LIGNOPHYTA

True roots +; lateral meristems: cork cambium producing cork abaxially, vascular cambium producing phloem abaxially and xylem adaxially.

EXTANT SEED PLANTS/SPERMATOPHYTA

Plant woody, evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins derived from (some) sinapyl and particularly coniferyl alcohols, thus containing p-hydroxyphenyl and guaiacyl lignin units, (lignins derived from p-coumaryl alcohol, i.e. S [syringyl] lignin units); true roots present, apex multicellular, xylem exarch, and branching endogenous; arbuscular mycorrhizae +; shoot apical meristem multicellular, interface specific plasmodesmatal network; stem with ectophloic eustele, endodermis 0, xylem endarch, branching exogenous; vascular tissue in t.s. discontinuous by interfascicular regions; vascular cambium + [xylem ("wood") differentiating internally, phloem externally]; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, plastids with starch grains; phloem fibres +; stem cork cambium superficial, root cork cambium deep seated; leaves with single trace from sympodium ["nodes 1:1"]; stomata ?; leaf vascular bundles collateral; leaves megaphyllous [determinancy evolved first, then ad/abaxial symmetry], spiral, simple, lamina with vein density up to 5 mm/mm² [mean for all non-angiosperms 1.8]; axillary buds associated with at most some leaves; prophylls [including bracteoles] two, lateral; plant heterosporous, sporangia eusporangiate, on sporophylls, sporophylls aggregated in indeterminate cones/strobili; true pollen [microspores, i.e. no distal pore for release of gametes] +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, crassinucellate, megaspore tetrad tetrahedral, only one megaspore develops, megasporangium indehiscent; male gametophyte development first endo- then exosporic, tube developing from distal end of grain, to ca 2 mm from receptive surface to egg, gametes two, developing after pollination, with cell walls, with many flagellae; female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large", first cell wall of zygote transverse, embryo straight, endoscopic [suspensor +], short-minute, with morphological dormancy, white, cotyledons 2; plastid transmission maternal; two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], nrDNA with 5.8S and 5S rDNA in separate clusters; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.

MAGNOLIOPHYTA

Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, non-hydrolysable tannins, quercetin and/or kaempferol +, apigenin and/or luteolin scattered, [cyanogenesis in ANITA grade?], S [syringyl] lignin units common, positive Maüle reaction [syringyl:guaiacyl ratio more than 2-2.5:1], and hemicelluloses as xyloglucans; root apical meristem intermediate-open; root vascular tissue oligarch [di- to pentarch], lateral roots arise opposite or immediately to the side of [when diarch] xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, with gelatinous fibres; 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 cells from same mother cell that gave rise to the sieve tube; sugar transport in phloem passive; nodes unilacunar [1:?]; stomata with ends of guard cells level with pore, paracytic, outer stomatal ledges producing vestibule; leaves petiolate, lamina [formed from the primordial leaf apex], development of venation acropetal, 2ndary veins pinnate, fine venation reticulate, veins (1.7-)4.1(-5.7) mm/mm², endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, polysymmetric, parts spiral [esp. the A], free, numbers unstable, development in general centripetal; P not sharply differentiated, with a single trace, outer members not enclosing the rest of the bud, often smaller than inner members; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], ± embedded in the filament, with at least outer secondary parietal cells dividing, each theca dehiscing longitudinally by action of hypodermal endothecium, endothecial cells elongated at right angles to long axis of anther; tapetum glandular, binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellar, endexine thin, compact, lamellate only in the apertural regions; nectary 0; G free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, dry [not secretory]; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across [crassinucellate], nucellar cap?; megasporocyte single, hypodermal, megaspore tetrad linear, functional megaspore chalazal, lacking sporopollenin and cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; P deciduous in fruit; seed exotestal; pollen binucleate at dispersal, trinucleate eventually, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing at 80-600 µm/hour, with pectic outer wall, callose inner wall and callose plugs, growing between cells, penetration of ovules via micropyle [porogamous] within ca 18 hours, distance to first ovule 1.1.-2.1 mm, tube moves between nucellar cells; double fertilisation +, endosperm diploid, cellular [micropylar and chalazal domains develop diffently, first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous, embryo cellular ab initio, minute; germination hypogeal, seedlings/young plants sympodial; Arabidopsis-type telomeres [(TTTAGGG)_n]; whole genome duplication, ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, paleo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]].

Evolution. Possible apomorphies for flowering plants are in bold. Note that the actual level to which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is because some taxa basal to the [magnoliid + monocot + eudicot] group have been surprisingly little studied, there is considerable homoplasy as well as variation within and between families of the ANITA grade in particular for several of these characters, and also because details of relationships among gymnosperms will affect the level at which some of these characters are pegged. For example, if reticulate-perforate pollen is optimized to the next node on the tree (see Friis et al. 2009 for a discussion), it effectively makes the pollen morphology of the common ancestor of all angiosperms ambiguous... For other features such as details of sugar transport in the phloem, their placement on the tree is frankly speculative. Finally, for features such as parietal tissue/a nucellus only one (Nymphaeales) to three cells thick above the embryo sac and a stylar canal lacking an epidermal layer, although plesiomorphous for basal grade angiosperms (Williams 2009), I am unsure where on the tree a thicker nucellus and a stylar epidermal layer are acquired.

[NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]]: vessels +, elements with elongated scalariform perforation plates; wood fibres +; axial parenchyma diffuse or diffuse-in-aggregates; tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.

Phylogeny. Relationships of the main groups within commelinids are unclear; for further information, see discussion preceding Dasypogonaceae, also Commelinales and Zingiberales.

[POALES [COMMELINALES + ZINGIBERALES]]: primary cell wall mostly with glucurono-arabinoxylans; stomata subsidiary cells with parallel cell divisions; endosperm reserves starchy.

Evolution. Divergence & Distribution. The stem group for this clade dates to about 120 million years before present, while Poales diverged from [Commelinales + Zingiberales] ca 117 million years before present (from Janssen & Bremer 2004); Magallón and Castillo (2009, which consult for more details) suggest ca 123 million years for relaxed and 111 million years for constrained penalized likelihood stem group datings of Poales, the stem group of the whole clade being 128 to 115 million years old (relaxed and constrained estimates again).

Plant-Animal Interactions. Sap-eating chinch bugs of the Hemiptera-Lygaeidae-Blissinae have been recorded from taxa throughout this clade, although they occur on Poales and especially Poaceae most frequently (Slater 1976).

Chemistry, Morphology, etc. For primary cell wall composition, see literature in Harris (2005); Arecaceae sampled are somewhat intermediate between this clade and other monocots. For stomatal development, see Tomlinson (1974) and Rudall (2000); development in Dasypogonaceae is apparently unknown.

POALES Small  Main Tree, Synapomorphies.

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; P = K + C; style well developed, stigmas small, dry; micropyle bistomal, both integuments ca 2 cells across; endosperm nuclear, embryo size?; cotyledon hyperphyllar, haustorial [?level]; mitochondrial sdh3 gene lost. - 17 families, 997 genera, 18325 species.

Evolution. Divergence & Distribution. Divergence within the Poales clade begins ca 113 million years before present (Janssen & Bremer 2004) or 109-106 million years before present (Leebens-Mack et al. 2005). However, Wikström et al. (2001) suggest a much younger age for the clade of 87-83 million years before present, divergence beginning 72-69 million years before present. Magallón and Castillo (2009, which consult for more details) suggest ca 109-108 million years for relaxed and 99 million years for constrained penalized likelihood crown group datings - probably underestimates. If the identity of Protoananas lucenae, 114-112 million years old and from Brazil, is confirmed - stem of Bromeliaceae (Leme & Brown 2011) - old dates for the clade are again suggested.

Magallón and Castillo (2009) suggest that Poales in the broad sense have the highest diversification rate in the monocots, about the same as Asparagales, but in both the rate is little over half that of Lamiales. Interestingly, Cornwell et al. (2008) found that litter decomposition of forbs was faster than that of graminoids - presumably mostly grasses and sedges - indeed, litter decomposition of monocots (sic) was slower that that of other angiosperms; such differences are connected with the rate of nutrient cycling in the environment.

Ecology & Physiology. C₄ photosynthesis is common in Poales, and origins are clustered in Briomeliaceae, Poaceae, and Cyperaceae.

Plant-Animal Interactions. Many host-plants of reed beetles, Chrysomelidae-Donaciinae, are scattered in Poales, especially in Typhaceae, Juncaceae, and Cyperaceae (Kölsch & Pedersen 2008: much discussion on the age and evolution of the group). They show close co-speciation with endosymbiotic bacteria (gamma proteobacteria-Enterobacteriaceae - near Buchnera), which are believed to produce the material that makes up the cocoon that characterises this beetle clade, which is also noted for the larvae being able to grow under water (Kölsch & Pedersen 2010).

Floral Biology & Seed Dispersal. For the repeated evolution of wind pollination in this clade, see Givnish et al. (2010a, b).

Chemistry, Morphology, etc. There is interesting variation in the way pollen is arranged in the pollen loculi; the plesiomorphous condition is likely to be central, i.e., some grains are not in contact with the tapetum, but in some taxa it is peripheral, all grains being in contact with the tapetum (Kirpes et al. 1996). General information is taken from Linder and Rudall (1993) and (2005: detailed discussion of morphological evolution and diversification in Poales); see Doyle et al. (1991) for chloroplast inversions, Prychid et al. (2004) for SiO₂ bodies, Ong and Palmer (2006) for the rps14 nuclear gene/mitochondrial pseudogene system, and for seedling morphology and evolution, see Tillich (2007).

Phylogeny. The order itself does not always have very strong support, but cf. e.g. Givnish et al. (2010b). 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 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 have septal nectaries (along with Rapateaceae) alone in Poales. Bromeliaceae and Typhaceae are often placed as basal branches with respect to other clades in Poales (Givnish et al. 2005, 2008 [but rooting]; also Graham et al. 2006). Nevertheless, Rapateaceae appear to be sister to all other Poales in some analyses (e.g. Davis et al. 2004), albeit with little support. 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; cf. Givnish et al. 2006b). Similarly, Typhaceae are placed sister to Bromeliaceae with weak jacknife support but strong Bayesian posterior probabilities (Bremer 2002). Other recent work also suggests that Typhaceae and Bromeliaceae form a clade sister to other Poales, and Rapateaceae are in turn sister to the remainder (Chase et al. 2006; see also Rudall & Linder 2005; Givnish et al. 2005, 2007, but rooting; Graham et al. 2006 for this latter position; Soltis et al. 2011, strong support, but sampling), although these relationships are not always obtained (Givnish et al. 2010a). Indeed, Givnish et al. (2010b) found quite strong support in both maximum parsimoney and maximum likelihood plastome analyses for the topology [Bromeliaceae [Typhaceae s.l. [Rapateaceae + rest of Poales]]] (see also Barrett & Davis 2011).

Within remaining Poales there are some well-supported groups, the Xyridaceae, Juncaceae, and Poaceae and their respective relatives, although the exact composition of the first clade remains somewhat unclear. 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).

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 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.

1. Cyperaceae and Eriocaulaceae and their relatives may form one clade. Xyridales of Kubitzki (1998c) had included Mayacaceae, Xyridaceae, Eriocaulaceae and Rapateaceae. However, there was some evidence for a group with the first three families, perhaps, but not very probably, also including Rapateaceae (Rapateaceae are sister to [Juncaceae + Xyridaceae + Poaceae groups] in Givnish et al. 2005). 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 are in adjacent branches along the spine of the tree, with one including Flagellariaceae, the Juncaceae group, some Xyridaceae, Mayacaceae, and perhaps Hydatellaceae. Note also that Xyridaceae and Mayacaceae have more or less clawed petals and anthers with an exothecium. Finally, some studies (ref.?) have linked Mayacaceae with Rapateaceae, and both have poricidal anthers. Clearly, there are a number of distinctive characters in this group of families, but relationships within the group remain unclear.

The situation may, however, be becoming tidier. Saarela et al. (2006, esp. 2007) conclusively showed that Hydatellaceae are completely misplaced and belong to Nymphaeales, being sister to other members of that clade, and this new position has very strong molecular and morphological support. The three members of the old Xyridales that remain here may form a grade at the base of the clade [Thurniaceae [Juncaceae + Cyperaceae]]: Mayacaceae are sister to the other members, then [Xyridaceae + Eriocaulaceae] are sister to Cyperaceae and their relatives (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.]. 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).

2. Poaceae and their immediate relatives form the other clade. (Note that in versions 6 [before November] and earlier of this site, Eriocaulaceae and their relatives were weakly linked to Poaceae et al.).

Includes Anarthriaceae, Bromeliaceae, Centrolepidaceae, Cyperaceae, Ecdeiocoleaceae, Eriocaulaceae, Flagellariaceae, Joinvilleaceae, Juncaceae, Mayacaceae, Poaceae, Rapateaceae, Restionaceae, Thurniaceae, Typhaceae, Xyridaceae.

Synonymy: Eriocaulineae Thorne & Reveal, Xyridineae Thorne & Reveal - Avenales Bromhead, Bromeliales Link, Centrolepidales Takhtajan, Cyperales Berchtold & J. Presl, Eriocaulales Nakai, Flagellariales Reveal & Doweld, Juncales Berchtold & J. Presl, Mayacales Nakai, Rapateales Reveal & Doweld, Restionales Berchtold & J. Presl, Typhales Berchtold & J. Presl, Xyridales Lindley

[Typhaceae + Bromeliaceae]: stomatal subsidiary cells with oblique divisions; leaf without distinct sheath; three-nucleotide deletion in the atpA gene.

TYPHACEAE Jussieu, nom. cons.   Back to Poales

Plant rhizomatous; flavonoids +; SiO₂ bodies 0; starch grains pteridophyte-type, amylophilic; leaves two-ranked; plant monoecious; inflorescences complex, gap between staminate and pistillate inflorescences; flowers very small; P chaffy; A 1-8; tapetum plasmodial, 8 nuclei/cell; pollen grains trinucleate, monoulcerate; nectary 0; G pseudomonomerous, style + [?], branches long, stigma rather elongated, on one side; ovule 1/carpel, pendulous, apotropous, nucellar cap ca 2 cells across, obturator +; seed coat ± obliterated; endosperm helobial, cell wall formation in small chalazal chamber before that in large micropylar chamber, perisperm thin, embryo long, slender; x = 15; ORF 2280 deletion; seedling with hypocotyl and collar hairs.

2/ca 25. More or less world-wide.

Sparganium L.

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: stigma papillate; antipodal cells multiply after fertilisation; fruit a spongy drupe, with micropylar plug, P persistent; testa membranaceous; 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).

Synonymy: Sparganiaceae Hanin, nom. cons.

Typha L.

(Styloids +); cuticular waxes as aggregated rodlets; leaf with distinct sheath; inflorescence densely spicate, (no gap between staminate and pistillate part); P 0; staminate flowers: A connate; tapetal cells ?8-nucleate; (pollen in tetrads); carpellate flowers: long hairs on pedicels; 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 - note that the map in Knobloch & Mai 1986 differs very considerably from its source, Meusel et al. 1965). [Photos - Collection]

• Sparganium is a rhizomatous aquatic with linear leaves and inflorescences with a few spherical heads of flowers, carpellate towards the base of the inflorescence and staminate towards the apex. Typha is a robust, rhizomatous herb that likes damp conditions and has erect, linear leaves and distinctive, elongated, densely cylindrical inflorescences, the part containing the carpellate flowers being borne below and separate from the part with the staminate flowers.

Evolution. Divergence & Distribution. Typhaceae are ca 109 million years old, the two genera included separating ca 89 million years before present (Janssen & Bremer 2004). For the rich fossil record of the family - although Cretaceous occurrences need re-evaluating - see Smith et al. (2010); Collinson and van Bergen (2004) found similar chemical signatures in fruits of extant and fossil representatives of both genera.

Bacterial/Fungal Associations. Similar rusts are shared by the two genera (Savile 1979).

Chemistry, Morphology, etc. Much information is taken from Kubitzki (1998d: general); see also D. Müller-Doblies (1970: inflorescence and flower) and Grayum (1992: pollen). The two genera are palynologically almost identical; for the pollen of Typha, see Albert et al. (2011).

For general information on Typha, see Thieret and Luken (1996: southeast U.S.A.). Some flowers of Sparganium may have a second, empty loculus, or there may even be three fertile loculi (Dahlgren et al. 1985). On the other hand, fossil Sparganium may have up to 7-locular fruits (Cook & Nicholls 1986)! See U. Müller-Doblies (1970) for flower and embryology.

Phylogeny. For phylogenetic relationships in Typha, see Kim and Choi (2011).

Classification. See Cook and Nicholls (1986, 1987) for a monograph of Sparganium.

BROMELIACEAE Jussieu, nom. cons.   Back to Poales

Rosette plants, usu. herbs; (C-glycosylated/6-oxygenated) flavones, flavonols +; vessel elements with scalariform perforation plates; mucilage +; cuticular waxes as aggregated rodlets; stomata with oblique cell divisions; water storage tissue in mesophyll, fibrous bundle sheaths +; indumentum lepidote; leaves spiral, curved, thick, horny, base dilated; inflorescence bracts often coloured; (A basally connate), (adnate to C); septal nectaries +, style + long, apically ± trifid, conduplicate-spiral, stigmas also wet; ovules 2-many/carpel, nucellar epidermis cells anticlinally elongated [?all]. (nucellar cap ca 2 cells across); fruit a septicidal capsule, K persistent; seeds testal-tegmic, testa to 7 cells across, cells variously thickened, tegmen ca 2 cells across, (exitegmen thickened), endotegmen tanniniferous; endosperm helobial, cell wall formation in small chalazal chamber precedes that in large micropylar chamber, embryo (long), cylindrical, often lateral; hypocotyl and hypophyll common; x = 25, chromosomes 2.75³ µm long.

57[list]/1770 - eight groups below. (Sub)tropical America; W. tropical Africa (map: from Givnish 2004a). [Photo - Flower.]

1. Brocchinioideae Givnish

(Tank bromeliads, stem erect and with intracauline adventitious roots); leaves with stellate chlorenchyma, margin ?; C minute; G ± inferior, septal nectary above the ovules; seeds caudate, (basal tuft of hairs +); n = ?9, 23.

1/21. South America, the Guyana Highlands (map: from Smith & Downs 1974).

[Lindmanioideae [Tillandsioideae [Hechtioideae [Navioideae [Pitcairnioideae [Puyoideae + Bromelioideae]]]]]]: cap cells of trichomes dead; septal nectaries below the ovular zone.

2. Lindmanioideae Givnish

Stellate chlorenchyma 0; leaf margin entire/serrate; K contorted; stigmas straight; seeds caudate; cotyledonary hypophyll blade-like.

1-2/43. South America, the Guyana Highlands.

[Tillandsioideae [Hechtioideae [Navioideae [Pitcairnioideae [Puyoideae + Bromelioideae]]]]]: (C often with subbasal scales and/or longitudinal callosities).

3. Tillandsioideae Burnett

Epiphytes, air bromeliads (also tank forming), roots often for attachment only (0); scales radially symmetrical; leaf margins entire; (flowers in inflorescence two-ranked); (pollen with raphides); ovules with long chalazal projection, (outer integument ca 5 cells across); seeds caudate because of greatly elongating outer integument, apical and/or basal tufts of hair usu. derived from longitudinal splitting of the outer integument; (n = 17, 21), karyotype bimodal; primary root none or soon aborting.

