EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, thalloid, with single-celled apical meristem, showing gravitropism; rhizoids +, unicellular; acquisition of phenylalanine lysase [PAL], phenylpropanoid metabolism [lignans +, flavonoids + (absorbtion of UV radiation)], xyloglucans +; plant poikilohydrous [protoplasm dessication tolerant], ectohydrous [free water outside plant physiologically important]; cuticle +; cell wall also with (1->3),(1->4)-ß-D-MLGs [Mixed-Linkage Glucans]; chloroplasts per cell, lacking pyrenoids; 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; blepharoplast, bicentriole pair develops de novo in spermatogenous cell, associated with basal bodies of cilia [= flagellum], multilayered structure [4 layers: L1, L4, tubules; L2, L3, short vertical lamellae] + spline [tubules from L1 encircling spermatid], basal body 200-250 nm long, associated with amorphous electron-dense material, microtubules in basal end lacking symmetry, stellate array of filaments in transition zone extended, axonemal cap 0 [microtubules disorganized at apex of cilium]; male gametes [spermatozoids] with a left-handed coil, cilia 2, lateral; oogamy; sporophyte dependent on gametophyte, multicellular, embryo initially surrounded by haploid gametophytic tissue, plane of first division horizontal [with respect to long axis of archegonium/embryo sac], early embryo spherical, developing towards the archegonial neck [from epibasal cell, exoscopic], with at least transient apical cell [?level], suspensor/foot +, cell walls with nacreous thickenings; sporangium +, single, terminal, 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 laid down in association with trilamellar layers [white-line centred lamellae], white-line centred lamellae increase in numbers; nuclear genome size <1.4 pg, main telomere sequence motif TTTAGGG, LEAFY and KNOX1 and KNOX2 genes present, precursor for starch synthesis in plastid, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes.
Many of the bolded characters in the characterization above are apomorphies of subsets of streptophytes along the lineage leading to the embryophytes, not apomorphies of crown-group embryophytes per se.
All groups below are crown groups, nearly all are extant. Characters mentioned are those of the immediate common ancestor of the group,  contains explanatory material, () features common in clade, exact status unclear.
Abscisic acid, ?D-methionine +; sporangium tapetum +, secreting sporopollenin, outer white-line centred lamellae obscured by sporopollenin, columella + [developing from endothecial cells], seta developing from basal meristem [between epibasal and hypobasal cells]; stomata +, on sporangium, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and in rhizoids/root hairs; spores trilete; polar transport of auxins and class 1 KNOX genes expressed in the sporangium alone; shoot meristem patterning gene families expressed; MIKC, MI*K*C* and class 1 and 2 KNOX genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns.
[Anthocerophyta + Polysporangiophyta]: archegonia embedded/sunken in the gametophyte; sporophyte long-lived, chlorophyllous; sporophyte-gametophyte junction interdigitate, sporophyte cells showing rhizoid-like behaviour.
Sporophyte branched, branching apical, dichotomous; vascular tissue +; stomata on stem; sporangia several, each opening independently; spore walls not multilamellate [?here].
EXTANT TRACHEOPHYTA / VASCULAR PLANTS
Photosynthetic red light response; plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; (condensed or nonhydrolyzable tannins/proanthocyanidins +); sporophyte soon independent, dominant, with basipetal polar auxin transport; lignins +; G- and S-type tracheids, sieve cells + [nucleus degenerating], tracheids +, in both protoxylem and metaxylem, plant endohydrous [physiologically important free water inside plant]; endodermis +; leaves spirally arranged, blades with mean venation density 1.8 mm/mm2 [to 5 mm/mm2]; sporangia not terminating the main axis, adaxial on sporophylls, derived from periclinal divisions of several epidermal cells, wall multilayered [eusporangium], lacking sporagia; columella 0; tapetum glandular; gametophytes exosporic, green, photosynthetic; basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; placenta with single layer of transfer cells in both sporophytic and gametophytic generations, root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Sporophyte branching ± indeterminate; endomycorrhizal associations + [with Glomeromycota]; root apex multicellular, root cap +, lateral roots +, endogenous; G-type 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; blepharoplasts +, paired, with electron-dense material, centrioles on periphery, male gametes multiciliate; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; LITTLE ZIPPER proteins.
Sporophyte woody; lateral root origin from the pericycle; branching lateral, meristems axillary; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].
Plants heterosporous; megasporangium surrounded by cupule [i.e. = unitegmic ovule, cupule = integument]; pollen lands on ovule; megaspore germination endosporic [female gametophyte initially retained on the plant].
EXTANT SEED PLANTS / SPERMATOPHYTA
Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins particularly with guaiacyl and p-hydroxyphenyl [G + H] units [sinapyl units uncommon, no Maüle reaction]; root stele with xylem and phloem originating on alternate radii, cork cambium deep seated; mitochondrial density in whole SAM 1.6-6.2[mean]/μm2 [interface-specific mitochondrial 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 +; cork cambium superficial; leaf nodes 1:1, a single trace leaving the vascular sympodium; stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; axillary buds +, exogenous; prophylls two, lateral; leaves with petiole and lamina, development basipetal, blade simple; plant heterosporous, sporangia borne on sporophylls, sporophylls spiral; microsporophylls aggregated in indeterminate cones/strobili; grains monosulcate, aperture in ana- position [distal], primexine + [involved in exine pattern formation with deposition of sporopollenin from tapetum there], exine and intine homogeneous, exine alveolar/honeycomb; megasporangium indehiscent; ovules with parietal tissue 2+ cells across, megaspore tetrad linear, functional megaspore single, chalazal, sporopollenin 0; gametophyte development initially endosporic, dependent on sporophyte, apical cell 0, rhizoids 0, development continuing outside the spore; male gametophyte with tube developing from distal end of grain, male gametes two, developing after pollination, with cell walls; female gametophyte initially syncytial, walls then surrounding individual nuclei; embryo cellular ab initio, plane of first cleavage of zygote transverse, shoot apex developing away from micropyle [i.e. away from archegonial neck; from hypobasal cell, endoscopic], suspensor +, short-minute, embryonic axis straight [shoot and root at opposite ends; plant allorhizic], cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, whole nuclear genome duplication [ζ - 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 trans- nad2i542g2 and coxIIi3 introns present.
ANGIOSPERMAE / MAGNOLIOPHYTA
Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANA grade?], lignin also with syringyl units common [G + S lignin, positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], hemicelluloses as xyloglucans; root apical meristem intermediate-open; 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, hypodermis suberised and with Casparian strip [= 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, secondary veins pinnate, fine venation hierarchical-reticulate, (1.7-)4.1(-5.7) mm/mm2, vein endings free; flowers perfect, pedicellate, ± haplomorphic; protogynous; 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], sporangium pairs dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, 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 lamellate only in the apertural regions, thin, compact, intine in apertural areas thick, pollenkitt +; nectary 0; carpels present, superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus at most short [shorter than ovary], hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry, extragynoecial compitum +; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across [crassinucellate], nucellar cap?; megasporocyte single, hypodermal, functional megaspore lacking cuticle; female gametophyte lacking chlorophyll, not photsynthesising, four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; ovule not increasing in size between pollination and fertilization; pollen grains land on stigma, bicellular at dispersal, mature male gametophyte tricellular, germinating in less than 3 hours, pollen tube elongated, unbranched, growing between cells, growth rate (20-)80-20,000 µm/hour, apex of pectins, wall with callose, lumen with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametes lacking cell walls, cilia 0, siphonogamy; double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; mature seed much larger than ovule when fertilized, small , dry [no sarcotesta], exotestal; endosperm +, cellular, development heteropolar [first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous; dark reversal Pfr → Pr; Arabidopsis-type telomeres [(TTTAGGG)n]; nuclear genome very small [1C = <1.4 pg, 1 pg = 109 base pairs], whole nuclear genome duplication [ε - 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, palaeo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]]; chloroplast chlB, -L, -N, trnP-GGG genes 0.
[NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]]: wood fibres +; axial parenchyma diffuse or diffuse-in-aggregates; pollen monosulcate [anasulcate], tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.
[AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood + [with gelatinous fibres: lignified primary cell wall + thick gelatinous wall]; 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 [extragynoecial compitum 0]; 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; stele oligo- to polyarch, medullated [with prominent pith], 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 and forming a fimbrial vein, transverse veinlets +, unbranched [leaf blade characters: ?level], vein/veinlet endings not free, margins entire, Vorläuferspitze +, base broad, ensheathing the stem, sheath open, petiole 0, 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; pollen reticulations coarse in the middle, finer at ends of grain, infratectal layer granular; G , with congenital intercarpellary fusion, opposite outer tepals [thus median member abaxial], placentation axile; ovule with outer integument often largely dermal in origin, parietal tissue 1 cell across; antipodal cells persistent, proliferating; fruit a loculicidal capsule; seed small to medium sized [mean = 1.5 mg], testal; embryo long, cylindrical, cotyledon 1, apparently terminal, with a closed sheath, unifacial [hyperphyllar], both assimilating and haustorial, plumule apparently lateral; primary root unbranched, not very well developed, stem-borne roots numerous, hypocotyl short, (collar rhizoids +); 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 cells [?level]; stomata anomocytic, (cuticular waxes as parallel platelets); colleters 0.
[[DIOSCOREALES + PANDANALES] [LILIALES [ASPARAGALES + COMMELINIDS]]]: nucellar cap 0; endosperm nuclear [but variation in most orders].
[LILIALES [ASPARAGALES + COMMELINIDS]]: (inflorescence branches cymose); protandry common.
[ASPARAGALES + COMMELINIDS]: style long.
Unlignified cell walls fluorescing blue under UV, green with NH3 [ferulic acid ester-linked]; exodermal cells monomorphic; (vessels in stem and leaves); SiO2 bodies +, in leaf bundle sheaths; stomata para- or tetracytic, (cuticular waxes as aggregated rodlets [looking like a scallop of butter]); inflorescence branches determinate, peduncle bracteate; P = K + C, bicyclic [stamens adnate to/inside corolla/inner whorl only]; pollen starchy; embryo short, broad.
[POALES [COMMELINALES + ZINGIBERALES]]: primary cell wall mostly with glucurono-arabinoxylans; stomata subsidiary cells with parallel cell divisions; endosperm reserves starchy.
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) and ca 88.8 m.y. in Tank et al. (2015: Table S2); Magallón and Castillo (2009) suggest an age of 123 to 111 m.y. and Wikström et al. (2001) again a younger age of (91-)87, 83(-79) m.y. ago. 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; 111-88 m.y. in Mennes et al. 2015), (126-)117, 109(-103) m.y. in Hertweck et al. (2015), and around 142 m.y., the highest, 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).
Genes & Genomes. The rate of molecular evolution in the plastome is high (with some notable exceptions) in this whole clade (Barrett et al. 2015).
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.
Phylogeny. For discussion of the relationships of Poales, see the Arecales page.
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 [succinate dehydrogenase 3] gene lost. - 15 families, 997 genera, 18,875 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., Bell et al. (2010) ages of (103-)93, 85(-73) m.y.a., while ca 101 m.y.a. is the estimate in Magallón et al. (2015); 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. and 104-82 m.y. in Mennes et al. (2013, 2015 respectively), while those in Hertweck et al. (2015) are (122-)113(-109) or (105-)99(-94) m.y. old.
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: (....) denotes a feature common in the clade, exact status uncertain, [....] includes explanatory material. 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 are the not-so-trivial issues of how character states are delimited and ancestral states are reconstructed (see above).
Evolution. Divergence & Distribution. Magallón and Castillo (2009) suggest that Poales have the highest diversification rates 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; bamboo wood is particularly slow to decompose (G. Liu et al. 2015). 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, noted for the larvae being able to live under water, 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 (γ proteobacteria-Enterobacteriaceae - near Burkholderia) which are believed to produce the material that makes up the cocoon that characterises this beetle clade, which is also .
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 [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, 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 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]: root hairs from unmodified rhizodermal cells; 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 date of these two families is about 75.9 m.y.a. (Magallón et al. 2015) or about 85.5. m.y. (Tank et al. 2015: Table S2) - 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) and Isles et al. (2015). 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). Since fossil Sparganium may have up to 7-locular fruits (Cook & Nicholls 1986), 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; chromosomes 3> µm long.
57[list]/3,350 - 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; n = ?
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; n = 25.
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 (tank-forming) epiphytes, roots often for attachment only (0); (CAM photosynthesis +); 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, 24 [quite common]).
9/1,335: 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.
1/66. 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
(CAM photosynthesis +); 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; (n = 24), (karyotype bimodal); hypocotyl quite long, cotyledonary hypophyll blade-like, (collar rhizoids - Pitcairnia).
5/632: Pitcairnia (450), Dyckia (160), 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; (CAM photosynthesis +); 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).
1/220. Especially mountains, 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 often serrate; (perianth tube/hypanthium +), (K asymmetric), (C with adaxial subbasal petal appendages); (pollen 2-polyporate), (inaperturate), (with raphides); G inferior, ovules with appendage at chalazal end (0), (micropyle also bistomal), (outer integument to 4 cells across), (nucellar epidermal cells not elongated anticlinally), parietal tissue 1-4 cells across; fruit baccate; seed without an appendage; sarcotesta [gelatinous] common; embryo lateral; (n = 16, 17 [quite common], 21, 22); (cotyledon not photosynthetic), collar rhizoids +, primary root prominent, short hypocotyl present; (n = 17).
31/722: "Aechmea" (275), 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. Most diversification within Bromeliaceae 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 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.o., crown ca 19 m.y.o.), so presumably there has been at least some 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). Diversification of the Andean Puya seems to have begun in Peru (along with other early branches of Bromelioideae), and then following the Andean orogeny north (Schmidt Jabaily & Sytsma 2010, esp. 2013; Madriñán et al. 2013); it has occurred within the last ten m.y. or so (Givnish et al. 2010). 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).
it is thought that the ancestor of Pitcairnia feliciana moved to Africa by long distance dispersal perhaps 12-9.3 m.y.a. (Givnish et al. 2008, 2011).
