/stigmatic surface long; (outer integument ³3 cells across), hypostase +; seeds testal-tegmic; endosperm helobial; chromosomes with diffuse centromeres; phanomer [photosynthetic unifacial cotyledonary hyperphyll] + (0), hypocotyl +, seedling collar inconspicuous, with rhizoids; 3-nucleotide deletion in atpA gene.
Age. The age for this node is estimated at ca 98 m.y. (Janssen & Bremer 2004; Besnard et al. 2009b), or ca 101.4 m.y. (Escudero & Hipp 2013)
Evolution. Genes & Genomes. Roalson et al. (2008) and Hipp et al. (2009) discuss chromosome evolution in the clade. Although diffuse centromeres are a apomorphy for it, only in Carex is there also considerable variation in chromosome number. For the atpA gene, see Davis et al. (2004).
Chemistry, Morphology, etc. Both Thurniaceae and Juncaceae have basically racemose (polytelic) inflorescence units (Köbele & Tillich 2001); for possible variation in Cyperaceae, see that family. The inflorescences themselves are often more or less scapose.
Phylogeny. Thurniaceae are sister to Juncaceae + Cyperaceae, with strong support (Givnish et al. 1999; Bremer 2002; Davis et al. 2004), although Oxychloë was not included.
THURNIACEAE Engler, nom. cons. Back to Poales
Root stock upright, trunk-forming or not; flavone C-glycosides +; vessel elements with scalariform perforation plates; stem angled; stem bundles amphivasal [Prionium], SiO2 also in parenchyma (0 - Prionium); (some foliar vascular bundles in pairs, abaxial member inverted; fiber/fiber bundles in leaf - Thurnia); cuticular waxes as aggregated rodlets; leaf sheath closed [Prionium]; inflorescence capitate and involucrate [Thurnia] or much branched; T tube +, short; tapetal cells?; pollen grains ulcerate, exine granular; (styles separate); ovules 1-few/carpel, ascending, (micropyle zig-zag); seeds arillate; testa of sclerenchymatous fibres and unthickened cells, (short hairs - Thurnia), tegmen tanniniferous; n =?
2[list]/4. South Africa and Guyana region, Amazonia (map: see Munro et al. 2001). [Photo - Thurnia Habit, Inflorescence, Prionium - Inflorescence.]
Age. Crown-group Thurniaceae are some 33 m.y. old (Janssen & Bremer 2004) or (52.9-)26.1(-15.8) m.y.a. (Bouchenak-Khelladi et al. 2014b).
Chemistry, Morphology, etc. For the embryology, etc., of Prionium, see Munro and Linder (1999); see Zimmermann and Tomlinson (1968) for stem anatomy, Tillich (1994) describes the seedling as being similar to those of Juncaceae.
Other information is taken from Kubitzki (1998d: general) and Givnish et al. (1999); see Williams and Harborne (1975) for chemistry, and Tiemann (1985) for micropyle type.
The family is poorly known.
Classification. See the World Checklist of Monocots.
Synonymy: Prioniaceae S. L. Munro & H. P. Linder
[Juncaceae + Cyperaceae]: luteolin +; mycorrhizae 0; chloroplast rpl23 gene absent.
Age. The age for this node is estimated to be ca 88 or ca 100 m.y.a. (Janssen & Bremer 2004; Besnard et al. 2009b); other ages are (74-)61, 55(-43) m.y. (Bell et al. 2010), ca 90.6 m.y. (Escudero & Hipp 2013) and a rather unlikely 39-28 m.y. (Wikström et al. 2001, 2004).
Evolution. Divergence & Distribution. The clade [Juncaceae + Cyperaceae] is notably speciose (Magallón & Sanderson 2001). The clade including both sedges and grasses is described as being perhaps seven times more speciose than its animal-pollinated sister clade, the bromeliads (sic) (Kay et al. 2006b: supplement not accessable xii.2012; Kay & Sargent 2009), but comparisons need to be made more locally.
Ecology & Physiology. For the role of leaf sheath in supporting the stem, particularly the region with the intercalary meristem, see Kempe et al. (2013 and references).
Bacterial/Fungal Associations. Mycorrhizae may not be very common (but c.f. some Cyperaceae), but cluster roots are common. The distributions of parasitic fungi suggest that Cyperaceae and Juncaceae are close (Savile 1979b); for fungal records on the two families, see Tang et al. (2007).
Clavicipitaceous endophytes have been recorded from some genera, but they are not as common as they are on Poaceae (Clay 1986, 1990); c.f. also the distribution of the parasitic Claviceps itself.
Plant/Animal Interactions. Bugs of the Hemiptera-Lygaeidae-Cyminae and -Pachygronthini are concentrated here (Slater 1976).
Chemistry, Morphology, etc. See Endress (1995b) for some details of floral morphology.
Phylogeny. Muasya et al. (1998) suggested that Oxychloë (Juncaceae), a cushion plant from Chile, was sister to Cyperaceae, with moderate support, other Juncaceae were paraphyletic, but with with poor support, while Prionium was sister to the whole clade, with good support (see also Muasya et al. 2000: sampling in Juncaceae poor). A study by Plunkett et al. (1995) even placed Oxychloë within Cyperaceae. The relationships of this genus remained unclear (Záveská Drábková et al. 2003), although a position in Juncaceae, near Distichia, also a cushion plant, seems likely (Simpson 1995: morphological data; Roalson 2005; see especially Záveská Drábková & Vlcek 2007). Part of the problem seems to have been caused by the misidentification of the material from which early molecular samples of Oxychloë were obtained (Kristiansen et al. 2005).
JUNCACEAE Jussieu, nom. cons. Back to Poales
Plant glabrous (not Luzula); (root hairs from short cells); endodermoid layer +; culm bundles in rings; (vessel elements with scalariform perforation plates); stem rounded; SiO2 bodies 0 (SiO2 sand - Juncus); leaves ([spirally] two-ranked), terete-unifacial or isobifacial, (margins entire), (sheath closed - Luzula), (auricles +), (ligule +); (flowers single); (flowers 2-merous; imperfect); (T large - Marsippospermum); (A 3); tapetal cells uninucleate; pollen grains central in loculus, aperture obscure; G shortly stipitate, (placentation parietal), (styles separate), (branches spirally twisted); ovules 1 basal to many central/carpel, micropyle often bistomal, (outer integument 4 cells across), funicular obturator [hairs] and hypostase +/0; seed (?arillate), with (mucilaginous) exotesta and endotegmen; (phanomer 0); n = 3 or more.
7[list]/430: Juncus (300: paraphyletic), Luzula (115). Worldwide, esp. Andes (3 endemic genera), S. South America-New Zealand (2 genera) (map: Vester 1940; Hultén 1961; Frankenberg & Klaus 1980; Balsev 1996; Australia's Virtual Herbarium xii.2012; FloraBase xii.2012). [Photo - Juncus Inflorescence, Luzula Flower.]
Age. Crown group Juncaceae are some ca 74 m.y.o. (Janssen & Bremer 2004) or (87-)71.8(-51) m.y.a. (Bouchenak-Khelladi et al. 2014b).
Evolution. Pollination Biology & Seed Dispersal. For the insect-pollinated flowers of Juncus allioides, see Barrett (2013) and Huang et al. (2013).
The seeds of Luzula are myrmecochorous (Lengyel et al. 2010).
Vegetative Variation. Yamaguchi et al. (2010) show how terete and laterally flattened leaves in Juncus are fundamentally similar, being abaxialized, laterally-flatened leaves also expressing the DL gene that is responsible for midrib formation in normal bifacial monocot leaves. For unifacial leaves, see also Yamaguchi and Tsukaya (2010) and Nakayama et al. (2013).
Chemistry, Morphology, etc. In Luzula stamens are opposite individual tepals (Payer 1857), the median tepal in the outer whorl may be adaxial, and a variety of bract structures are associated with the flower (Eichler 1874). Indeed, inflorescence morphology may repay investigation. For example, Záveská Drábková (2010) suggested that that both cymose and racemose inflorescences and flowers with two and no bracteoles were to be found in Juncus.
Some information is taken from Balslev (1998); for anatomy, see Cutler (1969), for some chemistry, see Williams and Harborne (1975), and for floral morphology, see Oriani et al. (2012), and for embryology, etc., of some Juncus and Luzula, see Laurent (1904).
Phylogeny. For a phylogeny, with Juncus perhaps being paraphyletic, see Záveská Drábková et al. (2003), Roalson (2005) and especially Záveská Drábková (2010). Záveská Drábková and Vlcek (2009) found that Juncus trifidus and J. monanthos were separate from other Juncus and sister to the rest of the family (recognized as Oreojuncus - Záveská Drábková & Kirschner 2013).
Classification. For a family monograph, see Kirschner et al. (2002a-c); see also the World Checklist of Monocots. However, generic limits - bar those of Luzula - are in a mess (Záveská Drábková 2010).
CYPERACEAE Jussieu, nom. cons. Back to Poales
Aurones, flavonoid sulphates, flavone C-glycosides, tricin, kestose and isokestose storage oligosaccharides [fructans] +; (velamen +); stems solid, angled; SiO2 bodies smooth, conical, with pointed apices, attached to cell walls; stomatal guard cells dumb-bell shaped, cuticular waxes as aggregated rodlets; leaves (two-ranked, tetrastichous, spiral), sheath closed, (contra)ligule +, (serrate); inflorescence units spikelets or heads; flowers usu. monosymmetric by reduction; T variously reduced; A (connate), endothecial cells with spiral thickenings; tapetal cells bi-multinucleate; pollen as pseudomonads, (grains 2-celled), (pontoperculate); gynoecium initiated as an annular primordium, (G ), (gynophore +); ovule one/flower, basal, parietal tissue to 4 cells across, micropylar/funicular obturator +; fruit an achene, (with bristles, etc.); testa and tegmen thin, ± coalescent, exotesta with SiO2 bodies, other testal layers fibrous; endosperm cellular, micropylar and chalazal haustoria +; seedling (mesocotyl +), coleoptile +; n = 5 -> 56; 3 bp 5.8S nrDNA insertion, rps14 gene to nucleus, pseudogene remaining in mitochondrion.
98[list]/5430. World-wide (Map; Hultén 1961; Vester 1940; Australia's Virtual Herbarium xii. 2012). [Photo - Carex Carpellate Inflorescence, Eleocharis Spikes.]
Age. Crown-group Cyperaceae have been dated to ca 76 m.y. or ca 52 m.y. (Janssen & Bremer 2004; Besnard et al. 2009b). Escudero et al. (2012) suggest a crown age of (87.6-)83.7(-78.5) m.y., while (85.6-)82.6(-75.9) m.y. is the age in Escudero and Hipp (2013) and (87.6-)82.3(-73.7) m.y. in Bouchenak-Khelladi et al. (2014b).
For fossils of the family, see S. Y. Smith et al. (2009a, b, 2010).
Phytoliths uncommon; leaves with petiole + blade; pseudanthia +, sterile bracts between stamens and terminal gynoecium; flowers imperfect; staminate flower: stamens in axils of bracts ["scales"]; pollen grains central in loculus, often spherical, monoporate, sexine thick; carpellate flowers: (micropyle bistomal, zig-zag - Hypolytrum).
6/166: Mapania (80), Hypolytrum (50). Largely tropical.
Age. Crown-group Mapanioideae have been dated to a mere ca 33 m.y.a. (Escudero et al. 2012), but c.f. the fossil record; another estimate is (67-)49.2(-33.5) m.y. (Escudero & Hipp 2013).
Synonymy: Mapaniaceae Shipunov
2. Cyperoideae Beilschmied
Fine roots dauciform; phytoliths common; plants monoecious or polygamous or all flowers perfect; inflorescence branching, with spikelets; (flowers monosymmetric by reduction); T + [= scales, bristles], (connate; inner tepals clawed), 0; A (2) 3, opposite the outer T whorl; pollen grains peripheral in loculi, ± cuneiform, with distal pore [ulcus] and with 2 or more lateral apertures, (spheroidal, monoporate - Coleochloa); (G 2, superposed, less often collateral); funicle with obturator hairs.
92>/5257: Carex (1776), Cyperus (950), Fimbristylis (250), Rhynchospora (250), Scirpus (200), Scleria (200), Eleocharis (120), Bulbostylis (100), Schoenus (100), Lepidosperma (75 - to 200<), Isolepis (70), Schoenoplectiella (50). Worldwide, but esp. N. Temperate.
Age. Diversification within Cyperoideae is estimated to have begun ca 77 m.y.a. (Escudero et al. 2012) or (85.6-)78.4(-70.9) m.y. (Escudero & Hipp 2013).
Synonymy: Kobresiaceae Gilly, Papyraceae Burnett, Scirpaceae Borkhausen, Scleriaceae Berchtold & J. Presl
Evolution. Divergence & Distribution. Magallón and Sanderson (2001) note that "Cyperales" were a very diverse clade, but with 11,022 species, it is unclear what clade they mean. For diversification rates in the family, quite strongly correlated with clade age, see Escudero and Hipp (2013: c.f. topology, lots of dates). Viljoen et al. (2013) looked at biogeographical relationships in their Schoeneae, where there was much trans-oceanic dispersal.
Mapanioid sedges are common as fossils (Volkeria messelensis, Caricoidea) in the Eurasian Eocene, where they perhaps grew in wet tropical forests and swamps as do the extant members of this group (S. Y. Smith et al. 2009a, b).
Escudero et al. (2012) suggest that crown group Carex can be dated to (54.9-)42.2(-29.7) m.y., major diversification in the genus, which began ca 8 m.y. later, being somewhat linked to decreasing temperatures which were especially marked ca 34 m.y.a. at the end-Eocene. Some clades within Carex have speciated quite rapidly, but it is difficult to link this to the evolution of any particular morphological feature. Although the Siderostictae clade, sister to all other Carex, lacks the wholesale chromosomal rearrangements that characterize the rest of the genus and has only a few species (Escudero et al. 2012), it is unclear why the rearrangements should affect the success of the genus. Divergence within Eleocharis occurred ca 20 m.y.a. (Besnard et al. 2009b).
Ecology & Physiology. Despite their diversity and abundance in many ecosystems, little is known about the ecology of the family (Barrett 2013). Cyperaceae are often particularly common in wet tundra habitats (ca 8% of the land surface), and include two of the seven major contributors to the biomass there (Chapin & Körner 1995); Eriophorum and Carex are the genera involved, the other five being ecto- or ericoid mycorrhizal core eudicots. It is probable that the roots of cyperaceous plants penetrate into the mineral soil below the shallow layer of soil dominated by the roots of mycorrhizal (ericoid, ecto-) members of the community (Read 1993). Cyperaceae-dominated communities were notably extensive during the last glacial maximum north of 550 N (Bigelow et al. 2003). Even today about 13% of all species growing in Quebec and Labrador north of 54o N belong to Carex, and 16% are Cyperaceae (Poaceae are next at 11%), and they they can be major components of plant cover especially in wetter habitats (Cayouette 2008; Escudero et al. 2012).
Habitats in alpine and other extreme conditions may also be dominated by Cyperaceae. Thus there are some 450,000 km2 between 3,000 and 5960 m altitude on the Tibetan plateau dominated by the ectomycorrhizal Kobresia pygmaea. This community may be of quite recent origin, reaching its current extent since the spread of the Tibetan empire in the seventh century CE (Miehe et al. 2008, see also Zhou 2001).
A number of Cyperoideae-Cariceae and -Rhynchosporeae (but not -Scirpeae) have dauciform roots, roots which develop a dense covering of very long root hairs and overall look rather carrot-shaped; these are believed to help in phosphorus uptake by the plant when growing in phosphorus-poor soils (Shane et al. 2005: some Juncaceae may also have such roots; Playsted et al. 2006). Epidermal cells in such roots are elongated at right angles to the long axis of the root (Shane et al. 2005). The plant secretes citrate chelating agents, etc., into the soil and phosophorus uptake is increased (Playsted et al. 2006). Some species of non-mycorrhizal Carex have distinctive, bulbous-based root hairs (Miller et al. 1999). Many, but not all, tundra-dwelling Cyperaceae, whatever their mycorrhizal status, take up nitrogen predominantly in an organic form (Raab et al. 1996, 1999).
About 1,500 species of Cyperaceae carry out C4 photosynthesis, and this has perhaps six origins in the family, as well as showing some reversals to C3 (Soros & Bruhl 2000; Besnard et al. 2009b; Bruhl & Wilson 2008; Roalson 2011; Larridon et al. 2011a; Sage et al. 2012). In some aquatic Cyperaceae with submerged leaves C4 photosynthesis may help increase nitrogen use efficiency (Besnard et al. 2009b; Bruhl & Wilson 2008; Roalson 2011). For the complexity of possible patterns of the evolution and loss of the C4 pathway and that of intermediate pathways within Eleocharis, see Roalson et al. (2010); there is only a single major C4 clade in Cyperus (Reid 2011; Larridon et al. 2013).
Besnard et al. (2008b, 2009b) suggested that evolution of C4 photosynthesis had occurred within the last ca 19.6 m.y., first appearing in Bulbostylis; genetic changes in the important enzymes phosphoenolpyruvate carboxylase and rbcl may have occurred in parallel. Martins and Scatena (2011) looked at the diversity of Kranz-type morphologies in the family from a developmental point of view.
A few taxa like Rhynchospora anomala are dessication-tolerant and arborescent; their roots, which make up the "trunk" of the plant along with the persistent leaf bases through which the roots run, have a well-developed velamen. Thus Cyperaceae are quite important components of the vegetation of inselbergs where soils are shallow and dry out fast (Porembski 2006).
Waterway et al. (2009) discuss ecological diversification in Cariceae. There are widespread wetland species, but the forest taxa are often more geographically restricted . Clones of Carex curvula may persist for 2,000 years or so in the Alps despite climatic fluctuations (Steinger et al. 1996: growth rate changes probably not important).
Some sieve tubes in the leaves that are adjacent to the xylem lack companion cells, are notably thick-walled, and seem to be involved in short distance transport of not very concentrated sugars (Botha 2013).
Pollination Biology & Seed Dispersal. Although Cyperaceae are normally thought of as being pollinated by wind, there have been some transitions to insect pollination (Wragg & Johnson 2011 and references).
Fruit dispersal mechanisms are very varied, including water, wind (e.g. the bristles surrounding the fruits of Eriophorum), animals (both epi- and endozoochory), and ants, attracted by a variety of elaiosomes (Allessio Leck & Schütz 2005: also seed dormancy and germination requirements; Barrett 2013).
Plant-Animal Interactions. R. L. Barrett (2013) noted a number of close associations between species of Lepidosperma and moths like the small grass-miner moth Elachista and the sun-moth Synemon.
Bacterial/Fungal Associations. Cyperaceae, like other plants in the tundra habitat (see above), often lack mycorrhizae (but c.f. Muthukumar 2004; Miller at al. 1999 for mycorrhizae in Carex). However, in Tibet and arctic tundra habitats, at least, Kobresia species are ectomycorrhizal (Gardes & Dahlberg 1996; Gao & Yang 2010). Largely ascomycetous fine endophytes are also commonly found in Cyperaceae from tundra habitats (Higgins et al. 2007), and are more prevalent than arbuscular mycorrhizal fungi. They may be members of Clavicipitaceae, elsewhere especially prominent on Poaceae-Poöideae (Schardl 2010). Dauciform roots (see above), dark septate hyphae and/or endomycorrhizae may all be found in the one species, whether in the same or a different locality (Michelsen et al. 1998; Gao & Yang 2010).
Smuts (Ustilaginales) are very diverse on Cyperaceae (Kukkonen & Timonen 1979; Savile 1979b).
Genes & Genomes. Carex is notable for the wide variation in chromosome number it shows because of extensive chromosome fission, fusion and translocation that is facilitated by the diffuse centromeres of the genus (Hipp et al. 2011); genome size is, however, little affected (Chung et al. 2012). Genome size and chromosome number are negatively correlated in diploid taxa, and although polyploids tend to have larger genomes than related diploids, they do not have absolutely large genomes (Lipnerová et al. 2013). For chromosome numbers and evolution, see Hipp (2007), Roalson (2008), Roalson et al. (2008a), and Hipp et al. (2009), for a nrDNA insertion, see Starr et al. (2008a).