9/1015: Tillandsia (620: polyphyletic), Vriesia (195: poly/paraphyletic), Guzmania (170), Werauhia (70), Racinaea (60). Almost the range of the family in America.[Photo - Flower]

Variation in stigma morphology is great (Brown & Gilmartin 1989).

For phylogenetic relationships, see Barfuss et al. (2004, 2005, the latter with a tribal classification and extensive discussion on morphology); generic limits need attention!

Synonymy: Tillandsiaceae Wilbread

[Hechtioideae [Navioideae [Pitcairnioideae [Puyoideae + Bromelioideae]]]]: ?

4. Hechtioideae Givnish

Plant xeromorphic; (CAM photosynthesis +); hypodermal sclerenchyma +, internal water storage tissue +, chlorenchyma undifferentiated; trichomes in parallel rows; leaf margin serrate (entire); plant dioecious; (G subinferior), stigma simple-erect; seeds winged (not); cotyledonary hypophyll blade-like.

1/51. Texas, Mexico, N. Central America.

[Navioideae [Pitcairnioideae [Puyoideae + Bromelioideae]]]: ?

5. Navioideae Harms

Xeromorphic; peripheral water storage tissue +, stellate chlorenchyma 0; leaf margin serrate/entire; C minute; seeds winged or not.

5/105: Navia (98). Guyana Highlands, N.E. Brasil.

[Pitcairnioideae [Puyoideae + Bromelioideae]]: ?

6. Pitcairnioideae Harms

Scales ± divided, or hairs stellate; leaf margin?; (flowers monosymmetric), G to inferior; ovules with chalazal appendage, (outer integument ca 5 cells across), (parietal tissue several cell layers across); seeds tailed, body cells differing from tails, winged, or not; embryo lateral or not; (karyotype bimodal); hypocotyl quite long, cotyledonary hypophyll blade-like, (collar rhizoids - Pitcairnia).

5/515: Pitcairnia (405), Dyckia (150), Forsterella (30). Mexico to Chile, Pitcairnia feliciana W. Africa.

[Puyoideae + Bromelioideae]: ?

7. Puyoideae Givnish

Rather xeromorphic; hypodermal sclerenchyma +, internal water storage tissue +, chlorenchyma undifferentiated; trichomes in parallel rows, foliar trichomes with well developed wings; 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.

1/195. Mountains, etc., Costa Rica and Guyana to Chile and Argentina. [Photos - Puya Flower, Puya Habit, Puya Habit.]

8. Bromelioideae Burnett

Epiphytes, often tank bromeliads, roots often for attachment only; CAM photosynthesis common; scales irregular peltate; leaf margin entire/serrate; (perianth tube/hypanthium +), (K asymmetrical), (C with adaxial subbasal petal appendages); (pollen porate), (with raphides); G inferior, ovules with chalazal [= funicular] appendage, micropyle also endostomal, stigma conduplicate, spiral; fruit baccate; seed usu. without an appendage; sarcotesta [gelatinous] common; embryo lateral; (n = 17, 21); (cotyledon not photosynthetic), collar rhizoids +, primary root prominent, short hypocotyl present; (n = 17).

31/722: Aechmea (185), Neoregelia (100), Billbergia (65), Bromelia (50), Hohenbergia (50), Nidularium (50). Mexico and the West Indies to Chile, esp. Brazil. [Photo - Flower, Fruit, Flower, Flower.]

• Bromeliaceae are often rosette plants, the leaves always being tough, spirally arranged, lacking a distinct sheath, and often with spiny-toothed margins; the indumentum is scaly (lepidote); and the terminal inflorescence is prominently bracteate, the bracts sometimes being coloured. The flowers have a calyx and corolla, and the petals, although free, are erect and form a tube.

Evolution. Divergence & Distribution. Stem-group Bromeliaceae are dated to ca 112 million years before present, divergence within the crown group to ca 96 million years before present (Janssen & Bremer 2004: Brocchinia not included). Wikström et al. (2001) suggests a stem group age of 72-69 million years before present... However, other estimates of divergence within the family are much more recent. Thus Givnish et al. (2004a, 2008a) suggest stem ages of 84 and crown ages of a mere 23-19 million years before present respectively, with radiation from an ancestral home on the Guayana Shield (see also Givnish et al. 1997, 2011a [q.v. for much more detail], b). Recent estimates are even more extreme, with a ca 80 million year hiatus between the origin of stem and crown Bromeliaceae (stem ca 100 million years, crown ca 19 million years) that is perhaps explained by the occurrence of much extinction (Givnish et al. 2011a, b). The situation is becoming yet more confused. Protoananas lucenae, from the Crato limestone of Brazil and some 114-112 million years old, has been assigned to a "putative ancestral stem-lineage of Bromeliaceae" (Leme & Brown 2011: p. 217), but also described 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).

Givnish et al. (2004a, 2008a) provide a phylogeny and discuss the biogeography of the group, while Givnish et al. (2008) also discuss the evolution of CAM, bird pollination, epiphytism and xeromorphic traits (see also Smith et al. 2005; Nyffeler & Eggli 2010b). For diversification rates in the family, particularly high in tank epiphytes, see Givnish et al. (2011b). For more details, see below.

Plant-Animal Interactions. Riodininae-Riodininae larvae may be found on Bromeliaceae (and Orchidaceae: Hall 2003 and references).

Floral Biology & Seed Dispersal. Bird pollination is common in Bromeliaceae (Stile 1981 and references; Givnish et al. 2008), although entomophily is the ancestral condition (Givnish et al. 2011b). It is odd that there appears to be no prezygotic reproductive isolation between species of Bromeliaceae growing together in southeastern Brazil; the flowers are not notably different morphologically and flowering times overlap extensively, yet hybrids are very uncommon (Wendt et al. 2008).

Dispersal is rather predictable: by animals or wind. However, recent work suggests that the coma on the seeds of Catopsis (Tillandsioideae) may also assist materially in both germination and the establishment of the seedling 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 water may be at a premium (Wester & Zotz 2011). Note that 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).

Ecology & Physiology. Some two thirds of Bromelioideae have some form of CAM metabolism and ca 44% have strong CAM, although details of the evolution of this feature remain unclear (Crayn et al. 2000, 2004; Reinert et al. 2003; Schulte et al. 2005). CAM has evolved more than once in the family, with considerable plasticity evident in Puya (Schulte et al. 2011). Quezada and Gianoli (2011) consider the acquisition of CAM photosynthesis to consist of a series of key innovations in Bromeliaceae; in five sister group comparisons the CAM clade was significantly more diverse than the non-CAM clade. Quezada and Gianoli (2011) suggest that CAM acquisition may have occured in the context of moving in to dry/arid habitats, rather than epiphytism.

The diversity of growth forms in Bromeliaceae is well known. Many taxa are terrestrial, and have a well-developed root system. Epiphytes are common. About 1,700 species - and so just over half the family - are epiphytic (Luther & Norton 2008: epilithic species not included). Roots in epiphytic Tillandsioideae may be for attachment only (see below), thus adult plants of Tillandsia usneoides (Spanish moss) entirely lack roots, the plants growing happily on any available support. A few Tillandsioideae also have tanks formed by the closely appressed overlapping bases of the leaves; the apical meristem is submerged and at the bottom of the tank, and these are especially well developed in Bromelioideae. In this latter subfamily there is a major clade that has tanks (taxa with tanks also often have asymmetric sepals and porate pollen - Schulte & Zizka 2008; Schulte et al. 2009). Roots may grow into the tank where they absorb the contents; Pittendrigh (1948) noted that such roots were mycorrhizal, while roots growing into the soil were not obviously mycorrhizal. A diverse fauna showing considerable endemism is associated with the tanks, the animals there including many insects, even specialised diving beetles (Dystiscidae) whose evolution may be almost contemporaneous with the appearance of the tank habitat (Balke et al. 2008), land crabs, earthworms, ostracod crustaceans, protists and the like (Thienemann 1934; Kitching 2000, general; Greeney 2001, bibliography) being found there, and in Trinidad, at least, mosquitoes that breed in the tanks help spread malaria (Pittendrigh 1948). Tanks are the habitat of a few carnivorous Utricularia, and also frogs may breed in them.

Hairs on the leaf surface are an integral part of how these various bromeliaceous growth forms function. Perhaps somewhat paradoxically, adaxial leaf surfaces in Bromelioideae and some other subfamilies are hydrophilic while abaxial surfaces are hydrophobic (Reuter & Brown 2009). Dense scales or a powdery epicuticular wax make the abaxial leaf surface wet and water-repellent so the stomata remain functional even in wet conditions, and it has 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); thus phosphate is taken up very efficiently by the hairs on the leaves in tank epiphytes like Aechmea fasciculata and either moved elsewhere in the plant or stored as phytin, the salt of a cyclic compound to which H₂PO₃ moieties are attached (Winkler & Zotz 2009; Gonsiska & Givnish 2009). The rather elegant multicellular peltate trichomes of Tillansioideae take in water and nutrients; they flex as they dry and pull away from the leaf surface, but when it rains they readily take up water and then lie flat on the surface (Benzing 1976; Pierce et al. 2001); water and nutrient absorbtion takes place then. Some Tillandsia use whatever they are growing on - branches, telegraph wires - simply for support (Wester & Zotz 2010 and references), leaves taking over the nutritional function of roots. Dried hairs in Tillandsia may also reflect light and so provide photoprotection (Pierce 2008).

Brocchinia is only a small genus and is restricted to the Roraima region, but it has a great variety of ways in which nitrogen is taken up, different growth forms, and it includes ant plants (B. acuminata); Givnish et al. (1997) discuss the diversification of the genus, which, although sister to the rest of the family, seems not to be that old (estimates of ca 14 million years - Givnish et al. 2004a, 2008a). For possible carnivory in Brocchinia reducta, see Givnish et al. (1984; Plachno & Jankun 2005). Since 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), it has been suggested that the former is a Müllerian mimic of the latter (Joel 1988). The tillandsioid Catopsis berteroniana traps terrestrial arthropods but also harbours larvae of the mosquito Wyeomyia (Frank & O'Meara 1984; Gonsiska & Givnish 2009).

Genes & Genomes. The rate of molecular evolution in Bromeliaceae is very low, ca 0.00059 substitutions/site/million years; although the family is not particularly woody, its members have a long generation time, which seems to be connected with this low rate of molecular evolution (Smith & Donoghue 2008).

Chemistry, Morphology, etc. The flowers of Tillandsia are shown as being inverted, but those of Bilbergia have the normal position with an abaxial median sepal (Spichiger et al. 2004); however, the former position is incorrect (W. Till, pers. comm.). Tapetum development is described as being intermediate, the cells being initially secretory, but tending to invade later (Sajo et al. 2005); 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 taxa with these "superior" ovaries (they are fused when the ovary is inferior). Variation in ovule morphology is extreme (e.g. Gross 1988a).

For information on petal appendages, Brown and Terry (1992), for stigma morphology, see Brown and Gilmartin (1988, 1989), for nectaries, Böhme (1988) and Sajo et al. (2004b), for the ovule, Sajo et al. (2004a), 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), for chromosomal evolution, see Gitaí et al. (2005), for phytoliths, see Piperno (2006), for cultivated bromeliads, Rauh (1990), etc., for rhizome and root anatomy, see Proença and Sajo (2008), for tetraporate pollen of Hohenbergia, see Albert et al. (2011), and for general information, Varadarajan and Gilmartin (1988b), Smith and Till (1998) and Benzing (2000).

Phylogeny. For phylogeny, etc., I largely follow Givnish et al. (2008a; 1 gene, good generic sampling, few species, but note rooting of their Fig. 1, also 2009, 2011a, b), which is rather similar to that in Schulte et al. (2005: focus on Bromelioideae). In earlier studies, Bromelioideae were monophyletic, even when Pitcairnioideae were included (Crayn et al. 2004: matK + rps16), however, in some studies (Horres et al. 2000) Puya did not link with them (see also Jabaily & Sytsma 2010). Hechtia (P: 55 - seeds with circumferential winging, as with Navia), were of uncertain position, not linking with either major group (Tillandsioideae, Bromelioideae + Pitcairnioideae) in 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). The subfamily is not apparent in Horres et al. (2000), although there is a group of Pitcairnioideae genera evident, 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). Givinish et al. (2011a) found strong support for most elements of the topology followed here, support for the monophyly of Pitcairnioideae and for the position of Navioideae improving over earlier studies, but the monophyly of Puyoideae was still not well supported; Puya may be paraphyletic.

For the association of Ayensua with Brocchinia and the phylogeny of the clade, see also Givnish et al. (1997) and Horres et al. (2000). Weising et al. (2011) outline phylogenetic relationships within Pitcairnioideae. For relationships within Bromelioideae, see Horres et al. (2007), Schulte and Zizka (2008) and especially Schulte et al. (2009). Bromelia serra alone may be sister to the rest of the subfamily, although support for this position is weak, and there is a large clade including it and other taxa that are all tank epiphytes. For relationships within Forsterella, Bromelioideae s. str., see Rex et al. (2009 and references). Relationships within the Tillandsia group appear to need substantial realignments (Barfuss et al. 2011). Relationships along the backbone of Puya are for the most part only weakly supported (Jabaily & Sytsma 2010: the morphological study of Puya subgenus Puya Hornung-Leoni & Sosa 2008 suggest somewhat different relationships); see Schulte et al. (2011) for relationships. For other phylogenetic studies, see Crayn et al. (2000), and Givnish et al. (2004b: ndhF).

Classification. The classic monograph of the family is that by Smith and Downs (1974, 1977, 1979), even if the supraspecific groups that they recognized are changing somewhat. The subfamilial classification of Givnish et al. (2008a) is followed here; see also the World Checklist of Monocots. Generic limits need attention in much of the family. Thus within Bromelioideae, Aechmea is hopelessly poly/paraphyletic (Schulte et al. 2009; Sass & Specht 2010) and generic limits there are generally unclear (Horres et al. 2007).

[Rapateaceae [[[Eriocaulaceae + Xyridaceae] [Mayacaceae [Thurniaceae [Juncaceae + Cyperaceae]]]] [[Anarthriaceae [Restionaceae + Centrolepidaceae]] [Flagellariaceae [[Joinvilleaceae + Ecdeiocoleaceae] Poaceae]]]]]: little oxalate accumulation; embryo minute, ± undifferentiated.

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 Anarthriaceae-Poacaeae clade. The exact condition of the embryo of the ancestor of this group is unclear. Malcomber et al. (2006) described the embryo of Joinvilleaceae and Ecdeicoleaceae as being undifferentiated, embryos of Centrolepidaceae seem to be undifferentiated (Hamann 1975), those of Restionaceae, largely undifferentiated (Linder et al. 1998), Mayacaceae, undifferentiated (Stevenson 1998), Eriocaulaceae, "poorly differentiated", or with "no exomorphological differentiation" (Stützel 1998). Embryos of the Cyperaceae group are described as being small, but they are more or less differentiated (e.g., see van der Veken 1965). Whatever its state of differentiation, the embryo is small and rather broad.

RAPATEACEAE Dumortier, nom. cons.   Back to Poales

Plants Al-accumulators, rhizomatous; (culm vascular bundles amphivasal); vessels in leaf?; mucilage cells +; cuticular wax with wax globules or wax 0, stomatal guard cells dumbbell-shaped; mucilage-producing multicellular hairs +; leaves (spirally) two-ranked, (petiole + lamina), sheath distinct, open or asymmetrical and conduplicate, uniseriate [slime-secreting] colleters +; inflorescence scapose, axis usu. indeterminate, units cymose, capitate (head subtended by spathaceous bracts), flowers with several basal "bracteoles", large; C basally connate; A basally connate, adnate to C or not, anthers dehiscing by pores, wall of the Reduced type; endothecial thickenings at apex of anther only (0); microsporogenesis simultaneous [tetrads tetrahedral]; (pollen grains with encircling aperture); style +, stigma capitate; ovules 1-many/carpel, (basal), apotropous, (micropyle endostomal), outer integument 3-10 cells across, nucellar epidermal cells often radially elongated [check], suprachalazal area ± massive, funicular obturator +; (antipodal cells several); fruit a septicidal capsule; (seeds carunculate, caruncle chalazal); 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; n = 11 [Maschalocephalus]; 26; seedling?

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.]

1. Rapateoideae Maguire

Involucral bracts long; ovule 1/carpel; seeds ovoid-oblongoid, (with papillate apical appendage).

3/29. The Guianas to Bolivia and the Matto Grosso.

2. Monotremoideae Givnish & P. E. Berry

Vessels with simple perforation plates; ovule 1/carpel; seeds ovoid-oblongoid, white-granulate [muriculate], with flattened apical appendage.

4/8. Guiana, upper Rio Negro in Colombia and Venezuela, Maschalocephalus dinklagei in Sierra Leone and Liberia.

3. Saxofridericioideae Maguire

(Leaves petiolate - Saxofridericieae; sheath with auricles - Stegolepis); seeds prismatic, pyramidal, lenticular or crescent-shaped.

9/54: Stegolepis (30+). N. South America, esp. the Guyana Highlands, Panama.

• Rapateaceae are rosette herbs with mucilage in the rosette. Their capitate, scapose inflorescences bear rather conspicuous flowers; the perianth is differentiated into calyx and corolla, there are six stamens, and the anthers dehisce by pores.

Evolution. Divergence & Distribution. Stem-group Rapateaceae are dated to ca 112 million years before present, divergence within the crown group to ca 79 million years before present (Janssen & Bremer 2004). Maschalocephalus dinklagei, the only African representative of the family, may have arrived there by long distance dispersal (Givnish et al. 2004a).

Chemistry, Morphology, etc. Septal nectaries seem not to occur in Rapateaceae except Monotremeae, but there are also reports of humming bird pollination of genera other than Monotremeae (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 (Tiemann 1985) they appear to be tenuinucellate.

Some information is taken from Stevenson et al. (1998a); for anatomy, see Carlquist (1966); for ovules and seeds, see Venturelli and Bouman (1988).

Phylogeny. Givnish et al. (2004a) provide a phylogeny of the group and discuss its biogeography.

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 + Centrolepidaceae]] [Flagellariaceae [[Joinvilleaceae + Ecdeiocoleaceae] Poaceae]]]]: (1->3),(1->4)-ß-D-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; pollen trinucleate; septal nectary 0; ovules with parietal tissue absent.

Evolution. Eco-Phsyiology. This clade in particular, but also core Caryophyllales, are the two major foci of the evolution of C₄ photosynthesis (Ehleringer et al. 1997). 24/62 of the independent 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 (2008) found a similar pattern. More recently, Givnish et al. (2010b) have 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); these glucans are sometimes present in only very small amounts and may be localized according to the thickening of the cell wall (see also Smith & Harris 1999). Rapateaceae were not examined. 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; K persistent in fruit; deletions in ORF 2280 region, full chloroplast accD and mitochondrial sdh4 genes lost.

Evolution. 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; see also Moore & Donoghue 2009).

Chemistry, Morphology, etc. Judd et al. (2002) note that the four families of Poales they mention - scattered through this part of the tree - have nuclear endosperm. 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., especially Hahn et al. (1995) and Katayama and Ogihara (1996). Note that the distinctive glucans in the clade are also found in Equisetum (Fry et al. 2009).

[Eriocaulaceae + Xyridaceae]: rosette plants; vessel elements with simple perforation plates; SiO₂ bodies 0; leaves spiral, also two-ranked; inflorescence terminal (axillary), scapose, with involucral bracts; (flowers monosymmetric, 2-merous); C clawed; A adnate to and opposite C, exothecium +; pollen more or less spiny; (ovary with commissural [?nectariferous] appendages); seed ± ridged, operculum +, tegmic in origin, cuticular layer between testa and tegmen.