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); geography and other factors can be added to the mix and localised to the appropriate part of the tree (Bouchenak-Khelladi et al. 2015; Donoghue & Sanderson 2015). Givnish et al. (2013) thought that extensive speciation depended on the evolution of ecological traits such as the adoption of the epiphytic habitat, the evolution of CAM in arid environments, or adaptations to understory life in forests, with subsequent geographic spread and radiation into different areas and environments. Features like bird pollination were probably not major drivers of speciation here.
Brocchinia, a small genus restricted to the Roraima region, includes different growth forms - tank plants and true terrestrials - and takes up nitrogen in different ways. Of the tank plants, B. reducta may acquire nitrogen through carnivory (see below), while the terrestrial B. acuminata is an ant plant. Givnish et al. (1997) discussed the radiation of the genus, which seems to have begun only ca 14 m.y.a. although, compared with other younger bromeliad clades this is hardly a very diverse=species-rich clade (Givnish et al. 2004a, 2008, 2011a; Givnish 2015b).
Ecology & Physiology. The ecological preferences of basal Bromeliaceae (and Typhaceae) are for wet and nutrient-poor conditions, and in Bromeliaceae this means conditions such as occur on the tepuis and surrounding areas of the Guiana shield (Crayn et al. 2015).
CAM photosynthesis has evolved some five times or more (there is phylogenetic uncertainty in Puyoideae and Bromelioideae). The number of CAM species decreases with altitude, although that of C3 reaches a maximum at around 2000 m, however, some CAM Puya grow at over 4000 m (Crayn et al. 2015). 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; Ming et al. 2015: parallelism understandable at the molecular level). 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) and seedlings of Ananas, at least, CAM when adult, are C3 plants (J. Zhang et al. 2014).
The diversity of growth form in Bromeliaceae is well known. Many taxa are terrestrial and have a well-developed root system. However, about 1,780 species (rather over half the family, ca 7% of all epiphytes) are epiphytic, and are especially common in montane habitats (Benzing 1990 for much discussion; Luther & Norton 2008: epilithic species not included). Tank and air epiphytes, along with the terrestrial species, make up the three main growth forms in the family, and the multicellular hairs on the leaf surface are integral to the ecology of these different growth forms. (Of course, tank bromeliads may be terrestrial, but they can be distinguished from terrestrial species by their overlapping, tank-forming leaves.)
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).
Perhaps somewhat paradoxically, adaxial leaf surfaces in Bromelioideae and some other subfamilies are hydrophilic while abaxial surfaces are hydrophobic (Reuter & Brown 2009; see also Fagaceae). 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).
Air epiphytes are common in Tillandsioideae, in some species roots are for attachment only, others have no roots. Tillandsioideae have rather elegant multicellular peltate trichomes that take in water and nutrients (see Mez 1904 for detailed early studies). Adult plants of species like Tillandsa usneoides (Spanish moss) lack roots, 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. In the hyperarid lomas of coastal Chile and Peru, bromeliads, especially Tillandisa, can dominate. They have the most biomass of any bromeliad community in the world, and practically no other angiosperms can stand conditions there (Rundel & Dillon 1998). The scales flex as they dry and so pull away from the leaf surface, but when there is fog or 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. This absorbtion is a two-step process. Thus on wetting the rosette-forming T. ionantha water is taken within minutes into the cells of the scales by capillary action, moving into the body of the leaf by the aid of aquaporins, proteins in plant cells walls, over the next three hours or so (Ohrui et al. 2007). It has also been suggested that the dry, white scales in Tillandsia may reflect light and so provide photoprotection (Pierce 2008); see also Orchidaceae for UV light and epiphytism.
Reyes-García et al. et al. (2014) compared water uptake in CAM tank, succulent air and non-succulent air epiphytes in Tillandisa; the non-succulent air epiphytes like T. usneoides, etc., caught water from fog while the tank epiphytes relied on water stored in their tanks, their stomata closing when it was used up. The rootless T. latifolia and T. purpurea are quite happy lying around in the full sun in Peruvian deserts (McWilliams 1974).
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 the former may even be a Müllerian mimic of the latter (Joel 1988).
Pollination Biology & Seed Dispersal. Perhaps 1,060-1,300 species of Bromeliaceae are pollinated by humming birds, and they are commonest at higher altitudes in the Andes, less common in 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). Only a few species of humming birds are the major bromeliad pollinators in southeastern Brazil (Snow & Snow 1986; Sazima et al. 1996; Placentini & Varassin 2007). It is odd that there appears to be no prezygotic reproductive isolation between sympatric bromeliads there; the flowers are not notably different morphologically and flowering times overlap extensively, yet hybrids are very uncommon (Wendt et al. 2008) as they are in the family as a whole. 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. Friar birds (Euphoniinae, near Fringillidae), mistletoe specialists, also eat the fruits of epophytic Bromeliaceae-Bromelioideae (Snow 1981; Restrepo 1987). 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). Tthe 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).
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 fleshy fruits, which also initially develop under water, are raised above the surface by the elongation of their pedicels.
Plant-Animal Interactions. Caterpillars of Nymphalinae-Riodininae eat Bromeliaceae (and Orchidaceae: Hall 2003 and references). Some epiphytic Bromeliaceae are more or less closely associated with ants, 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 that live in the tanks (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., even lower than in palms; although the family is not particularly woody, its members have a long generation time, which may be connected with this low rate (Smith & Donoghue 2008). However, the rate of evolution in the plastid genome of Typhaceae is also rather low Bennett et al. 2015), so this may be a feature of this whole clade.
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. Gitaí et al. (2014) suggest that the base chromosome number is 25, although that number is not known from Brocchinia; they also give details about genome size and chromosome length (Tillandsioideae tend to have longer chromosomes that do other subfamilies).
Chemistry, Morphology, etc. In at least some species that do develop roots, the radicle of the embryo aborts (Fiordi Cecchi et al. 1996; Magalhães & Mariath 2012).
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) did not record this, but illustrations suggest there can be at least 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 variation in the chalazal appendage.
For general information, see Varadarajan and Gilmartin (1988b), Rauh (1990: cultivated bromeliads), Smith and Till (1998) and Benzing (2000), and for additional information on phytoliths, see Piperno (2006), on rhizome and root anatomy, see Proença and Sajo (2008), on leaf anatomy of Pitcairnioideae, see Santos-Silva et al. (2013), on petal appendages, see Brown and Terry (1992), for microsporogenesis, esp. callose deposition, see Albert et al. (2014), for tetraporate pollen of Hohenbergia, see Albert et al. (2011), for stigma morphology, see Brown and Gilmartin (1989), for ovules, Sajo et al. (2004a), Fagundes and Mariath (2014: summary table) and Noguiera et al. (2015), for fruit anatomy, see Fagundes and Mariath (2010), for seed anatomy, Szidat (1922), Rohweder (1956), Gross (1988a) and Varadarajan and Gilmartin (1988a), for germination, Gross (1988b), and for chromosomal evolution, see Gitaí et al. (2005).
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); see also Escobedo-Sarti et al. (2013). 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. For other phylogenetic studies, see Crayn et al. (2000), and Givnish et al. (2004b: ndhF). In general, the very low rate of evolution in the markers used and in many "generic"-level studies the relatively recent divergence times has made disentangling relationships difficult.
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. Dyckia was monophyletic, but its internal relationships showed little resolution, and Encholirium was paraphyletic at its base (Krapp et al. 2014). A morphological analysis of Pitcairnia yielded little resolution of relationships (Saraiva et al. 2015).
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. Indeed, Evans et al. (2015) emphasize the variety of topologies obtained for the basal branchings in this clade obtained in earlier work. They find some support for the topology [Ochagavia et al. [Bromelia + The Rest]]; within The Rest there is some support for a Bilbergia-nidularoid clade and rather more for a Hohenbergia-Orthophytum clade, but overall relationships are still very much pectinate, with Aechmea being everywhere, even in the two clades just mentioned. In a study focussing on the Aechmea alliance, it, Canistrum and Portea were all polyphyletic (Heller et al. 2015). For relationships within Forsterella, see Rex et al. (2009 and references) and within Ronnbergia, see Aguirre-Santoro et al. (2015: polyphyletic). Bromelioideae with tanks also often have flowers with asymmetric sepals and porate pollen (Schulte & Zizka 2008; Schulte et al. 2009).
Given the poor support for many relationships, morphological analyses are being attempted, as by Donadí et al. (2015).
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. Escobedo-Sarti et al. (2013) estimated that only 14/58 of the genera with two or more species that they included in their analysis were monophyletic. Puya may be paraphyletic (Givnish et al. 2011a). Within Bromelioideae, Aechmea is hopelessly poly/paraphyletic (Schulte et al. 2009; Sass & Specht 2010; Evans et al. 2015) and generic limits in the subfamily are in general unclear (Horres et al. 2008; Evans et al. 2015).
[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., in Tank et al. (2015: Table S2) around 84.2 m.y.a., and in Magallón et al. (2015) ca 97.6 m.y. ago.
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.
The embryo is usually small, little differentiated and rather broad (but c.f. Cyperaceae, Poaceae). Thus Malcomber et al. (2006) described the embryo of Joinvilleaceae and Ecdeicoleaceae as being undifferentiated, embryos of Restionaceae-Centrolepidoideae also seem to be undifferentiated (Hamann 1975), those of other 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).
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
Supernumerary axillary buds +; involucral bracts long; middle layer of anther persistent; septal nectaries 0; ovule 1/carpel, ± basal; seeds ovoid-oblongoid, (with papillate apical appendage); n = ?
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; n = ?
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).Schoenocephalieae: (flower monosymmetric); C shorter than K (longer - Kunhartia); bracts enclose infloresecence
3. Saxofridericioideae Maguire
(Leaves petiolate - Saxofridericieae), (unifacial), (sheath with auricles - Stegolepis); septal nectaries 0, intra-ovarian trichomes +; ovules few-many/carpel; (bracts enclose infructescence); seeds prismatic, pyramidal, lenticular or crescent-shaped; n = ?
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).
Ecology & Physiology. Rapateaceae often grown on poor/waterlogged soil, white sand, or similar habitats (Stevenson et al. 998a).
Chemistry, Morphology, etc. In Spathanthus the inflorescence is adnate to the sigle large inflorescence bract that develops, with inSaxfridericia the inflorescence bracts are connate and the 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: general); for anatomy, see Carlquist (1966) and Ferrari et al. (2014: leaf and peduncle); 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-MLGs [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) and ca 93.8 m.y.a. by Magallón et al. (2015).
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). An extimated 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.
Age. The age of this clade is around 86.2 m.y.a. (Magallón et al. 2015).
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 protoxylem 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; tapetal cells uni-/binucleate; ovules straight, micropyle endostomal; parietal tissue 0, hypostase +; seed operculate; endotegmen tanniniferous/resiniferous; suspensor + [?level].
Evolution. Divergence and Distribution. Oriani and Scatena (2014) evaluated variation in many floral characters in the context of a clade [Mayacaceae [Eriocaulaceae + Xyridaceae]]; see also Nardi et al. (2015). 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.? Getting the phylogeny straight is also crucial...
[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; anther wall development of the monocot type, 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; seed endotestal, cuticular layer between testa and tegmen.
Age. Eriocaulaceae and Xyridaceae may have diverged ca 105 m.y.a. (Janssen & Bremer 2004) or about 77.1 m.y.a. (Magallón et al. 2015).
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, 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, Morphology, 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 are differently thickened (see below).
ERIOCAULACEAE Martinov, nom. cons. Back to Poales
Root cortex aerenchymatous, with continuous pericycle; (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; microsporocytes in a single row in each loculus; pollen spiraperturate; carpellate flowers: placentation axile; ovules 1/carpel, pendulous; antipodal cyst + [formed by fusion of antipodal cells]; fruit (indehiscent), K/C persistent; operculum tegmic; endotesta thickened on (anticlinal and) inner periclinal walls; 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).
1. Eriocauloideae Burnett
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.
1-2/420: Eriocaulon (400). Pantropical (to Temperate).
2. Paepalanthoideae Ruhland
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; bisporangiate, monothecal); pistillode +, nectariferous, (styluli separate); carpellate flowers: (K valvate), (C free); staminodes +; gynoecial primordium initially 3-lobed, ovule exposed, (carinal stylar appendages very small), (styles branched ± to the base); seeds exo/endotestal, the anticlinal walls with prominent rib-type thickenings, the outer periclinal wall breaking down and exposing the fuzzy-looking thickenings, (seed exotestal - Leiothrix).
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. Infloresences can be very long-lived (up to a year), and there is synchronization in the opening of the flowers so that all open flowers on a head are staminate or carpellate (see Stützel 1998 for a summary). Although the flowers of Eriocaulaceae are individually rather small and inconspicuous, pollination seems to be by insects. Eriocaulaceae are the Asteraceae of the monocots with their capitate inflorescences and tiny flowers that nevertheless show a great deal of variation. The dark-colored glands on the petals of Eriocaulon may produce nectar (Stützel 1985b; Hensold 1988). 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 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 short and not twisted; 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 distinction between staminate and carpellate flowers becomes apparent only late in development, and Wurdackia (= Rondonanthus) flabelliformis has perfect flowers (Stützel 1985b). The flowers of Eriocaulaceae are tiny, yet show a great deal of variation in meristicity, tepal texture, connation 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 (1985a) found that the morphologically apical glands on the petals of Eriocaulon were displaced by an abaxial outgrowth of tissue and became adaxial-subapical. The tetrasporangate anthers are described as being extrorse (Ike 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 (Ike 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 [Syngonanthus [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; 2k [lateral] persistent in fruit; operculum testal and tegmic; endosperm helobial [chalazal chamber smaller, nuclear divisions only]; 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).
1. Xyridoideae Arnott
(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, moniliform hairs on branch ends (hairs 0); anther wall development of the reduced type; 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 bistomal, funicle long, hypostase 0; (embryo sac bisporic, 8-celled [Allium type]); 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.]
2. Abolbodoideae Reveal
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); tapetum multilayered, plasmodial, microsporocytes as single row; pollen binucleate, spherical, inaperturate, (surface with large and small clavate projections), 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; 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), and de Oliveira (2015), 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), Winzieher (1914), Govindappa (1955), especially Nardi et al. (2015), Remizowa et al. (2012a), all Xyris, and Oriani and Scatena (2011, 2015: Abolbodoideae), all floral morphology, etc..