Chemistry, Morphology, etc. For inflorescence morphology, see Reutemann et al. (2012: individual variables listed); branching can be from the axils of prophylls, and/or from collateral or superposed meristems. Zhang et al. (2004) suggested that spikelets in Schoeneae, at least, were sympodial, however, those of Cyperoideae as a whole are indeterminate (Vrijdaghs et al. 2005c, 2008 [Schoenus], 2010 [esp. Cyperoideae]). Studies by Guarise et al. (2012) emphasized the diversity in development pathways that produced superficially similar capitate inflorescence in Cyperus; relatively few developmental changes could also produce substantial diversity in mature inflorescence morphology.
For the literature on the possible pseudanthial nature of some flowers in Cyperaceae-Mapanioideae, see Bruhl (1991); he noted that the "foliar" structures in the taxa he studied were outside the stamens, so they probably represented perianth parts. Recent studies confirm that mapanioid "flowers" are indeed pseudanthial (Prychid & Bruhl 2013; see also Vrijdaghs et al. 2004a; Richards et al. 2005, esp. 2006: Exocarya scleroides).
Scirpus sylvaticus has a relatively unspecialised flower to which the more derived morphologies in Cyperoideae can perhaps be related; the three stamens and the carpels are opposite the outer perianth members (Vrijdaghs et al. 2005a, 2009). In general, the stamens are shown as being opposite the outer perianth whorl (Bruhl 1991), the angles of the gynoecium (Goetghebeur 1998) or the style-stigma (Larridon et al. 2011b), all consistent with a flower in which members of the whorls alternate and the absence of the inner stamen whorl is of no consequence. The median carpel in Carex is shown as being adaxial (Eichler 1875), i.e. in the inverted position (see also Spichiger et al. 2004, but c.f. Reynders & Vrijdaghs et al. 2012). However, as Vrijdaghs et al. (2011) note, it is difficult to talk about carpels in Cyperoideae since the gynoecium develops from an annular primordium - on top of which there may be two- or three- (rarely even four-) branched styles; when there are two styles, there is no obvious carpel fusion (Reynders & Vrijdaghs et al. 2012; Lucero et al. 2014). I have placed "gynoecium initiated as an annular primordium" as characterizing the whole family (for Mapanioideae, see Prychid & Bruhl 2013), but Reynders and Vrijdaghs et al. (2012) note that this gynoecial initiation is also found in Luzula, and elsewhere, as in many Poaceae, so where it will end up is unclear.
The distinctive hairs of Eriophorum (Cyperoideae) arise centripetally on a perianth ring-primordium (Vrijdaghs et al. 2004b). Pollen apertures in Carex have a very thin underlying intine while that in interapertural areas is much thickened, i.e., the reverse of the normal condition (Halbritter et al. 2010). The nucellus of some Bulbostylis ovules may be only a single cell across (Maria & López 2010).
For a vast amount of additional information, see Bruhl (1995); other general information is in Naczi and Ford (2008). For anatomy, see Cutler (1969), for phytoliths, see Piperno (2006), for the prophyll, see Blaser (1944), for inflorescence morphology, see Eiten (1976) and Nijalingappa and Goetghebeur (1989: Ascopholis, bristle = axis), for floral morphology, see Bruhl (1991) and Vrijdaghs et al. (2006), for pollen, see van Wichelen et al. (1999), Nagels et al. (2009), Coan et al. (2010) and Furness and Rudall (2011), for the gynophore, etc., see Vrijdaghs et al. (2005b), for ovule and seed development, see Nijalingappa and Devaki (1978) and Coan et al. (2008), and for embryo morphology, see van der Veken (1965: hundreds of species).
Phylogeny. Mapanioideae and Cyperoideae are monophyletic (e.g. Simpson et al. 2003, esp. 2008; Hinchcliff & Roalson 2013). Within Mapanioideae Capitularia is sister to the rest (Escudero & Hipp 2013).
Within Cyperoideae, things are rather difficult. Trilepideae are sister to the remaining genera (Muasya et al. 2009a), while in a supermatrix analysis these other taxa were placed in a well-supported set of relationships [[Sclerieae + Biesboeckelereae] [Schoeneae [Rhynchospora [clade including Carex and Scirpus + clade including Eleocharis, Isolepis and Cyperus]]]] (Hinchcliff & Roalson 2013) - the first three clades are somewhat different to those in Muasya et al. (2009a). However, in a study based on the two just mentioned, Schoeneae were in three separate basal pectinations and Cryptangieae were in another, and then came [Rhynchospora + The Rest] (Escudero & Hipp 2013), while in a study focusing on schoenoid sedges, relationships in Cyperoideae were [Cladium (ex-Schoeneae) [[[Sclerieae + Biesboeckelereae] [[Cryptangieae + Schoeneae] [Rhynchospora + The Rest]]], although some nodes had little support (Viljoen et al. 2013). Jung and Choi (2013) emphasized relationships in Korean taxa and found relationships were [Trilepideae [[Sclerieae + Biesboeckelereae] [Schoeneae [Cryptangieae, Schoeneae [Schoeneae [Rhynchospora + The Rest]]]]], i.e. Schoeneae are very paraphyletic, but again there was little support for the basal nodes.
Cyperus is massively paraphyletic (e.g. Muasya et al. 2002; Larridon et al. 2011a, b; Hinchcliff & Roalson 2013). Larridon et al. (2013) suggested that C4 members of the clade were monophyletic and embedded in a paraphyletic C3 group, although relationships along the spine of the C4 clade were for the most part little supported. For other relationships, see Hinchcliff and Roalson (2013), for the relationships of Carpha and other Schoeneae, see Zhang et al. (2007); for relationships within Rhynchosporeae, see Thomas et al. (2009); and for relationships around Eleocharis, see Hinchcliff et al. (2010) and Roalson et al. (2010).
Relationships are beginning to be resolved within the large and complex Cariceae (Reznicek 1990 and associated papers; Yen et al. 2000; Roalson et al. 2001; Starr et al. 2006). Carex is paraphyletic, as has been demonstrated by several studies (see Yen & Olmstead 2000; Starr et al. 1999, 2004; Waterway & Starr 2008; King & Roalson 2008: use of nrDNA problematic; Starr & Ford 2009; Escudero & Luceño 2009; Gehrke et al. 2010: resolution at base of genus poor). Starr et al. (2008b) suggested that there are four major clades in the Carex area - [Uncinia, Kobresia, Cymophylla, some Carex] [Schoenoxiphium, some Carex] [Carex subgenus Vignea], and [Carex subgenus Carex, etc.], however, details of the relationships of Carex s.l. are unclear (Hinchcliff & Roalson 2013). Conventional wisdom in which a highly compound inflorescence is the plesiomorphic condition for Carex, taxa with simple spicate branches being derived, perhaps several times, seems the exact opposite of what actually happened (Ford et al. 2006). Similarly, species of Carex believed to be intermediate between that genus and Uncinia, with its hooked inflorescence axis protruding through the apex of the perigynium (prophyll), seem not to be (Starr et al. 2008b: support not strong). Evolution is not necessarily complex -> simple.
Naczi (2009) discussed the use of morphological characters in phylogenetic analyses; this is tricky because of the highly derived nature of cyperaceous flowers. This makes character coding difficult.
Classification. Carex is paraphyletic (see above) and genera like Kobresia, Cymophyllus, Uncinia and Schoenoxiphium should be included in it (or some species of Carex will have to be moved). For a general evaluation of generic limits in Cypereae, see Muasya et al. (2009b); Cyperus is to include about thirteen genera (see also Muasya et al. 2002; Hinchcliff et al. 2010; Larridon et al. 2011a, b, 2013; Reid 2011); Eleocharis is also to be slightly expanded (Hinchcliff et al. 2010). For pre-lapsarian nomenclature, etc., see Goetghebeur (1985); the World Checklist of Monocots (Govaerts et al. 2007) is a printed version of this). T. M. Jones provides a Carex interactive identification key; there is also a visual version.
[[Anarthriaceae + Restionaceae] [Flagellariaceae [Joinvilleaceae + Ecdeiocoleaceae] Poaceae]]]: flavones +; sieve tube plastids with cuneate and other less densely packed crystals; (chlorenchyma with peg cells [c.f. arm cells of some Poaceae?]); leaves two-ranked, with sheath; inflorescence branches spiral [?at higher level]; bracteoles 0; flowers small [<1 cm across]; P = T, membranous; endothecial cells with ± helical/girdle-like thickenings; pollen monoporate, margin annulate [ulcerate], wall scrobiculate [minute pores penetrating tectum and foot layer]; style branches long, stigmas plumose; ovule 1/carpel, apical, pendulous, straight; fruit a capsule; seedling with collar rhizoids.
Age. The age of this node may be ca 108 m.y.a. (Janssen & Bremer 2004: c.f. topology), but the age in Wikström et al. (2001: again c.f. topology) is only (52-)49, 45(-42) m.y., Bell et al. (2010) suggested an age of (76-)65, 58(-45) m.y..
Evolution. Divergence & Distribution. This is a notably speciose clade (Magallón & Sanderson 2001) with well over 11,000 species, although the diversification rate is lower than that of Cyperales. However, there is considerable asymmetry in clade size within this clade. Most species belong to Poaceae, with ca 11,400 species, the second most species-rich family (Restionaceae) having only some 535 species, fewer than 1/20th the species in Poaceae (Chase 2004; c.f. Linder & Rudall 2005 for diversification); this is discussed further under Poaceae below.
Chemistry, Morphology, etc. For the flavonoids of Anarthriaceae, Restionaceae and Ecdeiocoleaceae, see Williams et al. (1997a); the variation is complex and needs to be re-evaluated in light of the current position of the last family.
For inflorescences, see Kellogg et al. (2013). Linder and Ferguson (1985) discuss variation in pollen morphology. Flagellariaceae have "multicellular papillae" on their stigmas (Appel & Bayer 1998), but whether these are receptive in the same way as the multicellular branches of, say, Poaceae, needs clarification. Determining that the pollen is operculate can be tricky. In Poaceae, although the style is hollow, the pollen tubes grow between elongate transmitting cells of these multicellular branches (Lersten 2004). The ovule is scored as lacking any parietal tissue and so being tenuinucellate and the pollen as being tricellular for the whole group by Givnish et al. (1999, c.f. Appel & Bayer 1998 for these characters).
Information on the ORF 2280 region is taken from Hahn et al. (1995) and Katayama and Ogihara (1996: Ecdeiocoleaceae not included). For the loss of the rpoC1 gene, see Morris and Duvall (2010).
Phylogeny. An analysis of 26S rDNA suggested that Dasypogonaceae might be part of this clade, being very closely linked with Ecdeiocoleaceae, Anarthriaceae and Centrolepidaceae (= Restionaceae) (Neyland 2002b), slightly less so with the one member of Restionaceae included. However, data from atpB, rbcL, 18S, etc., have not confirmed this grouping (see e.g. Givnish et al. 2010b), and Dasypogonaceae are probably sister to Arecaceae (q.v.). Davis et al. (2004: very weak support) found that Flagellaria grouped with Mayacaceae, etc., rather than with the other Poales.
However, although the composition of this clade now seems settled, relationships within in are still somewhat unclear. Bremer (2002) found a sister group relationship between Ecdeiocoleaceae and Poaceae (see also Harborne et al. 2000). A combined morphological and molecular (mitochondrial and chloroplast genes) analysis placed Flagellariaceae, Ecdeiocoleaceae and Poaceae in an unresolved trichotomy (Michelangeli et al. 2002, esp. 2003), a not dissimilar result to that obtained by Davis et al. (2004). Graham et al. (2005) obtained a set of relationships [Flagellariaceae [Restionaceae [Ecdeiocoleaceae + Poaceae]]], perhaps a branch length or sampling problem. Using two chloroplast genes, Marchant and Briggs (2007) found strong support for a sister group relationship between Joinvilleaceae and Ecdeiocoleaceae (both genera of the latter were included), and these relationships were also found by Saarela and Graham (2010), but only in Bayesian analyses. More recently, Givnish et al. (2010b: plastome sequences) found good support for the [Ecdeiocoleaceae + Poaceae] clade, and this topology is tentatively preferred here.
[Anarthriaceae + Restionaceae] / restiid clade: sand-binding [capillaroid] roots +, root hairs usu. persistent, lignified, originating from any epidermal cells; culm with parenchymatous sheath, palisade chlorenchymatous tissue, and sclerenchymatous cylinder, vascular bundles inside; leaf blade ± unifacial; chlorenchyma with peg cells; plant dioecious; staminate flowers: anthers dorsifixed; pistillode 0; carpellate flowers: staminodes 0; seedling phanomer [photosynthetic unifacial cotyledonary hyperphyll] +; loss of rpoC1 gene.
Age. The age of this node is ca 96 or 97 m.y., depending on relationships (Janssen & Bremer 2004) or ca 80 m.y. (Litsios et al. 2014: "root" age for Restionaceae, Centrolepis, etc., not included).
Evolution. Ecology & Physiology. Most members of this clade flourish on nutrient-poor soils, whether in southern Africa or in Australia, indeed, at least some Restionaceae seem to be unable to benefit from transient nitrogen availability (Meney & Pate 1999b; Briggs et al. 2014). The rootlets of Restionaceae/Anathriaceae are sometimes described as being capillaroid, with dense, exceptionally long, and sometimes lignified root hairs that cause the roots to have a sheath of sand attached to them; there are other distinctive root morphologies like cluster/proteoid roots (Meney & Pete 1999b; Lambers et al. 2006). Cyperaceae and Proteaceae growing in similar phosphorus-poor environments develop analagous structures that are believed to facilitate phosphorus uptake. T. L. Bell et al. (2000) suggested that the total root length of the grasses tested was considerably greater than that of Restionaceae, although the dense root hairs of the latter were not taken into account.
Chemistry, Morphology, etc. See Malmanche (1919) for vegetative anatomy; the stomata he described would now be called brachyparacytic.
ANARTHRIACEAE D. F. Cutler & Airy Shaw Back to Poales
(Flavonol glycosides +); SiO2 0; stomata in grooves; leaves ligulate; culm branched or not; staminate flowers: pollen operculate; carpellate flowers: G opposite outer P; ovules?, hypostase +; seed coat?; endosperm type?, embryo?; ?collar rhizoids; n = 6, 9, 11; ORF 2280 +, trnL gene with 3bp deletion and 5bp insertion.
3[list]/11. West Australia (map: from FloraBase 2004). [Photo - Anarthria: Staminate & carpellate inflorescences © D. Woodland.]
Age. The age of crown-group Anarthriaceae is ca 55 m.y. (Janssen & Bremer 2004) or much younger, (60-)25.6(-17.2) m.y.a. (Bouchenak-Khelladi et al. 2014b).
Chemistry, Morphology, etc. The three genera are rather different. Anarthria lacks palisade tissue, a sclerechymatous cylinder and parenchyma sheath in the culm (or it could be interpreted as having a cylinder towards the middle of the culm, with scattered vascular bundles outside), it has two-ranked, isobifacial leaves, stomata in grooves, a deciduous spathe, and n = 11. Cronquist (1981) suggested that the flowers had bracteoles. Hopkinsia has G 1, with long style branches; the fruit is a nut with a fleshy pedicel and persistent perianth, and n = 9; the cotyledon is apparently not photosynthetic. Lyginia has fructans, the culm is unbranched, there are crystals and druses, the stamens are connate, the seeds are minutely spiny with a central hyaline flange, and n = 6. Hopkinsia and Lyginia have a culm with subepidermal chlorenchyma separated from cortex by parenchymatous and sclerenchymatous rings, leaves reduced to scales, and microverrucate pollen. Stigma papillae in Anarthria?
General information is taken from Linder et al. (1998) and Briggs and Johnson (2000). See also Cutler and Airy Shaw (1964: anatomy) and Linder and Rudall (1993: esp. Anarthria).
All in all, little is known about embryology and seed development.
Phylogeny. The phylogenetic structure of the family is [Anarthria [Hopkinsia + Lyginia]] (Briggs et al. 2000, 2014; papers in Meney & Pate 1999a).
Classification. Putting the three genera in three separate families seems a bit much, no hierarchical information being conveyed by this move, although the three are morphologically quite distinct. At the other extreme, Linder et al. (2000) suggested that these genera belonged to Restionaceae, albeit perhaps sister to the rest - they (but not Anarthria itself) have the distinctive culm anatomy of that family, and Lyginia, at least, has starch in the embryo sac, like Restionaceae.
Synonymy: Hopkinsiaceae B. G. Briggs & L. A. S. Johnson, Lyginiaceae B. G. Briggs & L. A. S. Johnson
RESTIONACEAE R. Brown, nom. cons. Back to Poales
Rhizome with endodermoid sheath; culm with lignified chlorenchymatous cells lining substomatal cavities [protective cells]; plant ± glabrous; (foliar epidermis with long and short cells); leaves much reduced, (sheath closed); (plant monoecious); inflorescence made up of spikelets; outer T hooded [?how common], (T 0), staminate flowers: A 3, opposite inner P, anthers bisporangiate, monothecal, (tetrasporangiate, e.g. Harperia); tapetal cells 1-4-nucleate, pollen central in loculus; pollen (binucleate), with coarse granules [exine fragments] on pore; pistillode 0; carpellate flowers: P variable; staminodes 0; G opposite outer P, (only 1 fertile), common style short or 0, stigmatic receptive cells on multicellular branches; ovule with cells of nucellar epidermis anticlinally elongated, suprachalazal zone ± massive, hypostase +; embryo sac with compound starch grains esp. surrounding polar nuclei, antipodal cells ± proliferating, persistent; exotesta persistent, ± thick-walled, tegmen tanniniferous; (cotyledon not photosynthetic), hypocotyl and collar at most small, collar rhizoids +, first seedling leaf with blade; 28 kb chloroplast genome inversion +/- [latter - Desmocladus, Elegia?].
61[list]/535 - four subfamilies below. Africa (inc. Madagascar), Hainan and Vietnam to Australia, New Zealand, Chile (map: from Good 1974; Trop. Afr. Fl. Pl. Ecol. Distr. 7. 2012). [Photos - Collection. Dovea tectorum is properly Chondropetalum tectorum.]
Age. Crown-group Restionaceae are dated to ca 74 m.y. (Janssen & Bremer 2004) or (72.6-)71.2(-64) m.y.a. (Bouchenak-Khelladi et al. 2014b).
1. Restionoideae Bartling
Flavonols, non-hydrolysable tannins, myricetin derivatives +, flavones less diverse; (spikelets 0); pollen grains with pores 4-10 µm across, (thickened foot layer +); n = 16, 20.
11-16/350: Africa south of the Sahara, Madagascar.
1a. Restioneae Bartling
SiO2 bodies often in parenchyma sheath, not in sclerenchyma cylinder; chlorenchyma cells radially elongated; styles 1-3, often widely separate; (fruit a soft-walled nut); germination phanerocotylar.
3-8/300: Restio (95), Ischyrolepis (48), Elegia (50), Thamnochortus (35). Madagascar, Africa south of the Sahara, especially the Cape Region. [Photo - Elegia, Habit.]
Synonymy: Elegiaceae Rafinesque
1b. Willdenowieae Masters
SiO2 bodies usually in sclerenchyma cylinder only; ridges of sclerenchyma often alternate with vascular bundles, chlorenchyma cells often radially short and squat (lignified chlorenchyma cells extending from ridges); [G 2], styles branches 2, (basally connate); ovule (micropyle endostomal - Willdenowia), (parietal tissue ca 1 cell across - ?Hypodiscus); proliferating antipodals?; fruit a nut, often with elaiosomes [fleshy pedicels]; young seed coat not tanniniferous; germination cryptocoylar.