Evolution. Divergence & Distribution. Eriocaulaceae and Xyridaceae may have diverged ca 105 million years before present, the crown group of the former beginning to diversify ca 58 million years before present and that of the latter ca 87 million years before present (Janssen & Bremer 2004).

Chemistry, Morpology, etc. 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). Note that Eriocaulaceae have a scape that is bractless (i.e., it is a "true" scape), while that of Xyridaceae may have bracts half way up. There may have been independent evolution of an androecium consisting of three antepetal-like stamens in the two families, which would then be a feature apomorphic for both Eriocaulaceae-Paepalanthoideae and Xyridaceae.

ERIOCAULACEAE Martinov, nom. cons.   Back to Poales

(Vessel elements with scalariform perforation plates); culm with endodermis, vascular bundles alternately on inside and outside, 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; plants mon(di)oecious; receptacle ± flat, scape spirally twisted, with closed basal sheath; flowers small; P with single trace, median K adaxial, K open (connate), C scarious, staminate flowers: (A dorsifixed); tapetum cells uni(bi)nucleate; (microsporogenesis simultaneous); pollen spiraperturate; carpellate flowers: staminodes common; ovules 1/carpel, pendulous, straight, micropyle endostomal, hypostase +; antipodal cyst [formed by fusion of antipodal cells] +; P persistent in fruit; radicle 0; n = 9, 15, 20, 25; (ORF 2280 present).

10[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; FloraBase 2004). 2 groups below.

1. Eriocauloideae

Plants usu. of aquatic habitats; roots and leaves with aerenchyma; C free, with black tips, glandular; staminate flowers: A 4-6, adnate to C; carpellate flowers: stigma in carinal position; testa poorly developed, tegmen tanniniferous.

1(-2?)/420: Eriocaulon (400). Pantropical (to Temperate).

2. Paepalanthoideae

Plants usu. terrestrial; (aerenchyma +); (hairs T-shaped); (C 0); staminate flowers: K C basally fused, (A bisporangiate/monothecal by fusion; antesepalous staminodes +), nectariferous pistillode +; carpellate flowers: (K valvate), (C often connate in the middle, free apically and basally); commissural stylar appendages +, nectariferous, carinal styles/stigmas not vascularized; seeds endotestal, the anticlinal walls prominent,.

9/760: Paepalanthus (485), Syngonanthus (200). New World, but esp. tropical South America.

• Eriocaulaceae are nearly always rosette plants readily recognised by their “pipe-brush” inflorescences. These have slender peduncles that are more or less spirally twisted and ridged or angled, and many small flowers with rather scarious and inconspicuous corollas that are aggregated into dense heads. The base of the inflorescence is surrounded by a single closed leaf sheath.

Evolution. Pollination ans Seed Dispersal. Although the flowers of Eriocaulaceae are individually rather small and inconspicuous, insect pollination seems to occur here. The dark-colored glands on the petals of Eriocaulon may be nectar-producing. Rosa and Scatena (2003) suggest that in at least some Paepalanthoideae the pistillode (in staminate flowers) and carinal nectariferous appendages on the gynoecium (carpellate flowers) are nectariferous (see also Rosa & Scatena 2007; cf. Ramos et al. 2005); the nectary in both cases is made up of much elongated epidermal cells (Oriani et al. 2009).Chemistry, Morphology, etc. In an anatomical survey of Brazilian Eriocaulaceae, secondary thickening was reported from species of Paepalanthus and Syngonanthus (Scatena et al. 2005). In Tonina the scape is not twisted, although it is also short; at the base is a sheathing adaxial prophyll that is shortly connate abaxially.

The flowers of Eriocaulaceae may be tiny, yet they show a great deal of variation in meristicity, connation of sepals and petals (this may vary between male and female flowers), presence of perianth glands, etc. (e.g. Giulietti & Hensold 1990). The basal part of the corolla may become secondarily free. With their capitate inflorescences and tiny flowers that nevertheless show a great deal of variation, Eriocaulaceae can be thought of as being the Asteraceae of the monocots! When the style is commissural, as in Paepalanthoideae, it is unvascularized; the ovarian appendages of Syngonanthus, etc., are in the position of the style of Eriocaulon, and both are vascularized (Coan & Scatena 2004; Rosa & Scatena 2007). Rosa and Scatena (2007) describe staminodial scales opposite to the ovary septae or adnate to the base of the petals in Paepalanthoideae.

There has been major movement of ribosomal protein and succinate dehydrogenase genes from the mitochondrion in Lachnocaulon, at least (Adams & Palmer 2003).

Much general information is taken from Unwin (2004) and also from Stützel (1998), that on anatomy from Malmanche (1919), inflorescence and flower from Stützel (1987), embryology and seed development are summarized in Arekal and Ramaswamy (1980), Scatena and Bouman (2001) and Coan and Scatena (2004), floral anatomy is described by Rosa and Scatena (2003), and pollen morphology detailed by de Borges et al. (2009).

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 phylogenetic resolution within the family.

Classification. Generic limits in Paepalanthoideae are in part unclear, but Syngonanthus needs to be divided (see Parra et al. 2010) and Paepalanthus, already large, expanded somewhat (Gomes de Andrade et al. 2010). See the World Checklist of Monocots for a listing of species.

XYRIDACEAE C. Agardh, nom. cons.   Back to Poales

(Plant caulescent; monopodial); anthraquinones +; root stele with xylem and phloem scattered; culm vascular bundles amphivasal; cuticle with insoluble [organic solvent] secretion; mucilage-producing multicellular hairs +; leaf sheath distinct; (flower monosymmetric), K (2 carinate), the median [abaxial] membranous, deciduous, or all persistent, C more or less clawed, ephemeral, connate or not, A extrorse or latrorse, (free; sporangia connate), anther wall of the Reduced type, exothecium +, endothecial thickenings spiral; stigma often complex and lobed/infundibular; ovules many/carpel; seed coat testal and tegmic, (operculum +, chalazal); deletions in ORF 2280 region [?whole family].

5[list]/260. Pantropical to warm temperate. 2 groups below.

1. Xyridoideae

Stem vascular bundles in a single ring; leaves distichous, equitant, isobifacial [oriented edge on to the stem], ligulate; (A 6), (endothecium lacking thickenings), staminodia 3, branched and with moniliform hairs on branch ends; tapetal cells binucleate; pollen (trinucleate), elongate, not spiny, (bisulcate); placentation (intrusive) parietal; ovules straight, hypostase 0; endotestal cells thickened; 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). [Photo - Xyris Flower, Infructescence © H. Wilson.]

Mucilage is secreted by hairs in the leaf axils of Xyris (cf. Mayacaceae?).

2. Abolbodoideae

Stem vascular bundles alternately on inside and outside of thickish sclerified ring, also scattered in center; leaves spiral (distichous, whether or not equitant, isobifacial - Achlyphila); (inflorescence branched; open - Achlyphila, some Abolboda; with 1 or more pairs of opposite bracts along the scape - Achlyphila, Abolboda); (K 2 - Abolboda), (A introrse), staminodes usu. 0 (filiform - some Abolboda); pollen spherical, inaperturate; G with nectariferous vascularized carinal [non-commissural] appendages on ovary, (0 - Achlyphila), style often solid; ovules anatropous (slightly campylotropous), suprachalazal tissue massive, hypostase +; (exotesta thick-walled, 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

• Xyridaceae are rosette plants that sometimes have equitant leaves; they can be recognised best by their inflorescences and flowers. The inflorescences normally bear one or more pairs of bracts along the inflorescence stalk; the flowers are borne in heads and have a conspicuous but ephemeral corolla.

Evolution. Bacterial/Fungal Associations. The family apparently lacks mycorrhizae.

Chemistry, Morphology, etc. The scape of Xyris is sometimes spirally twisted (cf. Eriocaulaceae!). Pollen is up to 185 µm in diameter in Orectanthe, these are about the largest grains in flowering plants. Placentation is very variable in Xyris, but that of the whole family may be basically parietal. Collar rhizoids are not drawn in Tillich (1994).

Additional information is taken from Winzieher (1914) and Govindappa (1955), both embryology of Xyris, Malmanche (1918: anatomy), Carlquist (1960: general, inc. seed anatomy [operculum]), Tomlinson (1969: vegetative anatomy), Tiemann (1985), Stützel (1990), Kral (1992, 1998), Rudall and Sajo (1999: flower and seed), Sajo and Rudall (1999: leaf anatomy), Scatena and Bouman (2001: seed operculum), Judd et al. (2002: general), Benko-Iseppson and Wanderley (2002: cytology), Campbell (2004: much information), Campbell and Stevenson (2008: floral morphology, esp. Aratitiyopea), and Oriani and Scatena (2011: floral morphology of Abolboda).

Phylogeny. There are suggestions that Xyridaceae may not be monophyletic (Michelangeli et al. 2003; Davis et al. 2004, support very weak), but sampling needs to be improved. Campbell (2004: q.v. for more information) carried out a detailed phylogenetic analysis of morphological variation. Abolboda is particularly distinctive and may be characterized as follows: stomata also tetracytic; K 2-3, C [3], staminodia filform, tapetum plasmodial, ovules crassinucellate; endotestal cells large, alternating with projecting exotegmic cells; endosperm helobial.

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].

MAYACACEAE Kunth   Back to Poales

Monopodial marsh plants; stem with endodermis, vascular bundles alternately on inside and outside; SiO₂ bodies 0; stomatal subsidiary cells with intersecting oblique divisions; leaves flat, apically bidentate, univeined, without a distinct sheath, uniseriate colleters +; flowers axillary, prophyll broad; C ± clawed; A 3, opposite sepals, dehiscing by pores, wall of the Reduced type, with exothecium, endothecium lacking thickenings, 2 persistent middle layers; tapetal cells uninucleate; placentation parietal, stigmatic lobes small; ovules 2-30/carpel, straight, micropyle endostomal, hypostase +; seed operculum +, endotegmic in origin, exotegmic cells with massive U-shaped lignifications; primary root and cotyledonary hypophyllar sheath 0; n = 8.

1[list]/4-10. Mostly tropical and American (inc. S.E. U.S.A.), 1 sp. from Africa (map: from Hamann 1961; Boutique 1971; Fl. N. Am. 22: 2000).

• Mayacaceae are small herbs of marshes looking rather like a club-moss. They have numerous spirally-arranged, apically-toothed leaves borne scattered along the stem and pink to white apparently axillary flowers with a clearly differentiated calyx and corolla.

Chemistry, Morphology, etc. Mayacaceae are vegetatively rather different from many other Poales. The vascular bundles on the outside of the endodermal ring are well separated from it (cf. Eriocaulaceae: Malmanche 1919).

The inflorescence is sometimes described as being terminal, but the flowers examined seemed to be axillary and associated with a broad, adaxial prophyll-like structure (pers. obs.). However, given the association of Mayacaceae with families that have scapose inflorescence with involucral bracts, the inflorescence of Mayacaceae bears re-examination. Anthers in some species are monothecal, and the stamens may be basically extrorse (Silveira de Carvalho et al. 2009). The nucellar epidermis is thick basally and the outer layer of endosperm has protein.

Some information is taken from Tomlinson (1974: stomata), Thieret (1975: general), Venturelli and Bouman (1986: ovule and seed), Stevenson (1998: general), and Endress (2008c: ovule, micropyle endostomal), but the family is poorly known. See also the World Checklist of Monocots.

[Thurniaceae [Juncaceae + Cyperaceae]]: 3-desoxyanthocyanins [1 + 2], luteolin 5-methyl ether +; starch grains pteridophyte-type, amylophilic; stem angled, leaves 3-ranked, sheaths closed; inflorescence racemose; flowers small; T scarious, undifferentiated; microsporogenesis simultaneous [tetrads tetrahedral], pollen in tetrads, porate, trinucleate; style short, branches/stigmatic surface long; ovules anatropous, micropyle endostomal, (outer integument ³3 cells across), hypostase +; seeds testal-tegmic; endosperm helobial; chromosomes with diffuse centromeres; phanomer [photosynthetic unifacial cotyledonary hyperphyll] + (0), hypocotyl +, seedling collar inconspicuous, with rhizoids.

Evolution. Divergence & Distribution. Divergence of this clade can be dated to ca 103 million years before present (Janssen & Bremer 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. The nucellus of some Bulbostylis ovules may be only a single cell across (Maria & López 2010). Roalson et al. (2008) and Hipp et al. (2009) discuss chromosome evolution in the clade; although diffuse centromeres are a apomorphy for the whole group, it is only in Carex that this is accompanied by considerable variation in chromosome number. A three-nucleotide deletion in the atpA gene also characterises this group (Davis et al. 2004).

THURNIACEAE Engler, nom. cons.   Back to Poales

Root stock upright, or trunk-forming; flavone C-glycosides +; vessel elements with scalariform perforation plates; stem bundles amphivasal [Prionium], SiO₂ also in parenchyma (0 - Prionium); cuticular waxes as aggregated rodlets; leaf margin serrate, (vascular bundles in pairs, abaxial inverted - Thurnia); stem angled; inflorescence capitate and involucrate or a much-branched panicle; perianth tube short; tapetal cells?; pollen grains ulcerate, exine granular; (styles separate); ovules 1-few/carpel, ascending, [micropyle zig-zag]; seeds arillate; testa of sclerenchymatous fibres and unthickened cells, (short hairs - Thurnia), tegmen tanniniferous; n =?.

2[list]/4. South Africa and Guyana region, Amazonia (map: see Munro et al. 2001). [Photo - Thurnia Habit, Inflorescence, Prionium - Inflorescence.]

• Thurniaceae can be recognised by their erect, leafy stems, serrate leaves, and pentacyclic flowers with a scarious perianth.

Evolution. Stem-group Thurniaceae are dated to ca 98 million years before present, the crown group diverged ca 33 million years before present (Janssen & Bremer 2004).

Chemistry, Morphology, etc. The family is poorly known. For the embryology, etc., of Prionium, see Munro and Linder (1999). Tillich (1994) describes the seedling as being similar to that of Juncaceae. See Tiemann (1985) for micropyle type, and Williams and Harborne (1975) for chemistry. Other information is taken from Kubitzki (1998d: general) and Givnish et al. (1999).

Phylogeny. Thurniaceae are sister to Juncaceae + Cyperaceae, with strong support (Givnish et al. 1999; Bremer 2002; Davis et al. 2004), although Oxychloe was not included.

Classification. See the World Checklist of Monocots.

Synonymy: Prioniaceae S. L. Munro & H. P. Linder

[Juncaceae + Cyperaceae]: luteolin +; mycorrhizae 0; chloroplast rpl23 gene absent.

Evolution. Divergence & Distribution. This clade diverged from Thurniaceae ca 98 million years before present, itself splitting ca 88 million years before present (Janssen & Bremer 2004; Besnard et al. 2009b); a less likely age for the clade is 39-28 million years before present (Wikström et al. 2001).

The clade [Juncaceae + Cyperaceae] is notably speciose (Magallón & Sanderson 2001), being perhaps seven times more speciose than its animal-pollinated sister clade (Kay & Sargent 2009).

Mycorrhizae appear to be absent, but cluster roots are common. Bugs of the Hemiptera-Lygaeidae-Cyminae and -Pachygronthini are concentrated here (Slater 1976). Clavicipitaceous endophytes have been recorded from some genera, but they are not as common as they are on Poaceae (Clay 1986, 1990); cf. also the distribution of the parasitic Claviceps itself.

Chemistry, Morphology, etc. 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). See Endress (1995b) for some details of floral morphology.

Phylogeny. Muasya et al. (1998) suggested that Oxychloe (Juncaceae) was sister to Cyperaceae, with moderate support, other Juncaceae are 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 Oxychloe within Cyperaceae. The relationships of the latter genus in particular remained unclear (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 Drábková & Vl&ctilde;ek 2007); part of the problem seems to have been caused by the identity of the material from which early molecular samples of the genus were obtained (Kristiansen et al. 2005).

JUNCACEAE Jussieu, nom. cons.   Back to Poales

Plant glabrous (not Luzula); (root hairs from short cells); endodermoid layer +; culm bundles in rings; (vessel elements with scalariform perforation plates); SiO₂ bodies 0 (sand - Juncus); (leaves [spirally] two-ranked); sheath usu. open (auricles +; ligule +), often unifacial [both terete and isobifacial]; (flowers single); (flowers 2-merous; imperfect), (T large - Marsippospermum), tapetal cells uninucleate; pollen grains central in loculus, ulcerate; (placentae parietal), (styles separate); ovules 1 basal to many central/carpel, micropyle often bistomal, (outer integument 4 cells across), funicular obturator [hairs] and hypostase +/0; seed 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; Balsev 1996, still incomplete).

• Juncaceae are glabrous (Luzula excepted) caespitose herbs that can be recognised by their solid, rounded stems, leaves that are also often rounded and have open sheaths, and pentacyclic flowers with a scarious perianth.[Photo - Juncus Inflorescence] [Photo - Luzula Flower]

Evolution. Divergence & Distribution. Stem-group Juncaceae are dated to ca 88 million years before present, the crown group diverge ca 74 million years before present (Janssen & Bremer 2004).

Floral Biology & Seed Dispersal. The seeds of Luzula are myrmecochorous (Lengyel et al. 2010).

Vegetative Variation. Yamaguchi et al. (2010) show how terete and laterally flattened leaves in Juncus are fundamentally similar, the latter also expressing the DL gene that is responsible for midrib formation in normal bifial monocot leaves. For unifacial leaves, see Yamaguchi and Tsukaya (2010).

Chemistry, Morphology, etc. In Luzula stamens are opposite individual tepals (Payer 1857) and the flowers may have the adaxial tepal in the outer whorl, and also a variety of bract structures associated with the flower (Eichler 1874). indeed, inflorescence morphology may repay investigation, Drábková (2010) suggesting that that both cymose and racemose inflorescences and flowers with two and no bracetoles occur in Juncus.

Some information is taken from Balslev (1998); for mebryology, etc., of some Juncus and Luzula, see Laurent (1904), for anatomy, see Cutler (1969), and for some chemistry, see Williams and Harborne (1975).

Phylogeny. For a phylogeny, with Juncus perhaps being paraphyletic, see Drábková et al. (2003), Roalson (2005) and especially Drábková (2010). Drábková and Vlcek (2009) also found that Juncus trifidus and J. monanthos were separate from the rest.

Classification. For a family monograph, see Kirschner et al. (2002a-c); see also the World Checklist of Monocots. However, the genera - bar Luzula - are a mess (Drábková 2010).

CYPERACEAE Jussieu, nom. cons.   Back to Poales

(Vesicular-arbuscular mycorrhizae +); aurones, flavonoid sulphates, flavone C-glycosides, tricin, kestose and isokestose storage oligosaccharides [fructans] +; (velamen +); stems solid; SiO₂ bodies smooth, conical, with pointed apices, attached to walls; stomatal guard cells dumb-bell shaped; cuticular waxes as aggregated rodlets; leaves (two-ranked; tetrastichous; spiral; petiole + lamina), sheath with (contra)ligule; flowers usu. monosymmetric by reduction; T variously reduced; A (connate); tapetal cells bi-multinucleate; pollen pseudomonads, (grains 2-celled), with distal pore [ulcus] and with 2 or more lateral apertures, (pontoperculate); (G [2]), (gynophore +); ovule single, 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 = ³5, -> 55, 56; 3 bp 5.8S nrDNA insertion, rps14 gene to nucleus, pseudogene remaining in mitochondrion.