Phylogeny. Xyridaceae may appear not to 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) or about 77.2 m.y.a. (Magallón et al. 2015).
MAYACACEAE Kunth Back to Poales
Marsh plants; plant ?monopodial; lateral roots originate opposite the phloem; vessels in leaves 0; stem with endodermis, vascular bundles often 3; stomatal subsidiary cells with intersecting oblique divisions; leaves scattered along the stem, amphistomatic, 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 surface reticulate; placentation parietal, style with dorsal and ventral carpellary bundles, stigmatic lobes small; ovules 2-30/carpel, obturator +; exotestal cells with 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).
Tomlinson (1969) described the flowers as being terminal, although evicted into an exillary position by the growth of an axillary shoot, but the flowers seem to be axillary and associated with a broad, adaxial prophyll-like structure. Given the possible association of Mayacaceae with families that have scapose inflorescences 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). Venturelli and Bouman (1986) thought that the seeds lacked an operculum, despite some reports to the contrary, and they drew developing seeds with large-celled nucellar tissue towards the base.
Some information is taken from Thieret (1975), Stevenson (1998) and Oriani and Scatena (2012), all general, Tomlinson (1969, 1974: anatomy), 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 holocentric; 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. Although holocentric chromosomes (= diffuse centromeres) are an apomorphy for the clade, only in Carex is there also considerable variation in chromosome number (Roalson et al. 2008; Hipp et al. 2009 for chromosome evolution). Indeed, localized centromeres have been reported in (?some) Scirpus (Nijalingappa 1974).
Smarda et al. (2014) noted that the genome of this group had a very low GC content as well as being very small, contrasting with Xyris (Xyridaceae) and Poaceae. 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. The relationships [Thurniaceae [Juncaceae + Cyperaceae]] have 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 blade margin serrate, 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), ?parietal tissue; seeds arillate; testa of sclerenchymatous fibres and unthickened cells, (short hairs - Thurnia), tegmen tanniniferous; ?embryo; 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; flowers protogynous; parietal tissue +; embryo well differentiated, plumule lateral; 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), around 86.2 m.y.a. (Escudero et al. 2012b), ca 90.6 m.y. (Escudero & Hipp 2013), about 55.2 m.y. (Magallón et al. 2015) and an 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 seem to be infrequent (but c.f. some Cyperaceae), although 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.
Entorrhiza forms root galls on Juncaceae and Cyperaceae world-wide; it has recently been described as a new fungal phylum perhaps sister to dikarya or basiomycetes (Bauer et al. 2015).
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 and its relationships 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 (hairs + - 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 often myrmecochorous (Lengyel et al. 2010), and myxospermy is also reported from here, and from Juncus (Western 2012).
Vegetative Variation. Yamaguchi et al. (2010) show how the terete and laterally flattened leaves in Juncus are fundamentally similar, being abaxialized, laterally-flattened leaves also expressing the DL gene that is responsible for "midrib" formation in normal bifacial monocot leaves - indeed, species with terete and those with laterally-flattened leaves can cross. For unifacial leaves, see also Yamaguchi and Tsukaya (2010) and Nakayama et al. (2013).
Genes & Genomes. In Luzula, at least, events in meiosis are reversed, homologous non-sister chromatids initially being held together by chromatic threads and separating only in anaphase II (Heckmann et al. 2014).
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] +, Si02 accumulation common; (also thick-walled sieve elements); stems solid, angled; chlorenchyma cells lobed; stomatal guard cells dumbbell 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]/5680. 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. (2012b) 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).
The fossil Volkeria messelensis, some 47 m.y.o., has been placed as stem group Mapanioideae so would provide a minimum age for this node (Isles et al. 2015).
1. Mapanioideae C. B. Clarke
SiO2 bodies wedge- or bridge-shaped, also conical?; leaves with petiole + blade, transverse veins often prominent; 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. 2012b); another estimate is (67-)49.2(-33.5) m.y. (Escudero & Hipp 2013).
Synonymy: Mapaniaceae Shipunov
2. Cyperoideae Beilschmied
Fine roots dauciform; (velamen +); SiO2 bodies smooth, conical, with pointed apices, attached to cell walls; 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>/5500: Carex (2000), Cyperus (950), Fimbristylis (250), Rhynchospora (250), Scirpus (200), Scleria (200), Eleocharis (120), Bulbostylis (100), Schoenus (100), Lepidosperma (75 - to 200<), Isolepis (70), Kobresia (60), Schoenoplectiella (50). Worldwide, but esp. N. Temperate.
Age. Diversification within Cyperoideae is estimated to have begun ca 77 m.y.a. (Escudero et al. 2012b) 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), while Bouchenak-Khelladi et al. (2015) found an increase in diversification rate in Cyperoideae and again in Cypereae, the latter, they thought, being triggered by the appearance of C4 photosynthesis.
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; see also Friis et al. 2011 for references).
Viljoen et al. (2013) looked at biogeographical relationships in their Schoeneae, where there was much trans-oceanic dispersal.
Escudero et al. (2012b) suggest that crown group Carex is around (54.9-)42.2(-29.7) m.y. old. Major diversification in the genus, which began 8-20 m.y. later, was somewhat linked to decreasing temperatures which were especially marked ca 34 m.y.a. at the end-Eocene. However, given the age of the clade, overall diversification rates were not particularly high (Escudero et al. 2012b). 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. 2012a), it is unclear why these rearrangements should affect the success of the genus (see also below). Divergence within Eleocharis occurred ca 20 m.y.a. (Besnard et al. 2009b).
Ecology & Physiology. Despite their diversity and their abundance in many ecosystems, rather little is known about the ecology of the family (Barrett 2013). Cyperaceae are often particularly common in wet tundra habitats (ca 8% of the earth's land surface), and Eriophorum and Carex are two of the seven major contributors to the biomass there (Chapin & Körner 1995), the other five being core eudicots with ecto- or ericoid mycorrhizae. Carex, with over 90 species, is the biggest genus in the Arctic, although not so much in the far north (Elven et al. 2011), and other genera of the family are prominent there. Cyperaceae-dominated communities were notably extensive during the last glacial maximum north of 550 N (Bigelow et al. 2003). Even today there are about 140 species in the Arctic, although few grow in the high Arctic; the parallel adoption of this habitat in sections Phacocystis and Vesicaria is discussed by Gebauer et al. 2014). Similarly, about 16% of all species growing in Quebec and Labrador north of 54o N are Cyperaceae (Poaceae are next at 11%), and 13% belong to Carex, and they they can be major components of plant cover especially in wetter habitats such as rich fens (Cayouette 2008; Escudero et al. 2012b).
Although the primary productivity of such communities can be relatively high, they may sequester less carbon than Sphagnum-dominated communities in poor fens (Flanagan 2014). Newsham et al. (2009, but c.f. Iversen et al. 2014) noted the frequency of arbuscular mycorrhizae in polar Cyperaceae. The roots of cyperaceous plants may penetrate into the mineral soil below the shallow layer of soil dominated by the roots of the ericoid and ectomycorrhizal members of the community (Read 1993; Iversen et al. 2014 for references), although in general the soil is often quite shallow. Eriophorum roots are notably short-lived - 1-2 years, versus >5 years for other plants (Iversen et al. 2014). Dark septate hyphae are known from Cyperaceae, and if the hyphae are dark because they have fungal melanin, this could have implications for carbon cycling (c.f. Clemmensen et al. 2014).
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 (= Carex parvula) (Miehe et al. 2008). 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). Other species of Kobresia, now to be placed in the Core Unispicate Clade of Carex (Global Carex Group 2015) in Tibet, Europe, Greenland and other high latitude areas are also ectomycorrhizal and may dominate the vegetation (e.g. Gardes & Dahlberg 1996; Muhlmann & Peintner 2008; Newsham et al. 2009 and references; Gao & Yang 2010).
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 look rather carrot-shaped; these may facilitate phosphorus uptake by the plant when growing in phosphorus-poor soils (Shane et al. 2005: some Juncaceae also have such roots; Lambers et al. 2008; Playsted et al. 2006), and these plants may be ectomycorrhizal (Gao & Yang 2010). 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). Many, but not all, tundra-dwelling Cyperaceae, whatever their mycorrhizal status, take up nitrogen predominantly in an organic form (Raab et al. 1996, 1999), although Carex seems to prefer NO3-, and that genus has high rates of P uptake, as do other Cyperaceae, although to a lesser extent (Iversen et al. 2014).
About 1,500 species of Cyperaceae carry out C4 photosynthesis, and this has perhaps six origins in the family and with some reversals to C3 (Soros & Bruhl 2000; Besnard et al. 2009b; Bruhl & Wilson 2008; Roalson 2011; Larridon et al. 2011a; Sage et al. 2012). 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). C4 Cyperaceae quite often grow in wet, fertile conditions, rather unlike many other C4 plants (Christin & Osborne 2014), and in some Cyperaceae with submerged leaves C4 photosynthesis may help increase nitrogen use efficiency (Besnard et al. 2009b; Bruhl & Wilson 2008; Roalson 2011).
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) and animals (both epi- and endozoochory), and ants and attracted by elaiosomes with a variety of morphologies (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; caterpillars of Satyrini (Hamm & Fordyce 2015) and the [Heteropterinae-Trapezetinae-Hesperiinae] clade of skippers (Warren et al. 2009) feed on Cyperaceae - and also Poaceae, of course.
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). Ectomycorrhizae are common in Kobresia (= Carex, see above: Gardes & Dahlberg 1996; Muhlmann & Peintner 2008; 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 ectomycorrhizae 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). Escudero (2015) found that diversification of Anthracoidea on Carex was largely the restult of speciation after shifting hosts, these shifts often being to species that were quite closely related to the original hosts.
Genes & Genomes. Carex is notable for the great variation in chromosome numbers that it shows - n = 6-62, the result of of extensive chromosome fission, fusion and translocation facilitated by the diffuse centromeres of the family (Hipp et al. 2011). The Carex Siderostictae clade, sister to all other Carex, lacks these rearrangements, and has large and few chromosomes, polyploidy - and includes only a few species (Escudero et al. 2012a). Genome size is little affected by chromosome number change, indeed, the two are negatively correlated in diploid taxa, and although polyploids tend to have larger genomes than related diploids, they do not have absolutely large genomes (Chung et al. 2012; Lipnerová et al. 2013). High chromosome number may promote recombination, and there is some correlation between high chromosome number and stable habitats, perhaps facilitating evolutionary innovation, and there are complex patterns of hybrid dysfunction and non-Mendelian segregation (Escudero et al. 2012a, 2015). 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. Vegetative variation is quite extensive, with a variety of more or less unifacial morphologies to be found in the family (Metcalfe 1969; c.f. in part Fisher 1971). Some species of non-mycorrhizal Carex have distinctive, bulbous-based root hairs (Miller et al. 1999).
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. X. 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 conventional monocot 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 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). Parietal tissue in some Bulbostylis ovules may be only a single cell across (Maria & López 2010).
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; 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 thatLuzula and many Poaceae have a similar gynoecium, so where it will end up on the tree is unclear.
For a vast amount of additional information, see Bruhl (1995); other general information is in Naczi and Ford (2008). For anatomy, see Cutler (1969 and references), 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 inflorescences in Carex, see the Global Carex Group (2015), for floral morphology, see Bruhl (1991) and Vrijdaghs et al. (2006), for pollen, see van Wichelen et al. (1999), Nagels et al. (2009), Ike 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 Ike Coan et al. (2008), for embryo morphology, see van der Veken (1965: hundreds of species) and Schneider (1932: also germination), and for the cytology of Kobresia, see Seeber et al. (2014).
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, relationships are still rather unclear. 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). In another study, 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. Fuireneae are also paraphyletic, although most are in Cypereae (Monfils et al. 2014). Léveillé-Bourret et al. (2014, 2015) found a quite well supported but paraphyletic Scirpeae that included Cariceae, although internal relationships were not well supported. Dulicheae may be sister to this clade, and the odd Khaosokia is also somewhere around here. The limits of Scirpus were adjusted by Léveillé-Bourret et al. (2015), although Eriophorum remains embedded in Scirpus s. str..
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 X. 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). Within Scirpeae, Eriophorum is embedded in Scirpus (Léveillé-Bourret et al. 2014).
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, 2015). Carex is paraphyletic, as has been demonstrated by several studies (see Yen & Olmstead 2000; Starr et al. 1999, 2004, 2015; 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.], and Carex is being expanded to cope. However, details of the relationships of Carex s.l. are unclear (Hinchcliff & Roalson 2013), although as more taxa from east and southeast Asia are being addeed, things are becoming more clear (Starr et al. 2015). Sectional limits can be severely awry, as in Carex section Racemosae (Gebauer et al. 2015). 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), while vicariance/long distance dispersal patterns in Carex section Racemosae are the result of homoplasy (Gebauer et al. 2015). Relationships are [[sect. Hypolytroides + Siderostictae] [Schoenoxiphium [core unispicate clade (inc. Kobresia) [Vignea clade [dissitiflora clade + core Carex]]]]] (Starr et al. 2015). Evolution is not necessarily complex → simple (see also the Global Carex Group 2015), and the variation in the taxa of these basal pectinations is very considerable, some being insect-pollinated, or with branch prophylls causing the inflorescence branches to spread (c.f. lodicules), or with broad petiolate leaf blades, etc. (Starr et al. 2015).
Naczi (2009) discussed the use of morphological characters in phylogenetic analyses. This is tricky because the highly derived/reduced nature of cyperaceous flowers 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); the Global Carex Group (2015) has formalized the extension of the genus. 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). Understanding the limits of Scirpus is difficult (Léveillé-Bourret et al. 2015). 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.
[Restionaceae [Flagellariaceae [[Joinvilleaceae + Ecdeiocoleaceae] Poaceae]]] / graminid clade: flavones +; primary cell walls with (1-3,1-4)-β-D glucans [?level]; root trichoblasts closest to apical meristem; 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, receptive cells on multicellular branches; 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.a., while around 80.8 m.y.a. is the age in Magallón et al. (2015).