8/50: Anthochortus (15). The Cape region of South Africa.
[Sporadanthoideae [Centrolepidoideae + Leptocarpoideae]: flavonols rare, except quercetin, non-hydrolysable tannins rare, flavones diverse, sulphated flavonoids +; chlorenchymatous cells palisade; pollen pore not annulate, pores 8-25 µm across, margins irregular, thickened foot layer 0; cotyledon not photosynthetic [ca half the genera], seedling culm internodes elongated, leaves terete; n = 6, 7, 9, 11, 12.
2. Sporadanthoideae Briggs & Linder
Myricetin +; sand-binding roots 0; spikelets often 0, flowers solitary and with bracteoles.
3/31: Lepyrodia (22). Australia and New Zealand.
[Centrolepidoideae + Leptocarpoideae]: (parietal tissue 1 cell across).
Plant ± caespitose, (annual); sand-binding roots 0; vascular bundles in culm on either side of thickened cylinder (not Gaimardia), palisade tissue 0; SiO2 ?0; epidermis with hairs and papillae; leaf blades well developed, rounded-unifacial, (ligulate); inflorescence scapose, capitate and with inflorescence bracts, or spicate, (inflorescence branches 2-ranked); flowers perfect; T 0; A 1-2; G [1-14(-45)]; ovule nucellar cap 0; antipodal cells usu. binucleate; fruit dehiscing abaxially or indehiscent; endotegmen alone persistent; embryo conoid; (phanomer 0), chlorenchymatous cells isodiametric or palisade; n = 10.
3[list]/35. Hainan, IndoChina and Malesia to New Zealand, S. South America (Gaimardia) (map: from Ding Hou 1957; Hamann 1960; van Balgooy 1984; Australia's Virtual Herbarium 1.2014). [Photo - Gaimardia Habit and Close-up, Centrolepis Habit.]
Age. Estimates of the crown-group age of this clade range from 45-97 m.y. depending in large part exactly where it is placed in the tree (Janssen & Bremer 2004); (40.8-)31.2(-22.8) m.y.a. is the age in Bouchenak-Khelladi et al. (2014b).
Synonymy: Centrolepidaceae Endlicher, nom. cons.
4. Leptocarpoideae Briggs & Linder
Flavones, sulphated flavonoids, (8-hydroxyflavonoids, e.g. gossypetin) +; chlorenchyma interrupted by pillar cells [radiating ± palisade-like and ± lignified cells of sclerenchyma sheath] (0), (sclerenchymatous bundle girders opposite outer vascular bundles +); protective cells 0, (elongated, thick walled epidermal cells +); (style strongly recurved [hair-pin style]); ovule (micropyle endostomal - some Leptocarpus); tegmen tanniniferous?; germination usually phanerocotylar.
28/117: Chordifex (20). Hainan and Vietnam to Australia, New Zealand, Chile (Apodasmia).
Centrolepidoideae are rather small more or less caespitose herbs. The inflorescence is scapose, being capitate and involucrate or spicate.
Evolution. Divergence & Distribution. There are ca 350 spp. of Restionaceae in the Cape region, diversification beginning in the late Eocene-early Oligocene some 43-28 m.y. ago (Hardy et al. 2004a; Linder & Hardy 2004; Hardy et al. 2008). Some diversification in Australian Restio may be associated with the aridification of the Nullarbor Plain some 14-13 m.y.a. separating what became eastern and western clades (Crisp & Cook 2007).
There are a number of records of pollen of Restionaceae (and Centrolepidaceae) from the northern hemisphere from sites in both the Old and New Worlds (Muller 1984), but the identification of these grains has been questioned (Linder 1987).
Ecology & Physiology. Restionaceae can be locally dominant in oligotropic conditions, whether wet or dry. Thus Restionaceae replace Poaceae in the graminoid layer in the nutrient-poor soils of the fynbos vegetation of the Cape Floristic region (Bell et al. 2000). The habitats they prefer are often subject to seasonal fires, and some species, sprouters, accumulate starch in their rhizomes, while others, non-sprouters, reproduce by seeds (c.f. Ericaceae). Overall diversification of reseeders in southern Africa is greater than that in Australia, perhaps in response to the greater climatic heterogeneity of the former, however, there are numerous resprouter species because of the frequency of the seeder -> resprouter transition (Litsios et al. 2014).
Pollination Biology & Seed Dispersal. In most Australian Restionaceae at least 10-12 months elapse between flowering and fruiting (Meney & Pate 1999a). Myrmecochory is common in the South African (Cape) Restionoideae-Willdenowieae, the nutlets having fleshy funicles that attract ants (Briggs & Linder 2009).
Chemistry, Morphology, etc. The culm has subepidermal chlorenchyma separated from the cortex by parenchymatous or sclerenchymatous rings; these may not be strictly comparable in different taxa (Cutler 1969) and so may not be an apomorphy for the family.
Information is taken from Linder (1984: African members of the family), Kircher (1986; guard cells not shown as being dumb-bell-shaped), Linder et al. (1998), Meney and Pate (1999a), all general, Williams et al. (1998) and Harborne et al. (2000), flavonoid patterns, Ronse Decraene et al. (2001a, 2002b: floral development, much variation), Borwein et al. (1949) and Krupko (1962), both embryology, Newton et al. (2002: seeds), and Linder and Caddick (2001: esp. seedlings). For Peter Linder's "Intkey thingy" on African Restionaceae - 2,000 pictures - see http://www.systbot.unizh.ch/datenbanken/restionaceae/.
The following information is about Centrolepidoideae (often as Centrolepidaceae). Cutler (1969) emphasized the fact that the root hairs arose from one side of the epidermal cell and that the root lacked a pericycle. He suggested that the peg cells of Centrolepidoideae and other Restionaceae might be rather different, peg cells s.s. perhaps being absent in the former. Also, whether or not Centrolepidoideae have SiO2 bodies needs confirmation.
For inflorescences, see Kellogg et al. (2013). There has been some discussion as to whether Centrolepidoideae have a flower or pseudanthium; Sokoloff et al. (2009b) reject the latter proposition. Sokoloff et al. (2010; see also Hamann 1962a; Remizowa et al. 2011) interpret the inflorescence of Centrolepis as being a racemose spikelet, not cymose. Hou (1957) described the anthers as being 1- or 2-celled. The separate carpels sometimes become more or less fused, the result being something that looks like a syncarpous gynoecium - or, in Centrolepis itself, the gynoecium is definitely syncarpous, and although the carpels there appear to be more or less one on top of each other, that is because of developmental gymnastics resulting in the greater development of one side of the receptacle (Sokoloff et al. 2009b). The ovule is described by Hamann (1975) and Cooke (1998) as being weakly crassinucellate and also as having a megasporocyte that lacks a parietal cell; although cells in the nucellar epidermis may have divided, this seems unlikely from the illustrations in Hamann (1962a).
Phylogeny. The position of the old Centrolepidaceae - morphologically quite a distinctive group - with respect to Restionaceae was uncertain for some time (e.g. Linder et al. 2000), most studies unfortunately concentrating on either the Australian or African Restionaceae rather than the broader studies needed to solve the problem. A position sister to Restionaceae was possible (Linder & Caddick 2001) as well as one within the family (Bremer 2002: support weak). In more recent studies Centrolepidaceae and Restionaceae were sister taxa in parsimony analyses of trnK and trnL-F, while in Bayesian analyses, and also in rbcL analyses, the relationships [Restionoideae [Sporadanthoideae [Leptocarpoideae + Centrolepidoideae]]] were recovered (Briggs & Linder 2009; Briggs et al. 2010). Briggs et al. (2014) again obtained this topology in Bayesian analyses, but in maximum parsimony analyses the topology [Restionoideae [[Sporadanthoideae + Leptocarpoideae] Centrolepidoideae]] was obtained; very long branches were associated with Centrolepidoideae.
Although adult plants of Centrolepidoideae have terete leaves, it is noteworthy that young seedlings of the clade of Restionaceae in which Centrolepidoideae are embedded also have terete leaves; Centrolepidoideae may be paedomorphic (see also Briggs et al. 2014 and references). Furthermore, the pollen apertures of Australian Restionaceae in particular are like those of Centrolepidaceae, a larely Malesian-Australasian group (Chanda 1966).
The variation in the presence of the 28kb chloroplast genome inversion within Restionaceae is remarkable (Michelangeli et al. 2003). For details of phylogenetic relationships, see Briggs et al. (2010).
Classification. For the classification of Restionaceae and characterization of the subfamilies, see Briggs and Linder (2009); Leptocarpoideae have been pulverized. Linder and Hardy (2010, see also Linder 1984, 1985) provide generic characterisations and an enumeration of the species of Restionaceae-Restioneae in southern Africa, although the limits of Restio itself are still unclear.
[Flagellariaceae [[Joinvilleaceae + Ecdeiocoleaceae] Poaceae]]: primary cell walls with branched mixed-linkage glucans; leaf blade with ligule; inflorescence branches with adaxial basal swellings; endothecial cells with complete base plate thickenings; nucellar cap +, suprachalazal zone massive; fruit indehiscent, fleshy; cotyledon not photosynthetic.
Age. This node has been dated to (76-)65, 58(-42) m.y. (Bell et al. 2010).
Evolution. Ecology & Physiology. Net venation, animal-dispersed propagules, tolerance of shady habitats, and a preference for well drained and fertile substrates are linked in some members of this group (Givnish et al. 2005, 2010b).
Chemistry, Morphology, etc. Data on polysaccharide wall composition (mixed-linkage glucans) can be found in Smith and Harris (1999: Joinvilleaceae not included) and Popper and Fry (2004: detected in members of Poaceae and Flagellariaceae, but not in Restionaceae, Juncaceae, and Cyperaceae [the only other Poales examined], nor in any other vascular plants).
For the cross (= transverse) veins in the leaf, see Soreng and Davis (1998). For alternating long and short cells, see Stevenson in Michelangeli et al. (2003) and Briggs in Givnish et al. (2010b). In the interpretation of floral morphology of Ecdeiocoleaceae I follow Rudall et al. (2005a) and especially Whipple and Schmidt (2006); see also the discussion after Poaceae. For thickening of the endothecial cell walls, see Manning and Linder (1990); these are difficult to categorize in Joinvilleaceae and Ecdeicoleaceae.
FLAGELLARIACEAE Dumortier, nom. cons. Back to Poales
Stem apices dichotomise; flavonols +; endodermal cells radially elongated; culm solid; SiO2 associated with vascular bundles only; neighbouring cells of stomata with oblique divisions; prophylls lateral; leaves with terminal tendril, ?auricles, sheath also closed; bracteole 0; T members with single trace [?level], whitish, soft; microsporogenesis simultaneous; style solid; micropyle endostomal, outer integument ca 4 cells across, parietal tissue 1 cell across; embryo sac bisporic, chalazal dyad, eight-celled [Allium-type], antipodal cells numerous; fruit a drupe, seed coat adnate to pericarp; outer periclinal wall of exotesta persisting; n = 19; ORF 2280 present?; seedling coleoptile at most short.
1[list]/4. Palaeotropics, to the Pacific Islands (map: van Steenis & van Balgooy 1966; Heywood 1978). [Photo - Flower.]
Age. Estimates of the age of crown-group Flagellariaceae are (102.5-)95.3(-85.8) m.y. (Bouchenak-Khelladi et al. 2014b).
Evolution. Genes & Genomes. There is disagreement as to whether or not the ORF 2280 gene is present (c.f. Hahn et al. 1995 and Katayama & Ogihara 1996).
Chemistry, Morphology, etc. Flagellaria indica is reported to have a dichotomising stem apex, the vegetative leaves of aerial shoots lacking axillary buds (Tomlinson & Posluszny 1977), however, Kircher (1986) interprets the dichotomy as being a stem apex plus modified axillary branch; either way, the particular configuration here is an apomorphy.
Since the seed coat is adnate to the fruit wall, I suppose the fruit is a caryopsis.... Is the coleoptile part of the cotyledon, as in Poaceae (Takacs et al. 2012), or the first foliage leaf?
Some information is taken from Subramanyam and Narayana (1972) and Rudall and Linder (1988), both embryology, Tillich (1996b: seed and seedling), Appel and Bayer (1998: general), Tillich and Sill (1999: general), Sajo et al. (2007: style), and Sajo and Rudall (2012: floral morphology).
[Joinvilleaceae [Ecdeiocoleaceae + Poaceae]]: epidermis with microhairs; foliar epidermis with long + short cell alternation [latter SiO2-containing] throughout, SiO2 bodies cubic; guard cells dumb-bell shaped; fusoid cells [large colourless cells in central mesophyll] +; culm hollow [level?]; endothecial cells with girdle thickenings [?Poaceae]; stimatic receptive cells on multicellular branches; first seedling leaf lacking blade [possible]; 28 and 6.4 kb chloroplast genome inversion.
Age. This age of this node may be ca 90 m.y. (Janssen & Bremer 2004).
Evolution. Ecology & Physiology. For dumb-bell shaped stomata and greater control over opening, see Franks and Farquahar (2006) and Haworth et al. (2011) and references.
Genes & Genomes. For chloroplast genome inversions, see Doyle et al. (1992); the 6.4 kb inversion has been reported in Ecdeiocoleaceae (Michelangeli et al. 2002, 2003; Marchant & Briggs 2007). For a trnT inversion, see Morris and Duvall (2010).
Chemistry, Morphology, etc. The microhairs are multicellular in Joinvilleaceae and some Poaceae. Ecdeiocoleaceae, a small family of small herbs, has recently been placed in this clade (see below); if their seedlings have leaf blades, they may provide a valuable source of data on epidermal anatomy.
See Endress (1995b) for some details of floral morphology; for endothecial thickening, see Sajo and Rudall (2012).
JOINVILLEACEAE Tomlinson & A. C. Smith Back to Poales
Microhairs multicellular; leaf vernation plicate, auricles or ligules +; T green-brown, rather dry, outer T hooded; microsporogenesis ?simultaneous; pollen grains peripheral in loculus; carpels with lateral bundles; ovule parietal tissue?; fruit a drupe, 1-3-seeded, T persistent; endotegmen tanniniferous; n = 18; rps14 gene to nucleus, pseudogene remaining in mitochondrion; starch grains compound.
1[list]/2. Malay Peninsula to the Pacific (map: from van Steenis & van Balgooy 1966; Newell 1969). [Photo - Habit, Flower.]
Age. Crown-group Joinvilleaceae are estimated to be some (79.7-)76.7(-43.5) m.y.o. (Bouchenak-Khelladi et al. 2014b).
Evolution. Divergence & Distribution. Joinvilleaceae are reported as fossils from late Miocene New Zealand, although they do not grow there now (Lee et al. 2001).
Chemistry, Morphology, etc. The outer tepals may have only a single trace (Newell 1969), although Sajo and Rudall (2012) describe both whorls of tepals as being supplied by three vascular traces.
Some information is taken from Bayer and Appel (1998: general).
Joinvilleaceae are little known.
[Ecdeiocoleaceae + Poaceae]: plant monoecious; flowers monosymmetric by reduction, imperfect; pollen with operculum, wall without scrobiculi, with intraexinous channels; fruit an achene, 1-seeded.
Age. The age of this node is ca 89 m.y. (Janssen & Bremer 2004).
ECDEIOCOLEACEAE D. F. Cutler & Airy Shaw Back to Poales
SiO2 as sand; vessels?; stomata in grooves down culm; ?microhairs; epidermal long + short cell alternation 0, silica phytoliths 0; leaves reduced, sheath closed, auricles +; culm branched; inflorescence branch swellings?, with spikelet-like heads; flowers monosymmetric; 2 P ± conduplicate and keeled, 4 P flat; staminate flowers: (A 4); pollen with operculum; carpellate flowers: carpels with lateral bundles; ovule with area of enlarged cells near embryo sac; embryo sac tetrasporic, 16-celled [Drusa type]; (fruit loculicidal capsule); ?perisperm +; exotestal cells large; n = ca 24, 32, 33; seedling?
2[list]/3. S.W. Australia (map: from FloraBase 2004).
Age. Crown-group Ecdeiocoleaceae are dated to ca 73 m.y.a. (Janssen & Bremer 2004), or rather younger, (48.6-)36.7(-16.3) m.y.a. (Bouchenak-Khelladi et al. (2014b).
Chemistry, Morphology, etc. The illustration in Linder et al. (1988) shows leaves on the inflorescence axis with quite well developed blades. There is no evidence of differentiated long/short epidermal cells (B. G. Briggs, in Givnish et al. 2010b).
In Georgeantha the two adaxial calyx members are keeled, in Ecdeiocolea the differentiation is somewhat less pronounced. The flowers of Ecdeicolea are monosymmetric; the four stamens probably represent the three stamens of the outer whorl plus the adaxial stamen of the inner whorl (Rudall et al. 2005a). The exotesta is very differently thickened in the two genera, and the fruits are quite different. Details of ovule morphology, etc., are taken from Ecdeiocolea.
Some information is taken from Briggs and Johnson (1998), Linder et al. (1998), Rudall (1990: embryology), and especially Rudall et al. (2005a: floral development, fruits).
POACEAE Barnhart, nom. cons.//GRAMINEAE Jussieu, nom. cons. et nom. alt. Back to Poales
(Aerial branching + [?level]); vesicular-arbuscular mycorrhizae +; 3 desoxyanthocyanins, flavone 5- and C-glycosides, tricin, flavonoid sulphates, (cyanogenic glycosides) +; primary cell wall rich in arabinoxylans, pectin 10³%, xyloglucans lacking fucose; sieve tube plastids also with rod-shaped protein bodies, P-proteins 0; arm and fusoid cells +; short cell pairs, SiO2 bodies over veins; cuticle waxes as aggregated rodlets; stomatal subsidiary cells conical to dome-shaped; microhairs bicellular; leaf with petiole and blade, ligulate, (ligule ± fringed with hairs), vernation supervolute(-plicate), midrib +; T with two adaxial outer members distinct, abaxial smaller; A centrifixed [?level]; pollen grains central in loculus; gynoecium initially annular, (G open in development), stigmas 3[?]; ovule one/flower, central, amphitropous or hemianatropous, micropyle endostomal, funicle short; seed coat closely adherent to pericarp [= caryopsis]; testa not persistent, hilum long; peripheral layer of endosperm meristematic, endosperm hard, embryo lateral, long, well differentiated, cotyledon = scutellum + coleoptile, lateral, plumule terminal, embryonic leaf margins overlapping; radicle 0, collar [epiblast, the ligule of the cotyledon] conspicuous; expansion of the inverted repeat [level?], chloroplast genome with [third!] trnT inversion in the single-copy region, only 17 introns [that in clpP absent], loss of accD, ycf1, ycf2 genes, x = 12 [genome duplication; duplication of AP1/FUL genes (= FUL1 and FUL2), etc.], rpoC2 gene insert, rps14 gene to nucleus, pseudogene remaining in mitochondrion, intergenomic translocation of chloroplast rpl23 gene; ADP-glucose pyrophosphorylase in cytosol.
707/11,337. Twelve subfamilies below. Worldwide (map: from Vester 1940; Hultén 1961). [Genera List]
Age. Crown group Poaceae are ca 83 m.y.o. (Janssen & Bremer 2004; see also Bremer 2002). Bouchenak-Khelladi et al. (2009, 2010a) suggest that crown grasses are (97-)76(-43) m.y.o. and Bouchenak-Khelladi et al. (2014b) a little younger at (74.4-)68.9(-65) m.y.o.; Jones et al. (2014) estimated around (248.1-)137.3, 113.6(-62.7) m.y.a. - and also some very much older ages. See also below for estimates of the age of the genome duplication that characterises this clade.