98[list]/5430. World-wide (Map; Hultén 1961; Vester 1940). [Photo - Carex Carpellate Inflorescence, Eleocharis Spikes.]

1. Mapanioideae

Phytoliths uncommon; flowers ?pseudanthia, flowers imperfect, sterile bracts between stamens and terminal gynoecium; staminate flower: stamens in axils of bracts ["scales"]; (pollen grains central in loculus, spherical, monoporate, sexine thick); (micropyle bistomal, zig-zag - Hypolytrum).

6/166: Mapania (80), Hypolytrum (50). Largely tropical.

Synonymy: Mapaniaceae Shipunov

2. Cyperoideae Beilschmied

Fine roots dauciform; phytoliths common; plants monoecious or polygamous or all flowers perfect; inflorescence branching, with spikelets; T + [= scales, bristles], (connate; inner tepals clawed), 0; A (2) 3; pollen grains peripheral in loculi, (spheroidal, monoporate - Coleochloa).

92/5257: Carex (1776), Cyperus (950), Fimbristylis (250), Rhynchospora (250), Scirpus (200), Scleria (200), Eleocharis (120), Bulbostylis (100), Schoenus (100), Isolepis (70). Worldwide, but esp. N. Temperate.

Synonymy: Kobresiaceae Gilly, Papyraceae Burnett, Scirpaceae Borkhausen, Scleriaceae Berchtold & J. Presl

• Cyperaceae are herbs with solid, sharply three-angled stems and leaves with closed sheaths. The flowers are very reduced and often aggregated into spikes or heads, the perianth, when recognisable, is scarious, and the fruit is an achene.

Evolution. Divergence & Distribution. Stem-group Cyperaceae have been dated to ca 88 million years before present, the crown group to ca 76 million years before present (Janssen & Bremer 2004; Besnard et al. 2009b); other ages suggested are ca 100 and 52 million years respectively. Diversification within Mapanioideae began a mere ca 33 million years ago, but within Cyperoideae, ca 77 million years. 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 - cf. Cyperoideae; for fossils of the family, see also Smith et al. 2010). Divergence within Eleocharis occurred ca 20 million years ago (Besnard et al. 2009b).

Ecology & Physiology. Cyperaceae (as well as Poaceae and Juncaceae) are often particularly common in tundra habitats, and communities dominated by these groups were notably extensive during the last glacial maximum (Bigelow et al. 2003). Tundra-dwelling Cyperaceae may take up nitrogen predominantly in an organic form, although some species can take it up in an inorganic form (Raab et al. 1999). Habitats in alpine and other extreme conditions may also be dominated by Cyperaceae. Thus there are some 450,000 square kilometers between 3,000 and 5960 m altitude on the Tibetan plateau dominated by Kobresia pygmaea. This community may be of quite recent origin and have reached its current extent since the spread of the Tibetan empire in the seventh century CE (Miehe et al. 2008, see also Zhou 2001). Kobresia species there appear to be ectomycorrhizal, although the same species may also have dauciform roots and perhaps form a variety of other fungal associations (Gao & Yang 2010); understanding the ecophysiology of this fascinating community will be very rewarding.

About one third of the family have C₄ photosynthesis, with perhaps six origins within the family as well as some reversals to C₃ photosynthesis, and in some species it may help increase the efficiency of the use of nitrogen in plants with submerged leaves (Soros & Bruhl 2000; Besnard et al. 2009b; Bruhl & Wilson 2008; Larridon et al. 2011a). For the complexity of possible patterns of the evolution and loss of the C₄ pathway and intermediates within the single, albeit large, genus Eleocharis, see Roalson et al. (2010); Martins and Scatena (2011) look at the diversity of Kranz-type morphologies in the family from a developmental point of view. Besnard et al. (2009b) suggested that evolution of C₄ photosynthesis had occurred since about 19.6 million years ago, with genetic changes in the important enzyme phosphoenolpyruvate carboxylase occurring in parallel.

A few taxa like Rhynchospora anomala are dessication-tolerant and arborescent; their adventitious roots, which make up the "trunk" of the plant along with the persistent leaf bases through which these roots run, have a well-developed velamen (Porembski 2006). A number of Cyperoideae-Cariceae and -Rhynchosporeae (but not -Scirpeae) have dauciform roots, roots which develop a dense covering of very long root hairs and overall look rather carrot-shaped; these are believed to help in phosphorous uptake by the plant when growing in phosphorous-poor soils (Shane et al. 2005: some Juncaceae may also have such roots). Epidermal cells in such roots are elongated at right angles to the long axis of the root (Shane et al. 2005). Some species of non-mycorrhizal Carex have distinctive, bulbous-based root hairs (Miller et al. 1999).

Waterway et al. (2009) discuss ecological diversification in Cariceae; there are widespread wetland species and often more geographically restricted forest taxa. Carex itself is notable for the wide variation in chromosome number it shows because of chromosome fission, fusion and translocation facilitated by the diffuse centromeres of the genus (Hipp et al. 2011).

Bacterial/Fungal Associations. Cyperaceae, as with other plants in the tundra habitat (see above), often lack mycorrhizae (but cf. Muthukumar 2004; Miller at al. 1999 for mycorrhizae in Carex). Smuts (Ustilaginales) are also very diverse on Cyperaceae (Kukkonen & Timonen 1979; Savile 1979b). Largely ascomycetous fine endophytes are commonly found in Cyperaceae from tundra habitats (Higgins et al. 2007), and these may be members of Clavicipitaceae, elsewhere especially prominent on Poaceae-Poöideae (Schardl 2010).

Floral Biology & Seed Dispersal. Although Cyperaceae are normally thought of as being a wind-pollinated clade, there have been some transitions to insect pollination (Wragg & Johnson 2011 and references).

Fruit dispersal mechanisms are remarkably varied, including water, wind (e.g. the bristles surrounding the fruits of Eriophorum), animals (both epi- and endozoochory), and ants (Allessio Leck & Schütz 2005: they also discuss seed dormancy and germination requirements).

Chemistry, Morphology, etc. Zhang et al. (2004) recently suggested that spikelet structure in Schoeneae, at least, was sympodial, although that of Cyperoideae as a whole is indeterminate (Vrijdaghs et al. 2005c, 2010 [esp. Cyperoideae]). Eriophorum (Cyperoideae) has its distinctive hairs arising centripetally on a perianth ring-primordium (Vrijdaghs et al. 2004b). For the literature on the possible pseudanthial nature of some flowers in Cyperaceae, see Bruhl (1991), who found that the "foliar" structures in the taxa he studied were ouside the stamens, so they probably represented perianth parts (see also Vrijdaghs et al. 2004a; Richards et al. 2005, esp. 2006: flowers of Exocarya scleroides [Mapanioideae] pseudanthial).

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). The median carpel in Carex is adaxial (Eichler 1875), i.e. in the inverted position (see also Spichiger et al. 2004), however, as Vrijdaghs et al. (2011) note, it is difficult to talk about carpels in cyperoid Cyperaceae since the gynoecium develops from an annular primordium - on top of which there may be two or three (rarely even 4) branched styles. Scirpus sylvaticus has a relatively unspecialised flower in which the three stamens and the carpels are opposite the outer perianth members (Vrijdaghs et al. 2005a); the scirpoid pattern is perhaps that from which other more derived developmental morphologies in Cyperoideae can be related (Vrijdaghs et al. 2009). Pollen apertures in Carex have a very thin underlying intine, that in interapertural areas is much thickened, i.e., the reverse of the normal condition (Halbritter et al. 2010).

For a vast amount of systematic information, see Bruhl (1995), for further general information, see Naczi and Ford (2008). For the prophyll, see Blaser (1944), for embryo morphology, see van der Veken (1965 - hundreds of species); for inflorescence units, see Eiten (1976), for floral morphology, see Goetghebeur (1998) and Vrijdaghs et al. (2006), for pollen, see van Wichelen et al. (1999), Nagels et al. (2009) and Coan et al. (2010), for the gynophore, etc., see Vrijdaghs et al. (2005b), for propagule dispersal, see Allessio Leck and Schütz (2005), for phytoliths, see Piperno (2006), for chromosome number and evolution, see Hipp (2007), Roalson (2008), Roalson et al. (2008a), and Hipp et al. (2009), for inflorescence morphology, see Vrijdaghs et al. (2008), for a nrDNA insertion, see Starr et al. (2008), for ovule and seed development, see Nijalingappa and Devaki (1978) and Coan et al. (2008), for pseudomonad pollen development, see Furness and Rudall (2011).

Phylogeny. Mapanioideae are sister to the rest of the family, Cyperoideae; Carex, sister to Eriophorum, is embedded within the latter (Simpson et al. 2003, esp. 2008). Trilepideae are sister to all other Cyperoideae (Muasya et al. 2009a). Within Cariceae, phylogenetic studies are beginning to resolve relationships (Reznicek 1990 and associated papers; Yen & Olmstead 2000; Yen et al. 2000; Roalson et al. 2001; Starr et al. 2004, 2006; Waterway & Starr 2008). Carex is paraphyletic, as has been demonstrated by several studies that are also clarifying relationships within this huge and difficult clade (see Yen & Olmstead 2000; Starr et al. 1999, 2004; Waterway & Starr 2008; King & Roalson 2008 [use of nrDNA problematic]; Starr & Ford 2009; Escudero & Luceño 2009; Gehrke et al. 2010: resolution at base of genus poor). Conventional wisdom in which a highly compound inflorescence is the plesiomorphic condition for Carex, taxa with simple branches being derived, perhaps several times, seems the exact opposite of what actually happened (Ford et al. 2006); again, evolution is not necessarily complex -> simple! Cyperus is massively paraphyletic (e.g. Muasya et al. 2002; Larridon et al. 2011a, b). For the relationships of Carpha and other Schoeneae, see Zhang et al. (2007); for relationships within Rhynchosporeae, see Thomas et al. (2009); and for relationships around Eleocharis, see Hinchcliff et al. (2010) and Roalson et al. (2010).

Naczi (2009) discusses the use of morphological characters in phylogenetic analyses; this is tricky because of the highly derived nature of the flowers of the family.

Classification. Carex is paraphyletic (see above) and genera like Kobresia, Cymophyllus, Uncinia and Schoenoxiphium should probably be included in it (or some species of Carex will have to be moved). For a general evaluation of generic limits in Cypereae, see Muasya et al. (2009b); Cyperus is to include about thirteen genera (see also Muasya et al. 2002; Hinchcliff et al. 2010; Larridon et al. 2011a, b); Eleocharis is to be slightly expanded (Hinchcliff et al. 2010). For nomenclature, etc., see Goetghebeur (1985); see also the World Checklist of Monocots (Govaerts et al. 2007 is a printed version of this). T. M. Jones provides a Carex interactive identification key.

[[Anarthriaceae [Restionaceae + Centrolepidaceae]] [Flagellariaceae [Joinvilleaceae + Ecdeiocoleaceae] Poaceae]]]: plant rhizomatous; flavones +; primary cell wall also with(1-3,1-4)-ß-D-glucans; sieve tube plastids with cuneate and other less densely packed crystals; (chlorenchyma with peg cells [cf. arm cells of some Poaceae?]); leaves two-ranked, with sheath; bracteoles 0; flowers small, imperfect; T membranous, undifferentiated; endothecial wall thickenings girdle-like; pollen scrobiculate [minute pores penetrating tectum and foot layer], monoporate, annulate ["ulcerate"]; style branches long, stigmas plumose, receptive cells on multicellular branches; ovule 1/carpel, apical, straight; seedling with collar rhizoids +.

Evolution. Divergence & Distribution. The Restionaceae-Poaceae clade began to diversify ca 109 million years ago, having originated ca 112 million years before present (Janssen & Bremer 2004), but note that in their study the topology of this part of the Poales differs from that in the tree above, while Wikström et al. (2001) suggest an origin only 49-45 million years before present, but again the topology of the tree from which this estimate was taken is rather different from that used here.

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 family size within the clade, with most species belonging to Poaceae, the second most species-rich family (Restionaceae) having only some 520 species (see also Chase 2004). Furthermore, given that there are five species-poor clades that are successively immediately sister below the PACMAD and BEP clades, the clades that contain nearly all the diversity in Poaceae, diversification is perhaps more properly described as diversification in the PACMAD and BEP clades of Poaceae (see also Linder & Rudall 2005 for diversification).

Chemistry, Morphology, etc. For the flavonoids of Anarthriaceae, Restionaceae and Ecdeiocoleaceae, see Williams et al. (1997a); the variation is complex and needs to be re-evaluated in light of the current position of the last family.

The leaf sheath is the last part of the leaf to develop. Although it is suggested above that an apomorphy for the clade is to have imperfact flowers, the situation is unclear, especially in the Flagellariaceae to Poaceae part of this clade. Linder and Ferguson (1985) discuss variation in pollen morphology. Flagellariaceae have "multicellular papillae" on their stigmas (Appel & Bayer 1998), whether these are receptive in the same way as the multicellular branches of, say, Poaceae, needs clarification. Note that 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 trinucleate for the whole group by Givnish et al. (1999, cf. Appel & Bayer 1998 for these characters). Joinvilleaceae in particular are largely unknown.

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 variation in 26S rDNA suggested that Dasypogonaceae may be part of this clade, being very closely linked with Ecdeiocoleaceae, Anarthriaceae and Centrolepidaceae (Neyland 2002b), slightly less so with the one member of Restionaceae included. However, data from atpB, rbcL, 18S, etc., do not suggest such a grouping (see e.g. Givnish et al. 2010b), so pending further study Dasypogonaceae remain unplaced at the base of the commelinids (q.v. for further discussion). Davis et al. (2004: very weak support) found Flagellaria to group with Mayacaceae, etc., rather than with the other familes of the clade recognised here, while Graham et al. (2005) obtain a set of relationships [Flagellariaceae [Restionaceae [Ecdeiocoleaceae [Poaceae]]], perhaps a branch length or sampling problem.

Bremer (2002) found a sister group relationship between Ecdeiocoleaceae and Poaceae, as had Harborne et al. (2000), although the latter did not include Joinvilleaceae and Flagellariaceae in their study. 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). However, in another two-gene study, although both genes were chloroplast genes, Marchant and Briggs (2007: both genera of Ecdeicoleaceae included) found strong support for a sister group relationship between Joinvilleaceae and Ecdeiocoleaceae, 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, so the phylogenetic relationships suggested here are questionable. However, monophyly of the whole clade, and other relationships in it, are in general strongly supported.

[Anarthriaceae [Centrolepidaceae + Restionaceae]]: root hairs originating from any epidermal cells; culm with parenchymatous sheath, palisade chlorenchymatous tissue, and sclerenchymatous cylinder, vascular bundles inside; chlorenchyma with peg cells; plant dioecious; A 3, opposite inner P, dorsifixed; phanomer [photosynthetic unifacial cotyledonary hyperphyll] +; loss of rpoC1 gene.

Chemistry, Morphology, etc. See Malmanche (1919) for vegetative anatomy; he records the stomata as being brachyparacytic.

ANARTHRIACEAE D. F. Cutler & Airy Shaw   Back to Poales

(Flavonol glycosides +); root hairs lignified; SiO₂ 0; stomata in grooves; leaves ligulate; plant dioecious; inflorescence racemose, culm branched; staminate flowers: pollen operculate; carpellate flowers: G opposite outer P; ovules?, hypostase +; seed coat?; endosperm type?, embryo?; ?collar rhizoids; n = 6, 9, 11; ORF 2280 +, trnL gene with 3bp deletion and 5bp insertion.

3[list]/11. West Australia (map: from FloraBase 2004). [Photo - Anarthria Staminate & carpellate inflorescences © D. Woodland]

Evolution. Divergence & Distribution. Stem-group Anarthriaceae are dated to ca 96 million years before present, the crown group diverge ca 55 million years before present (Janssen & Bremer 2004).

Chemistry, Morphology, etc. The three genera are rather different. Anarthria lacks palisade tissue, a sclerechymatous cylinder and parenchyma sheath in the culm (or it could be interpreted as having a cylinder towards the middle of the culm, with scattered vascular bundles outside), it has equitant isobifacial leaves, stomata in grooves, a deciduous spathe, and n = 11. Hopkinsia has G 1, with long branches on the style; 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; pollen microverrucate - and are associated with Anarthria (Briggs et al. 2000, see also papers in Meney and Pate 1999). Stigma papillae in Anarthria? Microsporogenesis?

Much information is taken from Briggs and Johnson (2000); note that no comparison is made there with Ecdeiocoleaceae. Other information is taken from Cutler and Airy Shaw (1964), Linder (1984: African members of the family), Linder and Rudall (1993) and Linder et al. (1998).

Phylogeny. Hopkinsia + Lyginia are sister taxa and are associated with Anarthria (Briggs et al. 2000, see also papers in Meney and Pate 1999).

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. Indeed, Linder et al. (2000) even suggested that these genera are Restionaceae, albeit perhaps sister to the rest - they (but not Anarthria itself) have the distinctive culm anatomy of that family, and Lyginia has starch in the embryo sac, like Restionaceae (Hopkinsia is unknown).

Synonymy: Hopkinsiaceae B. G. Briggs & L. A. S. Johnson, Lyginiaceae B. G. Briggs & L. A. S. Johnson

[Centrolepidaceae + Restionaceae]: mycorrhizae 0; plant ± glabrous; anthers bisporangiate/monothecal; pollen pore not annulate, margin irregular; cells of nucellar epidermis anticlinally elongated; embryo sac with compound starch grains esp. surrounding polar nuclei, antipodal cells ± proliferating, persistent.

Evolution. The group lacks mycorrhizae.

Phylogeny. The position of Centrolepidaceae with respect to Restionaceae has been uncertain (e.g. Linder et al. 2000); most studies unfortunately concentrating on either the Australian or African Restionaceae rather than the broader studies that are needed. As things stand, a position sister to Restionaceae is possible (Linder & Caddick 2001) as well as one - but with weak support - within the family (Bremer 2002). In a recent study Centrolepidaceae and Restionaceae were sister taxa in parsimony analyses of trnK and trnL-F, while in Bayesian analyses of these genes, and also in rbcL analyses, the relationships [Restionoideae [Sporadanthoideae [Leptocarpoideae + Centroplepidoideae]]] were recovered (Briggs & Linder 2009; Briggs et al. 2010); the latter set of relationships seems more likely. It may be relevant that the pollen apertures of Australian Restionaceae in particular are like those of Centrolepidaceae (Chanda 1966).

CENTROLEPIDACEAE Endlicher, nom. cons.   Back to Poales

± Caespitose herbs; vascular bundles in culm on either side of thick cylinder (not Gaimardia), palisade tissue 0; SiO₂ ?0; epidermis with hairs and papillae; leaves unifacial (ligulate); plants monoecious; inflorescence scapose, capitate and with inflorescence bracts, or spicate; P 0; staminate flowers: A 1-2; pollen trinucleate; carpellate flowers: G [1-14(-45)]; (parietal tissue 1 cell across), nucellar cap 0; antipodals usu. binucleate; fruit abaxially dehiscing or indehiscent; endotegmen alone persistent, tanniniferous; embryo conoid; (phanomer 0), first seedling leaf with lamina, 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; FloraBase 2004). [Photo - Gaimardia Habit and Close-up, Centrolepis Habit.]

• Centrolepidaceae are rather small more or less caespitose herbs. The inflorescence is scapose and spicate or capitate and involucrate.

Evolution. Divergence & Distribution. Estimates of the age of the Centrolepidaceae clade range from 45-97 million years before present depending in large part exactly where it is placed in this part of the tree (Janssen & Bremer 2004).