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 below.
Chemistry, Morphology, etc. For the flavonoids of 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 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.
Classification. This is the old Poales s. str.
[Anarthriaceae + Restionaceae]: sand-binding roots + ["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 usu. much reduced, ± 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), ca 80 m.y. (Litsios et al. 2014: "root" age for Restionaceae, Centrolepis, etc., not included), or about 75.9 m.y.a. (Magallón et al. 2015).
The 27.7 m.y.o. fossil Restiocarpum latericum was assigned to this node (Isles et al. 2015).
Evolution. Ecology & Physiology. Most members of this clade flourish on nutrient-poor soils (or in bogs or similar places), 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; initially, at least, these roots facilitate the uptake of water and nutrients, and even when dead the persistent sheath helps ensure the functioning of the vascular tissue (Shane et al. 2011). There are other distinctive root morphologies like cluster/proteoid roots in this clade (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. Meney et al. 91993) mention a few examples of vesicular arbuscular mycorrhizal associations.
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
(Vesicular arbuscular mycorrhizae +); (flavonol glycosides +); SiO2 0; stomata in grooves; leaves ligulate, (isobifacial); culm branched or not; staminate flowers: pollen operculate [exine inside annulus]; carpellate flowers: G opposite outer P; ovules?, hypostase +; (pollen grains in embryo sac); seed coat?; endosperm type?, embryo?; ?collar rhizoids; n = 6, 9, 11, chromosomes 1.7-7µm long; 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. 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).
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?
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); (leaf sheath closed); 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; chromosomes 0.7-2.4 µm long; 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; 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 extending all or part way through chlorenchyma and alternating with vascular bundles ["ribs"] (0), 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 elaiosome [fleshy pedicel]; 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 +; pollen pore not annulate, 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; flowers solitary and with bracteoles, (spikelets +).
3/31: Lepyrodia (22). Australia and New Zealand.
[Centrolepidoideae + Leptocarpoideae]: (parietal tissue 1 cell across).
3. Centrolepidoideae Burnett
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; (plane of distichy of vegetative branches transverse to the main axis; prophyll lateral); leaf blades well developed, rounded-unifacial, (ligulate); inflorescence scapose, capitate and with inflorescence bracts, or spicate, branches 2-ranked; plant monoecious; (bracts 0); (T 0-3, lacking vascular traces); A (1-2); G [1-14(-45)], styles separate, adaxially channeled; 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
(Vesicular arbuscular mycorrhizae +); flavones, sulphated flavonoids, (8-hydroxyflavonoids, e.g. gossypetin) +; chlorenchyma interrupted by pillar cells [radiating ± lignified cells of chlorenchyma, from epidermis to sclerenchymatous sheath] (0), (sclerenchymatous bundle girders opposite outer vascular bundles +); substomatal 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 (including Centrolepidoideae) from the northern hemisphere from sites in both the Old and New Worlds (Muller 1984), but the identity of these grains has been questioned (Linder 1987).
Although adult plants of Centrolepidoideae may have terete leaves, young seedlings of the clade of Restionaceae in which Centrolepidoideae are embedded also have terete leaves. Centrolepidoideae may be paedomorphic, the plant being reproductively mature while in a juvenile stage, i.e. progenetic (see also Briggs et al. 2014 and references). Sokoloff et al. (2015a) place the extensive vegetative and floral variation in this bizarre little clade in a phylogenetic context; Centrolepis racemosa is highly derived.
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, seeders, reproduce by seeds (c.f. Ericaceae). Overall diversification of seeders in southern Africa is greater than that in Australia, perhaps in response to the greater climatic heterogeneity of the former, however, there are numerous sprouter species because of the frequency of the seeder → sprouter transition (Litsios et al. 2014).
Empodisma minus (Leptocarpoideae) is a major component of ombrotrophic (rain-fed) peat/mire habitats in New Zealand, where its dense, negatively-geotropic capillaroid roots form dense mats that make up a major component of the peat there (Agnew et al 1993). Other dominants in similar conditions include Sporadanthus (Sporadanthoideae) and Apodasmia (Leptocarpoideae, also New Zealand, more coastal conditions).
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 pedicels that attract ponerine ants (Briggs & Linder 2009).
Vegetative Variation. Sokoloff et al. (2015a) question the interpretation of all centrolepidoid leaves as being unifacial. Furthermore, they equate the blade of these leaves with the hyperphyll, suggesting that it is developed from a different part of the leaf than the blade of grasses, which is a part of the hypophyll, the hyperphyll being represented by the Vorläuferspitze.
Genes & Genomes. The variation in the presence of the 28kb chloroplast genome inversion within Restionaceae is remarkable (Michelangeli et al. 2003).
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 dumbbell-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/.
Cutler (1969: as Centrolepidaceae) emphasized the fact that the root hairs in Centrolepidoideae 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. Whether or not Centrolepidoideae have SiO2 bodies needs confirmation.
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, not cymose, spikelet. Hou (1957) described the anthers as being 1- or 2-celled. The carpels are more or less fused, while in Centrolepis itself, although the gynoecium is definitely syncarpous, the carpels appear to be more or less one on top of each other 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 concentrating on either the Australian or African Restionaceae. 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. The pollen apertures of Australian Restionaceae in particular are like those of Centrolepidaceae, a larely Malesian-Australian group (Chanda 1966). Within Restionoideae, relationships are [Gaimarda [Aphelia + Centrolepis]].
For details of general phylogenetic relationships in Restionaceae, see Briggs et al. (2010, esp. 2014). Within Restionioideae, there is a Willdenowia and a Restio clade. In Sporadanthoideae, Sporadanthus is sister to the rest, and in Centrolepidoideae, Gaimardia is in that position. Within the large group Leptocarpoideae, the monotypic Eurychorda is well supported as sister to the others.
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. Centrolepidaceae should be included as a subfamily (c.f. Trias-Blasi et al. 2015), and Anarthriaceae, only recently separated from Restionaceae, are part of the same clade, so a single family is recognized by A.P.G. IV (2016). When there were three families, this was called the restiid clade.
[Flagellariaceae [[Joinvilleaceae + Ecdeiocoleaceae] Poaceae]]: primary cell walls with branched mixed-linkage glucans; leaf blade with ligule; inflorescence branches spiral [?level, ?interest], with adaxial basal swellings; endothecial cells with complete base plate thickenings; ovule 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) or about 74.7 m.y.a. (Magallón et al. 2015).
Evolution. Ecology & Physiology. Bouchenak-Khelladi et al. (2015) suggested that there was a slow-down in diversification rates at this node. 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, auriculate, 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, inner mesocarp sclereidal, endocarp also lignified, seed coat adnate to pericarp; outer periclinal wall of exotesta persisting; n = 19; ORF 2280 present?; seedling coleoptile at most short.
1[list]/5. 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. The rate of plastome molecular evolution is low (Barrett et al. 2015). 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 a part of the cotyledon, as in Poaceae (Takacs et al. 2012), or the first foliage leaf?
Some information is taken from Appel and Bayer (1998), Tillich and Sill (1999), both general, Wepfer and Linder (2014: revision), Sajo and Rudall (2012: floral morphology), Sajo et al. (2007: style), Thadeo et al. (2015: fruit), Subramanyam and Narayana (1972) and Rudall and Linder (1988), both embryology, and Tillich (1996b: seed and seedling).
[Joinvilleaceae [Ecdeiocoleaceae + Poaceae]]: epidermis with microhairs; foliar epidermis with long + short cell alternation [latter SiO2-containing] throughout], SiO2 bodies cubic; stomatal guard cells dumbbell shaped; culm hollow [level?]; endothecial cells with girdle thickenings [?Poaceae]; 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) or ca 58.6 m.y.a. (Magallón et al. 2015: note topology).
Evolution. Ecology & Physiology. For dumbbell shaped stomatal guard cells and relatively faster pore opening, see Franks and Farquhar (2006) and Haworth et al. (2011) and references. The stomata also have an enhanced response to blue light, perhaps advantageous in understorey conditions - Hetherington and Woodward (2003) discussed this in the context of the selective advantage of such stomata in the early evolution of grasses, but dumbbell-shaped stomata are also found in Rapateaceae and Cyperaceae, at least.
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. 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, epidermis and middle mesocarp lignified, T persistent; seeds 1-3; 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 fossil from late Miocene New Zealand, although they do not grow there now (Lee et al. 2001).
Genes & Genomes. The rate of plastome molecular evolution is low (Barrett et al. 2015).
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) and Thadeo et al. (2015: fruits).
Joinvilleaceae are little known.
[Ecdeiocoleaceae + Poaceae]: plant monoecious; flowers monosymmetric by reduction, imperfect; pollen operculate [exine inside annulus], 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 unisexual; flowers monosymmetric; 2 P ± conduplicate and keeled, 4 P flat; staminate flowers: (A 4, lateral members suppressed); 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 - Georgeantha); exotestal cells large, U-thickened, unlignified, or anticlinal walls lignified; n = 19; 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).
Pollination Biology & Seed Dispersal. Briggs and Tinker (2014) described synchronous/serial monoecy in the family. Zones of staminate and carpellate flowers alternated up the spike, and on one plant all inflorescences would be in the staminate or carpellate phase at any one time.
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 (1990a: 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) +, tannins 0; primary cell wall rich in arabinoxylans, pectin 10³%, xyloglucans lacking fucose; lateral roots initiating from pericycle and endodermis together [?level}; some sieve elements with thick walls, sieve tube plastids also with rod-shaped protein bodies, P-proteins 0; mesophyll cells with invaginated walls, fusoid cells +; short cell pairs, SiO2 bodies over veins; cuticle waxes as aggregated rodlets; stomatal subsidiary cells conical to dome-shaped; microhairs bicellular; plane of distichy of vegetative branches transverse to the main axis [but prophyll adaxial]; leaf with petiole and blade, ligulate, (ligule ± fringed with hairs), vernation supervolute(-plicate), midrib +, complex; T with two adaxial outer members distinct, abaxial smaller; wall with three layers [epidermis, endothecium, tapetum, = Reduced type], endothecium lacking thickenings on inner wall; tapetal cells binucleate; gynoecium initially annular, (G open in development), style solid; ovule one/flower, lateral, hemicampylotropous, funicle short [ovule broadly attached to ovule wall], micropyle endostomal; seed coat closely adherent to pericarp [= caryopsis]; testa not persistent, hilum long; peripheral layer of endosperm meristematic, endosperm hard, embryo lateral, well differentiated, cotyledon = scutellum + coleoptile, lateral, collar [= epiblast, the ligule of the cotyledon] conspicuous, plumule terminal, coleoptile enclosing plumule, embryonic leaf margins overlapping; coleorhiza enclosing radicle, radicle persisting for a few months; 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, ?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 also in cytosol.
707/11,337. Twelve subfamilies below. Worldwide (map: from Vester 1940; Hultén 1961). [List]
Age. Crown group Poaceae are estimated to be ca 83 m.y.o. by Janssen and 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 a 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 also below). The age of these amber deposits has been revised downwards to no earlier than Early Cenomanian at (99.4-)98.8(-98.2) m.y. (Shi et al. 2012), but this is still inconsistent with nearly all other age estimates for grasses.
The age of grasses, not to mention the animals, both vertebrates and insects, associated with them, and also the ages of other monocot groups, 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). Similarly, "bamboo cane" is reported from the Western Ghats at the K/P boundary (Cripps et al. 2005). By extrapolation, this would date the origination of the PACMAD-BEP clade to some 85-80 m.y. ago. Such fossils have been identified as Ehrhartoideae-Oryzeae (Prasad et al. 2011; see also Iles et al. 2015), and various grass phytoliths have been recovered from intertrappean deposits of about the same age, suggesting that grasses were quite diverse then, even if their ecology is as yet unknown (Strömberg et al. 2014). 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. 2014a; see also Jones et al. 2014: dates based on these fossils not included), 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 Caenozoic (see below).
To summarize: Dates from different lines of evidence are irreconcilably in conflict (Vicentini et al. 2008).
1. Anomochloöideae Potzdal
Microhairs 75-150 µm long [i.e., huge], basal cells constricted part way up; (SiO2 bodies transverse-unlobed); pseudopetiole with an apical pulvinus, midrib apparent on both surfaces; flowers perfect, protogynous; A centrifixed, basally connate, anthers ± latrorse; pollen in locule?; stigma not plumose; ovule endostomal, nucellar cap 3-5 cells across, suprachalazal nucellar tissue massive; embryo small, (scutellar cleft +), (embryonic leaf margins not overlapping); first seedling leaf lacking blade.
2/4. Central America to S.E. Brasil, scattered, forests (map: from Judziewicz et al. 1999).
Age. Divergence within Anomochloöideae 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).
1A. Anomochloa Brongniart
Leaves basal; ligule fringed, pulvinus also basal; inflorescence branches two-ranked; two "bracts" along each branch unit, two more "bracts" below each flower, one immediately below flower with sheath and blade; ring of fimbriate structures; A 4[inc. 3 members of the inner whorl]; style single; ovary with one, + two small, traces; testa lignified, persistent; n = 18.
1/1: A. marantoidea. Brazil, Bahia.
Synonymy: Anomochloaceae Nakai
1B. Streptochaeta Nees
Short cell pairs 0; leaves spiral; several spiral "bracts" below each flower, one with long awn, T = 3 + 3 [inner controlled by "lodicule genes"], coriaceous; microsporogenesis simultaneous; style long; ovary with three traces; epiblast 0; n = 11.
1/3. Tropical America, in Brazil only Espirito Santo.
Synonymy: Streptochaetaceae Nakai
[Pharoideae [Puelioideae [PACMAD + BEP clades]]] / the spikelet clade: inflorescence without inflorescence bracts, spikelets +, 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 [= inner whorl T], esp in staminate flowers, vascularized; stamens dangling; embryo long [?here]; x = 12; 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); microhairs 0; leaves resupinate, lateral veins running obliquely from midrib to margin; plants monoecious; inflorescence and spikelets with hooked [= uncinate] microhairs; spikelets dorsiventrally compressed, 1-flowered; staminate flowers: lodicules 2, minute; A (4-)6, anthers basifixed, latrorse; pollen fills anther loculus; carpellate flowers: lodicules 0; style hollow; ovule with micropylar beak, micropyle bistomal; (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.]