However, Poinar (2004) proposed that Programinis burmitis, found fossil in deposits from the Early Cretaceous of Myanmar some 100-110 m.y.a., represented an early bambusoid grass. To others, it seemed to have some vegetative features that are common in Poaceae, but not the distinctive features of the family and so was unlikely to be included there (Smith et al. 2010). Nevertheless, in a recent more detailed analysis of P. laminatus, Poinar (2011) affirmed that the silica bodies, etc., indeed supported a placement in Poaceae, particularly in Poöideae, so suggesting an age for that subfamily about twice that of other estimates (see below). The age of these amber deposits have been revised downwards somewhat to no earlier than Early Cenomanian at (99.4-)98.8(-98.2) m.y. (Shi et al. 2012), but this age is still inconsistent with nearly all other estimates of the age of grasses.
The age of grasses (as well as that of other monocot groups, not to mention the animals, both vertebrates and insects, associated with them) is also called into question, although somewhat less dramatically, by the discovery of well-preserved phytoliths of types to be found in the PACMAD and BEP clades in coprolites of sauropod dinosaurs from the Late Cretaceous 67-65 m.y. of central India (Prasad et al. 2005). This would date the origination of the PACMAD-BEP clade to some 85-80 m.y.a.; such fossils have been identified as Ehrhartoideae-Oryzeae (Prasad et al. 2011). A recent critical analysis of some ages in Poaceae comparing those obtained using or not using these fossils and comparing chloroplast and nuclear data, etc. (Christin et al. 2014; see also Jones et al. 2014, dates stemming from these fossils not included here), underscores the importance of confirming the identity of these fossils. Indeed, the fossil pollen genus Graminidites occurs widely (but not in Australia) in the Late Cretaceous (Srivastava 2011), even if at least locally not in association with dinosaurs. Although the enigmatic Late Cretaceous mammalian sudamericid gondwanatherians had hypsodont teeth and there is a record of a Cretaceous hadrosaurian dinosaur with carbon isotope ratios that suggests that it might have been eating C4 plants (Prasad et al. 2005; Bocherens et al. 1994), the origin of C4 grasses - and most other C4 plants - is usually put in the middle of the Tertiary (see below). To summarize: Dates from different lines of evidence are apparently irreconcilably in conflict (Vicentini et al. 2008).
1. Anomochlooideae Potzdal
Microhairs 75-150 µm long [i.e., huge], basal cells constricted part way up; (short cell pairs 0 - Streptochaeta), (SiO2 bodies transverse-unlobed); (leaves spiral - Streptochaeta); pseudopetiole with an apical (and basal) pulvinus, midrib projecting on both surfaces, (ligule 0); inflorescence (branches two-ranked? - Anomochloa), cymose, two "bracts" along each branch unit, two more "bracts" below each flower; flowers perfect, protogynous; P 2 (3) + 3; or flowers spirally arrranged along racemose axis, with several spiral "bracts" below each flower, = T, possibly 3 + 3, the latter coriaceous; A (4 - Anomochloa, 3 members of the inner whorl), centrifixed, basally connate, not dangling, anthers ± latrorse, wall with 2 persistent middle layers [Reduced type], endothecium lacking thickenings; (microsporogenesis simultaneous - Streptochaeta); style solid, stigma not plumose; nucellar cap 4-5 cells across [Anomochloa]; (testa lignified, persistent - Anomochloa); embryo small [Anomochloa], (scutellar cleft +), (epiblast +), (embryonic leaf margins not overlapping); n = 11, 18; first seedling leaf lacking blade.
2/4. Central America to S.E. Brasil, scattered, forests (map: from Judziewicz et al. 1999).
Age. Divergence within Anomochlooideae is estimated to have occurred (86-)68(-53) m.y.a. (Bouchenak-Khelladi et al. 2010c) or (167.3-)77.8, 65.2(-14.4) m.y.a., or still older (Jones et al. 2014).
Synonymy: Anomochloaceae Nakai, Streptochaetaceae Nakai
[Pharoideae [Puelioideae [PACMAD + BEP clades]]] / the spikelet clade: inflorescence without inflorescence bracts, spikelets +, laterally compressed, racemose, pedunculate, with two basal glumes [sterile bracts = spikelet bract + prophyll], flowers two-ranked, plane of symmetry of flower relative to spikelet horizontal; flower protandrous, with lemma and palea [?= bract and 2 adaxial connate outer-whorl T], lodicules 3 [= C/inner whorl T; esp. in staminate flowers], median member adaxial; 1 bp deletion in the 3' end of the mat K gene, intron loss in rpoC1 gene, rp123 pseudogenization, 1700 bp deletion.
Age. The spikelet clade may have originated in the Late Cretaceous (95-)74(-73) m.y.a. or (83-)67(-55) m.y. (Bouchenak-Khelladi et al. 2009, also 2010a, c.f. 2010c) or (197.4-) 114.7, 95.2(-55.6) m.y. - or substantially yet older (Jones et al. 2014).
2. Pharoideae L. G. Clark & Judziewicz
Inner bundle sheath multi-layered; intercostal epidermis with files of fibres alternating with files of normal long cells, (short cell pairs 0 - Pharus); microhairs 0; leaves resupinate, lateral veins oblique; plants monoecious; inflorescence and spikelets with uncinate microhairs; spikelets 1-flowered; (lodicules 0; 2, minute); staminate flowers: A (4-)6, anthers basifixed, latrorse, wall with three layers [epidermis, endothecium, tapetum - Reduced type], endothecium lacking thickenings [both Pharus]; tapetal cells uni- to binucleate; carpellate flowers: ovule with micropylar beak, micropyle bistomal [Pharus]; (scutellar cleft +), epiblast +; coleoptile [= sheathing base of cotyledon] with blade.
4/13. Pantropical, in forests (map: from Judziewicz 1987; Judziewicz et al. 1999). [Photo - Flower.]
Synonymy: Pharaceae Herter
[Puelioideae [[PACMAD + BEP clades]] / the bistigmatic clade: SiO2 bodies saddle-shaped [transverse elongation]; spikelets several-flowered, disarticulating above the glumes; anthers versatile[?]; pollen grains peripheral in loculus; stigmas 2, two orders of stigmatic branching; 15bp ndhF insertion.
Age. The age of this node may be (76.8-)58(-57.6) m.y.a. or ca 65 m.y.a. (Bouchenak-Khelladi et al. 2010a, c.f. 2010c) or (107.1-)74.7, 61.8(-46) m.y., or yet older (Jones et al. 2014).
3. Puelioideae L. G. Clark, M. Kobay., S. Mathews, Spangler & E. A. Kellogg
Culm hollow; (minute bracts subtending inflorescence branches); spikelets with several flowers, basal flowers staminate or sterile, apical pistillate or perfect; ?lodicules; A 6, ?anther wall; (stigmas 3); embryo small, otherwise unknown; seedling leaf unknown.
2/11. Tropical Africa (map: from Emmet Judziewicz, pers. comm.).
[PACMAD + BEP clades] / Crown Grasses: fructan levels low, (benzoxazinoids, ergot alkaloids [latter synthesized by endophytes] +), lignins acylated with p-coumarates or acetate; SiO2 bodies often axially elongated; arm cells 0, fusoid cells 0; transverse veins 0; pseudopetiole 0; flower type?; C/lodicules 2; A 3, opposite K/outer whorl of T, pollen wall ?development; G 2, styles separate; antipodal cells proliferating; scutellar cleft +, epiblast +;, 15 bp insertion in ndhF gene, Helminthosporium carbonum [HC]-toxin reductase gene [Hm1 gene].
Age. Molecular evidence suggests that the [PACMAD + BEP] clade may have begun to diversify (53.8-)51.9(-49) m.y.a. (Wu & Ge 2011: 95% c.i.). Other estimates including Vicentini et al. (2008: (60-)52(-44) m.y.), Bouchenak-Khelladi et al. (2010c: (55-)52(-50) m.y.) are similar, some are a little older - Kim et al. (2009 [MAD members not included]), 67.8-50 m.y., Bouchenak-Khelladi et al. (2010a), (75-)57(-51) m.y., Naumann et al. (2013) about 47.7 or 32.3 m.y., and Z. Peng et al. (2013), 64.5-53.9 m.y., while Bell et al. (2010), at (42-)31, 28(-17) m.y., provide a rather younger age. Estimates in Jones et al. (2014) are within these limits, except for fossil-based estimates.
Fossil spikelets assignable to this clade are known from the Palaeocene-Eocene boundary, about 55 m.y. before present (Crepet & Feldman 1991).
[Aristidoideae [Panicoideae [[Arundinoideae + Micrairoideae] [Danthonioideae + Chloridoideae]]]] / PACMAD clade: C4 photosynthesis prevalent; (ligule of hairs); SiO2 bodies dumb-bell shaped; lemma awned; starch grains compound; mesocotyl internode elongated, epiblast 0, embryonic leaf margins meeting; extension of ndhF gene from the short single copy region into the inverted repeat.
Age. This node may be approximately 45-37 m.y. old, rather younger than the crown-group BEP clade (see Bouchenak-Khelladi et al. 2010a); Bouchenak-Khelladi et al. (2010c) suggest an age of only (34-)28(-22) m.y..
4. Aristidoideae Caro
(Plants annual); (spikelet cylindrical), with one flower; lemma awn trifid, with basal column, or 3 (1); callus pubescent; (scutellar cleft 0); n = 11, 12; germination flap +.
3/365: Aristida (250-290), Stipagrostis (50). Warm temperate, few in Europe.
Age. Stem Aristidoideae date from (38-)29(-9) m.y.a. (sister group?), crown Aristidoideae date from (25.5-)20.3(-15.9) m.y.a. (Bouchenak-Khelladi et al. 2010a; Cerros-Tlatilpa et al. 2011).
[Panicoideae [[Arundinoideae + Micrairoideae] [Danthonioideae + Chloridoideae]]]: 6 bp insertion in the 3' end of the mat K gene [?whole clade]
5. Panicoideae Link
(Plant annual), (forest dwelling); (culms branched); (fusoid cells +); microhairs often with slender, elongated thin-walled apical cells [panicoid type]; (mesophyll differentiated into palisade and spongy tissues), (chlorenchyma cells lobed [c.f. arm cells]); culms usually solid; (pseudopetiole +), (midrib complex); (inflorescence bracts +); spikelet 2-flowered, lower flower staminate or sterile [gynoecial cell death caused by Tasselseed2], development basipetal, rachilla 0; plane of symmetry of flower relative to spikelet vertical; ?lemma awned; (style +); (nucellar cap ca 4 cells across); (spikelet disarticulation below the glumes); hilum punctate; (epiblast 0), embryonic leaf margins overlapping; starch grains simple; 5 bp insertion in the rpl16 intron; n = (5, 7) 9 [Paniceae], 10 (11, 12, 14); (epiblast +), germination flap +; rps14 pseudogene lost.
212/3316: Paspalum (330), Cenchrus (105: inc. Pennisetum), Andropogon (100), Panicum (100), Dicanthelium (55), Eriachne (40). Tropics to temperate.
Synonymy: Andropogonaceae Martinov, Arundinellaceae Herter, Cenchraceae Link, Ophiuraceae Link, Panicaceae Berchtold & J. Presl, Paspalaceae Link, Saccharaceae Berchtold & J. Presl, Zeaceae A. Kerner
[[Arundinoideae + Micrairoideae] [Danthonioideae + Chloridoideae]]: ?
[Arundinoideae + Micrairoideae]: (hilum short).
6. Arundinoideae Burmeister
Microhairs with elongated, slender, thin-walled apical cells [panicoid type]; callus pubescent; (embryonic leaf margins overlapping); n = 6, 9, 12.
19/46. Temperate to tropical, hydrophytic to xerophytic.
Synonymy: Arundinaceae Döll
7. Micrairoideae Pilger
(Annual plants); culms solid or hollow; leaves (spirally arranged - Micraira); (lemma awn 0); starch grains simple, embryo small; n = 10; germination flap +; (C4 photosynthesis - Eriachneae).
9/188: Isachne (100), Eriachne (35). Tropics.
[Danthonioideae + Chloridoideae]: lemma bilobed, awned from the sinus; hilum punctate.
8. Danthonioideae Barker & Linder
(Plants annual), with C3 photosynthetic pathway; (stomata with parallel-sided subsidiary cells)); prophylls bilobed [?distribution]; lemma awn trifid, or 3 awns; lodicules with microhairs; bases of styles well apart; embryo sac with haustorial synergid cells; n = 6, 7, 9.
17/281: Danthonia (100), Rytidosperma (90). Widespread, esp. Southern Hemisphere, few Southeast Asia-Malesian.
9. Chloridoideae Beilschmied
Plants tolerate drought, high saline conditions; C4 PCK subtype (phosphoenolpyruvate carboxykinase) + (0); microhairs with ± hemispherical and thick-walled apical cells the same thickness as the long base cell, latter with internal membranes and secretory [chloridoid type], also panicoid type; embryo with an epiblast; 4 bp insertion in the rpl16 intron; n = (6-8) 9, 10.
130/1721: Eragrostis (300), Muhlenbergia (155), Sporobolus (160), Chloris (55). Tropical to warm temperate, more or less dry environments especially in Africa and Australia.
Synonymy: Chloridaceae Berchtold & J. Presl, Cynodontaceae Link, Eragrostidaceae Herter, Lepturaceae Herter, Pappophoraceae Herter, Spartinaceae Link, Sporobolaceae Herter, nom. inval., Zoysiaceae Link
[Ehrhartoideae [Bambusoideae + Poöideae]] / BEP clade: SiO2 bodies transverse- or axial bilobate; endosperm softness gene +, ?embryo short; x = 12.
Age. Bouchenak-Khelladi et al. (2009, 2010a, c) suggested that the BEP clade began to diversify at the end of the Palaeocene about 53 m.y.a., while Magallón et al. (2013) gave a much younger age of around 38.5 m.y.. Wu and Ge (2011) offer an age of (53.8-)51.9(-50) m.y., and Z. Peng et al (2013) an age of ca 48.6 m.y.; (16-)15, 12(-11) m.y. is the age in Wikström et al. (2001).
10. Ehrhartoideae Link
(Silica bodies elongated transverse to the long axis of the leaf); (arm cells + - Oryzeae), (fusoid cells +); (longitudinal walls of epidermal cell straight); (microhairs 0); (ligule a ring of hairs); flowers perfect or not; spikelet with two basal sterile florets, apical floret fertile; A (1-)6, style branches separate almost from the very base; n = (10, 15); (first seedling leaf lacking blade - Oryzeae), (roots at scutellar node - Ehrharta).
17/111: Oryza (20), Leersia (20). Widespread, esp. S. hemisphere.
Synonymy: Ehrhartaceae Link, Oryzaceae Berchtold & J. Presl
[Bambusoideae + Poöideae]: ?
Age. Wu and Ge (2011) suggested that this node was some (51.6-)47(-40.8) m.y. old, while in Z. Peng et al (2013) the age was ca 47.8-46.9 m.y..
11. Bambusoideae Luersson
Woody; culm branched, development often biphasic, lignification and branch development in 2nd phase; fusoid cells +, arm cells +, strongly asymmetrically invaginated; microhairs with elongated, slender, thin-walled cap cells [panicoid type]; (multiple buds per node); leaves pseudopetiolate, blade deciduous, articulated, culm leaves different from the others, largely sheaths, outer ligule +; flowering synchronized, plants monocarpic; (inflorescence bracts +); lodicules 3, vascularized; A (2-)6(-140), (basally connate), (endothecial cells with ± U-shaped thickenings); (stigmas 1-3); (ovules ategmic, unitegmic), (nucellar cap 6-8 cells across); (fruit a berry); first seedling leaf without blade; much polyploidy.
116/2123. Tropical to temperate, often in forests (map: see Judziewicz et al. 1999; Sungkaew et al. 2009).
Age. Crown-group Bambusoideae diversified some (48-)29(-26) m.y.a. in the middle Oligocene (Bouchenak-Khelladi et al. (2009, 2010a, c); Wu and Ge (2011) dated the separation of Phyllostachys and Bambusa to (35.6-)22.5(-9) m.y.a.; stem Olyreae were estimated to be 38.2--26.9 m.y.o. (Burke et al. 2014).
The actual age of this clade may be more towards the upper end of the molecular estimates, since the earliest fossils ascribed to the subfamily, the small-leaved Chusquea oxyphylla, are Eocene (Frenguelli & Parodi 1941; see also L. Wang et al. 2013).
11a. Arundinarieae Ascherson & Graebner
Culms hollow, branch development basipetal; midrib complex; n = 24.
26/533: Fargesia (60), Sasa (40-60), Phyllostachys (55), Arundinaria (50). More or less temperate E. U.S.A., eastern Asia, also Africa, scattered, ± montane.
11b. Bambuseae Dumortier
Rhizomes massive; branch development acropetal or bidirectional; midrib complex; n = (10), 20, (22), 23, 24, etc. [x = 10, 12]
84-101/1470. Chusquea (200), Bambusa (120), Merostachys (50), Schizostachyum (50). Tropical to (warm) temperate.
Synonymy: Bambusaceae Berchtold & J. Presl, Parianaceae Nakai
11c. Olyreae Martinov
± Herbaceous; culm development uniphasic, branching slight; epidermal silica cells usu. with cross-shaped silica bodies in the costal zone and crenate [olyroid] silica bodies in the intercostal zone [not Buergersiochloa]; blade not articulated, culm leaves not very different from the others, outer ligule 0; flowering rarely synchronized and monocarpic; plant monoecious; spikelets unisexual, dimorphic, one-flowered, often dorsiventrally compressed, rachilla extension 0; (lodicules 0); n = 7, 9, 10, 11, (12).
21/120 Pariana (35). Central and South America and Africa, also New Guinea (Buergersiochloa).
Synonymy: Olyraceae Berchtold & J. Presl
12. Poöideae Bentham
Temperate habitats, (plants annual); Epichloë endophytes pervasive; aerial branching at most rare; fructose oligosaccharides in stem; root epidermal cell division forming trichoblast/atrichoblast pair asymmetric; longitudinal walls of epidermal cells straight [?level]; culms hollow; lemma usually with 5 nerves, (awned); lodicules at most slightly vascularized; style branches separate almost from the very base; (postament +); (endosperm with some non-starch soluble storage polysaccharides); embryo small; n = (2, 4-13); duplication of the ß-amylase gene.
177/3850. Largely North Temperate.
12A. Brachyelytreae Ohwi
Stomata subsidiary cells with parallel sides; n = 11.
1/3. Eastern Asia, E. North America.
[Nardeae [Phaenospermateae + The Rest]]: primary inflorescence branches 2-ranked [primary branches from two orthostichies]; embryo lacking scutellar cleft, embryonic leaf margins non-overlapping.
12B. Nardeae Koch
Lodicules 0; style and stigma 1; n = 10, 13.
Synonymy: Nardaceae Martynov
[Phaenospermateae + The Rest]: microhairs 0 (+ - some Stipeae); (stomata subsidiary cells with parallel sides)
21 bp insertion in in rpl32-trnL; n = 7, 12.
7/11. Central to East Asia, also Australia, Mexico, Balkans, Caucasus; scattered.
12D. The Rest [some characters not quite at right level; more phylogenetic resolution needed]: fructan concentration often high; style solid [Triticum]; primary inflorescence branches usu. 2-ranked; n = 7, chromosomes "large" (Stipeae - <2.0 µm).
169/3833: Festuca (470: inc. Lolium), Poa (200), Stipa (<300), Calamagrostis (230), Agrostis (220), Elymus (150), Nassella (122), Bromus (100), Anthoxanthum (50). Largely North Temperate.
Synonymy: Aegilopaceae Martynov, Agrostidaceae Berchtold & J. Presl, Alopecuraceae Martynov, Anthoxanthaceae Link, Avenaceae Martynov, Bromaceae Berchtold & J. Presl, Chaeturaceae Link, Coeleanthaceae Pfeiffer, Cynosuraceae Link, Echinariaceae Link, Festucaceae Sprengel, Glyceriaceae Link, Holcaceae Link, Hordeaceae Berchtold & J. Presl, Laguraceae Link, Loliaceae Link, Melicaceae Martynov, Miliaceae Link, Phalaridaceae Link, Phleaceae Link, Sesleriaceae Döll, Stipaceae Berchtold & J. Presl, Triticaceae Link
Evolution. Divergence & Distribution. The family may have originated in Africa (Bouchenak-Khelladi et al. 2010c) or South America (Bremer 2002) - either way, on Gondwanan continents.