Other. Centrolepidaceae may be neotenous Restionaceae, but their phylogenetic position with regard to that family needs to be clarified (e.g. Linder et al. 2000).

Chemistry, Morphology, etc. Cutler (1969) emphasized the fact that the root hairs arose from one side of the epidermal cell and that the root lacked a pericycle. He suggested that the peg cells of Centrolepidaceae and Restionaceae might be rather different, peg cells sensu stricto perhaps being absent in the former. Also, whether or not the family has SiO₂ bodies needs confirmation.

There has been some discussion as to whether Centrolepidaceae have a flower or pseudanthium; Sokoloff et al. (2009b) reject the latter proposition. Sokoloff et al. (2010; see also Hamann 1962a; Remizowa et al. 2011) interpret the inflorescence of Centrolepis as being a racemose spikelet, not cymose. Hou (1957) described the anthers as being 1- or 2-celled. The separate carpels sometimes become more or less fused, the result being something that looks like a syncarpous gynoecium - or, in Centrolepis itself, the gynoecium is definitely syncarpous, and although the carpels there appear to be more or less one on top of each other, that is because of developmental gymnastics resulting in the greater development of one side of the receptacle (Sokoloff et al. 2009b). The ovule is described by Hamann (1975) and Cooke (1998) as being weakly crassinucellate and also as having a megasporocyte that lacks a parietal cell; although cells in the nucellar epidermis may have divided, this seems unlikely from the illustrations in Hamann (1962a).

RESTIONACEAE R. Brown, nom. cons.   Back to Poales

Root hairs usu. persistent, lignified; rhizome with endodermoid sheath; culm with protective cells [lignified chlorenchymatous cells] lining substomatmal cavities +; leaves much reduced, (sheath closed); plant di(mon)oecious; inflorescence as spikelets; outer T hooded [?how common], (P 0), staminate flowers: (anthers tetrasporangiate, e.g. Harperia), tapetal cells 1-4-nucleate, pollen central in loculus; pollen (binucleate), with coarse granules [exine fragments] on pore; carpellate flowers: P variable; G opposite outer P, (only 1 fertile), common style short or 0; ovule (micropyle endostomal - Willdenowia, some Leptocarpus), (parietal tissue ca 1 cell across - Alexgeorgea, ?Hypodiscus), suprachalazal zone ± massive, hypostase +; antipodal cells proliferating; exotesta persistent, ± thick-walled; (cotyledon not photosynthetic), hypocotyl and collar at most small, collar rhizoids +, first seedling leaf with lamina; 28 kb chloroplast genome inversion +/- [latter - Desmocladus, Elegia?].

58[list]/500 - four groups below. Africa (inc. Madagascar), Hainan and Vietnam to Australia, New Zealand, Chile (map: from Good 1974). [Photos - Collection. Dovea tectorum is properly Chondropetalum tectorum]

1. Restionoideae Bartling

Flavonols, non-hydrolysable tannins, myricetin derivatives +, flavones less diverse; pollen grains with pores 4-10 µm across, margins annulate [raised], (thickened foot layer +); n = 16, 20.

11-16/350: Africa south of the Sahara, Madagascar.

1a. Restioneae Bartling

SiO₂ bodies often in parenchyma sheath, not in sclerenchyma cylinder; chlorenchyma cells radially elongated; styles 1-3, often widely separate; (fruit a soft-walled nut); young seed coat tanniniferous.

3-8/300: Restio (95), Ischyrolepis (48), Elegia (50), Thamnochortus (35). Madagascar, Africa south of the Sahara, especially the Cape Region. [Photo - Elegia, Habit.]

Synonymy: Elegiaceae Rafinesque

1b. Willdenowieae Masters

SiO₂ bodies usually in sclerenchyma cylinder only; ridges of sclerenchyma often alternate with vascular bundles, (lignified chlorenchyma cells extending from ridges); chlorenchyma cells often radially short and squat; [G 2], styles 2, (basally connate); proliferating antipodals?; fruit a nut, often with elaiosomes [fleshy pedicels]; young seed coat not tanniniferous.

8/50: Anthochortus (15). The Cape region of South Africa.

[Sporadanthoideae + Leptocarpoideae]: flavonols rare, except quercetin, non-hysrolysable tannins rare, flavones diverse, sulphated flavonoids +; chlorenchymatous cells palisade; pollen grains with pores 8-25 µm across, not annulate, irregular, thickened foot layer 0 [cf. also Centrolepidaceae!]; cotyledon not photosynthetic [ca half the genera], seedling culm internodes elongated, leaves terete; n = 6, 7, 9, 11, 12.

2. Sporadanthoideae Briggs & Linder

Myricetin +; spikelets often 0, flowers solitary and with bracteoles.

3/31: Lepyrodia (22). Australia and New Zealand.

3. Leptocarpoideae Briggs & Linder

Flavones, sulphated flavonoids + [(8-hydroxyflavonoids, e.g. gossypetin]; chlorenchyma interrupted by pillar cells [radiating ± palisade-like and ± lignified cells of sclerenchyma sheath] (0), (sclerenchymatous bundle girders opposite outer vascular bundles +); protective cells 0, (elongated, thick walled epidermal cells +).

28/117: Chordifex (20). Hainan and Vietnam to Australia, New Zealand, Chile (Apodasmia).

• Restionaceae are sometimes quite large rush-like herbs with very much reduced leaves; the flowers are small, imperfect but usually with a perianth, and usually aggregated into spikelets.

Evolution. Divergence & Distribution. Stem-group Restionaceae are dated to ca 96 million years before present, the crown group diverge ca 74 million years before present (Janssen & Bremer 2004). There are ca 350 spp. of Restionaceae in the Cape region, diversification beginning in the late Eocene-early Oligocene some 43-28 million years before present (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 million years ago separating what became eastern and western clades (Crisp & Cook 2007)

Ecology & Physiology. Restionaceae can be locally dominant in oligotropic conditions, whether wet or dry. Thus Restionaceae replace Poaceae in the graminoid layer in the nutrient-poor soils of the fynbos vegetation of the Cape Floristic region (Bell et al. 2000). The habitats they prefer are often subject to seasonal fires, and some species, sprouters, accumulate starch in their rhizomes, while others, non-sprouters, reproduce by seeds (cf. Ericaceae). The rootlets of Restionaceae are also described as being capillaroid, with dense and exceptionally long root hairs, although there are other distinctive root morphologies (Lambers et al. 2006); Cyperaceae and Proteaceae growing in similar phosphorous-poor environments develop analagous structures that are believed to facilitate phosophorus uptake by the plant. Interestingly, one study suggested that the total root length of the grasses tested was considerably greater than that of Restionaceae, although the dense root hairs of Restionaceae were not taken into account (Bell et al. 2000). [What is the relationship with lignification of root hairs?]

Floral Biology & Seed Dispersal. Myrmecochory is common in the African clade Restionoideae-Willdenowieae, the nutlets having fleshy funicles that attract ants (Briggs & Linder 2009).

Chemistry, Morphology, etc. The culm has subepidermal chlorenchyma separated from the cortex by parenchymatous or sclerenchymatous rings; these may not be strictly comparable (Cutler 1969) and so may not be an apomorphy for the family.

Information is taken from Borwein et al. (1949) and Krupko (1962), both embryology, Kircher (1986; he does not draw the guard cells as being dumb-bell-shaped), Linder et al. (1998: general), Meney and Pate (1999), Linder and Caddick (2001: esp. seedlings), Ronse Decraene et al. (2001a, 2002b: floral development, much variation) and Newton et al. (2002: seeds). Williams et al. (1998) and Harborne et al. (2000) describe flavonoid patterns in the family. For Peter Linder's "Intkey thingy" on African Restionaceae - 2,000 pictures - see http://www.systbot.unizh.ch/datenbanken/restionaceae/.

Phylogeny. The variation in the presence of the 28kb chloroplast genome inversion within Restionaceae is remarkable (Michelangeli et al. 2003); is the family polyphyletic?! For phylogenetic relationships, see Briggs et al. (2010).

Classification. For the classification of Restionaceae and characterization of the subfamilies, see Briggs and Linder (2009); Leptocarpoideae have been pulverized. Linder and Hardy (2010, see also Linder 1985) provide generic characterisations and an enumeration of the species of Restionaceae-Restioneae in southern Africa, although the limits of Restio itself are still unclear.

[Flagellariaceae [[Joinvilleaceae + Ecdeiocoleaceae] Poaceae]]: primary cell walls with mixed-linkage glucans; leaf blade with cross veins, ligule +; inflorescence paniculate, branches with adaxial swellings; flower type?; nucellar cap +, suprachalazal zone massive; fruit indehiscent, fleshy; cotyledon not photosynthetic.

Evolution. Ecology & Physiology. Net venation, animal-dispersed propagules, tolerance of shady habitats, and preference for well drained amnd fertile substrates are linked in 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 scoring of cross 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.

FLAGELLARIACEAE Dumortier, nom. cons.   Back to Poales

Stem apices dichotomise; flavonols +; endodermal cells radially elongated; culm solid; SiO₂ associated with vascular bundles only; neighbouring cells of stomata with oblique divisions; prophylls lateral; leaves with terminal tendril, ?auricles, sheath also closed; flowers perfect, prophylls 0; P pseudo-uniseriate; style solid; micropyle endostomal, outer integument ca 4 cells across, parietal tissue 1 cell across; embryo sac bisporic, eight nucleate [Allium-type]; fruit a drupe, seed coat adnate to pericarp; outer periclinal wall of exotesta persisting; n = 19; ORF 2280 present?; seedling with collar hairs +, coleoptile at most short.

1[list]/4. Palaeotropics, to the Pacific Islands (map: van Steeenis & van Balgooy 1966; Heywood 1978). [Photo - Flower]

• Flagellariaceae are robust, climbing or scrambling rather grass-like plants that can be recognised by their leaves that terminate in a sensitive tendril by which the plant is attached to its support. The rather large, paniculate inflorescences have many small, perfect flowers.

Evolution. Divergence & Distribution. Flagellariaceae may be ca 108 million years old (Janssen & Bremer 2004: but note the topology).

Chemistry, Morphology, etc. Flagellaria indica has dichotomising stem apices; vegetative leaves of aerial shoots lack axillary buds (Tomlinson & Posluszny 1977). The stigma has "multicellular papillae". Since the seed coat is adnate to the fruit wall, I suppose the fruit is a caryopsis s.l... There is disagreement as to whether or not the ORF 2280 gene is present - or perhaps there is variation (cf. Hahn et al. 1995 and Katayama & Ogihara 1996).

Some information is taken from Subramanyam and Narayana (1972) and Rudall and Linder (1988), both embryology, Tillich (1996: seed and seedling), Appel and Bayer (1998: general), Tillich and Sill (1999: general), and Sajo et al. (2007: style).

[Joinvilleaceae [Ecdeiocoleaceae + Poaceae]]: SiO₂ bodies cubic; epidermis with microhairs; foliar epidermis with long and short cells [latter SiO₂-containing] throughout; guard cells dumb-bell-shaped; fusoid cells [large colourless cells in central mesophyll] +; culm hollow [level?]; endothecial cells with girdle thickenings [?Poaceae]; first seedling leaf lacking lamina [possible]; 28 and 6.4 kb chloroplast genome inversion +.

Evolution. Divergence & Distribution. This clade may have originated ca 103 million years before present (Janssen & Bremer 2004), although note that Flagellariaceae are not associated with it in that analysis; it diversified only ca 90 million years before present.

Chemistry, Morphology, etc. The microhairs are multicellular in Joinvilleaceae and some Poaceae. Ecdeiocoleaceae, a small family of small herbs, has recently been placed in this clade (see below). If their seedlings have leaf blades, they may provide a valuable source of data on epidermal anatomy. See Endress (1995b) for some details of floral morphology. For chloroplast genome inversions, see Doyle et al. (1992); the 6.4 kb inversion has recently been reported in Ecdeiocoleaceae (Michelangeli et al. 2002, 2003; Marchant & Briggs 2007). For a trnT inversion, see Morris and Duvall (2010).

JOINVILLEACEAE Tomlinson & A. C. Smith   Back to Poales

Microhairs multicellular; leaf vernation plicate, auricles or ligules +; flowers perfect; outer T hooded; ovule straight, parietal tissue?; fruit a drupe, 1-3-seeded, P persistent; endotegmen tanniniferous; n = 18; rps14 gene to nucleus, pseudogene remaining in mitochondrion; first seedling leaf lacking lamina.

1[list]/2. Malay Peninsula to the Pacific (map: from van Steenis & van Balgooy 1966; Newell 1969). [Photo - Habit, Flower.]

• Joinvilleaceae are robust, grass-like plants with plicate leaves and terminal panicles of small, perfect, brownish flowers.

Evolution. Divergence & Distribution. Joinvilleaceae may be some 90 million years old (Janssen & Bremer 2004); they are reported as fossils from New Zealand, although they do not grow there now (Lee et al. 2001).

Chemistry, Morphology, etc. The outer tepals may have only a single trace (Newell 1969).

Some information is taken from Newell (1969: revision) and Bayer and Appel (1998: general).

[Ecdeiocoleaceae + Poaceae]: flowers monosymmetric by reduction; fruit 1-seeded.

ECDEIOCOLEACEAE D. F. Cutler & Airy Shaw   Back to Poales

SiO₂ as sand; vessels?; stomata in grooves down culm; ?microhairs; epidermal long and short cells 0; leaves reduced, sheath closed, auricles +; plant monoecious, culm branched, inflorescence branch swellings?, with "spikelets"; flowers imperfect, monosymmetric by reduction; P 2, conduplicate and keeled, + 4, flat; staminate flowers: A 4 [Ecdeiocolea]; pollen with operculum, wall without scrobiculi, with intraexinous channels; carpellate flowers: ovule apical, straight, area of enlarged cells near embryo sac; embryo sac tetrasporic, 16-celled [ovule, etc. - all Ecdeiocolea]; fruit 1-seeded, achene or capsule; ?perisperm +; exotestal cells large; n = ca 24, 32, 33; seedling?

2[list]/3. S.W. Australia (map: from FloraBase 2004).

Evolution. Divergence & Distribution. Stem-group Ecdeiocoleaceae are dated to ca 89 million years before present, the crown group diverge ca 73 million years before present (Janssen & Bremer 2004).

Chemistry, Morphology, etc. There is no evidence of differentiated long/short epidermal cells here (B. G. Briggs, in Givnish et al. 2010b).

In Georgeantha only the two adaxial calyx members are keeled, while in Ecdeiocolea the differentiation is somewhat less pronounced. The flowers of Ecdeicolea are monosymmetric; the four stamens probably represent 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.

Some information is taken from Briggs and Johnson (1998), Linder et al. (1998), Rudall (1990: embryology), and especially Rudall et al. (2005a: floral development, fruits).

POACEAE Barnhart, nom. cons.//GRAMINEAE Jussieu, nom. cons. et nom. alt.   Back to Poales

(Aerial branching + [?level]); vesicular-arbuscular mycorrhizae +; 3 desoxyanthocyanins, flavone 5- and C-glycosides, tricin, flavonoid sulphates, (cyanogenic glycosides) +; primary cell wall rich in arabinoxylans, pectin 10³%, xyloglucans lacking fucose; lignins acylated with p-coumarates [?level]; sieve tube plastids also with rod-shaped protein bodies, P-proteins 0; arm and fusoid cells +; cuticle waxes as aggregated rodlets; stomatal subsidiary cells conical to dome-shaped; microhairs bicellular; leaves pseudopetiolate, ligulate, vernation supervolute(-plicate), midrib +; flowers monosymmetric by reduction; T with two adaxial outer members distinct, abaxial smaller; A centrifixed [?level]; pollen grains central in loculus, with operculum, wall without scrobiculi, with intraexinous channels; G (open in development), style solid [?level], stigmas 3[?]; ovule single, central, amphitropous or hemianatropous, micropyle endostomal, funicle short; fruit an achene, the tegmen closely adherent to pericarp [= caryopsis], testa not persistent, hilum long [reverses]; peripheral layer of endosperm meristematic, embryo lateral, long, well differentiated, cotyledon lateral, plumule terminal; primary root 0, collar [epiblast, the ligule of the cotyledon] conspicuous; n = ?; 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, duplication of AP1/FUL genes [= FUL1 and FUL2], rpoC2 gene insert, rps14 gene to nucleus, pseudogene remaining in mitochondrion, intergenomic translocation of chloroplast rpl23 gene; ADP-glucose pyrophosphorylase in cytosol.

668/11160. Thirteen subfamilies below. Worldwide (map: from Vester 1940; Hultén 1961). [Genera List] [Photo - Flower.]

1. Anomochlooideae Potzdal

(Leaves spiral - Streptochaeta); pseudopetiole with an apical (and basal) pulvinus; ligule as a fringe of hairs; inflorescence branches cymose, two "bracts" along each branch unit, two more "bracts" below each flower; flowers perfact; P 2 (3) + 3; or flowers spirally arrranged along racemose axis, with several spiral "bracts" below each flower, = T, possibly 3 + 3, the latter coriaceous; A (4 - Anomochloa), sub-basifixed, basally connate, not dangling, [anthers latrorse, wall development of the Reduced type, endothecium lacking thickenings; microsporogenesis simultaneous; stigma not plumose - all Streptochaeta]; 21bp [long] subrepeats in rpoC2 gene insert; n = 11, 18; first seedling leaf lacking lamina.

2/4. Central America to S.E. Brasil, scattered, forests (map: from Judziewicz et al. 1999).

Synonymy: Anomochloaceae Nakai, Streptochaetaceae Nakai

[Pharoideae [Puelioideae [PACMAD + BEP clades]]] / the spikelet clade: leaves with ± membranous ligules, whether or not also ciliate; inflorescence of laterally compressed, racemose, pedunculate spikelets, with two basal glumes [sterile bracts = spikelet bract + prophyll], flowers few, two-ranked, each with lemma and palea [?= bract and 2 adaxial connate outer-whorl tepals], inverted, lodicules [= inner whorl/C?] 3 [median member adaxial]; n = 12; 1 bp deletion in the 3' end of the mat K gene, loss of rpoC1 gene, 39bp subrepeats in rpoC2 gene insert.

Evolution. Bouchenak-Khelladi et al. (2009, see also 2010a) estimated that the spikelet clade originated ca 75 million years ago in the Late Cretaceous, (83-)67(-55) million years, while Bouchenak-Khelladi et al. (2010c) give an estimate of (83-)67(-55) million years.

2. Pharoideae L. G. Clark & Judziewicz

Microhairs 0; leaves resupinate, lateral veins oblique; plants monoecious; spikelets 1-flowered; staminate flowers: A 6, anthers latrorse, wall of the Reduced type, endothecium lacking thickenings [both Pharus]; carpellate flowers: style solid; micropyle bistomal [Pharus]; coleoptile [= first seedling leaf] with lamina.

3/14. Pantropical, in forests (map: from Judziewicz 1987; Judziewicz et al. 1999).

Synonymy: Pharaceae Herter

[Puelioideae [[PACMAD + BEP clades]] / the bistigmatic clade: phytoliths saddle-shaped; spikelets disarticulating above the glumes; anthers versatile[?]; pollen grains peripheral in loculus; stigmas 2, two orders of stigmatic branching; 15bp ndhF insertion.

3. Puelioideae L. G. Clark, M. Kobay., S. Mathews, Spangler & E. A. Kellogg

Characters?; flowers perfect; A 6; seedling leaf unknown.

2/11. Tropical Africa (map: from Emmet Judziewicz, pers. comm.).