Microscopic details in characterization above nearly all from Pharus alone.
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; wall with cell layer between endothecium and tapetum, endothecium with inner walls fibrous; pollen grains peripheral in loculus; stigmas 2; 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); spikelet ?compression, basal flowers staminate or sterile, apical pistillate or perfect; ?lodicules; ?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 [e.g. DIMBOA], ergot alkaloids [latter synthesized by endophytes] +), lignins acylated with p-coumarates or acetate; SiO2 bodies often axially elongated; mesophyll cells with invaginated walls 0, fusoid cells 0; transverse veins 0; pseudopetiole 0; spikelets laterally compressed; flower type?; C/lodicules 2; A 3, opposite K/outer whorl of T; 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. (see also Christin et al. 2008a: ca 54.9 m.y.a.), 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]]]] / the PACMAD clade: C4 photosynthesis prevalent; SiO2 bodies dumbbell shaped; ligule often hairy; 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., while (50.6-)32.7, 32.4(-11.9) m.y. are the estimates in Cotton et al. (2015).
4. Aristidoideae Caro
(Plants annual); (spikelets not compressed [cylindrical]), with one flower; lemma awn trifid and with basal column, or 3 (1); callus pubescent; germination flap +, (scutellar cleft 0); n = 11, 12 [x = 11].
3/365: Aristida (304), Stipagrostis (56). 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); the stem-group age in Cotton et al. (2015: sister to the CMAD clade) is (46.6-)31.2, 20.5(-10.5) m.y. ago.
[Panicoideae [[Arundinoideae + Micrairoideae] [Danthonioideae + Chloridoideae]]]: 6 bp insertion in the 3' end of the mat K gene [?whole clade]
5. Panicoideae A. Braun
(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 +); spikelets dorsiventrally compressed, 2-flowered, development basipetal, lower flower staminate or sterile [gynoecial cell death caused by Tasselseed2], rachilla with appendages/0; plane of symmetry of flower relative to spikelet vertical; glumes, palea, lemma awned or not; (style +); (nucellar cap ca 4 cells across); (spikelet disarticulation below the glumes); caryopsis 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), Digitaria (227), Urochloa (135), Cenchrus (121: inc. Pennisetum), Andropogon (122), Dicanthelium (120), Setaria (115), Axonopus (104), Panicum (100), Ischaemum (87), Schizachyrium (64), Cymbopogon (59), Dimeria (59), Arundinella (57), Dicanthelium (55), Chrysopogon (48). Tropics to temperate.
Age. Crown-group Panicoideae may be (36.8-)23.6, 20.2(-7.9) m.y.o. (Cotton et al. 2015: [Thysanolaena + Centotheca] sister to the rest).
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]]: ?
Age. The age for this clade is (38.2-)25.8, 19.1(-9.5 m.y. (Cotton et al. 2015).
[Arundinoideae + Micrairoideae]: C3 photosynthesis; (hilum short).
Age. The age of this clade is estimated to be (34.3-)22.6, 17.3(-7.3) m.y. (Cotton et al. 2015).
6. Arundinoideae Beilschmied
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); (C4 photosynthesis - Eriachneae); culms solid or hollow; leaves (spirally arranged - Micraira); (lemma awn 0); starch grains simple, embryo small; n = 10; germination flap +.
9/188: Isachne (103), Eriachne (48). Tropics.
[Danthonioideae + Chloridoideae]: lemma bilobed, awned from the sinus; hilum punctate; scutellar cleft +.
8. Danthonioideae Barker & H. P. Linder
Usually temperate habitats; (plants annual), with C3 photosynthetic pathway; (stomata with parallel-sided subsidiary cells); ligule a fringe of hairs; awn trifid, or 3 awns; lodicules with microhairs; style bases 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); (culm solid); 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; silica bodies cross-shaped; (testa free from pericarp); embryo epiblast +; 4 bp insertion in the rpl16 intron; n = (6-8) 9, 10.
130/1721: Eragrostis (300), Muhlenbergia (155), Sporobolus (180), Chloris (55), Bouteloua (50). 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
[Oryzoideae [Bambusoideae + Poöideae]] / the BEP clade: SiO2 bodies transverse- or axial bilobate; ligule often membranous; endosperm softness gene +, ?embryo short; first seedling leaf lacking blade; 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. years. 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. Oryzoideae Beilschmied
(Some silica bodies elongated transverse to the long axis of the leafb>); (arm cells + - Oryzeae), (fusoid cells +); (longitudinal walls of epidermal cell straight); (microhairs 0); (ligule a ring of hairs); spikelet maturation basipetalb>, glumes 0, 2, apical floret alone fertile, two basal florets sterile; flowers perfect or not; A (1-)6, style branches separate almost from the very base; n = (10, 15); (roots at scutellar node - Ehrharta).
15/112: Oryza (20), Leersia (20). Widespread, esp. S. hemisphere.
Age. Fossils accepted as belong to stem-node Oryzeae (= crown-group Oryzoideae) are ca 66 m.y.o. (Iles et al. 2015; see also Prasad et al. 2011), in some conflict with the molecular dates immediately above.
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.o., while in Z. Peng et al (2013) the age was ca 47.8-46.9 m. years.
11. Bambusoideae Luersson
Culm branched; (inflorescence bracts +); lodicules 3, strongly 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), (testa free from pericarp).
116/1441. 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 some of the earliest fossils ascribed to the subfamily, the small-leaved Chusquea oxyphylla, are Eocene (Frenguelli & Parodi 1941; see also L. Wang et al. 2013). However, "bamboo cane" has been reported from the Western Ghats at the K/P boundary ca 66 m.y.a., and if confirmed this would upend the molecular estimates (Cripps et al. 2005).
11a. Olyreae Spenner
± 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 often dorsiventrally compressed, unisexual, dimorphic, one-flowered,rachilla extension 0; (lodicules 0); n = 7, 9, 10, 11, (12) [x = 11].
21/122: Pariana (35). Central and South America and Africa, also New Guinea (Buergersiochloa).
Synonymy: Olyraceae Berchtold & J. Presl
[Arundinarieae + Bambuseae]: plant woody; culm 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, contraligule +, culm leaves different from the others, largely sheaths, outer ligule +/0; flowering synchronized, plants monocarpic; polyploidy common.
11b. Arundinarieae Ascherson & Graebner
Rhizomes slender; 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.
11c. Bambuseae Dumortier
Rhizomes massive; branch development acropetal or bidirectional; outer ligule +; midrib complex; n = (10), 20, (22), 23, 24, etc. [x = 10, 12]
63/784. Chusquea (200), Bambusa (120), Merostachys (50), Schizostachyum (50). Tropical to (warm) temperate.
Synonymy: Bambusaceae Berchtold & J. Presl, Parianaceae Nakai
12. Poöideae Bentham
Temperate habitats, (plants annual); Epichloë endophytes pervasive; 1-aminopyrrolizidine [loline] and indole alkaloids +, fructose oligosaccharides in stem; root epidermal cell division forming asymmetric trichoblast/atrichoblast pair, hypodermal cells lacking Casparian strips; longitudinal walls of epidermal cells straight [?level]; culms hollow, branching at most rare; lemma usually with 5 nerves, (awned); lodicules at most slightly vascularized; style branches separate from the very base; (postament +); (endosperm with some non-starch soluble storage polysaccharides); embryo small, epiblast +, internode between coleoptile and scutellum traces 0; n = (2, 4-13); duplication of the ß-amylase gene.
177/3850. Largely North Temperate.
12A. Brachyelytreae Ohwi
Stomata subsidiary cells with parallel sides; microhairs 0; spikelets terete to dorsiventrally compressed; n = 11.
1/3. Eastern Asia, E. North America.
[Nardeae [Duthieae [[Phaenospermateae + Meliceae] [Stipeae [Diarrheneae [Brachypodieae + The Rest]]]]]: primary inflorescence branches 2-ranked [primary branches from two orthostichies]; spikeletes laterally compressed; lodicules not vascularized; embryo lacking scutellar cleft, embryonic leaf margins non-overlapping.
12B. Nardeae W. D. J. Koch (inc. Lygeeae)
Lodicules 0; style and stigma 1; n = 10, 13.
Synonymy: Nardaceae Martynov
[Duthieeae [[Phaenospermateae + Meliceae] [Stipeae [Diarrheneae [Brachypodieae + The Rest]]]]]: ?
12C. Duthieeae Röser & Jul. Schneider
[[Phaenospermateae + Meliceae] [Stipeae [Diarrheneae [Brachypodieae + The Rest]]]]: microhairs 0 (+ - some Stipeae); style +.
[Phaenospermateae + Meliceae]: ?
12D. Phaenospermateae Renvoize & Clayton
(Leaf blade resupinate - Phaenosperma); 21 bp insertion in rpl32-trnL; n = 7, 12.
7/11. Central to East Asia, also Australia, Mexico, Balkans, Caucasus; scattered.
12E. Meliceae Endlicher
5/125: Melica (80). Global, esp. North Temperate.
Synonymy: Melicaceae Martynov
[Stipeae [Diarrheneae [Brachypodieae + The Rest]]]: ?
Age. Fossils assigned to stem-node Stipeae are estimated to be 36.7-34.1 m.y.o. (Isles et al. 2014).
12F. Stipeae Dumortier
Spikelets not compressed; chromosomes <2.0 µm long.
/557. Stipa (<300).
Synonymy: Stipaceae Berchtold & J. Presl
[Diarrheneae [Brachypodieae + The Rest]]: ?
1/4. East Asia, North America.
[Brachypodieae + The Rest]: stomata subsidiary cells with parallel sides.
Age. The age of this node is around 39-32 m.y.a. (International Brachypodium Initiative 2010).
1/16 Temperate, tropical montane.
12I. The Rest / core Poöideae. (Bromeae/Hordeae/Aveneae/Poeae)
Fructan concentration often high; (stomata subsidiary cells with parallel sides); style solid [Triticum]; primary inflorescence branches usu. 2-ranked; n = 7, chromosomes "large".
166/3831: Poa (500), Festuca (470: inc. Lolium), Calamagrostis (230), Agrostis (220), Elymus (150), Nassella (122), Bromus (100), Anthoxanthum (50), Leymus (30). Largely North Temperate.
Age. The age of this node is around 33.5-26 m.y. (Sandve & Fjelheim 2010).
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, Miliaceae Link, Phalaridaceae Link, Phleaceae Link, Sesleriaceae Döll, 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: a stunning underestimate). 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 similarly small 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 (e.g. Christin et al. 2014a; Spriggs 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 morphological 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, 2015: the spikelet clade). 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). Episodes of diversification are perhaps associated with some, but not all, C4 clades during the Miocene expansion of grasslands within the last 15 m.y. (Spriggs et al. 2014).
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). 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. years. For diversification of the large Poa alliance (Hoffmann et al. 2013; Birch et al. 2014), see below; much is Pleistocene or younger.
Pharus has a number of features in common with Anomochloöideae, perhaps because they are both plants of the forest floor (Sajo et al. 2007, 2012). Although Pharus itself has numerous distinctive features, whether other members of Pharoideae have these features is unknown, and Puelioideae are also very poorly known (see also Judziewicz & Clark 2008; Kellogg 2013b).
Ecology & Physiology. For summaries of the ecology of grasses and grasslands, see Coupland (1992, 1993), White et al. (2000), 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, e.g., ca 20% of the earth's surface (Hall et al. 2000; Sabelli & Larkins 2009). The figures depend in part on the definitions of grassland, savanna and forest (see also Dixon et al. 2014). 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 1992, 1993; esp. White et al. 2000, Map 1, for more details; see also Clade Asymmetries). Bouchenak-Khelladi et al. (2015) suggest that there was an increase in diversification rates at the spikelet node, the evolution of spikelets themselves, open vegetation and dry environments being the triggers.1. Grasses and C4 photosynthesis.
1. 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 Caenozoic 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 some 5,920 species of the PACMAD clade (Sage et al. 1999, 2012; Grass Phylogeny Working Group II 2011; see Osborne et al. 2014 for a global database of C4 grasses). For a summary of C4 photosynthesis, see e.g. Sage et al. (2012) and Kellogg (2013a).
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; Christin et al. 2015 and references). 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 mechanisms of C4 photosynthesis and the anatomies associated with it are particularly variable in Paniceae - in Panicoideae alone C4 photosynthesis may have evolved between four and eight times (Kellogg 2000; Giussani et al. 2001; Christin et al. 2007a, 2009a; Washburn et al. 2015), but resolution of the phylogeny of the tribe is needed, chloroplast and nuclear genes do not always tell the same story (Washburn et al. 2015). The relatively uncommon C4 PEPCK 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; c.f. Y. Wang et al. 2014: the pure PEPCK subtype does not really exist...).
There are a few intermediates with C2 photosynthesis in Poaceae (Monson & Rawsthorne 2000; Bauwe 2011 for references). Although anatomy has been used to characterize subtypes of C4 photosynthesis, the correlation of anatomy with photosynthetic pathway may not be that good (Ingram 2010), and very importantly, the typology needs to be revisited (Y. Yang et al. 2014; Washburn et al. 2015). In a broad survey of C4 plants Lundgren et al. (2014) noted that concentration of chloroplasts in the area in which the Calvin cycle went on was about the only feature common to all of them.
The adoption of C4 photosynthesis is associated with 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 2013a; see Pengelly et al. 2011 for vein spacing; Sack & Scoffoni 2013 for literature suggesting that this potentiated the repeated evolution of C4 grasses). In Cleome s.l., at least, a delay in differentiation of the mesophyll cells is connected with increased venation density of C4 plants (Külahoglu et al. 2014). Genes involved in root endodermal development have been coopted in bundle sheath development, suberin in the the bundle sheath cells probably helping the maintain the concentration of CO2 in the bundle (Slewinski et al. 2012; P. Wang et al. 2013; Slewinski 2013; Mertz & Bruntnell 2014).