The Poaceae group of families has been described as being notably speciose (Magallón & Sanderson 2001), but there is considerable asymmetry in clade size within this larger clade. The great majority of species belong to Poaceae, which may be seven times more speciose than their animal-pollinated sister clade (Kay & Sargent 2009: surely a stunning underestimate?). Even within Poaceae there are three species-poor clades that are successively immediately sister below the PACMAD and BEP clades (to add to the two to three more such clades successively sister below the family). Thus any foci of diversification are likely to be found within the PACMAD and BEP clades (c.f. Linder & Rudall 2005; Smith et al. 2011; and especially Bouchenak-Khelladi et al. 2010c). However, diversification estimates depend on clade ages, and there are major problems here (Christin et al. 2014); until these ages stabilize, it is difficult to worry too much about diversification. Burleigh et al. (2006) suggest that by some measures Poaceae show a notable shift (increase) in complexity.
With the above caveats in mind, Hodkinson et al. (2008) discuss increases of diversification rates in Poaceae in the context of a supertree; there seems to have been one increase when true spikelets developed, at the Puelioideae node, etc. (see also Bouchenak-Khelladi et al. 2010c). The age of the PACMAD/BEP node is broadly in line with that of the age of a genome duplication in Poaceae estimated at 70-50 m.y.a. (Blanc & Wolfe 2004; Schlueter et al. 2004; Paterson et al. 2004; Kim et al. 2009). Schranz et al. (2012) thought that there was a lag time between this genome duplication and subsequent diversification increases, although the two might be linked; the evolution of the PACMAD and the BEP clades are associated with other shifts in diversification rates (Bouchenak-Khelladi et al. 2010c).
Pharus has a number of features in common with Anomochlooideae, perhaps because they are both plants of the forest floor (Sajo et al. 2007, 2012). Although it has numerous distinctive features, whether other members of the subfamily are similar is unknown, and Puelioideae are also very poorly known (see also Judziewicz & Clark 2008; Kellogg 2013).
Ecology and diversification has been examined at finer levels and in various groups. Thus the herbaceous habit and annual life cycle appear to be correlated with species richness (Salamin & Davies 2004; Smith & Donoghue 2008), however, the speciose Bambusoideae are woody. Poöideae are largely temperate; C4 photosynthesis (see below) has arisen many times in the PACMAD clade, and clades with C4 photosynthesis tend to be more speciose than their sister clades with C3 photosynthesis; Chloridoideae tolerate drought and saline conditions particularly well; and so it goes.
Much diversification in crown Aristidoideae is considerably younger than the (25.5-)20.3(-15.9) m.y. crown age (Bouchenak-Khelladi et al. 2010a; Cerros-Tlatilpa et al. 2011, q.v. for other estimates). Linder et al. (2013) discussed the distribution of the largely austral Danthonioideae; they thought that the main variables were the distance between suitable areas and their extent, but not wind direction, extent of water gaps, etc., while Linder et al. (2014) emphasized topographic activity/heterogeneity ad drivers of radiation. The very diverse Old World members of Arundinarieae are a mere 15 m.y.o.. and tropical Old and New World bamboos may have diverged 24.8-40.2 m.y.a. (Burke et al. 2012: c.f. other ages there). Within Poöideae-Stipeae, genomes from extinct clades persist in their hybrid descendents (Romaschenko et al. 2014). Inda et al. (2008a) discussed the biogeography of Loliinae, which seems to have involved multiple dispersal events from a centre in the Mediterranean region over the last ca 13 m.y.
Ecology & Physiology. For summaries of the ecology of grasses and grasslands, see Coupland (1993a, b), White et al. (2000) and Gibson (2009). The global extent of contemporary grassland, including savanna with its C4 grasses, is 52.5x106 km2, or somewhere between 41-56x106 km2, that is, 31-43% of the total land surface area (Gibson 2009: excluding Greenland and Antarctica). Other estimates are lower, ca 20% of the earth's surface (Hall et al. 2000; Sabelli & Larkins 2009), the figures depending in part on the definitions of grassland, savanna and forest. Grasses in the Great Plains alone cover slightly over 3x106 km2, the Campos Cerrado ca 2x106 km2 - see also the map, where rather virulent green = more or less pure grassland, and olive green = communities with trees and shrubs as well as substantial grass (map: from endpapers in Coupland 1993a, b; esp. White et al. 2000, Map 1, for more details; see also Clade Asymmetries).
Grasses and C4 photosynthesis.
Although there have been suggestions that C4 photosynthesis persisted through the Mesozoic (Keeley & Rundel 2003 for literature), its appearance in clades of extant angiosperms is a Tertiary phenomenon. Only some 7,500 species of flowering plants have the C4 photosynthetic syndrome, and of these about 4,500 are grasses, where they make up about three quarters of the almost 5,900 species of the PACMAD clade (Sage et al. 1999, 2012; Grass Phylogeny Working Group II 2011). For a summary of C4 photosynthesis, see Sage et al. (2012) and Kellogg (2013).
Within grasses, there has been massive parallelism in the acquisition of C4 photosynthesis, with some 22-24 separate origins of this feature in the PACMAD clade (e.g. Kellogg 2000; Roalson 2011: 12-19 transitions; Christin et al. 2008a, 2009 b; Vicentini et al. 2008; Cerros-Tlatilpa & Columbus 2009 and Christin & Besnard 2009 [both Aristidoideae]; Grass Phylogeny Working Group II 2011; Sage et al. 2011, 2012; Morrone et al. 2012). Interestingly, both origins of and reversals from C4 photosynthesis may be clustered, although reversals are not very common (Vicentini et al. 2008; for reversals, see also Ibrahim et al. 2009). The relatively uncommon C4 PCK subtype (phosphoenolpyruvate carboxykinase) may be basal in Chloridoideae, being subsequently lost and reacquired (Christin et al. 2009b; Christin et al. 2010a: reversals; Ingram et al. 2011b: a reversal that wasn't). A few intermediates in which there is C2 photosynthesis are known from the family (Monson & Rawsthorne 2000; Bauwe 2011 for references).
The adoption of C4 photosynthesis is associated with well-known anatomical changes, such as closer spacing of the veins, the development of a sheath of chloroplast-rich cells around the vascular bundles, etc., i.e., the Kranz anatomical syndrome, although the control of this is still poorly understood (Kellogg 2013; see Pengelly et al. 2011 for vein spacing; Sack & Scoffoni 2013 for literature suggesting that this potentiated the repeated evolution of C4 grasses). The mechanisms of C4 photosynthesis and the anatomies associated with it are particularly variable in Panicoideae where C4 photosynthesis may have evolved up to eight times alone (Kellogg 2000; Giussani et al. 2001; Christin et al. 2007a, 2009a). Although anatomy has been used to characterize subtypes of C4 photosynthesis, the correlation of anatomy and photosynthetic pathway may not be that good (Ingram 2010), and the typology needs to be revisited (E. A. Kellogg, pers. comm.).
S. H. Taylor et al. (2010) and Ripley et al. (2010) compared the ecophysiology of C3 and C4 grasses, the latter sometimes being more sensitive to drought and recovering more slowly from it. When stomata close in plants with C4 photosynthesis transpiration losses are reduced, so mitigating the effect of higher temperatures and water stress, however, carbon fixation is not necessarily reduced and damaging photorespiration is avoided, so mitigating the negative effects of the decrease in CO2 concentration (Morgan et al. 2011; Sage et al. 2012). Interestingly, taxa like Miscanthus x giganteus carry out C4 photosynthesis under decidedly cooler conditions than is common (Wang et al. 2008), while the C3 Lolium perenne can also tolerate water stress (Holloway-Phillips & Brodribb 2010, see below).
Christin et al. (2013) have suggested particular anatomical changes that facilitated the transition to C4 photosynthesis in grasses. They suggest that veins - or at least bundle sheaths - became closer in the common ancestor of the PACMAD + BEP clade - and a high proportion of vascular bundle sheath tissue facilitated this transition (for venation densities, ca 5.1 vs 10.6 mm mm-2 in C3 vs C4 plants, see Ueno et al. 2006). C4 photosynthesis did not develop in the BEP clade, because the outer bundle sheath cells subsequently became smaller, but it did in the PACMAD clade because they became larger (although they were sometimes lost there, but then the inner sheath cells became dramatically larger). Finally, mesophyll cells were sometimes lost in the PACMAD clade (Christin et al. 2013). In a less elaborate analysis, Griffiths et al. (2012) suggested that bundle sheath proliferation had begun before any change in vein densities.
The numerous acquisitions of C4 photosynthesis within the PACMAD clade may reflect an underlying change that faciltated subsequent "independent" acquisitions of the pathway (Grass Phylogeny Working Group II 2011: gene duplication not involved; Williams et al. 2012; see Marazzi et al. 2012). Parallelisms may even be at the level of particular amino acids being substituted, similar changes occurring independently in the phosphoenolpyruvate carboxylase gene in grasses (Christin et al. 2007a, esp. b, 2009a). Indeed, a mutation to serine at position 780 seems to have occurred in all plants with C4 photosynthesis (Bläsing et al. 2000; see also Brown et al. 2011 for C4 parallelisms between grasses and Capparidaceae; Grass Phylogeny Working Group II 2011), and functionally important parallelisms are also found in rbcL (Christin et al. 2008b). John et al. (2014) also discuss extensive parallelism in C4 grasses.
Lateral transfer of genes may also have been involved in putting together C4 pathways. The sequential transfer of genes over a period of millions of years from quite unrelated grasses, perhaps via movement of genes from pollen of a grass that lands on the stigma of a plant that it cannot pollinate, may explain the nature of the C4 pathway in Allopteropsis (Panicoideae). No other genes seem to be involved, and a taxon embedded in the clade has ordinary C3 photosynthesis (Christin et al. 2012). This is difficult to get one's head around...
Grasslands, Fire and Forests.
This discussion applies both to C4 grasses and to the more cold tolerant grasses, most of which are C3; the evolution of cold tolerance per se is discussed later.
Understanding the ecological relationship between grasslands and woodlands over time is important since the two differ greatly in associated flora and fauna and in their effects on the biosphere. Poaceae may initially have been forest dwellers (e.g. Bouchenak-Khelladi et al. 2010a, c: Puelioideae not included; Givnish et al. 2010b), and although most Bambusoideae are woody (3 m or more tall) and forest dwellers, these are derived features. Most or all of the species-poor largely forest-dwelling basal clades had diverged by the end of the Cretaceous; diversification of the PACMAD/BEP clade, largely consisting of plants growing in more open habitats, is probably entirely Tertiary in age. Jones et al. (2014) suggest that forest-dwelling grasses had been around for about 50 m.y., moving into more open habitats as forest retreated with increased temperatures and dryness 56.5-53 m.y.a., the Palaeocene-Eocene thermal maximum (PETM).
The factors that favoured the initial development of grasslands, caused the clustering of origins and losses of different photosynthetic mechanisms, and were involved in the great spread and expansion to dominance of late Miocene C4 grasslands, remain unclear (see also Tipple & Pagani 2007; Jacobs et al. 1999; Sage & Kubien 2003; Fox & Koch 2004; Osborne & Beerling 2006; Bond 2008; Westhoff & Gowick 2010) and will be still less clear if some of the older clade ages are confirmed (Christin et al. 2014). Some combination of temperature, low atmospheric CO2 concentration, fire and water stress is now emphasized (e.g. Bond et al. 2003; Edwards & Still 2008; Vincentini et al. 2008; Edwards 2009; Strömberg & McInerney 2011; Christin et al. 2011b; Kellogg 2013; Forrestel et al. 2014). There was a decline - perhaps quite rapid - in atmospheric CO2 concentration ca 30 m.y.a. in the Oligocene (Pagani et al. 2005; Zachos et al. 2008; Gerhart and Ward 2010; Arakaki et al. 2011) perhaps caused by the activities of ectomycorrhizal plants (L. L. Taylor et al. 2009; see above). Temperatures in the late Miocene were also decreasing (Arakaki et al. 2011). Indeed, grasslands may be very sensitive to changing climates. For instance, in some reconstructions of the effect of the current increase in CO2 in the atmosphere, the spread of C3 grasslands is quite extensive (e.g. Collatz et al. 1998; Hall et al. 2000; Knapp & Smith 2001). Of course, the initial move of grasses from woodlands to open habitats and their subsequent and much more recent rise to dominance may have quite different precipitating causes.
C4 grasses, grasslands and savanna may be favoured in environments with some combination of high temperatures and low CO2 concentrations. Declining CO2 concentrations may have made trees less competitive (Pagani et al. 2009). Many C4 origins seem to be correlated with a reduction in annual rainfall, and grasslands transpire less than the woodlands they may have replaced (Retallack 2001). The dense - and sometimes remarkably deep - root masses of grasses also make the establishment of woody vegetation in grassland difficult (D'Antonio & Vitousek 1992); the seedling/young plant stage is critical here (Bond & Midgley 2000). Grassland soils are notably moister than corresponding woodland soils, with increased weathering, yet somewhat paradoxically grasslands support a drier climate, transpiration being relatively low. Woodlands have a higher albedo and transpire more, so their soil is drier (Retallack 2001, 2013). Increasing temperature, open habitats, and perhaps especially decreasing precipitation would all increase water stress, although by no means all C4 grasses are drought tolerant (e.g. Edwards & Still 2007, esp. 2008; Edwards et al. 2007; Edwards 2009). In a comparative study, Pinto et al. (2014) found that C4 grasses used nitrogen and water more efficiently that C3 or C3-C4 intermediates in low (glacial) CO2 concentrations. However, in North America, at least, McInerney et al. (2011) suggest that the late Neogene expansion of C4 grasses was at the expense of C3 grasses rather than of woody vegetation, while with decreasing temperatures survival of tree seedlings in the forest-grassland transition is increased (Will et al. 2013).
The amount and persistence of litter in grasslands may be an important factor in their success. Grasslands accumulate litter very easily, and there is a negative correlation between silicon concentration - especially high in annual grasses - and rate of leaf decomposition (Cook & Leishman 2011b). The relatively low nitrogen content in grass litter, especially the litter of C4 grasses, also means that it decomposes slowly and accumulates (Knapp & Seastedt 1986; Wedin 1995; Pérez-Harguindeguy et al. 2000: Bromeliaceae could be similar!; Cornelissen et al. 2001; decomposition fast; Chapin & Körner 1995, but comparison with mosses). Leaves of poöid monocots in general, presumably including sedges, decompose more slowly than do those of other angiosperms (Cornwell et al. 2008).
Thus grasslands are particularly flammable because of litter accumulation (Scheiter et al. 2012; Sage et al. 2012); certainly, charcoal from fires has become abundant since the Late Miocene about 10 m.y.a. (Bond & Scott 2010). The high flammability of dry grasses, disturbance by grazers, and windiness are among the factors, many related, that would lead to the increase of fires and further spread of grasslands (Retallack 2001; Woodward et al. 2004; Bond & Scott 2010). Scheiter et al. (2012) see an interaction between increased temperatures, favouring C4 grasses, relatively low atmospheric CO2, favouring the invasion of C3 grassland by C4 grasses, and fire, allowing the expansion of grassland and also the development of savanna, with its shade intolerant and fire-resistant trees and abundant C4 Andropogoneae (see also Lehmann et al. 2011; Forrestel et al. 2014). Since grasses have their perennating parts underground, they are not harmed by fire, while burning suppresses woodland by kiling fire-susceptible trees; nitrogen is also volatilized and lost (e.g. Knapp & Seastedt 1986). Both would favour grasses: The habitat was opened, and C4 grasses in particular have a reduced requirement for photosynthetic enzymes and so a lower nitrogen requirement (Wedin 1995; Forrestel et al. 2014). Although panicoid grasses recover well after fires, C4 grasses do not always perform better in this respect than C3 grasses (Ripley et al. 2011; Forrestel et al. 2014). Bond et al. (2005) estimated that if there were no fires, about 52% of C4 grassland and 41% of C3 grassland would revert to forest; of the latter, over half would be dominated by gymnosperms. Indeed, the productivity of tall-grass prairies is negatively affected by the accumulation of litter, so fires benefit them here (Knapp & Seastedt 1986). A further wrinkle is that fires may have increased over the last 50,000 years because of the widespread extinction of megaherbivores by humans and/or climate (Lorenzen et al. 2011; Gill 2013), However, Forrestel et al. (2014) specifically noted that the reponse of Andropogoneae to fire was overall independent of whether or not there was grazing, although that might not be true for individual species. The diversity of grasses in any one place is also affected by the particular fire regime, although not in any simple way (Forrestel et al. 2014).
Some vegetation simulations show circum-Arctic grasslands early in the Tertiary (Shellito & Sloan 2006), although this is unlikely. Palaeosol and other evidence suggests that grassland grasses began diversifying in the Eocene (e.g. Bouchenak-Khelladi & Hodkinson 2011), and the grasses involved are mostly caespitose bunch grasses (Retallack 2013). Most open habitat grasses, probably C3, appear in the Middle Eocene ca 42 m.y.a., and may have become locally dominant (Strömberg 2011); they diversified taxonomically in North America in the early Oligocene ca 34 m.y.a. (Strömberg 2005). Evidence from palaeosols suggest that there may have been grasslands in the Great Plains in the late Oligocene ca 24 m.y.a., although some Argentinian grasslands may be older, Eocene in age (Retallack 1997b; Edwards et al. 2010). From the examination of phytolith assemblages, grass-dominated open habitats in Patagonia did not develop before ca 18.5 m.y.a., and it was open-habitat C3 poöid grasses that were dominant then (Strömberg et al. 2011).
C4 grasses may have originated in the Oligocene ca 33 m.y.a., and C4 photosynthesis is known from grasses from the Early to Middle Miocene in both the Great Plains and Africa, some 25-12.5 m.y.a. (e.g. Ehleringer 1997 and references; Christin et al. 2008a, 2011b). However, such grasses made a major contribution to overall vegetation biomass - only in the late Miocene 9-8 m.y.a., the process being complete as recently as the late Pliocene 3-2 m.y.a. (Bouchenak-Khelladi et al. 2009, 2014a; Edwards et al. 2010; Strömberg & McInerney 2011; McInerney et al. 2011 for North America; Strömberg et al. 2011: South America; Arakaki et al. 2011; Sage et al. 2012). Thus there is a pronounced lag at both global and local scales between the initial evolution and diversification of grasses that carry out C4 photosynthesis and their ecological expansion (e.g. Strömberg & McInerney 2011) - a lag of over 20 m.y.. The extensive Brazilian Cerrado, savanna vegetation with flammable C4 grasses and plants, a number woody, that have become adapted to a fire regime, developed only within the last (10-)5 m.y. (Pennington et al. 2006b; Simon et al. 2009; Simon & Pennington 2012). Indeed, the Neogene has been called the age of grasses (c.f. Palaeos).