[PACMAD + BEP clades]: (benzoxazinoids, ergot alkaloids [latter synthesized by endophytes] +); arm and fusoid cells 0; foliar cross veins 0; pseudopetiole 0 flower type?; C/lodicules 2; A 3; G 2, styles separate; antipodal cells proliferating; x = 12; genome duplication, 15 bp insertion in ndhF gene, disease resistance by the Hm 1 gene.

These are mostly non-forest grasses.

[Aristidoideae [Panicoideae [[Arundinoideae + Micrairoideae] [Danthonioideae + Chloridoideae]]]] / PACMAD clade: ligule often of hairs; phytoliths dumb-bell-shaped; mesocotyl internode elongated, epiblast 0; extension of ndhF gene from the short single copy region into the inverted repeat.

Evolution. Bouchenak-Khelladi et al. (2009, see also 2010a) suggest that the PACMAD clade diversified towards the end of the Eocene some 45-37 million years ago.

4. Aristidoideae Caro

(C₄ photosynthesis); ligule with line of hairs; spikelet elongated-cylindrical, disarticulating above glume; lemma awn trifid, or 3 (1) awns, with basal column; callus sharp; n = 11, 12; germination flap +; C₄ photosynthesis prevalent.

3/349: Aristida (250-290), Stipagrostis (50). Warm temperate, few in Europe.

[Panicoideae [[Arundinoideae + Micrairoideae] [Danthonioideae + Chloridoideae]]]: (C₄ photosynthesis); 6 bp insertion in the 3' end of the mat K gene [?whole clade]

5. Panicoideae Link (includes Centothecoideae Soderstrom - see Sánchez-Ken & Clark 2010)

(Culms branched); (fusoid cells +); microhairs elongated, with slender, thin-walled cap cells ["panicoid type"]; (mesophyll differentiated into palisade and spongy tissues; chlorenchyma cells lobed [cf. arm cells]); culms usually solid; spikelet development basipetal, dorsally compressed, rachilla 0, 2-flowered, lower flower staminate or sterile [gynoecial cell death caused by Tasselseed2], spikelet dispersed as a 1-seeded unit by disarticulation below the glumes; (style +); hilum non-linear; overlapping embryonic leaf margins; C₄ photosynthesis common; 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.

218/3236: Panicum (500 s.l., but polyphyletic, 100 s. str., Dicanthelium [55] - see e.g. Zuloaga et al. 2007), Paspalum (330), Cenchrus (105: inc. Pennisetum), Andropogon (100), Panicum s. str. (100), Dicanthelium (55), Eriachne (40). Tropics to temperate.

Synonymy: Andropogonaceae Martinov, Arundinellaceae Herter, Cenchraceae Link, Panicaceae Berchtold & J. Presl, Paspalaceae Link, Saccharaceae Berchtold & J. Presl, Zeaceae A. Kerner

[[Arundinoideae + Micrairoideae] [Danthonioideae + Chloridoideae]]: ?

[Arundinoideae + Micrairoideae]: ?

6. Arundinoideae Burmeister

Microhairs elongated, with slender, thin-walled cap cells ["panicoid type"]; hilum short; n = 6, 9, 12.

14/45. Temperate to tropical, hydrophytic to xerophytic.

The exact contents of this subfamily are still unclear.

Synonymy: Arundinaceae Döll

7. Micrairoideae Pilger

Stomata with dome-shaped subsidiary cells; ligule with fringe of hairs; lemma awn +/0; embryo small, starch grains simple; n = 10; germination flap +; (C₄ photosynthesis - Eriachneae).

8/188: Isachne (100), Eriachne (35). Tropics.

Micraira has spirally arranged leaves and at least some species are resurrection plants.

For further information, see Sánchez-Ken et al. (2007).

[Danthonioideae + Chloridoideae]: hilum short, punctate.

8. Danthonioideae Barker & Linder

Prophylls bilobed [?distribution]; leaf blades symmetrical, (not Merxmuellera); lemma awn trifid, or 3 awns; bases of styles well apart; synergid cells haustorial; n = 6, 7, 9.

17/281: Danthonia (100), Rytidosperma (90). Widespread, esp. Southern Hemisphere, few Southeast Asia-Malesian.

9. Chloridoideae Beilschmied

C₄ PCK subtype (phosphoenolpyruvate carboxykinase) + (0); microhairs usu. with ± hemispherical and thick-walled distal cells and long base cell, latter with internal membranes and secretory ["chloridoid type"]; leaf blades symmetrical (Merxmullera - not); spikelets disarticulating above the glumes; embryo with an epiblast, mesocotyl +, leaf margins not overlapping; 4 bp insertion in the rpl16 intron; n = (6-8) 9, 10; C₄ photosynthesis prevalent.

130/1607: Eragrostis (300), Muhlenbergia (155), Sporobolus (160), Chloris (55). Tropical to warm temperate, more or less dry environments especially in Africa and Australia.

Synonymy: Chloridaceae Berchtold & J. Presl, Cynodontaceae Link, Eragrostidaceae Herter, Lepturaceae Herter, Pappophoraceae Herter, Spartinaceae Link, Sporobolaceae Herter, nom. inval., Zoysiaceae Link

[Panicoideae + Centothecoideae] Arundinoideae + Chloridoideae: 6 bp insertion in the 3' end of the mat K gene.

Arundinoideae + Chloridoideae + Aristidoideae + Danthonioideae: ligule hairy; lemma awned; starch grains compound.

Panicoideae + Centothecoideae: hilum non-linear; overlapping embryonic leaf margins.

The first character could also be used to unite Panicoideae + Arundinoideae + Centothecoideae + Chloridoideae.

[Ehrhartoideae [Bambusoideae + Poöideae]] / BEP clade: endosperm softness gene +, [?embryo short]; x = 12.

For the evolution of a grain softness (HA-like gene) trait in the common ancestor of Ehrhartoideae and Poöideae, see Charles et al. (2009).

10. Ehrhartoideae Link

(Arm cells + - Oryzeae); (longitudinal walls of epidermal cell straight); (microhairs 0); spikelet deveklopmental basipetal, with only one carpellate floret fertile and with basal carpellate or sterile florets, glumes very small; A (1-)6, styles separate almost from the very base; n = (10, 15); (roots at scutellar node - Ehrharta).

17/111: Oryza (20), Leersia (20). Widespread, esp. S. hemisphere.

Synonymy: Ehrhartaceae Link, Oryzaceae Berchtold & J. Presl

Bambusoideae + Poöideae: embryo morphology [that of Brachyelytrum is like Bambusoideae...], embryonic leaf margins overlapping.

Evolution. Divergence & Distribution. Wu et al. (2012) suggest that this clade diverged (48.8-)42.8(-36.6) million years.

11. Bambusoideae Luersson

Woody; culms often branched; fusoid cells and strongly asymmetrically invaginated arm and fusioid cells +; microhairs elongated, with slender, thin-walled cap cells ["panicoid type"]; (multiple buds per node); leaves pseudopetiolate, often with inner and also outer ligules, culm leaves often very different from the others; (lodicules 3); A (2-)6(-140), (basally connate); stigmas (1-)2-3; (fruit a berry); first seedling leaf without lamina; n = 7, 9-12, much polyploidy.

84-101/1470. Bambusa (120), Chusquea (200), Sasa (60), Phyllostachys (55), Arundinaria (50). Tropical to temperate, often in forests (map: see Judziewicz et al. 1999; Sungkaew et al. 2009).

Synonymy: Bambusaceae Berchtold & J. Presl, Olyraceae Berchtold & J. Presl, Parianaceae Nakai

12. Poöideae Bentham

Epichloe endophytes pervasive; aerial branching at most rare; fructose oligosaccharides in stem; root epidermal cell division forming trichoblast/atrichoblast pair asymmetric; longitudinal walls of epidermal cells straight [?level]; lemma usually with 5 nerves; lodicules at most slightly vascularized; styles separate almost from the very base; (postament +); hilum often short; (endosperm with some non-starch soluble storage polysaccharides); embryo small, epiblast +, scutellar cleft 0 [scutellum not peltate], mesocotyl 0; n = (2, 4-13); duplication of the ß-amylase gene.

179/3850. Festuca (470: inc. Lolium), Poa (200), Stipa (300), Calamagrostis (230), Agrostis (220), Elymus (150), Bromus (100). Largely North Temperate.

Brachyelytreae Ohwi

Stomata subsidiary cells with parallel sides; n = 11.

1/3. Eastern Asia, E. North America.

Poöideae minus Brachyelytreae: primary inflorescence branches 2-ranked; embryo lacking scutellar cleft, embryonic leaf margins non-overlapping.

Nardeae Koch

Lodicules 0; style and stigma 1; n = 10, 13.

2/2. Europe.

Synonymy: Nardaceae Martynov

Poöideae minus Brachyelytreae, Nardeae: microhairs 0 (+ - some Stipeae); (stomata subsidiary cells with parallel sides); n = 7 [chromosomes "large"].

Synonymy: Aegilopaceae Martynov, Agrostidaceae Berchtold & J. Presl, Alopecuraceae Martynov, Anthoxanthaceae Link, Avenaceae Martynov, Bromaceae Berchtold & J. Presl, Chaeturaceae Link, Cynosuraceae Link, Festucaceae Sprengel, Glyceriaceae link, Holcaceae Link, Hordeaceae Berchtold & J. Presl, Laguraceae Link, Loliaceae Link, Melicaceae Martynov, Miliaceae Link, Phalaridaceae link, Phleaceae Link, Sesleriaceae Döll, Stipaceae Berchtold & J. Presl, Triticaceae Link

• Poaceae can be recognised by their leaves that have long, usually open sheaths and ligules at the sheath-lamina junction, round and often hollow stems/culms, and inflorescences whose basic unit is a spikelet. Individual flowers are small, lacking an obvious perianth and with a gynoecium that usually has two plumose stigmas and a single ovule. In the dry, achenial fruit (often called a caryopsis), the rather large embryo is lateral, lying next to the seed coat.

• The large tribe Andropogoneae, with almost 1,100 species, can be distinguished from all other grasses because they have paired spikelets.

Evolution. Divergence & Distribution. Stem-group Poaceae are dated to ca 89 million years before present, the crown group diverge ca 83 million years before present (Janssen & Bremer 2004: Streptochaeta included, see also Bremer 2002; dates in Wikström et al. 2001 are far younger). Bouchenak-Khelladi et al. (2009, 2010a) suggest that grasses originated ca 90 million years ago, although Bouchenak-Khelladi et al. (2010c) estimated that the basal split in the family was rather younger, (86-)68(-53) million years, i.e. in the Late Cretaceous (in their Fig. 1 it is ca 72 million years). Interestingly, Bouchenak-Khelladi et al. (2010c) suggest that the family originated in Africa; Bremer () had suggested that its origin was in South America - either way, it seems to be Gondwanan. The family may initially have been forest dwellers, and the species-poor clades, as well as the stem PACMAD clade, may have diverged by the end of the Cretaceous (Bouchenak-Khelladi et al. 2010c - but Puelioideae not included).

Molecular evidence suggests that the bulk of the family, i.e. the [PACMAD + BEP] clade, may have begun to diversify (53.8-)51.9(-59) million years ago (Wu & Ge 2012: 95% c.i.). Most other estimates are broadly similar. Thus Vicentini et al. (2008) suggested ages of (60-)52(-44) million years for the clade, Kim et al. (2009: MAD members not included) dated it 67.8-50 million years (see also Bouchenak-Khelladi et al. 2010a), and Bouchenak-Khelladi et al. (2010c) estimate ages of (55-)52(-50) million years.

However, Poinar (2004) proposed that Programinis burmitis, found fossil in deposits from the Early Cretaceous of Myanmar some 100-110 million years ago, represented an early bambusoid grass. However, 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 here (Caroline Stömberg, pers. comm.; Smith et al. 2010). Nevertheless, in a recent more detailed analysis of the fossil P. laminatus, Poinar (2011) affirms that the silica bodies, etc., indeed support a placement in Poaceae, particularly in Pooideae, so suggesting an age for that subfamily about twice that of other estimates (see below). The age of grasses (as well as that of other monocot groups, not to mention the animals, both vertebrates and insects, associated with them) is also questioned, 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 (71-65 million years before present) of central India (Prasad et al. 2005), and this would date the origination of the PACMAD-BEP clade to some 85-80 million years ago. This record needs confirmation, although the enigmatic Late Cretaceous mammalian sudamericid gondwanatherians also had hypsodont teeth and there is a record of a hadrosaurian dinosaur with carbon isotope ratios that suggests that it might have been eating C₄ plants (Prasad et al. 2005; Bocherens et al. 1994); of course, the origin of C₄ grasses - and most other C₄ plants - is usually put in the middle of the Tertiary. 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. The bottom line is that dates from these different lines of evidence are apparently irreconcilably in conflict (Vicentini et al. 2008).

Fossil spikelets assignable to the [PACMAD + BEP] clade are known from the Palaeocene-Eocene boundary, about 55 million years before present (Crepet & Feldman 1991), and this estimate is broadly in line with an estimate of the age of a genome duplication in Poaceae (70-50 million years before present: Blanc & Wolfe 2004; Schlueter et al. 2004; Paterson et al. 2004; Kim et al. 2009) and other estimates like that of Vicentini et al. (2008) and Bouchenak-Khelladi et al. (2010a) - (60-)52(-44) million years old. Bouchenak-Khelladi et al. (2009, 2010a, c) suggested that the BEP clade began to diversify at the end of the Palaeocene about 55-53 million years ago, while Wu and Ge (2012) offer a slightly younger age of (51.6-)46.7(-40.8) million years. The PACMAD clade itself may have diversified rather later, some 45-37 million years ago (see Bouchenak-Khelladi et al. 2010a for other dates), although Bouchenak-Khelladi et al. 2010c suggest a younger age of (34-)28(-22) million years. Bouchenak-Khelladi et al. (2009, see also 2010a, c) suggested that Bambusoideae diversified only some (39-)32(-24) million years ago in the middle Oligocene (see also Wu & Ge 2012). Stem Aristidoideae date from (38-)29(-9) million years ago, crown diversification dates from (25.5-)20.3(-15.9) million years ago, but much diversification there is considerably younger (Bouchenak-Khelladi et al. 2010a; Cerros-Tlatilpa et al. 2011, q.v. for other estimates).

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, with most species belonging to Poaceae themselves. The second most species-rich family (Restionaceae) in the Poaceae group has only some 520 species, and the other families are tiny. Poaceae themselves may be seven times more speciose than their animal-pollinated sister clade (Kay & Sargent 2009: surely a stunning underestimate?). But again, even within Poaceae there are three species-poor clades that are successively immediately sister below the PACMAD and BEP clades (to add to the two to three more such clades successively sister below the family), so calling the whole family speciose is not very accurate; any foci of diversification may be within the PACMAD and BEP clades (see also Linder & Rudall 2005; Smith et al. 2011; and especially Bouchenak-Khelladi et al. 2010c for diversification).

So such statements about diversification can be refined, as by Bouchenak-Khelladi et al. (2010c). 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, and several others elsewhere in the family (see also Bouchenak-Khelladi et al. 2010c). The herbaceous habit and annual life cycle appear to be correlated with species richness (Salamin & Davies 2004; Smith & Donoghue 2008). However, Soreng and Davis (1998) in particular show how difficult it is to be sure of the position on the tree of many of the characters mentioned above.

Ecology & Physiology. Much has been written on the evolution of C₄ photosynthesis in grasses, e.g. see Kellogg (1999), etc. Over half the species with the C₄ photosynthetic pathway occur in Poaceae - in total there are a mere 6,000-6,500 species involved (R. F. Sage, pers. comm.) of which about 4,500 species are grasses (Sage et al. 1999; Grass Phylogeny Working Group II 2011), and ca 50% of the PACMAD species alone have C₄ photosynthesis. The adoption of C₄ photosynthesis is associated with well-known anatomical changes, such as closer spacing of the veins, the development of a sheath of chloroplast-rich cells around the vascular bundles, etc. - the Kranz anatomical syndrome (see Pengelly et al. 2011 for vein spacing). Anatomy is also used to characterize subtypes of photosynthetic pathways; however, the correlation may not be that good (Ingram 2010), and the typology needs to be revisited (E. A. Kellogg, pers. comm.). Details of the mechanisms of C₄ photosynthesis and the morphologies associated with it are very variable in Panicoideae, and C₄ photosynthesis has evolved more than once there (Kellogg 2000 and references; see also Giussani et al. 2001; Christin et al. 2007a, 2009a).

There has been massive parallelism in the acquisition of C₄ photosynthesis, perhaps reflecting an underlying change that faciltated the "independent" acquisitions (Grass Phylogeny Working Group II 2011). Thus C₄ photosynthesis may have evolved up to eight times in Panicoideae alone (Giussani et al. 2001); it has also evolved independently in Micrairoideae, Aristidoideae (twice) and Chloridoideae, etc., for a total of perhaps 22-24 independent origins (Kellogg 2000 and references; Christin et al. 2008, 2009a, b; Vicentini et al. 2008; Cerros-Tlatilpa & Columbus 2009 and Christin & Besnard 2009 [both Aristidoideae]; Sage et al. 2011; Grass Phylogeny Working Group II 2011). Interestingly, both origins of and reversals from C₄ photosynthesis may be clustered, although reversals are not very common (Vicentini et al. 2008, for reversals from C₄, see also Ibrahim et al. 2009). It has been suggested that the relatively uncommon C₄ PCK subtype (phosphoenolpyruvate carboxykinase) is basal in Chloridoideae, being subsequently lost and reacquired (Christin et al. 2009b, but see Christin et al. 2010a for reversals; also Ingram et al. 2011b for a reversal that wasn't).

Indeed, parallelism here may be at the level of particular amino acid being substituted, similar changes occurring independently in the phosphoenolpyruvate carboxylase gene in grasses (Christin et al. 2007a, esp. b, 2009a). In particular, 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).

Although members of the basal pectinations of Poaceae are largely woodland dwellers, grasses of the [PACMAD + BEP] clade predominantly prefer more open habitats - although of course some Bambusoideae are forest dwellers. The factors that favoured the initial development of grasslands, that might later cause clustering of origins and losses of different photosynthetic mechanisms, and that were involved in the great spread and expansion to dominance of late Miocene C₄ grasslands, remain unclear (see also Tipple & Pagani 2007; Christin et al. 2008, for the early origins of of C₄ photosynthesis and its subsequent development; Jacobs et al. 1999 and especially Retallack 2001 for the paleoecology of Poaceae; Sage & Kubien 2003; Fox & Koch 2004; Osborne & Beerling 2006; Bond 2008; Osborne 2008 for fires, etc.; Osborne & Freckleton 2009: open habitats, then drier conditions; Arakaki et al. 2011). Open habitat grasses, probably C₃, appear in the Middle Eocene ca 42 million years ago, and may have become locally dominant (Strömberg 2011). Taylor et al. (2010) and Ripley et al. (2010) make ecophysiological comparisons between C₃ and C₄ grasses, the latter sometimes being more sensitive to drought and recovering more slowly from it. But in the late Miocene declining CO₂ in the atmosphere may also have helped things along again (Arakaki et al. 2011), and certainly fires become common from the Late Miocene onwards (Bond & Scott 2010). Recent work suggests that C₄ grasses may also be favoured by the combination of increasing temperatures and increasing CO₂ concentrations, since stomata close and hence transpiration losses are reduced (the effect of temperature) but C fixation is not necessarily reduced (the effect of CO₂ concentration) (Morgan et al. 2011). It may be noted that taxa like Miscanthus x giganteus carry out C₄ photosynthesis under decidedly cooler conditions than is common (Wang et al. 2008).