S. H. Taylor et al. (2010, 2011) and Ripley et al. (2010) compared the ecophysiology of C3 and C4 grasses, the former sometimes being more sensitive to drought and recovering more slowly from it (see also H. Liu & Osborne 2014 for drought response). 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 because of the high concentration of CO2 released e.g. from C4 malate in the bundle sheath cells, so avoiding the negative effects of a decreased CO2 concentration (Morgan et al. 2011; Sage et al. 2012). Although both C3 and C4 grasses have very small stomata, because of the efficiency in CO2 use in the latter, their stomatal density is substantially less (to half) than that in the former (Franks & Beerling 2009: a density of 400 stomata/mm2 tends to separate the two; Taylor et al. 2011). Within C4 grasses, Chloridoideae have smaller and denser stomata than do Panicoideae (H. Liu & Osborne et al. 2014). Such variation will affect stomatal conductivity, indeed, C4 and C3 grasses photosynthesize at the same rate (e.g. Long 1999), but stomatal conductance of the former is lower (Taylor et al. 2011). Interestingly, taxa like Miscanthus x giganteus carry out C4 photosynthesis under decidedly cooler conditions than is common (Wang et al. 2008), while C3 grasses like Lolium perenne can also tolerate water stress (Holloway-Phillips & Brodribb 2010, see below).
Christin et al. (2013) suggested that particular anatomical changes facilitated the transition to C4 photosynthesis in grasses. 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). Of the three main kinds of C4 photosynthesis in grasses, both NAD-ME and NADP-ME types evolved in parallel, while PCK/PEPCK evolved in parallel from both these types (the PCK pathway may occur in the other two types and not exist as an independent pathway - H. Liu & Osborne 2014; Y. Wang et al. 2014). Parallelisms may even be at the level of particular amino acids being substituted, similar changes occurring independently in the phosphoenolpyruvate carboxykinase 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 the parallelisms in C4 grasses.
Lateral transfer of genes may 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...
2. Grasslands, Fire and Forests.
This discussion includes both C4 grasslands and the more cold-tolerant C3 grasslands; 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; Cotton et al. 2015), members of the basal pectinations in the family favouring this habitat and having broad leaf blades, etc. (of course, 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 Caenozoic in age. Jones et al. (2014) suggest that forest-dwelling grasses were around for about 50 m.y., grasses moving into more open habitats as forest retreated with increasing temperatures and dryness 56.5-53 m.y.a. around the Palaeocene-Eocene thermal maximum (PETM); the dates in Cotton et al. (2015) were substantialaly younger (ca. 32.6 m.y.a.), and the latter suggested that the rapid radiation of the PACMAD clade was at the Eocene-Oligocene transition, with temperatures falling at around that time. Of course, the initial move of grasses from woodlands to open habitats, the evolution of C4 photosynthesis, and the rise to dominance of grasses in more temperate and more tropical environments may all have quite different precipitating causes.
The ecological/environmental 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; Christin & Osborne 2014) and will be still less clear if some of the older clade ages (see above) are confirmed (Christin et al. 2014a). Some combination of higher temperatures, low atmospheric CO2 concentration, fire and water stress is now emphasized (e.g. Ehrleringer et al. 1997; Bond et al. 2003; Edwards & Still 2008; Vincentini et al. 2008; Edwards 2009; Strömberg & McInerney 2011; Christin et al. 2011b; Kellogg 2013a; 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). Grasslands spread in North America during the mid-Miocene Climatic Optimum of 17-14.5 m.y.a. (Harris et al. 2014) - MAT ca 3o warmer, CO2, at 900-1100 p.p.m., quite high - then temperatures in the late Miocene decreased (Arakaki et al. 2011).
Different C4 clades respond differently to these factors, with phylogeny (especially linked with structural [stomatal] traits), C4 photosynthetic subtype (linked with physiological traits) and habitat interacting. Thus members of four C4 subfamilies sorted out along gradients of disturbance (grazing), moisture, temperature abd fire frequency (Visser et al. 2011). NAD-ME species (Chloridoideae) favour drier habitats, NADP-ME species (esp. Panicoideae) wetter habitats, while even within Chloridoideae NAD-ME species may be more drought-avoidance plants and PCK species more drought-tolerant plants (H. Liu & Osborne 2014).
The forest ↔ savanna transition is a major transition, and depends on events such as suppressed saplings becoming trees and the timing of successive fires (Hoffmann et al. 2012). 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; Estep et al. 2104). C4 grasses, grasslands and savanna may be favoured in environments with some combination of high temperatures and low CO2 concentrations. C4 grasses seem to be able to tolerate drier conditions than non C4members of the PACMAD clade, at least (Christin & Osborne 2014), but different groups of C4 grasses behave differently. Many C4 origins seem to be correlated with a reduction in annual rainfall, and aridity may favour the expansion of grasses (Sage 2004), although seasonality is important, too. Evidence from palaeosols suggests that grasses replaced woodland. Grassland soils are notably moister than corresponding woodland soils, yet somewhat paradoxically grasslands support a drier climate, transpiration being relatively low; woodlands have a lower albedo and transpire more, so their soil is drier (Retallack 2001, 2013a). Declining CO2 concentrations may also have made trees less competitive (Pagani et al. 2009), while at higher temperatures photorespiration becomes more likely, so favouring C4 plants (Christin & Osborne 2014 for a summary). Once established, the dense - and sometimes quite deep - root masses of grasses make the invasion of grasland by woody vegetation difficult (D'Antonio & Vitousek 1992); the seedling/young plant stage is critical here (Bond & Midgley 2000). 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). K. Yu and D'Odorico (2015) noted that that woody plants obtain water from deeper layers of the soil and during the night, in particular, some water returns to shallow layers of the soil (the phenomenon of hydraulic lift) where it is scavenged by the shallower-rooting grasses there (see also Holdo & Nippert 2015 for the rooting pattern: 40 vs 5 cm); overall, savannas are favoured in marginal conditions that might otherwise support woodlands. Indeed, trees like the African Entandrophragma cylindricum (Meliaceae) have roots descending to 6 m or so depending on the rock/soil type, woody Fabaceae to well over 2 m (Freycon et al. 2015 and references). In a comparative study, Pinto et al. (2014) found that C4 grasses used nitrogen and water more efficiently that C3 or C3-C4 intermediates at 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 another 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 that 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, presumably including sedges, decompose more slowly than do those of other angiosperms (Cornwell et al. 2008). Grasslands are particularly flammable because of their litter accumulation (Scheiter et al. 2012; Sage et al. 2012) and charcoal from fires has become abundant since the Late Miocene about 10 m.y.a., the time during which grasslands have spread (e.g. Bond & Midgley 2000; Keeley & Rundel 2005; Bond & Scott 2010). In monsoon-like climates biomass produced during the growing season would later dry out and burn, and this is consistent with the record of fossi;l charcoal (Keeley & Rundel 2005: check). 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). Since grasses have their perennating parts underground, they are not harmed by fire, while burning suppresses woodland by killing 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). The productivity of tall-grass prairies is negatively affected by the accumulation of litter, but fires improve productivity (Knapp & Seastedt 1986). 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). 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 local diversity of grasses is also affected by the particular fire regime, although not in any simple way (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. 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). Grassland and savannas remain dynamic entities, and grasslands may be very sensitive to changing climates. Thus some reconstructions show the current increase in atmospheric CO2 being accompanied by quite extensive spread of C3 grasslands (e.g. Collatz et al. 1998; Hall et al. 2000; Knapp & Smith 2001). However, seedlings of forest trees show decreased survivorship as temperatures rise (Will et al. 2013). More generally, simulations suggest that with increasing atmospheric CO2 concentrations the possibility for the coexistence of several stable biomes within Africa, at least, will be lost (Moncrieff et al. 2103). How increasing temperature affects above-ground woody biomass in savannas depends on the continent, thus projections suggest that above-ground woody biomass will tend to increase in Africa and decrease in Australia and South America (Lehmann et al. 2014). Changing rainfall patterns also affect the balance between savanna and grassland. Thus grasses, when dry, are more susceptible to water stress than savanna trees, but when conditions are wetter they have a much higher relative growth rate, so at least initially they will tend to spread at the expense of the trees (Xu et al. 2015).y
Some vegetation simulations show circum-Arctic grasslands early in the Caenozoic (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), the grasses involved being mostly caespitose bunch grasses (Retallack 2013a). 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 prominent then (Strömberg et al. 2011).
C4 grasses may have first appeared 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). Grasslands, both C3- and C4-dominated, spread in North America during the mid-Miocene Climatic Optimum of 17-14.5 m.y.a. (Harris et al. 2014), however, C4 grasses made a major contribution to overall vegetation biomass only in the late Miocene 9-8 m.y.a., C4 grassland becoming widespread only 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 C4 grasses and their ecological expansion (e.g. Strömberg & McInerney 2011) - a lag of over 20 m. years. Interestingly, allopolyploidy has been extremely common in C4 Andropogoneae, and many allopolyploid events date to the period of grassland expansion, even if most have not been followed by anything notable in the way of speciation (Estep et al. 2014).
The extensive Brazilian Cerrado and African savanna vegetation with abundant flammable C4 grasses and woody plants that have become adapted to a fire regime has also developed only within the last (10-)5 m.y., and they replaced woodland (Pennington et al. 2006b; Simon et al. 2009; Simon & Pennington 2012; Hoffmann et al. 2012; Maurin et al. 2014; Pennington & Hughes 2014). In both Cerrado and savanna there has been widespread evolution of geoxylic suffrutices, "underground trees" with massive subterranean fire-protected perennating woody axes (White 1976), that flourish under a regime of frequent fires and moderate rainfall. In the Cerrado, clades including 50 or so fire-resistant species evolved, although comparable clades in Africa are smaller (Pennington & Hughes 2014). By and large, however, phylogenetic signal in the woody plants adapted to environments in the South American Cerrado vegetation and the underground forests of Africa is small (Simon & Pennington 2012).
The total C sequestration of 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 Caenozoic 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, 2013a). 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, 2013a).
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). Grasslands are made up of rather small plants, but estimates of the proportion of below-ground biomass in grasslands is as high as 80-95% (Dormaar 1992) and this accounts 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 (2013a). More general figures for tropical savannas and grasslands together - the latter are likely to be C4 grasses - in Carvalhais et al. (2014: Tables S1 + S2) are ca 338 Pg total C, a carbon density of ca 17.7 kgC m-2 and a mean turnover time of (12.2-)16(-22.1) years, while comparable figures for temperate grasslands and shrublands are ca 187 Pg total C, and a carbon density of ca 16.7 kgC m-2 with a mean turnover time of (32.8-)41.3(-54.6) years; the residence time for the carbon in temperate grasslands is much longer, largely because of the cooler temperatures. Overall, grasslands function as a long-term carbon and water sink, and one consequence of their activities is long-term global cooling (Retallack 2001, 2013a).
What makes grasslands and savannas still more distinctive ecologically is not just the abundance of grasses and their caespitose or rhizomatous 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, Edwards et al. (2010) estimated that only some 600 species, most C4 photosynthesizers of the PACMAD clade, dominate ecologically in grasslands and savanna, while Kellogg (2015) estimated that fewer than 10% of the grass species made up most of the biomass in major grasslands, for instance, four species dominating in tall grass prairie in North America. Andropogoneae, with some 1,200 species and 90 genera, are notable in their positive response to annual burning (Forrestel et al. 2014 and references), and in African, Australian and North American grasslands and savannas in particular members of the ASH clade (Andropogon, Hyparrhenia, Schizachyrum), with some 244 species, are prominent among the dominants (Estep et al. 2014). 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 - or perhaps a bit before (Spriggs et al. 2014). It was then that grasslands and savannas 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). Indeed, the Neogene has been called the age of grasses (c.f. Palaeos).
3. Grasses, Grasslands, Herbivory and the Silicon Cycle.
There have often been suggestions that C4 grasses in particular, grasslands in general, and grazing are connected (e.g. Retallack 2013a; Katz 2015). Thus Bouchenak-Khelladi and Hodkinson (2011) thought that there were "adaptive co-evolutionary processes" (unspecified) going on between grass and grazer, and Bouchenak-Khelladi et al. (2009) had 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. Bouchenak-Khelladi and Hodkinson (2011) noted that hypsodonty has been gradually increasing for 20 m.y., but the spread of grasslands was not contemporaneous with this increase. Indeed, 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). There was also a Miocene radiation of scarab beetles into the new habitat of plentiful dung in large part left by these grazers (Ahrens et al. 2014).
Grazing mammals in different parts of the world independently evolved hypsodont or hypselodont dentition; in the former teeth have high crowns, enamel extends below the gum lines, and the roots are short, and in the latter, teeth are ever-growing, and both apparently can deal with the wear caused by eating abrasive grasses with their complex silica bodies (phytoliths). However, tooth enamel is harder than the silica encountered in grasses (Sanson et al. 2007), although surprisingly little is known about the mechanics of tooth action (Sanson 2006); Sanson and Heraud (2010) suggested that the silica in silica bodies might not be in crystalline form and so would not cause wear on the enamel of mammalian teeth. In fact, 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), and hypsodont and hypselodont teeth probably evolved to deal with silica in dust-covered foliage in environments that were becoming drier and more open, hypselodont lagomorphs in particular cropping their food very close to the ground; this is the "grit not grass" hypothesis (Jardine et al. 2012).
Thus the relationship between silica, herbivory, and the mechanical protection of plant tissues is not straightforward. Although prairie grasses expanded in Nebraska in the Early Miocene ca 23 m.y.a., moderately hypsodont ungulates and rodents were already around by then, but some evolved later (Strömberg 2004, 2006; Mihlbacher et al. 2011; Jardine et al. 2012), while hypselodont lagomorphs (hares, etc.) date from the Eocene-Oligocene boundary (Jardine et al. 2012). 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. In Patagonia hypsodont teeth became common in the now-extinct notoungulates in the late Eocene-Oligocene 39-21 m.y.a., a time before grasses were a major component of the vegetation (Strömberg et al. 2013b; Dunn et al. 2015). High SiO2 in grasses = hypsodonty is not a formula that explains the evolution and rise to dominance of grasses in some ecosystems and the evolution of grazing animals.