Grasslands affect the biosphere because the total C sequestration grasslands is greater than that of the forests they in many cases they seem to have replaced, with a shift in the sequestration pattern from above-ground parts to the soil (McGuire et al. 1992; Retallack 2001). Some Oligocene palaeosols approach mollisols, a soil type known only from the Tertiary and uniquely associated with grasslands (Retallack 1997b). Short sod grassland (the grasses are mostly rhizomatous) with shallow soils may have appeared in the early Miocene ca 20 m.y.a. in relatively warmer and wetter (400< mm/yconditions (Retallack 2001, 2013). Tall sod grasslands made up mostly of C4 grasses and with deeper soils appeared in the late Miocene ca 7-5 m.y.a. in areas with up to 750 mm annual precipitation, and it was these grasslands that had true mollisols. In their fullest development, mollisols are dark and deep (the carbon-rich layer may be 1 m or so); carbon is mixed with rounded clods of clay 2-3 mm across, they are nutrient-rich, with carbonate and easily-weathered minerals, and are densely permeated by grass roots (Retallack 1997b). Grassland soils, being relatively moist (see above), will support increased rock weathering (Retallack 2001, 2013)
To conclude. The relationships between C3 and C4 grasses, temperature, trees, moisture, atmospheric CO2 concentration and fire are complex and dynamic. Grasslands and savanna currently cover about 40% of the land surface of the globe, about half that area being within the tropics (Gibson 2009 for references). The global distribution of C4 vegetation, which of course includes more than just grasslands, has been estimated at ca 18.8 x 106 km2, somewhat over 15% of the total (Still et al. 2003). All told C4 photosynthesis accounts for about 23-28% of terrestrial gross primary productivity, although the biomass of C4 plants is only ca 5% of the global total (Still et al. 2003: GPP = 35.3 vs 114.7 Pg C yr-1, simulated biomass, leaf, wood, root = 18.6 vs 389.3 Pg C; Ito & Oikawa 2004; see also Lloyd & Farquhar 1994; Ehleringer et al. 1997; Retallack 2001). Another estimate suggests that grasslands in general - both C3 and C4 species - currently account for 11-19% of net primary productivity on land (Hall et al. 2000). Estimates of the proportion of below-ground biomass in grasslands is as high as 80-95% (Dormaar 1992) accounting for 10-30% of global soil carbon storage (Hall et al. 2000); Gibson (2009) estimated as much as ca 33% total C storage - 650-810 Gt, broadly in line with the estimates in Retallack (2013). Overall, grasslands can be considered a long-term carbon and water sink, and one of the consequences of their activities is long-term global cooling (Retallack 2001, 2013).
What makes grasslands and savannas still more distinctive ecologically is not just the abundance of grasses and their distinctive growth habit, but that relatively few species of grasses are ecologically dominant in any one place, and most of these seem to be C4 grasses; of the some 11,300 species of grasses, only some 600 species dominate ecologically in grasslands and savanna, and most of these are C4 photosynthesizers of the PACMAD clade (Edwards et al. 2010). Andropogoneae are notable here in their positive response to annual burning (Forrestel et al. 2014 and references). Finally, although C4 grasses in particular may have first appeared in the Oligocene ca 33 m.y.a. and began to diversify soon after, they made a major contribution to overall vegetation biomass only in the late Miocene 9-8 m.y. ago. It was then that grasslands began to spread rapidly, the process being complete as recently as the late Pliocene 3-2 m.y.a. (e.g. Bouchenak-Khelladi et al. 2009, 2014a; Edwards et al. 2010; Strömberg & McInerney 2011; McInerney et al. 2011; Strömberg et al. 2011; Arakaki et al. 2011; Sage et al. 2012).
Grasses, Grasslands, Herbivory and the Silicon Cycle.
There are also suggestions that C4 grasses in particular, grasslands in general, and grazing are connected (e.g. Retallack 2013). Thus Bouchenak-Khelladi and Hodkinson (2011) thought that there were "adaptive coevolutionary processes" (unspecified) going on between grass and grazer. C4 plants tend to be less attractive to herbivorous animals because of their lower nitrogen concentration and greater amount of fibrous tissue - they have more sclerenchyma because their veins are closer (Caswell et al. 1973; Schoonhoven et al. 2005 for references: Taylor et al. 2010 suggested that the N content of C3 and C4 grasses was similar). The persistent dead leaves of most grasses may also decrease their palatability to grazers (Antonelli et al. 2010). Be this as it may, diversification of grazers began in the Oligocene ca 35 m.y.a. and there was a Miocene radiation of grazing mammals (Thomasson & Voorhies 1990; MacFadden 1997; Retallack 2001; Keeley & Rundel 2003) that has been linked to the spread of prairie and savanna grasses (see also Cerling et al. 1997; Bouchenak-Khelladi et al. 2009, 2010a: considerable detail and many dates; Mihlbachler et al. 2011). Most extant grazers eat C4 plants, but C3 grazers, now uncommon, were found in a diversity of ecosystems before 7 m.y.a. (MacFadden 1997). Grazing mammals evolved hypsodont or hypselodont dentition, the former teeth with high crowns, enamel extending below the gum lines, and short roots, and the latter, ever-growing teeth, both apparently to deal with the wear caused by eating the abrasive grasses with their complex silica bodies (phytoliths).
However, tooth enamel seems to be harder than the silica encountered in grasses (Sanson et al. 2007), although surprisingly little is known about the mechanics of tooth action (Sanson 2006). It is probably dust particles, likely to be more numerous in food eaten by a grazer than by a browser, that are the most abrasive element in the food ingested (e.g. Kay and Covert 1983). Bouchenak-Khelladi et al. (2009) noted that the density of silica bodies in the leaf epidermis seems to have increased in a number of grass groups, perhaps as a defence against herbivory, however, Sanson and Heraud (2010) suggested that the silica there might not be in crystalline form and so would not cause wear on the enamel of mammalian teeth. But silica bodies do affect the feeding behaviour of at least some smaller herbivores, both mammals and insects, even if they are not the immediate "cause" of hypsodonty in mammalian teeth (for rabbits, see Cotterill et al. 2007). Higher silica in grasses decreases the amount of nitrogen taken up by both armyworm (Spodoptera exempta) larvae and voles (Microtus), and in the former in particular there are long-term negative effects on the growth of the caterpillar, perhaps via damage to the larval midgut. Moreover, chitin is not as hard as enamel, and the mandibles of armyworm larvae are worn down by silica; grass tissues produced after attack by a herbivore (but not after comparable purely mechanical damage) have an increased silica concentration and are less attractive to the animals (see Schoonhoven et al. 2005; Massey & Hartley 2006, 2009; Massey et al. 2007b; Katz et al. 2014 for literature).
The relationship between silica, herbivory, and the mechanical protection of plant tissues is clearly not straightforward. Although prairie grasses expanded in Nebraska in the Early Miocene ca 23 m.y.a., hypsodont ungulates were already around by then (Strömberg 2004, 2006; Mihlbacher et al. 2011). Massive diversification of North American ungulates is largely a Miocene phenomenon, Bovidae and Cervidae starting to diversify by at least 26 m.y.a. (Bouchenak-Khelladi et al. 2009), and herbivores that are now specialists on C4 grasses seem to have evolved before those grasses came to dominate ecosystems (Edwards et al. 2010). Grazers in South America appeared earlier than in North America, ca 50 m.y.a., and were "pervasive" there by the Oligocene ca 35 m.y.a. (MacFadden 1997, esp. p. 185), probably eating C3 plants. Establishing connections between the evolution and rise to dominance of grasses in some ecosystems and the evolution of grazing animals and of hypsodonty needs more work; it is likely that the two are linked, but not at such a simplistic level as high SiO2 = hypsodonty (see also Retallack 2001 for a summary); similarly, Bouchenak-Khelladi and Hodkinson (2011) noted that hypsodonty has been gradually increasing for 20 m.y., but there is no documentation of the comparable spread of grasslands.
Of course, silica is not the only defence that grasses have (Massey et al. 2007a), for instance, they vary in toughness (C4 grasses are notably tough) and may contain noxious metabolites, sometimes because of their association with endophytes (see above). In some grasses defence against herbivores is mediated by the production of volatile mono- and sesquiterpenes which can, for example, attract nematodes (to attack Diabrotica - the chrysomelid corn root-worm - larvae) or parasitic wasps (to attack caterpillars) (Degenhardt 2009).
There is a further ecological dimension of silica and grazing. Silica becomes mobilized during digestion, particularly in ruminants because grasses stay in their guts for a long time, and hence there is a massive mobilization of silica in grazed grasslands. The spread of grasses in the Miocene and the increased activity of herbivores may have increased the flux of silica into fresh waters, so sparking the Early Miocene increase of diatomite (diatomaceous earth, kieselguhr) deposits and diamtom diversity in fresh waters; the cell walls (frustules) of diatoms are made up of silica (Kidder & Gierlowski-Kordesch 2005; Vandevenne et al. 2013). Whether diatom growth in the sea was actually stimulated is unclear, certainly, marine diatom diversity peaked at the Eocene/Oligocene boundary well before the spread of grasslands (Rabosky, D. L., & Sorhannus 2009), after that period the calcite compensation depth (the depth below which calcite dissolves) considerably increased, with calcium carbonate nanofossil ooze replacing siliceous radiolarian ooze (Coxall et al. 2005; Tripati et al. 2005) in connection with the developing ice caps.
There are other aspects of the eco-physiology of Poaceae to take into account.
1. Hydraulic Conductance. Woody bamboos, some 1,300 species, can grow to 30 m tall or more, and may live for 100 years before flowering; palms and bamboos are the two major woody monocot clades. Given that there is no secondary thickening in bamboos, how the vascular tissue of these plants remained functional was unclear. However, Cao et al. (2012 and references) found that in the bamboos they studied root pressure was sufficient to drive water up the entire height of the plant; root pressure and plant height were strongly correlated. This would help in the repair of embolisms in the xylem.
In the poöid Lolium perenne, leaf hydraulic conductance may decrease during the day, with cavitation presumably occuring, yet photosynthetic rates may stay high, the stomata remaining open. The plant was able to recover from quite extreme daytime hydraulic dysfunction, although here root pressure seemed not to be involved (Holloway-Phillips & Brodribb 2010). It will be interesting to see how widespead such behaviour is in the family.
2. Cold Tolerance. The ecological success of Poaceae is not just because some adopted C4 photosynthesis. Cooler temperate grasslands in the northern hemisphere are dominated by Poöideae, all of which are C3 grasses. Thus although about 16% of all species growing in Quebec and Labrador north of 54o N are Cyperaceae, Poaceae, all members of Poöideae, are next at 11% (Escudero et al. 2012). Poöideae have a complex relationship between freezing tolerance, day length, vernalization, and flowering (e.g. Edwards 2009; Edwards & Smith 2010; Dhillon et al. 2010). Core Poöideae evolution may be linked with the cooling at the beginning of the Oligocene ca 33-27 m.y.a. (Strömberg 2005; Sandve et al. 2008; c.f. Christin et al. 2014), gene families implicated in low temperature-induced stress response expanding prior to Poöideae diversification (Sandve & Fjellheim 2010); the genes seem to have been under positive selection (Vigeland et al. 2013: clades downstream from Brachypodium not examined). Proteins that inhibit ice recrystallization are known from the group (Sidebottom et al. 2000; Tremblay et al. 2005; Sandve et al. 2010). Furthermore, low levels of fructan - specifically levans - accumulation have been noted in many Poaceae, but notably high levels are found only in Poöideae, although not in taxa of the "basal" pectinations like Nardus, Stipa and Phalaridinae (Smouter & Simpson 1989; Hendry 1993; Pollard & Cairns 1991). Fructans may enable Poöideae that accumulate them to survive drought or frost better, and they have been implicated in stabilizing cell membranes at low temperatures (Livingston et al. 2009; Sandve & Fjellheim 2010). The establishment of vernalization requirements may have contributed to the diversification of Poöideae (Preston & Kellogg 2008), although how widely they occur outside the subfamily is unclear. Finally, the development of the Epichloë/Poöideae relationship may have been involved in the spread of Poöideae from shady to sunny open habitats in the predominantly cool-season climates that they favor (Kellogg 2001), the mutualism aiding the plant's defences against herbivores and drought (Schardl et al. 2008; Schardl 2010).
Other grasses also tolerate cooler condition, including the more northerly temperate bamboos (Bambusoideae: Arundinarieae) and the austral Danthonioideae. In the latter, evolution of cold tolerance is estimated to have begun ca 25 m.y.a. during the late Oligocene in Africa (Humphreys & Linder 2013; see also Linder et al. 2013). The two species of Danthonioideae studied (Chionochloa) seemed to tolerate cold conditions by controlling ice nucleation (Wharton et al. 2010).
3. Stomatal Opening. The dumb-bell shaped stomata of grasses show remarkably rapid stomatal movements, very much faster than those few other stomata have been examined (Franks & Farquhar 2006; Haworth et al. 2011). However, since the stomata of quite a number of other Poales are similar, it is unclear if they are a major component of the ability of grasses to spread as climates became drier at the end of the Eocene (Hetherington & Woodward 2003).
4. Roots. Much goes on in grass roots. Prominent rhizosheaths - mucilage from root cap cells, soil particles, bacteria, etc., all anchored to root hairs - occur in many Poaceae (McCulley 1995), especially those growing in drier conditions, although the distribution of such roots is poorly known. They are found in other Poales, but are apparently rare in broad-leaved angiosperms. Interestingly, C4 grasses have roots with long root hairs yet may respond positively in terms of phosphorus uptake when forming endomycorrhizal associations - long root hairs and endomycorrhizal associations tend to be thought of as alternative ways of securing phosphorus supply, etc. (Schweiger et al. 1995 and references). Some crops, including maize and wheat, show a substantial uptake of nitrogen from bacteria that are either in the rhizosphere are are endophytic (Santi et al. 2013). Finally, Poaceae, apparently alone in flowering plants (Römheld 1987), acquire iron through chelation of ferric ions with non-protein amino acid siderophores which are then taken up by the roots; iron (and zinc) are commonly limiting trace elements in alkaline soils (Schmidt 2003; Kraemer et al. 2006). Interestingly, ectomycorrhizal plants, also noted for dominating the communities in which they occur, also produce siderophores.
5. Allelopathic Reactions. Some Poaceae show allelopathic reactions with other plants, Sorghum roots producing an allelopathic quinone (an oxygen-substituted aromatic compound) and Festuca roots meta-tyrosine, a non-protein amino acid (Bertin et al. 2007). Benzoxazinoids, cyclic hydroxamic acids, are largely restricted to Poaceae, and are found in both Panicoideae and Poöideae. They confer resistance to fungi, insects (volatilized, they attract wasps parasitizing herbivorous insects), and even herbicides, and are also allelopathic, but less so to other grasses than other plants (Frey et al. 1997, 2009; Gierl & Frey 2001; Sicker et al. 2000: ecological role; Dick et al. 2012; Schullehner et al. 2008: non-grasses).
6. Salt Tolerance. Poaceae such as Spartina and Puccinellia are major elements of salt marshes. The C4 Spartina (Chloridoideae) is a particularly prominent component of temperate salt marshes where it dominates large areas; there has been past hybridisation in the genus, and hybridization also occurs between introduced and native species, some of the products (like S. anglica) being very invasive (Srong & Ayres 2013). Salt tolerance in grasses is quite widespread, and two thirds of the species are also C4 plants (Flowers & Colmer 2008). Some 200+ species are involved, and weak salt tolerance - tolerance of salinity up to ca 80mM NaCl - has evolved some 76 times (Bennett et al. 2013). Euhalophytes, tolerating at least 200mM NaCl, about half the salinity of sea water, have evolved some 43 times, and in both cases the clades involved are young and small; A number of grasses in different subfamilies accumulate glycine betaines and other compounds commonly associated with allowing plants to grow in saline conditions (Rhodes & Hanson 1993). Bambuseae (sic) and Danthonioideae are notable for lacking even weak halophytes (Bennett et al. 2013).
7. Bamboos and Dominance. Woody bamboos tend to colonize forest gaps and edges and can dominate in the canopy and understory of both temperate and tropical forests, particularly in mountainous regions. In western Amazonia around 160,000 km2 of forests is dominated by two species of Guadua, possibly because of the activities of the geoglyph builders who became active around 4,000 years ago ((McMichael et al. 2014). Even herbaceous bamboos (Olyreae) may dominate understory vegetation (Bamboo Phylogeny Group 2012b for details and references). However, although bamboos are the second most important woody monocot clade (after palms), they do not appear in the very top ranks of any of the important ecological traits studied by Cornwell et al. (2014).
Bamboos play a very important role in forest dynamics, not simply because of their dominance but because of their synchronised monocarpic flowering (see below), an extreme form of masting. This monocarpic behaviour can allow broad-leaved angiosperms to become established in areas where bamboos grow if they can establish themselves when the bamboos die after fruiting..
8. Fungus Attack. Sindhu et al. (2008) suggested that the whole PACMAD/BEP clade can be characterized by a gene that protects the plant against toxins produced by the ascomycete Cochliobolus (anamorph Helminthosporium) carbonum; they describe the gene as "a guardian of the grass family" (ibid.; p. 1766). This gene could be an apomorphy of the whole clade, but its wider distribution in monocots is unknown.
9. Phloem transport. Some sieve tubes, especially in the cross-veins in the leaves, that are adjacent to the xylem lack companion cells, are notably thick-walled, and are symplastically isolated from "normal" sieve tubes. They seem to be involved in short distance transport of not very concentrated sugars (Botha 2013). They are quite common in grasses, and probably evolved well before 7-5 m.y.a. (c.f. Botha 2013); although their distribution in other monocots is unclear, they are also reported from Cyperaceae.
10. Other. For the role of the leaf sheath in supporting the stem, particularly the region with the intercalary meristem, see Kempe et al. (2013 and references). The pattern of evolution of the Rp1 disease resistance gene family in the PACMAD/BEP clade is complex (Luo et al. 2010). At least some species of Micraira (Micrairoideae) are resurrection plants (Sanchez-Ken et al. 2007).
Bacterial/Fungal Associations. Ascomycete clavicipitaceous endophytes are widely distributed among grasses (Clay 1990: review; Leuchtmann 1992: distribution and host specificity of grass endophytes; Schardl 2010; Rodriguez et al. 2009: endophytes in general); the association could be ca 40 m.y. old (Schardl et al. 2004). Some 30% or more Poöideae are involved in these associations, and there is both horizontal and in particular vertical transmission of the fungus. One of the most important fungi involved is Epichloë (Clavicipitaceae), a systemic endophyte restricted to Poöideae; Neotyphodium is its asexual stage, perhaps representing hybrids of Epichloë species (Roberts et al. 2005; Moon et al. 2005; Rodgers et al. 2009: patterns of infection of the two forms). These hybrid fungi may increase the competitive ability of the host grass under stressful conditions (Saari & Faeth 2012), although under some conditions they severely reduce sexual reproduction (Oberhofer et al. 2013: both greenhouse experiments). The larvae of Phorbia (or Botanophila) flies live on Epichloë stroma, and the adults transmit the fungal spermatia in a fashion analogous to insect pollination of flowers (Bultman 1995). Indeed, Epichloë synthesizes unique compounds that specifically attract the flies (Steinebrunner et al. 2008) and which may also be toxic to other fungi that secondarily invade the fungal stromata (Schiestl et al. 2006). However, the equilibrium of such relationships can easily be disturbed (Eaton et al. 2010). For details of the phylogeny and evolution of the endophyte association see Schardl (1996, 2002, 2010), Craven et al. (2001), Clay and Schardl (2002), Jackson (2004: possible codivergence), and Gentile et al. (2005).
Clavicipitaceae-Balansiae (Clay 1986; White et al. 2003: review) are now included in Hypocreales, the old Clavicipitaceae having been split up. Hypocreales include many insect pathogens, plant parasites, and especially parasites of other fungi, but also yeast-like obligate symbionts (of leaf hoppers). There has been widespread cross-kingdom host switching (e.g. Vega et al. 2009; Kepler et al 2012). Hypocreales may ancestrally have been plant parasites, although the immediate ancestor of grass endophytes may have been an insect pathogen (e.g. Spatafora et al. 2007; Vega et al. 2009). Some fungi like Metarhizium robertsii may even be both endophyte and insect pathogen (e.g. Sasan & Bidochka 2012).