There is a pronounced lag at both global and local scales between the initial evolution and diversification of grasses that carry out C₄ photosynthesis and their ecological expansion (e.g.Srömberg & McInerney 2011) - a lag of over 20 million years. The balance of the evidence suggests that C₄ photosynthesis in grasses appeared first in the Oligocene, some 32 million years ago as global CO₂ levels in the atmosphere declined (e.g. Christin et al. 2008, 2011b; Vicentini et al. 2008; Bouchenak-Khelladi et al. 2009 - but see below). It is known from grasses from the Early to Middle Miocene in both the Great Plains and Africa, some 25-12.5 million years before present, as C₄ photosynthesis became energetically advantageous in some environments (e.g. Ehleringer 1997 and references; Christin et al. 2008, 2011b). The great expansion of grasses with C₄ photosynthesis seems to have occurred considerably later - i.e. in the late Miocene only 9-4 million years before present - than the initial evolution of this photosynthetic syndrome (e.g., for Aristidoideae, see Cerros-Tlatilpa et al. 2011).

Understanding the ecological relationship between grasslands and woodland over time is important. Recent work suggests that many C₄ origins are correlated with a reduction in annual rainfall - and grasslands transpire less than the woodlands they seem initially to have replaced (Retallack 2001). This may be connected with declining late Miocene temperatures, as Arakaki et al. (2011) point out - which perhaps favoured the expansion of more open habitats in which these grasses thrived (Edwards & Smith 2010). The spread of grasslands may be associated with a CO₂ decrease (Arakaki et al. 2011) perhaps connected with the activities of ectomycorrhizal taxa (Taylor et al. 2009; see Gerhart and Ward 2010 and Zachos et al. 2008 for past CO₂ concentrations) which made trees less competitive (Pagani et al. 2009). Increasing temperature, open habitats, and perhaps especially decreasing precipitation (e.g. Edwards & Still 2007; Edwards et al. 2007; esp. Edwards & Still 2008 - although by no means all C₄ grasses are drought tolerant; Edwards 2009), the high flammability of dry grasses, and windiness are all factors that would lead to the increased occurrence of fires (D'Antonio & Vitousek 1992 on exotic grasses; Bond & Scott 2010). Interestingly, there is a negative correlation between silicon concentration - especially high in annual grasses - and rate of leaf decomposition (Cook & Leishman 2011b). Fires are likely to have caused the death of trees and also the loss of nitrogen by volatilizing it. Both would favour grasses: The habitat was opened, and C₄ grasses have a reduced requirement for photosynthetic enzymes and so a lower nitrogen requirement (Wedin 1995). The relatively low nitrogen content in grass litter means that this builds up, so making grasslands still more prone to fire (Wedin 1995). However, although panicoid grasses recover well after fires, it is unclear if C₄ grasses perform better in this respect than C₃ grasses (Ripley et al. 2011). Note, however, that McInerey et al. (2011) suggest that the late Neogene expansion of C₄ grasses in North America was at the expense of C₃ grasses rather than woody vegetation. Grasses also have dense - and sometimes remarkably deepp - root masses that would make the establishment of woody vegetation in grassland difficult.

Cooler temperate grasslands are dominated by the derived Poöideae, all of which are C₃ grasses, and understanding diversification in Poöideae entails understanding the evolution of cold tolerance (Edwards 2009; Edwards & Smith 2010). Core Poöideae evolution may be linked with a period of cooling at the beginning of the Oligocene ca 33-27 million years ago (Strömberg 2005; Sandve et al. 2008; Sandve & Fjellheim 2010). Gene families implicated in low temperature stress response expanded prior to Poöideae diversification (Sandve & Fjellheim 2010), and proteins that inhibit ice recrystallization are known from the group (Sandve et al. 2010; Tremblay et al. 2005). There is a complex relationship between day length, freezing tolerance and flowering (Dhillon et al. 2010). Furthermore, although only low levels of fructan - specifically levans - accumulation have been noted in many Poaceae, notably high levels are found only in Poöideae, although not in the taxa of the "basal" pectinations (see Hendry 1993 for taxa involved; Pollard & Cairns 1991). Storing carbohydrates as fructans may enable these Poöideae to survive drought or frost better, fructans being implicated in stabilizing cell membranes at low temperatures (Livingston et al. 2009; Sandve & Fjellheim 2010). Another factor contributing to the diversification of Poöideae may be the establishment of vernalization (Preston & Kellogg 2008), although how widely this occurs outside the subfamily is unclear. Finally, the establishment 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).

To summarize: Grasses now cover about 20% of the land surface, about half that area being within the tropics (Hall et al. 2000; Sabelli & Larkins 2009 for references). In warmer grasslands C₄ grasses now predominate, and all told C₄ photosynthesis accounts for about 18-21% of terrestrial gross primary productivity (Lloyd & Farquhar 1994; Ehleringer et al. 1997). Similarly, it has been suggested that grasslands - both C₃ and C₄ species are of course involved - currently account for 11-19% of net primary productivity on land and 10-30% of soil C storage (Hall et al. 2000). What makes grasslands still more distinctive ecologically is not just the abundance of grasses and their distinctive growth habit, but that relatively few species of grasses are ecologically dominant in any one place, and most of these seem to be C₄ grasses (Edwards et al. 2010). Open-habitat grasses - these were mostly C₃ grasses initially - diversified taxonomically in North America in the early Oligocene ca 34 million years ago and became ecologically dominant in the late Miocene 11-7 million years later (Strömberg 2005), although grasslands of the Great Plains may be late Oligocene ca 24 millions year in age and Argentinian grasslands even older (Edwards et al. 2010). Some C₄ grasses may have originated in the Oligocene ca 33 million years ago, but again they became diverse - and made a corresponding major contribution to overall vegetation biomass - only in the late Miocene 9-8 million years ago, the process being complete as recently as the late Pliocene, a mere 3-2 million years ago (Bouchenak-Khelladi et al. 2009; Edwards et al. 2010; Strömberg & McInerney 2011; McInerny et al. 2011 for North America; Arakaki et al. 2011). Indeed, the Neogene has been called the age of grasses (cf. Palaeos). Not that this implies that species-poor ecosystems function adequately; evidence suggests that diversity improves ecosystem functioning, although this also depends on rainfall, temperature, levels of soil nutrients and CO₂, etc. (see e.g. Chapin et al. 1997; Zavaleta et al. 2003; Maestre et al. 2012, and references).

The Miocene radiation of grazing mammals (Thomasson & Voorhies 1990) has been linked to the spread of prairie and savannah grasses (see also Cerling et al. 1997; Bouchenak-Khelladi et al. 2009, 2010a, the latter with considerable detail and many dates; Mihlbachler et al. 2011). These mammals evolved hypsodont dentition, i.e. teeth with high crowns, enamel extending below the gum lines, and short roots, apparently to deal with the wear caused by eating the abrasive grasses with their complex silica bodies. However, recent findings suggest that tooth enamel is harder than silica (Sanson et al. 2007; Sanson 2006, for silica, see also below), and that dust particles, more numerous in food eaten by a grazer than by a browser, may be the most abrasive element in the food ingested (e.g. Kay and Covert 1983). Futhermore, the persistent dead leaves of most grasses may also decrease their palatability (Antonelli et al. 2010), while C₄ grasses may be less palatable than C₃ grasses, having more sclerenchyma because the veins are closer (see Caswell et al. 1973 in part), although the nitrogen content of C₃ and C₄ grasses seems to be similar (Taylor et al. 2010).

Experiments have shown that silica bodies do affect the feeding behaviour of herbivores, both mammals and insects, even if they are not the immediate "cause" of hypsodonty in mammalian teeth. Higher silica in grasses decreases the amount of nitrogen taken up by both voles (Microtus) and armyworm (Spodoptera exempta) larvae, and in the latter in particular there are long-term negative effects on the growth of the caterpillar, perhaps via damage to the larval midgut. The mandibles of armyworm larvae are indeed worn down by silica, moreover, it is well known that at least some grasses tissues produced after attack by a herbivore (but not after comparable mechanical damage) have an increased silica concentration and are less attractive to the animals (see Massey & Hartley 2006, 2009; Massey et al. 2007b). Of course, silica is not the only defence that grasses have (Massey et al. 2007a), for instance, they vary in toughness, and may contain noxious metabolites, sometimes because of their association with endophytes (see above). In some grasses, at least, defence against herbivores is mediated by the production of volatiles which attract nematodes (to attack Diabrotica larvae) or parasitic wasps (to attack caterpillars: Degenhardt 2009).

Any relationship between silica and mechanical protection of plant tissues is not straightforward. Although prairie grasses expanded in Nebraska in the Early Miocene ca 23 million years before present, hypsodont ungulates were already around by then (Strömberg 2004); Bovidae and Cervidae started diversifying at least 26 million years ago (Bouchenak-Khelladi et al. 2009). Massive diversification of ungulates is largely a Miocene phenomenon (Bouchenak-Khelladi et al. 2009), and specialists on C₄ grasses seem to have evolved before those grasses dominate ecosystems (Edwards et al. 2010). Bouchenak-Khelladi et al. (2009) noted that the density of silica bodies in the leaf epidermis seems to have increased in a number of grass groups, perhaps as a defence against herbivory, however, Sanson and Heraud (2010) suggested that the silica there might not be in crystalline form and so be unable to cause wear on the enamel of mammalian teeth. Establishing connections between the evolution and rise to dominance of grasses in some ecosystems and the evolution of grazing animals needs more work, but it is likely that the two are linked, even if not at such a simplistic level as "high SiO₂ = hypsodonty" (see also Retallack 2001 for a good summary; Sanson 2006 for the mechanics of tooth action, about which surpisingly little is known).

There are additional eco-physiological factors to bear in mind. A number of grasses scattered in different subfamilies accumulate glycine betaines and other compounds commonly associated with allowing plants containing them to grow in saline conditions (Rhodes & Hanson 1993). Some Poaceae have allelopathic reactions with other plants, Sorghum roots producing a quinone (an oxygen-substituted aromatic compound) and Festuca roots meta-tyrosine, a non-protein amino acid (Bertin et al. 2007). Benzoxazinoids, cyclic hydroxamic acids, are known from members of Poaceae including both Panicoideae and Poöideae; they confer resistance to fungi, insects, and even herbicides, and they, too, are allelopathic (Frey et al. 1997, 2009). They are very uncommon in other angiosperms (Schullehner et al. 2008). Sindhu et al. (2008) note that the PACMAD clade are characterized by a gene that protects the plant against attack by the ascomycete Cochliobolus carbonorum. Leaves of pooid monocots (presumably including sedges) decompose more slowly than do those of other angiosperms (Cornwell et al. 2008), which may increase the accumulation of dead material in grasslands and their susceptibility to fire.

The dumb-bell shaped stomata of grasses show remarkably rapid stomatal movements, very much faster than those few other stomata have been examined (Franks & Farquhar 2006). However, the significance of this is unclear given that quite a number of other Poales have similar stomata; whether the evolution of these stomata is a major component of th ability of grasses to spread as climates became drier at the end of the Eocene remains to be seen (Hetherington " Woodward 2003). Prominent rhizosheaths - mucilage from root cap cells, soil particles, bacteria, etc., all anchored to root hairs - occur in many Poaceae (McCulley 1995), especially those growing in drier conditions, although the distribution of such roots is poorly known - they certainly occur in other Poales, but are apparently rare in broad-leaved angiosperms. Interestingly, C₄ grasses have roots with long root hairs yet may respond positively in terms of phosphorous uptake when forming endomycorrhizal associations - long root hairs and endomycorrhizal associations tend to be thought of as alternative ways of securing phosphorous supply, etc. (Schweiger et al. 1995 and references). Finally, it may be worth mentioning that 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). Ectomycorrhizal plants, also noted for dominating the communities in which they occur, also produce siderophores.

Bacterial/Fungal Associations. Clavicipitaceous endophytes (class 1 endophytes: Rodriguez et al. 2009) are widely distributed among grasses. Leuchtmann (1992) discussed the distribution and host specificity of grass endophytes in general (Clay 1990 is a still useful general review; see also Schardl 2010). Some 30% or more of Poöideae are involved in such associations, and both horizontal and in particular vertical transmission of these fungi occurs. They have been placed in ascomycetes-Clavicipitaceae-Balansiae (Clay 1986, but see below); for a review, see White et al. (2003). This endophyte-grass relationship is usually described as being one of mutualism, although this may sometimes, at least, not be so (see Saikkonen et al. 1998; Gundel et al. 2006; Ren & Clay 2009), and the more that is found out about this relationship, the more complex it appears to be. One of the most important fungi involved is Epichloë (Clavicipitaceae), a systemic endophyte restricted to Poöideae; Neotyphodium is its asexual stage, perhaps hybrids of Epichloë species (Roberts et al. 2005; Moon et al. 2005). For 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), and for the patterns of infection of the two fungal forms, see Rodgers et al. (2009). The association could be ca 40 million years old (Schardl et al. 2004).

The endophyte fungi involved are closely related to - and may have evolved from - fungi that are insect pathogens. Clavicipitaceae are now included in Hypocreales, and the old Clavicipitaceae have been split up. Hypocreales include many insect pathogens and especially parasites of other fungi, but also yeast-like obligate symbionts (of leaf hoppers). They may ancestrally have been plant parasites (e.g. Spatafora et al. 2007; Vega et al. 2009), but there has been widespread cross-kingdom host switching in the clade (e.g. Vega et al. 2009). A variety of insect pathogens have been found to be endophytes; thus Metarhizium robertsii may be both endophyte and insect pathogen (e.g. Sasan & Bidochka 2012). These fungi synthesize a diversity of secondary metabolites (Spatafora et al. 2007), and some of the insect pathogens are also antagonistic to plant pathogens (Vega et al. 2009 and references).

There are four groups of alkaloids that are synthesized by Epichloë: indole diterpenes, lolines, peramine, and the ergot alkaloids (Fleetwood et al. 2007). Indeed, a variety of "grass" alkaloids, including loliine (pyrrolizidine) and ergot alkaloids (ergolines), are synthesized by the fungal member of the endophyte-plant association. Loliine alkaloids are primarily active against insects (Schardl et al. 2007; Zhang et al. 2009), and so the presence of endophytes affects both the palatability of grasses to herbivores and of their seeds to granivorous birds, the animals eating the infected material sometimes not thriving at all; the level of aphid infestation and that of their parasites and parasitoids; and endophytes also affect the level of infestation by nematodes, resistance of the host plant to the effects of water stress, and even the pattern and rate of decomposition of dead grass are also affected (e.g. Madej & Clay 1991 - birds; Popay & Rowan 1994 - general; Omacini et al. 2001 - aphids; Lemmons et al. 2005 - decomposition; Tanaka et al. 2005 - insect herbivory; Hahn et al. 2007 - water deficit; Schardl 2010). Fungal endophytes may also affect root growth and root hair production (Sasan & Bidochka 2012). Furthermore, the larvae of Phorbia (or Botanophila) flies live on Epichloë stroma, and the adults transmit the fungal spermatia in a fashion analogous to insect pollination of flowers (Bultman 1995). Indeed, Epichloë synthesizes unique compounds that specifically attract the flies (Steinebrunner et al. 2008) and which may also be toxic to other fungi that secondarily invade the fungal stromata (Schiestl et al. 2006). However, the equilibrium of such relationships can easily be disturbed (Eaton et al. 2010).

Many species of other apparently symptomless endophyte species (class 3 endophytes) may grow together on Poaceae, but little is known about their interactions with the host. Márquez et al. (2007) found 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, while Marks and Clay (2007) discuss growth rate of endophyte-infected and -free plants under various conditions. For fungal records - very numerous and diverse - on grasses, see Tang et al. (2007); there are at least 1933 species of fungi from bamboos alone. Some root-associated endophytic fungi (class 4) are also coprophilic (Herrera et al. 2009), perhaps aiding in their dispersal.

Bacteria, too, may be endophytic in grasses, and several bacterial endophytes are implicated in fixing 1/3 to 1/5 the nitrogen needed by sugarcane in Brazil - the bacteria include Gluconacetobacter (alpha-Proteobacteria) and Herbaspirillum and Burkholderia (ß-Proteobacteria, for the latter, see also Fabaceae) (de Carvalho et al. 2011).

Parasitic rusts and smuts are common on Poaceae, and those on Bambusoideae, Poöideae (inc. Stipa and relatives) are particularly distinctive (Savile 1979b); two thirds of Ustilaginales (smuts) - close to 600 species - are found on Poaceae (Kukkonen & Timonen 1979; Stoll et al. 2003). Some seventy species of Berberis are alternate hosts (the aecial stage) for Puccinia graminis, the black stem rust of wheat and other grain crops in Poöideae - this species (or complex) infects some 77 genera of mostly pooid 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).

Plant/Animal Interactions. Despite the silica bodies mentioned above, as well as the presence alkaloids and other defences, Poaceae provide food for both adults (as pollen) and larvae (as roots) of Chrysomelidae-Galerucinae-Luperini-Diabrotica beetles (Jolivet & Hawkeswood 1995).

Caterpillars of nymphalid butterflies, in particular the browns, Satyrini, and the related tribes like Morphini, Melantinini, etc., are common on Poaceae, where they are the only common grazing insects. Satyrinae as a whole diverged from other Nymphalidae some 80-85 million years ago (or perhaps at the K/T boundary: Heikkilä et al. 2011), but the main (subtribal) clades did not diverge until the later part of the Palaeocene. Stem Satyrini themselves may have diverged about 65-55 million years ago, but divergence of the crown group is much later in the later Eocene, (41.7-)36.6(-31.5) million years ago (Peña & Wahlberg 2008; Wahlberg et al. 2009 - age depends on calibration points, the position of Satyrini varies). Other Satyrinae eat commelinid monocots, sometimes including grasses, but none of the subtribes involved has more than 110 species, compared to the some 2,200 species of Satyrinae-Satyrini.

Satyrini larvae almost exclusively eat grasses, and the main diversification within the clade, some 36.6 million years ago (see above), was perhaps contemporaneous with the initial spread of grasses (Peña et al. 2006, 2011; Peña & Wahlberg 2008). However, it may have been the move of satyrine butterflies from forests to more open environments where grasses are so abundant, not grass feeding per se, that helped spur the diversification of Satyrini (Peña et al. 2011). Diversification has also gone on in more forested habitats. Thus caterpillars of the largely South American Pronophilina, with well over 400 named species (?600 species total), are largely bamboo feeders to be found on Chusquea. They are mostly denizens of Andean cloud forests, and only a few species are to be found in comparable forests in east Brazil and Central America. They are most diverse just below the cloud forest-paramo transition at ca 3050-3250 m altitude, but some species are found in the paramo, where the bamboo Swallenochloa grows (Pyrcz et al. 2009; Casner & Pyrcz 2010).

Galling dipterans, especially Cecidomyiidae, are quite common in grasses (Labandeira 2005). Thus cecidomyiid gall midges, notably Mayatiola (M. destructor is the Hessian fly), are quite common on Poöideae in North America (Gagné 1989). Shoot flies (Diptera - Chloropidae) are form galls on monocots, especially grasses, but they are also simple herbivores and have other life styles (de Bruyn 2005). Chinch bugs of the Hemiptera-Lygaeidae-Blissinae have been most commonly observed on members of the PACMAD clade, less commonly on the BEP clade; Teracrini are also concentrated on Poaceae (Slater 1976).

Water often congregates in the hollow stems of bamboos, and a distinctive fauna lives there (Kitching 2000).