But silica bodies do affect the feeding behaviour of at least some smaller herbivores, both mammals and insects (for rabbits, see Cotterill et al. 2007). In Poaceae there is a positive correlation between the annual habit and high silicon concentration (Cooke & Leishman 2011b) .More 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 increased silica and are less attractive to animals (see Schoonhoven et al. 2005; Massey & Hartley 2006, 2009; Massey et al. 2007b; Cook & Leishman 2011; and Katz et al. 2014 for literature).
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 below). 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. Grasses have up to 7% silica and it 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 diatom diversity in fresh waters; the cell walls (frustules) of diatoms are made up of silica (Kidder & Gierlowski-Kordesch 2005; Vandevenne et al. 2013). Marine diatom diversity peaked at the Eocene/Oligocene boundary well before the spread of grasslands but at the time when the Himalayan orogeny was beginning, and again in the later Miocene onwards (Rabosky & Sorhannus 2009; Cermeño et al. 2015). The calcite compensation depth (the depth below which calcite dissolves) considerably increased in post-Eocene times, with calcium carbonate nanofossil ooze replacing siliceous radiolarian ooze (Coxall et al. 2005; Tripati et al. 2005) in connection with the developing ice caps. However, the mobilization of silica, in part associated with the spread of grasslands in the later Miocene (in the sea Si is available as orthosilicic acid - H4SiO4), contributed to this later peak in diatom diversity; interestingly, the thickness of radiolarian tests decreased over this whole period, in part through competition with diatoms for Si (Cermeño et al. 2015).
4. Grasses, especially Poöideae, and Endophytes.
The endophyte-grass relationship exemplified by the Poöideae-Neotyphodium/Epichloë (see below) is usually described as a mutualism, although this may sometimes, at least, not be so (see Saikkonen et al. 1998; Gundel et al. 2006; Ren & Clay 2009). The effects of endophytes on gene expression is considerable, over 1/3 the genome being differentially expressed (most downregulated), far more than in endomycorrhizal associations (Dupont et al. 2015). Endophytic fungi synthesize a diversity of secondary metabolites (Spatafora et al. 2007), and "grass" alkaloids synthesized by Epichloë include indole diterpenes, loline (1-aminopyrrolizidines), peramine, and the ergot (ergoline) alkaloids (Fleetwood et al. 2007; Schardl et al. 2007; Simpson et al. 2014). Loliines are primarily active against insects whether as toxins or feeding deterrents (Schardl et al. 2007; D.-X. Zhang et al. 2009; Simpson et al. 2014). However, the more that is found out about the relationship, the more complex it appears to be. For instance, in the absence of herbivory the grass genotype may be more important in determining the outcome of of intraspecific competition than presence of an endophyte (Cheplick et al. 2014). The asexual stage (Neotyphodium) may increase the competitive ability of the host grass under stressful conditions (Saari & Faeth 2012; see also Dupont et al. 2015), although under some conditions they severely reduce sexual reproduction (Oberhofer et al. 2013: both greenhouse experiments). Endophytes that are insect pathogens may also be antagonistic to plant pathogens (Vega et al. 2009 and references). Perhaps not surprisingly, 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), 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). Endophytes improve the resistance of Lolium perenne and Bromus laevipes, for example, to the effects of water stress (Hahn et al. 2007; Afkhami et al. 2014). In the latter case the habitable range was increased, but when conditions were more mesic, the plant was less likely to have the endophyte (Afkhami et al. 2014). Similarly, Poa leptocoma, with endophytes, grew in wetter soil (and was also more colonized by endomycorrhizae) than did P. reflex, lacking endophytes (Kazenel et al. 2015). In Elymus virginicus the presence of Epichloë resulted in the plant diverting more of its resouces to producing seeds, through which the fungus is transmitted, and less to producing pollen (Gorischek et al. 2013); it is unclear if this was to the benefit of the plant. 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; esp Simpson et al. 2014).
Endophyte-grass associations appear to be less common in areas with Mediterranean climates, being found in less than 10% of grasses in California, for example (Afkhami 2012).
Other aspects of the eco-physiology of Poaceae to be taken into account:
5. 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.
6. 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, it is Poaceae that are next at 11%, and all are members of Poöideae (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. 2014a), 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). Fructans are probably also involved in cold tolerance. 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; Sandve et al. 2011). 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). However, Epichloë also down-regulates the genes involved in responding to heat stree and up-regulates those responding to cold stress (Dupont et al. 2015).
As mentioned, the evolution of Poöideae may initially be linked with cooling at the onset of the Oligocene, but much subsequent diversification is later and associated with the later Pleistocene cooling. Thus the Poa alliance, whose 775 species are about 1/5th of all Poöideae, may have begun diversifying in the Miocene ca 15 m.y.a., but most is Palaeocene and younger, occurring within the last 4 m.y. (Hoffmann et al. 2013). Furthermore, the diversification rates are very high, up to 3.93 species/million year, although this depends on dating, and much is not connected with obvious island-like areas (Hoffmann et al. 2013; see also Birch et al. 2014: ages slightly older).
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); there are no vernalization requirements. The two species of Danthonioideae studied (Chionochloa) seemed to tolerate cold conditions by controlling ice nucleation (Wharton et al. 2010).
7. Stomatal Opening. The dumbbell-shaped stomata of grasses have a large stomium when fully open and the rate of opening/closing is very fast indeed, very much faster than in those few other species have been examined (Franks & Farquhar 2006: Triticum aestivum, compared with Tradescantia virginiana and two other non-angiosperm species; Haworth et al. 2011). However, since the stomata of quite a number of other Poales are similar (see above), it is unclear if the dumbbell shape per se is a major element of the ability of grasses to spread as climates became drier at the end of the Eocene (Hetherington & Woodward 2003).
8. 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; they can be up to several metres long and are impermeable to water (Kellogg 2015). The general distribution of such roots is poorly know, but they are known from some other Poales and 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 a 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 or are endophytic (Santi et al. 2013), while ammonia and nitrous oxide were scavenged from the air by bacteria associated with the roots of Leptochloa fusca (Hurek et al. 1988). Glasshouse experiments suggested that the bacteria were transmitted via the caryopses, and affected root growth (roots were positively geotropic) and the development of root hairs; grasses produced reactive oxygen species during the day that denatured bacterial proteins that were broken down at night by root and microbial proteases, organic nitrogen then being taken up by the plant (White et al. 2015). However, plant roots of at least some eudicots also produce proteases (Paungfoo-Lonhienne et al. 2008; Adamczyk 2010), and what, if anything, is unique in such aspects of grass root physiology is unclear. 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.
9. 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 like DIMBOA (2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one), 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 that parasitize the herbivorous insects earting them), 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; Pentzold et al. 2014; Schullehner et al. 2008: non-grasses; Nüutzmann & Osbourne 2014: clustering of gene involved in their synthesis, clusters can be split).
10. Salt Tolerance. Poaceae such as Spartina (= Sporobolus sect. Spartina) and Puccinellia are major elements of salt marshes. The C4 Sporobolus sect. 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), possibly being preceed by the acquisiition of C4 photosynthesis (Bromham 2015). 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. Functioning salt glands are known only from Chloridoideae (Céccoli et al. 2015). 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).
11. 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). Their wood, very dense, decomposes more slowly than that of other angiosperms (G. Liu et al. 2015).
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.
12. 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.
13. 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. For mineral movement at nodes, with different types of vascular bundles and different patterns of movement between between xylem and phloem depending on the mineral, see Yamaji and Ma (2014 and references); again, there is little comparative knowledge..
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).
Pollination Biology & Seed Dispersal. Despite the small size of the flowers, there is quite considerable variation in floral morphology in the family (see e.g. Le Roux & Kellogg 1999; Chuck 2010 for the development of unisexual flowers; also Rudall & Bateman 2004; Ronse de Craene 2010; Kellogg 2015); floral reduction in the family has been achieved in a variety of ways.
Poaceae are predominantly wind-pollinated and usually have protandrous flowers with dangling anthers. Given this pollination mode and the ability of a number of grasses to live in quite dry conditions, it is surprising that grass pollen is partly hydrated (>30% water content) and sensitive to dessication, i.e. it is recalcitrant (Franchi et al. 2002; Smarda et al. 201a). 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).
Apomixis is quite common in Poaceae (Asker & Jerling 1992; Hörandl et al. 2007, and references); cleistogamy is very common, occuring in over 300 species (Kellogg 2015).
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; Nakamura et al. (2009 and references) describe the quite considerable variety of fruit development in the family. However, the fruit proper is rarely the dispersal unit except in taxa like 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). Fleshy fruits ("bacoid caryopses") evolved at least seven times in Bambusoideae alone during the Late Miocene when the climate was notably warm and wet; these fruits are viviparous, or germination begins as soon at they fall to the ground (Ruiz-Sanchez & Sosa 2015). 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 well 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, that plant - and all the plants of the species - 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 like birds and rats 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. How this reproductive behaviour is controlled is largely unknown, although it may well have originated by successive small multiplications of the initial synchronization intervals (Veller et al. 2015) - but why is this behaviour overall so uncommon in plants?
Bacterial/Fungal Associations. Ascomycete clavicipitaceous endophytes are widely distributed among grasses (Clay 1990: review; Leuchtmann 1992: distribution and host specificity; Schardl 2010; Rodriguez et al. 2009: endophytes in general); the association could be ca 40 m.y. old (Schardl et al. 2004). Leuchtmann (1992) thought that 20-30% Poaceae might be involved in these associations (4% were known to be infected), 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 (in some literature Acremonium is recorded from Poöideae - see Leuchtmann 1992), and Epichloë species may hybridize (Roberts et al. 2005; Moon et al. 2005; Rodgers et al. 2009: patterns of infection of the two forms). There may be a fair degree of host specificity of the fungus (Simpson et al. 2014 for literature). Balansieae have also been found on other Poaceae, especially C4 grasses (Leuchtmann 1992). 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-Balansieae (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). Interestingly, Epichloë is rather like a parasite in the extent of its effect on the gene expression of the host, ca 38% of the genes being affected (Dupont et al. 2015). Some fungi like Metarhizium robertsii can even be both endophyte and insect pathogen (e.g. Sasan & Bidochka 2012).
The relationship of the plant and fungus is complex and is discussed further above The larvae of Phorbia (or Botanophila) flies develop on fertilized Epichloë stromata, and the adults transmit fungal spermatia in a fashion analogous to insect pollination of flowers (Bultman 1995; Schardl et al. 2004). 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).
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 (α-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); a number ofother live on Cyperaceae. 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, with around 2,400 species, 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; the around 2,400 species of browns are about 1/8 of all butterflies. Although Satyrini are a clade in which diversification rates have increased (perhaps through a reduced extinction rate), this increase occured within a larger clade in which Poaceae are also a major food plant, so it is not simply linked to any host-plant shift (Hamm & Fordyce 2015).
The larvae of Nymphalidae-Satyrini and some smaller tribes 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. 2014). 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). There are few Pronophilina in high-altitude forests in east Brazil and Central America.
Another major clade of butterflies whose caterpillars eat mostly Poaceae is the [Heteropterinae-Trapezetinae-Hesperiinae] clade of skippers that has around 2,250 species, most being grass skippers, Hesperiinae (Warren et al. 2009). They, too, are found on bamboos in the Andes, the large genus Dalla, with perhaps 100 species, being an example. Although Warren et al. (2009) suggest an origin of skippers as a whole in the mid-Cretaceous, more precise dates seem to be unknown.
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).
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).
Ligule variation is extensive, although taxa like Streptochaeta lack a ligule (Judziewicz & Clark 2008), or quite frequently the ligule is a ring of hairs. The ligule and auricle together act as a kind of hinge, so the leaf blade is held at an angle to the stem; developmentally, a number of the genes involved in ligule development in maize are expressed elsewhere (base of leaf, branches) where they mark developmental boundaries (Zhu et al. 2013; Johnston et al. 2014).
Genes & Genomes. Nuclear 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). Genome evolution in Triticeae has been particularly accelerated (M. C. Luo et al. 2009; see also Messing & Bennetzen 2008; Salse et al. 2009a).p>
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; Vanneste et al. 2014a). Yockteng et al. (2013) date duplication of SEPALLATA genes here to around 82-58.2 m.y. ago. 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). Soltis et al. (2009) suggested that diversification in Poaceae might be connected with this genome duplication, and the evolution of a cytosolic ADPglucose phosphorylase, unique to this clade, has been associated with this duplication (Comparot-Moss & Denyer 2009). However, diversification of the groups including the C3 cereals may have occurred ca 20 m.y. later (Paterson et al. 2004; c.f. International Brachypodium Initiative 2010). There has been a genome duplication in a clade that includes Zea (21-)20.4(-19.7) m.y.a. and in the Phyllostachys clade (21-)19.7(-18.7) m.y.a. (Vanneste et al. 2014a).
For an entry into the extensive cytological work that has been carried out on the family, see Kellogg (2015). X = 12 is still found in rice (Oryza), for example, while x = 10 in Panicoideae. (Hilu  suggested that the base chromosome number for the whole family might be x = 11.) 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), while within Panicoideae-Saccharinae there has been quite recent extensive and high polyploidy, but reduction in chromosome number seems already to be underway (C. Kim et al. 2014).
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). Indeed, developmental gene duplication and subsequent functional divergence may have played a major role in facilitating 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).
Other more recent duplication events clearly involve hybridization. Thus a genome duplication/hybridization in the ancestor of Zea has been dated to ca 4.8 m.y.a. (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). In general, allopolyploidy has been very common in Andropogoneae, but few allopolyploidization events have been followed by anything much in the way of speciation, altough the [Zea + Tripsacum] clade is one modest exception (Estep et al. 2014). Bamboos are diffcult, indeed, relationships there differ depending on whether the genes analysed are from the chloroplast (a [Bambuseae + Olyreae] clade) or nucleus ([Bambuseae + Arundinarieae]: Wysocki et al. 2014). The over 500 species of temperate bamboos (Arundinarieae) form a clade that is descended from an allotetraploid ancestor (Triplett et al. 2011), while Triplett et al. (2014) suggesting several hybridization events involving three main genomes and two minor genomes that link Bambuseae and Arundinarieae; diploids with those genomes are extinct, while Olyreae have yet another genome that has doubled by autopolyploidy. Z. Peng et al. (2013) suggest that genome dupication occurred in the ancestor of the giant bamboo Phyllostachys heterocycla (P. edulis) (15-)11.5-7.7 m.y. ago. The complex relationships within Danthonioideae may also be linked to extensive past hybridizations (Pirie et al. 2008, 2009), while in Poöideae-Stipeae genomes from extinct clades persist in their hybrid descendents (Romaschenko et al. 2014).