The endophyte-grass relationship is usually described as being one of mutualism, although this may sometimes, at least, not be so (see Saikkonen et al. 1998; Gundel et al. 2006; Ren & Clay 2009), indeed, the more that is found out about the relationship, the more complex it appears to be. These endophytic fungi synthesize a diversity of secondary metabolites (Spatafora et al. 2007). Four groups of "grass" alkaloids are synthesized by Epichloë: Indole diterpenes, loliine (1-aminopyrrolizidines), peramine, and the ergot (ergolines) alkaloids (Fleetwood et al. 2007). Loliines are primarily active against insects (Schardl et al. 2007; Zhang et al. 2009). Endophytes that are insect pathogens may also be antagonistic to plant pathogens (Vega et al. 2009 and references). Furthermore, the presence of endophytes affects both the palatability of grasses to herbivores and of their seeds to granivorous birds (Madej & Clay 1991), animals eating the infected material sometimes not thriving at all. The level of aphid infestation and that of their parasites and parasitoids is also affected by these metabolites (Omacini et al. 2001), as is the infestation of the plant by nematodes, insect herbivory (Tanaka et al. 2005), the resistance of the plant to the effects of water stress (Hahn et al. 2007), and even the pattern and rate of decomposition of dead grass (Lemmons et al. 2005; see also Popay & Rowan 1994; Schardl 2010). Fungal endophytes may also affect root growth and root hair production (Sasan & Bidochka 2012). It has recently been suggested that some of these endophyte-mediated affects can be co-opted for developing improved strains of forage grasses (Gundel et al. 2013).
Many other species of apparently symptomless endophytes (= class 3 endophytes: Rodriguez et al. 2009) are also found in Poaceae, but little is known about their interactions with their hosts. Márquez et al. (2007) noted that only when the endophytic fungus (Curvularia) was infected with a virus was Dicanthelium lanuginosum, the host of the fungus, able to grow in volcanically-heated soils, suggesting the complexity of such relationships. Marks and Clay (2007) discuss growth rate of endophyte-infected and -free plants under various conditions. Some root-associated endophytic fungi (class 4) are also coprophilic (Herrera et al. 2009), perhaps aiding in their dispersal. For fungal records - very numerous and diverse - on grasses, see Tang et al. (2007); there are at least 1933 species of fungi known from bamboos alone.
Bacteria, too, may be endophytic in grasses, and several bacterial endophytes are implicated in fixing one third to one fifth of the nitrogen needed by sugarcane in Brazil - the bacteria include Gluconacetobacter (alpha-Proteobacteria) and Herbaspirillum and Burkholderia (ß-Proteobacteria) (de Carvalho et al. 2011), for Burkholderia, see also Fabaceae, Primulaceae-Myrsinoideae and Rubiaceae. A wide variety of bacteria has been isolated from the roots of Chrysopogon zizanioides (vetiveria) where they are implicated in the synthesis of terpenoids, etc., in the prized essential oils that the plant produces (del Guidice et al. 2008).
Parasitic rusts and smuts are common on Poaceae, and those on Bambusoideae and Poöideae are particularly distinctive (Savile 1979b); two thirds of Ustilaginales (smuts) - close to 600 species - are found on Poaceae (Kukkonen & Timonen 1979; Stoll et al. 2003). Some seventy species of Berberis are alternate hosts (the aecial stage) for the basidiomycete Puccinia graminis, the black stem rust of wheat and other grain crops in Poöideae; this species (or complex) infects some 77 genera of mostly poöid grasses (Abbasi et al. 2005 and references).
Cyclic hydroxamic acids are widely distributed in the family and confer resistance against a variety of fungal and insect pathogens (Frey et al. 1997); for protection against toxins produced by the ascomycete Cochliobolus carbonum, see Sindhu et al. (2008), also above.
Plant/Animal Interactions. Despite the silica bodies mentioned above, as well as alkaloids and other defences, caterpillars of nymphalid butterflies, in particular the browns, Satyrini, and related subtribes like Morphini, Melantinini, etc., are common on Poaceae. Estimates are that Satyrinae as a whole diverged from other Nymphalidae some 80-85 m.y.a. (or perhaps at the K/T boundary: Heikkilä et al. 2011; see also Peña et al. 2011), but the main clades within it did not diverge until the later Palaeocene. Other subtribes of Satyrinae are also found on commelinid monocots, sometimes also including grasses, but none has more than 110 species, compared to the some 2,200 species of Satyrinae-Satyrini.
The larvae of Satyrini eat grasses almost exclusively, and they are the only common grazing insects there. Stem Satyrini may be about 65-55 m.y. old, and the crown group is later Eocene, some (47.8-)41.8, 36.6(-31.5) m.y. (Peña & Wahlberg 2008; Wahlberg et al. 2009; Peña et al. 2006, 2011: age depends on calibration points, position of Satyrini varies), perhaps contemporaneous with the initial spread of grasses (Peña et al. 2006, 2011; Peña & Wahlberg 2008). Although the move of satyrine butterflies from forests to more open environments may have helped spur their diversification, rather than grass feeding per se (Peña et al. 2011), diversification has also occurred in Satyrini of more forested habitats. Thus caterpillars of the largely western South American subtribe Pronophilina, with well over 400 named species (?600 species total), are largely bamboo feeders that eat Chusquea (for a phylogeny, see Fisher et al. 2104). They are most diverse in the Andes just below the cloud forest-páramo transition at ca 3050-3250 m altitude, but some species are found in the páramo itself, where Swallenochloa and some other bamboos grow (Pyrcz et al. 2009; Casner & Pyrcz 2010; Sklenár et al. 2011). Only a few Pronophilina are found in comparable forests in east Brazil and Central America.
Galling dipterans, especially Cecidomyiidae, are quite common in grasses (Labandeira 2005). Cecidomyiid gall midges, notably Mayatiola (M. destructor is the Hessian fly), grow on Poöideae in North America (Gagné 1989). Shoot flies (Diptera-Chloropidae) form galls on monocots, especially grasses, but they are also simple herbivores and have other life styles (de Bruyn 2005). Chinch bugs (Hemiptera-Lygaeidae-Blissinae) have been most commonly observed on members of the PACMAD clade, less commonly on the BEP clade; the lygaeid Teracrini are also concentrated on Poaceae (Slater 1976). Poaceae provide food for both adults (as pollen) and larvae (as roots) of Chrysomelidae-Galerucinae-Luperini-Diabrotica beetles (Jolivet & Hawkeswood 1995).
Water often congregates in the hollow stems of bamboos, and a distinctive fauna lives there (Kitching 2000).
Pollination Biology & Seed Dispersal. Poaceae are predominantly wind-pollinated and usually have protandrous flowers with dangling anthers. However, some forest-dwelling grasses, especially Bambusoideae-Olyreae, small plants of the forest floor in the New World, are pollinated by insects (Soderstrom & Calderón 1971: Parinari, Olyra). Streptochaeta may also be animal pollinated, since it lacks a plumose stigma and its anthers do not dangle; the flowers are protogynous (Sajo et al. 2008). Lodicules, modified members of the inner tepal whorl, help in the opening of the staminate or perfect flowers; they may be absent from carpellate flowers (see Sajo et al. 2007; Reinheimer & Kellogg 2009 for references). There is considerable variation in flower type in the family (see e.g. Le Roux & Kellogg 1999; Chuck 2010 for the development of unisexual flowers).
The caryopsis is often described as being the distinctive fruit type of Poaceae, and is a variant of an achene in which the testa and pericarp are fused (but see Nakamura et al. 2009 and references for the variety of fruit development in Poaceae). However, the fruit proper is rarely the dispersal unit (but c.f. the fleshy-fruited Alvimia [Bambusoideae]), and there is a variety of diaspores and dispersal mechanisms in the family (e.g. Werker 1997). Dispersal is quite often by animals, attracted by structures like elaiosomes (Davidse 1987), while a variety of hooks and spikes attach other grass diaspores to passing animals (Centotheca is a good example). Wind-dispersal is quite common, for example, Andropogon has long hairs on the awns, while Spinifex and a few other genera are tumbleweeds. Awns can aid in both wind and animal dispersal, while the surface microstructure on awns, minute retrose bristles, may cause the achene to become "planted" in the ground (Elbaum et al. 2007; Humphreys et al. 2010b) or to move along the surface (Kulic et al. 2009; see also Davidse 1987). This is by a ratchet principle similar to that which operates when you put an entire inflorescence of Hordeum up your sleeve; the inflorescence migrates up your arm and sometimes also down your back as you walk along. Despite the apparent advantages of having an awn, this has been lost several times in Danthonioideae, at least, perhaps in association with the adoption of the annual habit where passive burial of seeds suffices (Humphreys et al. 2010b).
Woody bamboos are known for their tendency to dominate the vegetation and their synchronized flowering and fruiting, evident even when transported thousands of miles from their native habitat. Plants are monocarpic, flowering may occur only every 120 years or so, and after a rather protracted period of reproduction, the plant dies. This has profound effects both on the general vegetation and all organisms dependent on bamboos for food and shelter. The fruits are used as food by humans and they also attract animals - birds, rats, etc. - in very large numbers (Janzen 1976; Judziewicz et al. 1999). This behaviour is also found in some herbaceous bamboos and, depending on relationships within Bambusoideae, may even be plesiomorphic for the subfamily; it is an extreme form of masting (Curran & Leighton 2000 and references), although bamboos are not known to be ectomycorrhizal plants, as is common in other masting taxa.
Vegetative Variation. Woody bamboos, for example Chusquea, may have a hundred or so branches at a node, all borne in a fan-like arrangement. They are produced by a combination of multiple buds and axillary shoots with very short internodes, all nodes producing branches (see e.g. McClure 1973; Judziewicz et al. 1999; Tyrrell et al. 2012: Fisher et al. 2014 for a phylogeny of Chusquea).
Genes & Genomes. Genome evolution in Poaceae has been particularly active. Comparisons of expressed sequence tags, etc., suggest that the genomes of Poaceae are much more different from the genome of Allium (Asparagales-Asparagaceae-Allioideae) than the genome of Allium is from that of Arabidopsis (Brassicales-Brassicaceae: Kuhl et al. 2004).
As in other groups, genome duplication is thought to have played a major role in the evolution of the family. A duplication of the whole genome in a clade that includes at least Zea, Oryza, Hordeum and Sorghum, i.e. the PACMAD/BEP clade, has been dated to ca 70/70-66/70-50/73-56/50-40 m.y. (Goff et al. 2002; Paterson et al. 2004; X. Wang et al. 2005; Schlueter et al. 2004; International Brachypodium Initiative 2010). Yockteng et al. (2013) date duplication of SEPALLATA genes here to around 82-58.2 m.y.. Although Vandepoele et al. (2003) think that this may be an aneuploidy event, duplication of the whole genome is the favoured hypothesis, with x = 5 -> x = 10 (polyploidy) -> x = 12 (two interchromosomal translocations and fusions) in the ancestor of the PACMAD/BEP clade, with much subsequent rearrangement, chromosome number reduction, etc. (Bennetzen 2007; Salse et al. 2008, 2009a, b; Bolot et al. 2009; Abrouk et al. 2010; Murat et al. 2010). (Hilu  suggested that the base chromosome number for the whole family might be x = 11.) X = 12 is still found in rice (Oryza), for example, while x = 10 in Panicoideae. Certainly one or more rounds of genome duplication have occurred, with subsequent independent reductions in chromosome numbers (Schnable et al. 2009; Abrouk et al. 2010 and references). Within Poöideae there have been independent reductions in chromosome number from n = 12, for example, Brachypodium has n = 5 (International Brachypodium Initiative 2010; Murat et al. 2010).
Soltis et al. (2009) suggested that diversification in Poaceae might be connected with this genome duplication, and the development of a cytosolic ADPglucose phosphorylase, perhaps unique to this clade, has been associated with it (Comparot-Moss & Denyer 2009), however, diversification of the groups including the cereals may have occurred ca 20 m.y. later (Paterson et al. 2004; c.f. International Brachypodium Initiative 2010).
Whatever the cause, there has been very extensive duplication of genes, e.g. the API, AG and SEP families, but not genes of the AP3 lineage (Zahn et al. 2005a; see also Saski et al. 2007 for other duplications in the family). Malcomber and Kellogg (2005) suggest that there has been duplication of LOFSEP genes within Poaceae, while the duplication of AP1/FUL gene, apparently in stem-group Poaceae, may be involved in the evolution of the spikelet (Preston & Kellogg 2006). Developmental gene duplication and subsequent functional divergence seem to have played a very important role in allowing the development of the baroque diversity of inflorescences in the family (Malcomber et al. 2006; Zanis 2007; see also Doust & Kellogg 2002; Reinheimer & Vegetti 2008). For the evolution of the NADP-malate dehydrogenase gene following its duplication, see Rondeau et al. (2005).
There are other important and more recent duplication events involving hybridization. Thus a genome duplication/hybridization in the ancestor of Zea has been dated to ca 4.8. m.y. (Swigonová et al. 2004) - the two ancestors may have diverged ca 11.9 (Swigonová et al. 2004) or 20.5 m.y.a. (Gaut & Doebley 1997). The over 500 species of temperate bamboos form a clade that is descended from an allotetraploid ancestor (Triplett et al. 2011). Z. Peng et al. (2013) suggest that genome dupication occurred in the ancestor of the giant bamboo Phyllostachys heterocycla (P. edulis) 11.5-7.7 m.y. ago. The complex relationships within Danthonioideae may be connected with extensive past hybridizations (Pirie et al. 2008, 2009).
There has been very substantial genome evolution in grasses, with that in Triticeae being particularly accelerated (Luo et al. 2009; see also Messing & Bennetzen 2008; Salse et al. 2009a). Indeed, Triticeae (Poöideae) are notorious for the extent and complexity of the reticulating relationships that they show (Jacob & Blattner 2006; G. Petersen et al. 2006a; Mason-Gamer 2008; Meimberg et al. 2009; Sun & Komatsuda 2010; Fan et al. 2013: Elymus s.l. and the Y genome; Martis et al. 2013: rye), with subsequent polyploidy, chromosome duplication, genome re-arrangement and introgression complicating the picture. Many Triticeae have massive genomes in part because of changes in base chromosome number (Jakob et al. 2004). Winterfeld (2006) discussed cytogenetic evolution, mainly in Aveneae (= Poöeae). In general, genome size varies considerably and at least in part independently of chromosome number, both increasing and decreasing (Caetano-Anollés 2005; Smarda et al. 2008; Schnable et al. 2009). For a possible relationship between genus size, life form and polyploidy, see Hilu (2007).
There has also been substantial evolution in the chloroplast genome in particular (Leseberg & Duvall 2009; Guisinger et al. 2010 for literature), although details on where on the tree (and so when) particular changes occurred await more extensive sampling in Poales and "basal" Poaceae; the rate of plastid evolution may have since slowed down. These rate changes are placed at the level of Poaceae as a whole above, although they might more correctly be put at the PACMAD/BEP node... Morris and Duvall (2010) discuss aspects of chloroplast genome evolutiom, focusing on Anomochloa. For a series of inversions in the single copy region and expansion of the inverted repeat at the single copy-inverted repeat boundary, see Hiratsuka et al. (1989) and Saski et al. (2007). For accD gene loss, see Katayama and Ogihara (1996), for deletions, etc., in the 3' end of the mat K gene, see Hilu & Alice (1999), for loss of introns in chloroplast genome, see Daniell et al. (2008) for references, and for subrepeat size in the rpoC2 insert region, see Jones et al. (2014).
The mitochondrial coxII.i3 intron has developed a moveable element-like sequence (Albrizio et al. 1994), but there is a fair bit of variation in other monocots, too. Transposable elements, Mutator-like elements (MULEs), seem to have moved fairly recently by lateral transfer between rice, East Asian bamboos, and a number of Panicoideae-Andropogoneae (Diao et al. 2006), while Stowaway Miniature Inverted repeat Transposable Elements (MITEs) are common in the BEP clade, especially in Poöideae (Minaya et al. 2013).
Economic Importance. Glémin and Bataillon (2009) take a comparative viewpoint and look at how grasses in general have evolved under domestication. Sang (2008) noted that single genes are involved in a number of major morphological transitions in the domestication of grains, such as the development of non-shattering rhachises; the genes may be quite different in unrelated species.
Among the C3 domesticates, several are Poöideae-Triticeae, which include important grain genera such as Triticum (wheat), Hordeum (barley) and Secale (rye) (see above for genome evolution in this group). Wheat (mostly Triticum aestivum - Poöideae), which provides one fifth of the calories eaten by humans, began to be domesticated ca 10,000 years ago; see Israel Journal of Plant Sciences 55(3-4). 2007, for an entry into the literature on domestication, also Fuller (2007), Baum et al. (2009: haploid genomes) and Carver (2009: general). Most domesticated forms are polyploid, and genome plasticity in connection with this polyploidy has been implicated of the success of wheat in cultivation (Dubcovsky & Dvorak 2007). For the domestication of barley (Hordeum vulgare), see Fuller (2007), Pourkheirrandish and Komatsuda (2007) and Azhaguvel and Komatsuda (2007).
Another major C3 grain is rice (Oryza spp.). For a phylogeny of Oryzeae (Ehrhartoideae), see Guo and Ge (2005), and for information on the complex history of domestication of rice, which occurred in two places, at least, see Sweeney and McCouch (2007) and Fuller (2007).
Sorghum and Zea (Panicoideae) are among the important C4 grain genera. The domestication of maize seems to have occurred in seasonal tropical forests in southwestern Mexico, perhaps the Balsas valley, some 8,700 years ago (Piperno et al. 2009; Ranere et al. 2009: summarized in Hastorf 2009); for a detailed summary of all aspects of maize biology, see Bennetzen and Hake (2009). For the domestication of pearl millet (Pennisetum glaucum), see Fuller (2007), and for that of sorghum (Sorghum spp.), see Dillon et al. (2007). For the domestication of sugarcane (Saccharum officinarum) in New Guinea, see Dillon et al. (2007) - note that Sorghum bicolor and Saccharum officinarum can be hybridized (e.g. Nair 1999).
Chemistry, Morphology, etc. Because of their great economic importance, many aspects of grass morphology, anatomy, cytology, etc., have been surveyed over the years. By no means all of these really useful early surveys are cited below, although most are easily traceable in the literature.
The primary cell wall hemicellulose and pectin polysaccharides of grasses are very different from those of other seed plants, both in overall composition and particularities of the composition of the xyloglucans (O'Neill & York 2003), and the polysaccharides are less branched than those elsewhere - but overall sampling is very poor. Hatfield et al. (2009) discuss acylation of lignin in grasses, and Boerjan et al. (2003) note that grasses in particular have a variety of minor lignin monomer units; p-coumarate units are usually terminal pendant units in grasses (Ralph 2009; see also Petrik et al. 2014). There is evidence that ADP-glucose pyrophosphorylase, involved in starch synthesis, is very largely present in the cytosol, not in the plastids, in the endosperm of members of the PACMAD/BEP clade in grasses. It occurs in plastids in the starch-storing organs of other seed plants, probably even including the starchy endosperm of other commelinid monocots, but the sampling here, too, is poor (Beckles et al. 2001; Comparot-Moss & Denyer 2009).
Whether or not the division resulting in the trichoblast/atrichoblast pair in roots is asymmetric (Poöideae) or not, and, if it is symmetric, whether or not subsequent development of the two cells is the same, both vary (Kim & Dolan 2011). The sampling is poor, with no species from the basal pectinations and only one species each in Ehrhartoideae and Bambusoideae examined (Row & Reeder 1957: exceptions are no longer so; Kim & Dolan 2011). Poaceae have a nodal vascular plexus (Arber 1919), but I have no idea as to its general distribution and significance. Microhair variation in the family is extensive and of some use in delimiting major groups (Liphschitz & Waisel 1974; Amarasinghe & Watson 1988, 1990; Liu et al. 2010; Oli et al. 2012). Ligule variation is also extensive: Anomochlooideae are sometimes described as lacking a ligule (Judziewicz & Clark 2008, q.v. for other characters), or the ligule is described as being a ring of hairs. The leaf blades of Neurolepis (Bambusoideae) may be up to 4 m long.
For inflorescence morphology, see Kellogg et al. (2013), and for summaries of floral development in grasses, see Ciaffi et al. (2011); see also Rudall and Bateman (2004) and Ronse de Craene (2010). The grass palea, which is often bicarinate, has often been interpreted as being prophyllar/bracteolar in nature, monocots commonly having bicarinate prophylls. However, in this scenario bracteoles would probably have had to be regained, since the immediate outgroups to Poaceae lack them. In early studies of gene expression, the palea and perhaps even lemma appeared to be calycine in nature while the lodicules were corolline (Ambrose et al. 2000); A-type genes are expressed in both the palea and lemma (Whipple & Schmidt 2006). General comparative morphology might suggest that the lemma is a bract and the palea represents two connate tepals of the outer whorl; if the lemma is a perianth member, then loss of bracts is an apomorphy for all or most of Poaceae. The tepaloid nature of the lodicules is relatively uncontroversial (see Sajo et al. 2007; Reinheimer & Kellogg 2009; Yoshida 2012).
Understanding the flowers of Streptochaeta and Anomochloa presents a challenge (see also Judziewicz & Soderstrom 1989). Flowers of Streptochaeta can be interpreted as having an outer perianth whorl of two (adaxial) members - c.f. the single, bicarinate palea (there are sometimes three members in this outer whorl), and an inner perianth whorl of three members - c.f. the lodicules. The three stamens common in grass flowers would then be those opposite the three members of the outer perianth whorl (see Whipple & Schmidt 2006; Preston et al. 2009; Reinheimer & Kellogg 2009 for further details). If Ecdeicoleaceae and Joinvilleaceae are sister taxa (Marchant & Briggs 2006) and given the likelihood that the flowers of Anomochloa are sui generis, the floral morphology of Streptochaeta may be plesiomorphic for the family, or aspects of it are apomorphies for the genus. Sajo et al. (2008) suggested that the flowers of Streptochaeta could be interpreted in more or less conventional terms, with a whorl of three rather coriaceous "bracts" being equivalent to lodicules and two adaxial "bracts" outside this perhaps representing the palea (although the structure interpreted as being a lemma was also adaxial...). Sajo et al. (2011, esp. 2012: floral structure assumed rather than demonstrated) described the flowers of Anomochloa as having glumes, palea and lemma (bracteoles, prophylls respctively), lodicules, etc.; there is basically a single carpel, although there are vascular traces to three. The flowers of Ecdeicolea in particular are notably monosymmetric, with the two adaxial tepals of the outer whorl larger and keeled, and comparable differentiation in the outer perianth whorl occurs in Xyridaceae (q.v.); these are likely to be parallelisms.
It is difficult to understand the arrangement of the pollen grains in the small anthers of Streptochaeta; they may be peripheral, at least initially (Kirpes et al. 1996; Sajo et al. 2009).
Some grasses have pendulous, straight ovules (when the ovules are young?). Although ovules both with and without parietal tissue are reported for grasses, reports of the former (e.g. Guignard 1882) need confirmation - parietal tissue is likely to be absent (Rudall et al. 2005a; see also Nakamura et al. 2009). When there are three carpels, the abaxial member is fertile (Kircher 1986). The gynoecium is often annular in early development, although in Pharus it is quite strongly 3-lobed (Sajo et al. 2007). The caryopsis is often described as being a distinctive fruit type of the Poaceae; in a caryopsis, the seed coat and pericarp are fused, and it is basically a variant of an achene. However, as Nakamura et al. (2009 and references) note, fruits may develop in a variety of ways. Guérin (1899) suggested that the persistent part of the seed coat was tegmic, and he sometimes showed the exotegmen in particular as having quite large cells, or quite thick walls, during development.
Poaceae are noted for their well developed, lateral embryo with a scutellum, coleoptile, coleorhiza, and mesocotyl (Tillich 2007). The scutellum is the distinctively-shaped haustorial part of the single cotyledon of other monocots (= the haustorial cotyledonary hyperphyll if one wants to be technical), and the coleoptile is the sheathing base of the cotyledon, the scutellum and coleoptile originating on the same side of the embryo (Kaplan 1997: 1 ch. 5; Takacs et al. 2012). The mesocotyl could be an elongating nodal region or a structure that represents (part of) the hypocotylar region to which the cotyledonary stalk is adnate, while the coleorhiza may be part of the hypocotylar region. The "radicle" is endogenous in origin, and is a lateral root; Poaceae thus lack a radicle proper, and so are homorhizic (Kaplan 1997: 1 ch. 4, 5). Alpha prolamin genes, involved in the synthesis of seed storage proteins, evolved in Panicoideae-Andropogoneae 26-21 m.y.a. (Xu & Messing 2008).
See Kellogg (2014) for a comprehensive account of the family. Arber (1934) remains a classic treatment, and Chase (1964) an introduction; see also the Grass Phylogeny Working Group (2001, 2011); McClure (1966) gives an account of bamboos (see also the Bamboo Phylogeny Group 2012b), and Bell and Bryan (2008) a good general treatment of grass morphology.
For the occurrence of ergot alkaloids, see Gröger and Floss (1998), for cell wall composition; see Fincher (2009), for non-starch soluble storage polysaccharides in the seed and fructans in vegetative parts, see MacLeod and McCorquodale (1958) and Meier and Reid (1982), for anatomy, see Metcalfe (1960), for C4 photosynthesis, see also Kellogg (1999), for phytoliths (SiO2 bodies) and their distribution, see Piperno and Pearsall (1998), Piperno and Sues (2005), Piperno (2006) and Rudall et al. (2014: patterns and types complex). For inflorescence morphology and development, see Vegetti and Anton (1996), Vegetti and Weberling (1996 and references: classical approach), Perreta et al. (2009) and Thompson and Hake (2009), for floral/spikelet evolution, see Yuan et al. (2009) and Thompson et al. (2009), for aerial branching, Malahy and Doust (2009), for a quantitative analysis of the hitherto supposedly taxonomically rather uninformative pollen, see Mander et al. (2013), for the style of Triticum, see Li and You (1991), for ovules, see e.g. Bhanwra and Sharma (1991, 2001), for embryo variation, see Reeder (1957), for proliferating antipodal cells, Anton and Cocucci (1984) and Wu et al. (2011), for endosperm and its development, see Olsen (2007) and Sabelli and Larkins (2009), for the morphology of starch grains in the endosperm, see Shapter et al. (2008), and for cytology, Roodt and Spies (2003) and Winterfeld (2006).
For general information on Bambusoideae, see Clark (1997), Judziewicz et al. (1999), and Judziewicz and Clark (2008), for foliar epidermis, see H.-Q. Yang et al. (2008a); for pollen in Chloridoideae, see Liu et al. (2004: not much variation). For Micrairoideae, see Sánchez-Ken et al. (2007).
Phylogeny. General. For overviews of the phylogeny of the family, see Kellogg (2000a, 2014) and the Grass Phylogeny Working Group (2001, 2011); Duvall et al. (2010) provide a preliminary tree based on whole chloroplast genomes, and Ruhfel et al. (2014) looked at the genomes of some 35 taxa, the general relationships they found being those discussed below. Zhang and Clark (2000) restricted the limits of Bambusoideae to those accepted here; most taxa in what is now the basal grade of Poaceae have been included in the bamboos at one time or another. In a multi-gene study, Bouchenak-Khelladi et al. (2008) did not find strong evidence for the monophyly of Anomochlooideae, Streptochaeta possibly being sister to all other Poaceae; Micrairoideae might not be monophyletic, Isachne not having a fixed position; there was support for a sister relationship between Danthonioideae and Chloridoideae (see also Pirie et al. 2008); and Streptogyna might be sister to the whole PACCMAD clade - and it lacks the possible synapomorphies of that clade (Bouchenak-Khelladi et al. 2008; see also Bouchenak-Khelladi et al. 2009; Hisamoto et al. 2008).
Relationships of the major clades within the PACCMAD (as it used to be called) and BEP clades were initially for the most part unclear. Thus the relationships of Poöideae (Hodkinson et al. 2007; Duvall et al. 2008a) and Ehrhartoideae (Cahoon et al. 2010, as Oryzoideae) are unclear in some analyses (see also Saarela & Graham 2010; c.f. Davis & Soreng 2008; Christin et al. 2008a: BEP clade paraphyletic and immediately basal to the PACCMAD clade). Relationships in the PACCMAD clade remained particularly difficult (Saarela & Graham 2010: sampling). However, the Grass Phylogeny Working Group II (2011) have found strong support for many of the relationships in the PACMAD (as it is now called) and BEP clades, although support for the first two branches in the PACMAD clade is still only weak.
Duvall et al. (2007) had found strong support for the BEP clade, albeit the taxon sampling was slight (see also Grass Phylogeny Working Group 2001); relationships between the three subfamilies were initially uncertain (e.g. Hisamoto et al. 2008). Peng et al. (2010: 43 genes, only 10 taxa) found strong support for the relationships [E [B + P]] (ML and Bayesian analyses) and even stronger support for the relationships [B [E + P]] (neighbour joining), but the analyses of Wu and Ge (2011: 76 genes, 22 taxa; see also Bouchenak-Khelladi et al. 2008; Kelchner & the Bamboo Phylogeny Group 2013) supported the former set of relationships, and these are followed here. However, Blaner et al. (2014) found that Brachelytrum moved outside Poöideae in analyses using nuclear rather than chloroplast data.
Panicoideae. For discussions of the relationships - close and becoming ever more entwined - between Panicoideae and the old Centothecoideae, see Duvall et al. (2008a) and especially Sánchez-Ken and Clark (2008); the two are to be combined (Sánchez-Ken & Clark 2010; Teerawatananon et al. 2012), hence PACCMAD -> PACMAD. For relationships within Paniceae, see Zuloaga et al. (2000), Gómez-Martínez and Culham (2000) and Morrone et al. (2010, esp. 2012), for the bristle clade of Paniceae, see Doust et al. (2007), and those within Panicum itself, see Aliscioni et al. (2003) and Sede et al. (2008), within Pennisetum, in which Cenchrus is embedded, see Donadío et al. (2009) and Chemisquy et al. (2010), and within Setaria, see Kellogg et al. (2009); see also Sede et al. (2009) for two new genera. Salariato et al. (2010) examined relationships within Melinidae, particularly fromn the point of view of inflorescence evolution. Ng'uni et al. (2010) looked at relationships with Sorghum, and López and Morrone adjusted the limits of Axonopus. For the phylogeny of Andropogoneae, see Kellogg (2000c) and Mathews et al. (2002), and for that of Paspalum, basically monophyletic, see Rua et al. (2010) and Scataglini et al. (2014). Finally, for more information on relationships within Panicoideae, including those of some of its constituent genera, see papers in Aliso 23: 503-562. 2008.
Chloridoideae. Peterson et al. (2009, 2010a, 2011) suggest that relationships are something like [Centropodieae [[Triraphidae - Neyraudia (panicoid microhairs) + Triraphis] [Eragrostideae [Zoysieae + Cynodonteae (the bulk of the group)]]]]. Eragrostis and Sporobolus may be polyphyletic, while Muhlenbergia is paraphyletic, but there are a number of well supported (and with morphology, too) clades (Peterson et al. 2010b; Columbus et al. 2010); Leptochloa is polyphyletic (Peterson et al. 2012). For a morphological phylogenetic analysis of the subfamily, see Liu et al. (2005), for other relationships, see papers in Aliso 23: 565-614. 2008.
Danthonioideae. For a phylogeny of the Pentaschistis group, also character evolution there, see Galley & Linder (2007), for relationships in the subfamily as a whole, see Barker et al. (2007a), Pirie et al. (2008) and Cerros-Tlatilpa et al. (2011). Some relationships within Danthonioideae are reticulating (Pirie et al. 2008, 2009).
Ehrhartoideae. The relationships of Oryzeae have been much studied (Guo & Ge 2005; L. Tang et al. 2010 and references); for diversification within Oryza itself, see Zou et al. (2008). The position of Streptogyna remains unclear, but it may be close to Ehrhartoideae.
Bambusoideae. See the Bamboo Phylogeny Group (2012b) for a summary of phylogenetic work on the subfamily. Burke et al. (2012) looked at relationships based on analyses of whole plastid genomes. Clark and Triplett (2006) discussed relationships within the subfamily, previously divided into the woody Bambuseae and the herbaceous Olyreae. The woody temperate Arundinarieae may be sister to the rest of the subfamily; the monotypic Buergersiochloa, from New Guinea, is sister to the rest of the herbaceous Olyreae, which are plants of the New World (e.g. Kellogg & Watson 1993; W. Zhang & Clark 2000; Bouchenak-Khelladi 2008). Sungkaew et al. (2009; five plastid genes; Kelchner & the Bamboo Phylogeny Group 2013) retrieved the relationships [Arundinarieae [Olyreae [Neotropical (strictly) Bambuseae + Paleotropical & Austral Bambuseae]]] and mapped the distributions of each of these groups. However, Kelchner and the Bamboo Phylogeny Group (2013) noted that the position of Olyreae in particular was not secure, and it might be sister to the rest of the subfamily. For a phylogeny of the woody bamboos, see Clark et al. (2008: resolution poor), of neotropical woody bamboos, see Clark et al. (2008) and Fisher et al. (2009), of neotropical bamboos, see Burke et al. (2014), of palaeotropical woody bamboos, see H.-Q. Yang et al. (2008b: resolution o.k., baccate fruit arose in parallel), of Bambusa and its relatives, see J. B. Yang et al. (2010) and Goh et al. (2010), of Dendrocalamus, see Sungkaew et al. (2010), of temperate bamboos, see Peng et al. (2008), and of Bambuseae-Arthrostylidiinae, see Tyrrell et al. (2009, 2012). Disentangling relationships in Arundinarieae is proving difficult. Zeng et al. (2010) found rather little resolution despite sequencing ca 9,000 base pairs. The extent of the problem has been confirmed: A Phyllostachys clade that was recovered in plastid analyses was pulverised into 24 bits in nuclear gene analyses; hybridization is involved (Y.-X. Zhang et al. 2012; see also H.-M. Yang et al. 2013). For hybridization in the ancestor of temperate bamboos, see Triplett et al. (2011), and for hybridization in paleotropical bamboos, see Goh et al. (2013). Relationships within the large neotropical Chusquea are discxussed by Fisher et al. (2014).
Poöideae. There are several papers on Poöideae in Aliso 23: 335-471. 2008; see also Soreng and Davis (2000) and Schneider et al. (2009) for relationships within the whole subfamily. For the ndhF gene, structural features of chloroplast and nuclear genomes, etc., and the phylogeny of Poöideae, see Davis and Soreng (2008). It is not certain the the duplication of the ß-amylase gene is an apomorphy here; one of the gene copies breaks down starch into fermentable sugars in the endosperm, while the other is more broadly expressed in the plant, as it is in other Poaceae (Mason-Gamer 2005). For relationships and morphology in Phaenospermateae (inc. Duthieae), see Schneider et al. (2011); Phaenosperma itself is a very distinct plant previously included in Bambusoideae. For a phylogeny of Poeae, which should now include Aveneae, see Grebenstein et al. (1998), Quintinar et al. (2007, also Döring et al. 2007; Soreng et al. 2007; Saarela et al. 2010, 2011; Gillespie & Soreng 2011), for that of Poa itself, see Gillespie and Soreng (2005), Gillespie et al. (2009) and Soreng et al. (2010, 2011). See also Gillespie et al. (2008, 2010) for relationships in Poinae, Quintanar et al. (2010) for those in Koeleriinae, Essi et al. (2008) for relationships around Briza, and Consaul et al. (2010) for polyploid speciation in Puccinellia. For a phylogeny of Stipeae, see Romashchenko et al. (2008, 2010, 2011, 2012, 2014; Jacobs et al. 2008; Barkworth et al. 2008): Macrochloa may be sister to the rest of the tribe and there are parallel diversifications in the Old and New Worlds, so characters traditionally thought to be phylogenetically important appear not to be so. For New World Stipeae, see Ciadella et al. (2010: sampling) and for relationships within Nassella, to include Amelichloa, see Ciadella et al. (2014). A number of taxa show complex reticulating patterns of relationships; for those in Triticeae, see G. Petersen et al. (2006a), Mason-Gamer (2008), Sun and Komatsuda (2010) and Fan et al. (2013) and references. For the Anthoxanthum/Hierochloë (Phalarideae) problem, the resolution of which also depends on understanding patterns of hybridization, see Pimentel et al. (2013), while in Stipeae, Romaschenko et al. (2014) disentangled relationships in which old hybridization was again involved.
Classification. The Grass Phylogeny Working Group (2001: a few small taxa remained unplaced in subfamilies, 2011) outlined the basic classification of the family; there have been further changes in detail, but the main outline now seems clear. Watson and Dallwitz (1992b onwards) includes generic treatments, etc., and a more current account is to be found in Kellogg (2014).
Peterson et al. (2010) provide a detailed suprageneric classification of Chloridoideae (see also Columbus et al. 2010: Muhlenbergia; Peterson et al. 2012: Leptochloa and relatives, 2014: some Cynodonteae). Sánchez-Ken and Clark (2010) outline a tribal classification for Panicoideae s.l. (including Centothecoideae), while Morrone et al. (2012) provide a comprehensive classification of Paniceae and their immediate relatives. Setaria will have to be dismembered (Kellogg et al. 2009). Panicum itself is getting pulverized, perhaps rather too much (Lizarazu et al. 2014 and references); Panicum s.l. has about 500 species, s. str. ca 100 species, while Dicanthelium has about 55 species (Zuloaga et al. 2007). Cenchrus is to include Pennisetum (Chemisquy et al. 2010). Linder et al. (2010) offer a subfamilial classification of Danthonioideae; generic limits are difficult there and there has been some confusing hybridization (Pirie et al. 2009; Humphreys et al. 2010a).
For a suprageneric classification of Bambusoideae, see the Bamboo Phylogeny Group (2012a, b); generic limits are proving especially problematic here. For generic delimitation in the temperate bamboos, see Peng et al. (2008); the whole clade is descended from an allotetraploid ancestor, and, complicating the issue, there has been hybridization since (Triplett & Clark 2010; Triplett et al. 2011). There are also generic problems in Bambusoideae-Arundinarieae (Zeng et al. 2010) and -Bambuseae-Arthrostylidiinae (Tyrrell et al. 2009, 2012); Chusquea must include Neurolepis (Fisher et al. 2009).
Schneider et al. (2009) outlined tribal limits within Poöideae. For generic limits around Piptatherum, see Romaschenko et al. (2011). For a catalogue of New World Poöideae, see Soreng et al. (2003). Genera are certainly not monophyletic in Triticeae, but are based on different genome combinations that are (hopefully) correlated with morphological variation (Dewey 1984; Löve 1984); Barkworth (2000) summarised the history of the classification of this group (see also Goncharov 2011 for taxonomic confusion in Triticum; Fan et al. 2013 for Elymus s.l.).
Apparently the earliest name for Chloridoideae was Chondrosoideae Link (Thorne & Reveal 2007), a sort of resurrection name - Googling it (as of 3.vii.2007) returned only Thorne and Reveal themselves, apparently the only people to have used it for some time, and about 42,100 returns for Chloridoideae. However, the name Chloridoideae has since been used by Reveal himself (2012). Chondrosoideae was something of a false alarm, but priority is a very unhelpful tool in such situations (see also et al. 2014).
Given all the ongoing work in the family, web-based lists are much to be desired, so Grassworld, which has just started up, may be preferred over GrassBase and the lists dependent on it like the World Checklist of Monocots. The need is to stay current with all the changes that are being proposed; Vorontsova and Simon (2012) estimated that 10-20% of the species names will need to have been changed by the time all the phylogenetic rearrangements going on in the family are complete. The temptation is to chip off small monophyletic taxa from a paraphyletic residue; the temptation should be resisted, and synthesis will be needed.
Botanical Trivia. A typical sheep consumes more than 10 kg of silica phytoliths per year (Baker et al. 1959), yet this may affect its teeth very little (Sanson et al. 2007).
Thanks. I am very grateful to E. A. Kellogg for discussions about the evolution of this family.