Triticeae (Poöideae, the old Hordeeae) 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; Sha et al. 2014: Leymus; Sun 2014: Elymus; R. R. Wang & Lu 2014: perennial species; Dong et al. 2015: Elymus s.l. and the St genome), with polyploidy, genome re-arrangements and introgression making for a very complex 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). Polyploidy in Sesleria (Poöideae) has been followed by reduction in genome size (Lazarevic et al. 2015). For a possible relationship between genus size, life form and polyploidy, see Hilu (2007).
The grass genome has the highest GC content of any land plant, particularly evident in grasses growing in grassland biomes that are seasonally stressed, but not in forests or in wetlands (Smarda et al. 2014). For genic GC content in monocots as a whole, perhaps basally bimodal, not simply in Poaceae, see Clément et al. (2014).
There has been substantial evolution in the chloroplast genome (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). There seems to be a higher substitiuion rates in the chloroplast genome in herbaceous Olyreae compared with other Bambusoideae, which are predominantly woody (Wysocki et al. 2015).
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). There appears to have been horizontal gene transfer from the mitochondrion to the plastid in Bambusoideae-Olyreae (Wysocki et al. 2015).
Economic Importance. Glémin and Bataillon (2009) and Fuller (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. Hua et al. (2014) discuss the molecular basis of the loss of barbs on the awns and the shortening of the awns in the context of domestication of Oryza. The initial transition from wild plants to domesticates may be a gradual and quite slow process, as with other crop plants (Purugganan & Fuller 2011), and in barley at least there is a complex pattern of movement of genes from local wild populations into landraces (Poets et al. 2015).
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 are old hybrids, 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); for hybridization, etc., see Brassac et al. (2012), and for a series of papers on Triticeae, see J. Syst. Evol. 52(6). 2014. A very important plant for the study of C3 cereals is Brachypodium (Girin et al. 2014), although its exact relationships within Poöideae are unclear.
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. There have been comprehensive surveys of many aspects of grass morphology, anatomy, cytology, etc., 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). The leaf blades of Neurolepis (Bambusoideae) may be up to 4 m long.
For inflorescence morphology, see Kellogg et al. (2004, 2013). Where dehiscence occurs in grass spikelets varies considerably (Doust et al. 2014), and spikelets of closely related species in Andropogoneae may vary in features of both early and late development (Hodge & Kellogg 2014).
Ciaffi et al. (2011) and Kellogg (2015) summarize floral development. Unfortunately, the immediate relatives of Poaceae are unclear, the flowers of Anomochloa are sui generis, and those of Streptochaeta are not that simple... (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; Sajo et al. 2008: c.f. diagrams; Preston et al. 2009; Reinheimer & Kellogg 2009 for further details). Although Sajo et al. (2011, esp. 2012) tentatively described the flowers of Anomochloa as having palea and lemma (bracteoles, prophylls respectively), lodicules, etc., working out similarities between its flowers and those of other monocots around here is difficult. 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; the lateral stamens are suppressed.
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 suggests that the lemma is a bract and the palea represents two connate tepals of the outer whorl. The tepaloid nature of the lodicules is relatively uncontroversial (see Sajo et al. 2007; Reinheimer & Kellogg 2009; Yoshida 2012; Glover et al. 2015) and they can be surprisingly (for a non-agrostologist) variable (Wölk & Röser 2014).
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).
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, in which the seed coat and pericarp are fused, is often described as being a distinctive fruit type of the Poaceae; it is basically a variant of an achene. However, as Nakamura et al. (2009 and references) note, fruits 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.
All Poaceae have a well-differentiated 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, thus the scutellum and coleoptile originate 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. Kaplan (1997: 1 ch. 4, 5) thought that the "radicle" was endogenous in origin and was really a lateral root; Poaceae thus lacked a radicle proper, and so were homorhizic. 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 (2015) 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 pyrrolizidine alkaloids, see Nurhayati et al. (2009), 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, 2015) 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. W. 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, as have some genera in Poöideae, etc.. In a multi-gene study, Bouchenak-Khelladi et al. (2008) did not find strong evidence for the monophyly of Anomochloöideae, 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 largely uncertain. The relationships of Poöideae (Hodkinson et al. 2007; Duvall et al. 2008a) and Ehrhartoideae (Cahoon et al. 2010, as Oryzoideae) were also 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 within 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 = [Aristidoideae [Panicoideae [[Arundinoideae + Micrairoideae] [Danthonioideae + Chloridoideae]]]]) and BEP (= [Ehrhartoideae [Bambusoideae + Poöideae]]) clades, although support for the first two branches in the PACMAD clade is still only weak (see also Spriggs et al. 2014). Indeed, the positions of the first two subfamilies in the PACMAD clade were reversed in the complete plastome analysis of Cotton et al. (2015), although the other subfamilial groups were the same and support was mostly strong; however, relationships were scrambled in mitochondrial analyses.
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 now combined (Sánchez-Ken & Clark 2010; Teerawatananon et al. 2012), hence PACCMAD → PACMAD - Silva et al. (2015) provide a summary phylogeny. For relationships within Paniceae, see Zuloaga et al. (2000), Gómez-Martínez and Culham (2000), Morrone et al. (2010, esp. 2012). Core subtribes include [Panicinae [Melinidinae + Cenchrinae]] (Washburn et al. 2015: some conflict between the genomic compartments). For the bristle clade of Paniceae, see Doust et al. (2007), and for relationships within Panicum itself, see Aliscioni et al. (2003) and Sede et al. (2008); see also Sede et al. (2009) and Zuloaga et al. (2015) for new genera, etc.. Paniceae-Cenchrineae include Pennisetum, in which Cenchrus is embedded (see Donadío et al. 2009; Chemisquy et al. 2010), and also Setaria (for relationships here, see Kellogg et al. 2009). Salariato et al. (2010) examined relationships within Paniceae-Melinidinae, particularly from the point of view of inflorescence evolution. Other relationships include [Paspaleae [Arundinelleae + Anropogoneae]] (e.g. Washburn et al. 2015). For the phylogeny of Andropogoneae, see Kellogg (2000c) and Mathews et al. (2002); for Saccharinae and Sorghinae, see Kellogg (2013b: summary). Ng'uni et al. (2010) and Hawkins et al. (2015) looked at relationships within Sorghum; the genus is polyphyletic, with a segregate, Sarga, being sister to Saccharum and Miscanthus. In Paspaleae, for the relationships of Paspalum, basically monophyletic, see Rua et al. (2010) and Scataglini et al. (2014), López and Morrone adjusted the limits of Axonopus, and for two new genera, see Silva et al. (2015). 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, although the bulk of Sporobolus, with the inclusion of a few genera like Spartina, forms a well-supported clade with considerable internal structure (Peterson et al. 2014b), 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). Peterson et al. (2015a, b) provide a phylogeny for Cynodonteae-Eleusininae and -Boutelouinae respectively, and within the latter there is some quite wide hybridization. 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).
Oryzoideae. The relationships of Oryzeae have been much studied (Guo & Ge 2005; L. Tang et al. 2010 and references); for diversification within Zizaniinae, see L. Tang et al. (2015) and 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. However, the woody temperate Arundinarieae may be sister to the rest of the subfamily, thus 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 (see also Ruiz-Sanchez & Sosa 2015). However, Kelchner and the Bamboo Phylogeny Group (2013) noted that the position of Olyreae in particular was not secure, and they might be sister to the rest of the subfamily, indeed, relationships may differ depending on whether the genes analysed are from the chloroplast ([Bambuseae + Olyreae]) or nucleus ([Bambuseae + Arundinarieae]) (Wysocki et al. 2014, esp. 2015: plastome analysis).
For a phylogeny of the woody bamboos, see Clark et al. (2008: resolution poor); Triplett et al. (2014) suggested several hybridization events involving three main genomes and two minor genomes that link Bambuseae and Arundinarieae; diploids with those genomes are extinct, while Olyreae have yet another genome that has doubled by autopolyploidy. Indeed, hybridization seems to pervade this clade. For the phylogeny of neotropical woody bamboos, see Clark et al. (2008) and Fisher et al. (2009), and for hybridization here, see Goh et al. (2013), for neotropical Bambusoideae, see Burke et al. (2014). For relationships in 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), and of Bambuseae-Arthrostylidiinae, see Tyrrell et al. (2009, 2012). Disentangling relationships in Arundinarieae, the temperate woody bamboos, is proving difficult (see Peng et al. 2008). 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 plastome analyses was pulverised into 24 bits in nucleome analyses; hybridization is involved (Y.-X. Zhang et al. 2012; see also H.-M. Yang et al. 2013); all Arundinarieae may be descended from an allotetraploid ancestor (Triplett et al. 2011). Although P.-F. Ma et al. (2014) found substantial resolution in a chloroplast phylogenomic study, this is only part of this bigger issue. Ma et al. (2014) recovered Angulocalamus as sister to the rest of the tribe, and even with their rather restricted sampling, Indocalamus and Arundinaria were polyphyletic. Relationships within the large neotropical Chusquea are discussed by Fisher et al. (2014). Within Olyreae, a herbaceous clade, the monotypic Buergersiochloa, from New Guinea, may be sister to the rest, which are plants of the New World (e.g. Kellogg & Watson 1993; W. Zhang & Clark 2000; Bouchenak-Khelladi 2008). However, much remains uncertain about relationships within this clade in combined analyses, with 17/32 nodes collapsing in a strict consensus (Oliveira et al. 2014).
Poöideae. There are several papers on Poöideae in Aliso 23: 335-471. 2008; see also Soreng and Davis (2000), Schneider et al. (2009), Blaner et al. (2015) and Hochbach et al. (2015: inc. nuclear genees, their tree followed above) for relationships within the subfamily; some of the more basal clades used to be in Bambusoideae. 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; see also Minaya et al. 2015). For relationships and morphology in Phaenospermateae (inc. Duthieae), see Schneider et al. (2011), but c.f. in part Blaner et al. (2015) and Hochbach et al. (2015); Phaenosperma itself is a very distinct plant previously included in Bambusoideae. Relationships in the Phaenospermateae-Stipeae-Diarrheneae area remain unclear. Saarela et al. (2015; see Romaschenko et al. 2014) suggested that Ampelodesmeae are hybrids between Stipeae (the maternal parent, hence the placement of the former within the latter in chloroplast analyses) and Phaenospermateae, hence some of the phylogenetic conflict in this area. An analysis of 45 plastomes yielded the relationships [Brachyelytreae [Phaenospermateae [Meliceae [Stipeae [Diarrheneae [Brachypodieae + The Rest]]]]] (Saarela et al. 2015), but Nardeae, Duthieae, Brylkineae, Lygeae, and genera like Littledalea were not included, and also comparisons of plastome trees with relationships suggested by the nuclear genome are going to be important. Furthermore, the single species of Brachypodium included, an annual, was on a very long branch, and Saarela et al. (2015) discuss uncertainties as to the exact position of Brachypodieae - Brachypodium is very important plant for research on C3 cereals (see above). For relationships and hybridization in Triticeae, see Sha et al. (2014), Sun (2014), and R. R. Wang and Lu (2014).
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, 2015; Gillespie & Soreng 2011). Saarela et al. (2015) found that the Poeae they examined fell into two well-supported clades, both with numerous indels. For relationships in Poa itself, see Gillespie and Soreng (2005), Gillespie et al. (2009), Soreng et al. (2010, 2011), Hoffmann et al. (2013) and Birch et al. (2014: Australasian species). 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. Genera like Ampelodesmos and Stephanachne may end up in Stipeae or Duthieae, depending on the analyses, perhaps suggesting ancient hybridization (Blaner et al. 2015). For the Anthoxanthum/Hierochloë (Phalarideae) problem, the resolution of which also depends on understanding patterns of hybridization, see Pimentel et al. (2013), in Stipeae, Romaschenko et al. (2014) disentangled relationships in which old hybridization was involved, and the distribution of topoisomerase 6 copies in the African Trisetiopsis (Helicotrichon area) shows some species with a copy currently known only from New World grasses (Wölk & Röser 2014).
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 (2015), while at Soreng et al. (2000 onwards) is a phylogenetic classification - a bit splitty - of the family that is kept current (see Soreng et al. 2015 for a static version).
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, 2014a: some Cynodonteae, 2014b: Sporobolinae, with an infrageneric breakdown of Sporobolus, which includes Spartina as a section; 2015b: infrageneric classification of Bouteloua). 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, but they remain unclear (e.g. see Saarela et al. 2015 for two different classifications). 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.). Poa is not monophyletic, so its limits will have to be extended or the genus split (Hoffmann et al. 2013).
Thorne and Reveal (2007) thought that the earliest name for Chloridoideae was Chondrosoideae Link, a sort of resurrection name - Googling it (as of 3.vii.2007) returned only references to 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 very unhelpful in such situations even if the literature has been correctly interpreted (see also Welker et al. 2014).
Vorontsova and Simon (2012) estimated that 10-20% of all species names will 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 firmly resisted, and synthesis will be needed. Given all the ongoing work in the family, web-based lists are much to be desired, so Soreng et al. (2000 onwards - see Catalogue of New World Grasses), and at the same address "A worldwide phylogenetic classification of Poaceae (Gramineae): cao, capim, çayir, çimen, darbha, ghaas, ghas, gish, gramas, graminius, gräser, grasses, gyokh, he-ben-ke, hullu, kasa, kusa, nyasi, pastos, pillu, pullu, zlaki, etc." that includes all recognized suprageneric taxa) may be preferred over GrassBase and the lists dependent on it like the World Checklist of Monocots. There are also other resources like GrassWorld (Simon 2007), although this is likely to become static after 2020, and the challenge is to integrate information from different sources/with different goals and different classifications into a single resource (Vorontsova et al. 2015).
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.