Floral Biology & Seed Dispersal. Poaceae are predominantly wind-pollinated and they have protandrous flowers with dangling anthers. However, insect pollination is known from some forest-dwelling grasses, especially smaller Bambusoideae (Soderstrom & Calderón 1971). Streptochaeta may also be animal pollinated, since it lacks a plumose stigma and the anthers do not dangle; the flowers are protogynous (Sajo et al. 2008). Woody bamboos are known for their synchronized flowering (see below). Lodicules, modified members of the inner tepal whorl, seem to be involved in the opening of the staminate or perfect flowers; they can be absent from carpellate flowers (see Sajo et al. 2007; Reinheimer & Kellogg 2009 for references).

The caryopsis is often described as being a distinctive fruit type of the Poaceae; it is basically a variant of an achene in which the testa and pericarp are fused. In fact, there is quite a variety of fruit types in the family when it comes to thinking about how dispersal is accomplished (e.g. Werker 1997). Dispersal is quite often by animals, and although few Poaceae have true fruits as dispersal units - an example is Alvimia (Bambusoideae) - there are other structures attracting animals such as elaiosomes (Davidse 1987), as well as hooks and spikes by which the diaspores attach to passing animals (Centotheca is a good example). A number of taxa are wind-dispersed, 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; the surface microstructure on awns - minute retrose bristles - may result in the achene becoming "planted" in the ground (Elbaum et al. 2007; Humphreys et al. 2010b) or moving along the surface of the ground (Kulić et al. 2009). This is by a ratchet principle similar to that which operates when you put an entire inflorescence of Hordeum up your sleeve; the whole inflorescence migrates up your arm and sometimes also down your back. Davidse (1987) notes a number of taxa with "creeping diaspores" which can move using this mechanism. Despite the apparent advantages of having an awn, this has been lost several times in Danthonioideae, at least, perhaps in association with the adoption of the annual habit where passive burial of seeds suffices (Humphreys et al. 2010b).

Woody bamboos are known for their tendency to dominate the vegetation and their synchronized flowering, even when transported thousands of miles from their native habitat. Plant are monocarpic; flowering may occur only every 120 years or so, and after a rather protracted period of reproduction, the plant dies. This has profound effects both on the general vegetation and all organisms dependent on bamboos for food and shelter. The fruits are used as food by humans and they also attract animals - birds, rats, etc. - in very large numbers (Janzen 1976; Judziewicz et al. 1999). This behaviour is also found in some herbaceous bamboos and, depending on relationships within Bambusoideae, may even be plesiomorphic for the subfamily - it is an extreme form of masting (see Curran & Leighton 2000 and references).

Genes & Genomes. the complex relationships within Danthonioideae may be connected with extensive reticulation there in the past (Pirie et al. 2009), as is notoriously the case in Triticeae (G. Petersen et al. 2006a; Mason-Gamer 2008; Sun & Komatsuda 2010), polyploidy and introgression further complicating the picture. For a possible relationship between genus size, life form and polyploidy, see Hilu (2007a).

Aside from fairly recent polyploidy, there has been a duplication of the whole genome in a clade that includes at least Zea, Oryza, Hordeum and Sorghum, i.e. the PACMAD/BEP clade, and this duplication has been dated to ca 70/70-66/70-50/73-56/50-40 million years before present (Paterson et al. 2004; X. Wang et al. 2005; Schlueter et al. 2004; The International Brachypodium Initiative 2010; Goff et al. 2002). Soltis et al. (2009) suggest that diversification in Poaceae may be connected with this genome duplication, and the development of a cytosolic ADPglucose phosphorylase, perhaps unique to this clade, has been associated with this duplication (Comparot-Moss & Denyer 2009). Diversification of the groups including the cereals may have occurred ca 20 million years later (Paterson et al. 2004, but cf. The International Brachypodium Initiative 2010). 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). Alpha prolamin genes, involved in the synthesis of seed storage proteins, evolved in Panicoideae after they split from other subfamilies (or perhaps in the BEP clade: Xu & Messing 2008). There has been very extensive duplication of genes - API, AG and SEP families - but not in genes of the AP3 lineage (Zahn et al. 2005a; see also Saski et al. 2007 for other duplications in the family). In general, developmental gene duplication and subsequent functional divergence seem to have played a very important role in allowing the development of the baroque diversity of inflorescences in the family (Malcomber et al. 2006; Zanis 2007).

Salse et al. (2008, 2009a, b) and Abrouk et al. (2010) discuss genome evolution in the family, suggesting that the base chromosome number (x) is 5, but in the [PACMAD + BEP] clade at least x increased to 12 after a genome duplication (to x = 10) and two interchromosomal translocations and fusions (to x = 12). n = 12 is still found in rice (Oryza), for example, while x = 10 in Panicoideae. However, Hilu (2004) 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). 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). Within Poöideae there seems to have been independent reduction in chromosome number from n = 12 (The International Brachypodium Initiative 2010). Overall, there has been very substantial evolution in the genome of grasses, with genome evolution in Triticeae (Poöideae) being particularly accelerated (Luo et al. 2009; see also Messing & Bennetzen 2008; Salse et al. 2009a) - many Triticeae have massive genomes in part because of changes in base chromosome number (Jakob et al. 2004). Indeed, comparisons of expressed sequence tags and general genomes suggest that the genomes of Poaceae are much more different from the genome of Allium (Alliaceae, Asparagales) than is the genome of Arabidopsis (Brassicaceae, Brassicales, rosid II) from that of Allium (Kuhl et al. 2004). There has also been substantial evolution in the chloroplast genome (Guisinger et al. 2010 for literature), although details on where on the tree (and so when) particular changes occurred await more extensive sampling of the chloroplast genome in Poales and even "basal" Poaceae, and the rate of this plastid evolution may have since slowed down; these rate changes are placed at the level of Poaceae as a whole, although they might more correctly be put at the PACMAD/BEP node...

Economic Importance. Wheat (mostly Triticum aestivum - Poöideae), which provides one fifth of the calories eaten by humans, began to be domesticated ca 10,000 years ago; see Israel Journal of Plant Sciences 55(3-4). 2007, for an entry into the literature on domestication, also Fuller (2007), Baum et al. (2009: haploid genomes) and Carver (2009: general). Most domesticated forms are polyploid, and genome plasticity in connection with this polyploidy has been implicated of the success of the crop in cultivation (Dubcovsky & Dvorak 2007). For the domestication of barley (Hordeum vulgare), see Fuller (2007), Pourkheirrandish and Komatsuda (2007) and Azhaguvel and Komatsuda (2007). Sorghum and Zea (Panicoideae) and Oryza (Ehrhartoideae) are three other important 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 before present (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 a phylogeny of Oryzeae, see Guo and Ge (2005), and for information on the complex history of domestication of rice (Oryza spp.) - which occurred in two places, at least - see Sweeney and McCouch (2007) and Fuller (2007). For the domestication of pearl millet (Pennisetum glaucum), see Fuller (2007), and for that of sorghum (Sorghum spp.), see Dillon et al. (2007). Sang (2008) notes 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. 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). Glémin and Bataillon (2009) take a comparative viewpoint and look at how grasses in general have evolved under domestication.

Chemistry, Morphology, etc. Because of their great economic importance, many aspects of grass morphology, anatomy, cytology, etc., have been surveyed over the years, and recent phylogenetic work is clarifying patterns of variation of these characters and suggesting additional sampling. Niot all these really useful surveys are cited below, although all are easily trackable in the literature.

The primary cell wall hemicellulose and pectin polysaccharides of grasses are very different from that 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. There is evidence that ADP-glucose pyrophosphorylase, which is 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, and in plastids elsewhere in starch-storing organs of other seed plants, probably 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 is asymmetric (Pooideae) 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 eamined (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 (Amarasinghe & Watson 1988, 1990; Liu et al. 2010). Ligule variation is also extensive: Anomochlooideae are sometimes described as lacking a ligule (Judziewicz & Clark 2008, which see for other distinctive characters), or the ligule is described as being represented by a ring of hairs... The leaf blades of Neurolepis (Bambusoideae) may be up to 4 m long.

The style is hollow in Pharus. In addition, the anther wall consists solely of epidermis and endothecium (i.e. it is of the Reduced type), the latter degenerating before anthesis (Sajo et al. 2007). All in all, Pharus has numerous distinctive features that need to be integrated with the phylogenetic tree; see also Judziewicz and Clark (2008).

A common interpretation of the grass palea, which is often bicarinate, has been that it is prophyllar/bracteolar in nature, monocots commonly having bicarinate prophylls. However, in this scenario bracteoles would probably have to be regained, since the immediate outgroups to Poaceae lack them. For suggestions, based on early studies of gene expression, that the palea and perhaps even lemma are calycine in nature and the lodicules are corolline, see Ambrose et al. (2000); A-type genes are expressed in both the palea and lemma (Whipple & Schmidt 2006). General comparative morphology might suggest that the lemma is a bract and the palea represents two connate tepals of the outer whorl; if the lemma is a perianth member, then loss of bracts will be an apomorphy for all or most of Poaceae. The flowers of Streptochaeta can be interpreted as having an outer perianth whorl of two (adaxial) members that ultimately become the single, bicarinate palea (there are sometimes three members in this outer whorl), and an inner perianth whorl of three members that ultimately become the lodicules. The three stamens common in grass flowers would then be those opposite the three members of the outer perianth whorl (see Whipple & Schmidt 2006; Preston et al. 2009, and Reinheimer & Kellogg 2009 for further details). Given the sister-group relationships between Ecdeicoleaceae and Joinvilleaceae recently found by Marchant and Briggs (2006) and the likelihood that the flowers of Anomochloa are sui generis, the floral morphology of Streptochaeta may be plesiomorphic in the family, or represent an apomorphy for that genus. Recently Sajo et al. (2008) suggested that the flowers of Streptochaeta could be interpreted in more or less conventional terms, with a whorl of three rather coriaceous "bracts" being equivalent to lodicules and two adaxial "bracts" outside this perhaps representing the palea (although the structure interpreted as being a lemma was also adaxial...); Sajo et al. (2011) interpreted the flowers of Anomochloa as having glumes, palea, and lemma (bracteoles, prophylls respctively). Interestingly, the flowers of Ecdeicolea are also notably monosymmetric, with the two adaxial tepals of the outer whorl larger and keeled, and although this is not directly relevant, comparable differentiation in the outer perianth whorl occurs in Xyridaceae (q.v.); these are all likely to be parallelisms. The tepaloid nature of the lodicules is relatively uncontroversial (see Sajo et al. 2007; Reinheimer & Kellogg 2009 for references). For a summary of floral development in grasses, see Ciaffi et al. (2011).

It is difficult to interpret the arrangement of the pollen grains in the small anthers of Streptochaeta; they may be peripheral, at least initially (Kirpes et al. 1996; Sajo et al. 2009). Some grasses have pendulous, atropous ovules; although both crassi- and tenuinucellate ovules are reported for grasses, Rudall et al. (2005a) suggest that the reports of the former (e.g. Guignard 1882) need confirmation - parietal tissue is likely to be absent. When there are three carpels, the abaxial member is fertile (Kircher 1986). The caryopsis is often described as being a distinctive fruit type of the Poaceae; in a caryopsis, the seed coat and pericarp are fused, so it is basically a variant of an achene. Guérin (1899) suggests that the persistent part of the seed coat is tegmic, and he sometimes showed the exotegmen in particular with quite large cells, or with quite thick walls, during development. Poaceae are noted for their well developed, lateral embryo with a scutellum - this latter is nothing more than a distinctively-shaped haustorial part of the cotyledon that is common in other monocots (= the haustorial cotyledonary hyperphyll if one wants to be technical - see Tillich 2007 for the grass embryo).

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 Andropogonoideae (Diao et al. 2006). For the Hm1 resistance gene, see Sindhu et al. (2008), and for the complex evolution of the Rp1 disease resistance gene family, see Luo et al. (2010).

Additional information is taken from Judziewicz and Soderstrom (1989) and the Grass Phylogeny Working Group (2001; a few small taxa remain unplaced in subfamilies there). For embryo variation, see Reeder (1957), 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 and their distribution, see Piperno and Pearsall (1998), Piperno and Sues (2005) and Piperno (2006). For the occurrence of ergot alkaloids, see Gröger and Floss (1998), for inflorescence morphology and development, see Malcomber et al. (2006), Reinheimer et al. (2008: Paniceae), and Thompson and Hake (2009), for floral/spikelet evolution, see Whippple and Schmidt (2006), Yuan et al. (2009) and Thompson et al. (2009), for cell wall composition; see Fincher (2009), for aerial branching, Malahy and Doust (2009), for aspects of inflorescence morphology, Perreta et al. (2009), 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), and for the morphology of starch grains in the endosperm, see Shapter et al. (2008). See Bell and Bryan (2008) for a good general treatment of grass morphology, and for a summary of grass systematics, see Hilu (2007b). Arber (1934) remains the classic account of the family. There is also a useful general bibliography on Poaceae, while Chase (1964) provides a introduction to the family.

For general information on Bambusoideae, see Clark (1997), Judziewicz et al. (1999), and Judziewicz and Clark (2008), for foliar epidermis, see Yang et al. (2008a). For pollen in Chloridoideae, see Liu et al. (2004: not much variation).

Phylogeny. For overviews of the family phylogeny, see Soreng and Davis (1998), Kellogg (2000a) and the Grass Phylogeny Working Group (2001, 2011). Duvall et al. (2010) provide a preliminary tree based on whole chloroplast genomes. In a multi-gene study, Bouchenak-Khelladi et al. (2008) clarified relationships in the core Poales, while at the same time questioning others. Thus they did not find strong evidence for the monophyly of Anomochlooideae, Streptochaeta possibly being sister to all other Poaceae; Micrairoideae might not be monophyletic, Isachne not having a fixed position; there was support for a sister relationship between Danthonioideae and Chloridoideae (see also Pirie et al. 2008); and Streptogyna may 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). Relationships of the major clades within the PACCMAD (as it used to be called) and BEP clades were initially for the most part unclear. Thus the position of Poöideae (Hodkinson et al. 2007, and references; Duvall et al. 2008a) and Ehrhartoideae (Cahoon et al. 2010, as Oryzoideae) are not clear in some analyses (see also Saarela & Graham 2010; cf. Davis & Soreng 2008; Christin et al. 2008: BEP clade paraphyletic and immediately basal to the PACCMAD clade). Relationships in the PACCMAD clade appeared to remain particularly difficult (Saarela & Graham 2010, but sampling). However, more recently the Grass Phylogeny Working Group II (2011) have found strong support for many of the relationships in the PACMAD (as it is now called) and BEP clades, although support for the first two branches in the PACMAD clade is still only weak.

Duvall et al. (2007) had found strong support for the BEP clade, albeit the taxon sampling was slight, while Ehrhartoideae and Poöideae had weak to moderate support as sister taxa (Bambusoideae not included: Saski et al. 2007: see also grass Phylogeny Working Group 2001). Where exactly Streptogyneae wre to be placed, whether in Bambusoideae, Ehrhartoideae, or in a separate subfamily, was unclear (Hisamoto et al. 2008), as were relationships between the three subfamilies. Thus Peng et al. (2010: 43 genes, only 10 taxa) had found strong support for the relationships [E [B + P]] (ML and Bayesian) and even stronger support for the relationships [B [E + P]] (neighbour joining, but the analyses of Wu and Ge (2012: 76 genes, 222 taxa; see also Bouchenak-Khelladi et al. 2008) supported the former set of relationships, and these are followed here.

For a discussion of the relationships - close, and perhaps even entwined - between Panicoideae and Centothecoideae, see Duvall et al. (2008a) and especially Sánchez-Ken and Clark (2008); recent work suggests that the two should be combined (Sánchez-Ken & Clark 2010). Panicoideae have been much studied because of the important crops they contain, e.g. see Giussani et al. (2001). For relationships in the Paniceae, see Zuloaga et al. (2000), Gómez-Martínez and Culham (2000) and Morrone et al. (2010), for the bristle clade of Paniceae, see Doust et al. (2007), and those within Panicum itself, see Aliscioni et al. (2003) and Sede et al. (2008), within Pennisetum, in which Cenchrus is embedded, see Donadío et al. (2009) and Chemisquy et al. (2010), and within Setaria, see Kellogg et al. (2009); see also Sede et al. (2009a) for two new genera. Salariato et al. (2010) examined relationships within Melinidae, particularly fromn the point of view of inflorescence evolution. Ng'uni et al. (2010) looked at relationships with Sorghum. For general information on Paniceae, see Crins (1991), for unisexuality, see Le Roux and Kellogg (1999), for inflorescence evolution, see Doust and Kellogg (2002) and Reinheimer and Vegetti (2008), and for the evolution of the NADP-malate dehydrogenase gene following its duplication, see Rondeau et al. (2005). For the phylogeny of Andropogoneae, see Kellogg (2000c) and Mathews et al. (2002), and for that of Paspalum, basically monophyletic, see Rua et al. (2010). Finally, for more information on relationships within Panicoideae, including those of some of its constituent genera, see papers in Aliso 23: 503-562. 2008.

Relationships within Chloridoideae are something like [Centropodieae [[Triraphidae - Neyraudia (panicoid microhairs) + Triraphis] [Eragrostideae [Zoysieae + Cynodonteae (the bulk of the group)]]]] (Peterson et al. 2009); Peterson et al. (2010a, 2011) provide a detailed phylogeny of the clade. Eragrostis and Sporobolus may be polyphyletic, while Muhlenbergia is paraphyletic, including a number of well supported (and with morphology, too) clades (Peterson et al. 2010b; Columbus et al. 2010). For a morphological phylogenetic analysis of the subfamily, see Liu et al. (2005), for other relationships, see papers in Aliso 23: 565-614. 2008.

For a phylogeny of the Pentaschistis group (Danthonioideae), also character evolution there, see Galley & Linder (2007), for relationships in the subfamily as a whole, see Barker et al. (2007a) and Pirie et al. (2008). Some relationships within Danthonioideae are reticulating (Pirie et al. 2009).

Cerros-Tlatilpa et al. (2011) has clarified the phylogeny of Danthonioideae.

Zhang and Clark (2000) clarified relationships of Bambusoideae, restricting the limits of the subfamily to that now generally accepted; most of the basal grade of Poaceae had been included in bamboos at one time or another. Clark and Triplett (2006) discussed relationships within the subfamily, previously divided into the woody Bambuseae and the herbaceous Olyreae. However, the woody temperate bamboo group may be sister to the rest of the family; the monotypic Buergersiochloa, from New Guinea, is a member of the monophyletic and otherwise entirely New World woody bamboo group, and the Olyreae are derived (e.g. Bouchenak-Khelladi 2008). Sungkaew et al. (2009; five plastid genes) retreived the relationships [Arundinarieae [Olyreae [Neotropical (strictly) Bambuseae + Paleotropical & Austral Bambuseae]]] - and map the distributions of each of these groups. For a phylogeny of the woody bamboos, but with rather little resolution, see Clark et al. (2008), of neotropical woody bamboos, see Clark et al. (2008) and Fisher et al. (2009), of palaeotropical woody bamboos, see Yang et al. (2008b: resolution o.k., baccate fruit arose in parallel), of Bambusa and its relatives, see Yang et al. (2010) and Goh et al. (2010), of dendrocalamua, see Sungkaew et al. (2010), of temperate bamboos, see Peng et al. (2008), of Arundinarieae, see Zang et al. (2010: again rather little resolution despite ca 9,000 bp sequences), and of Bambuseae - Arthrostylidiinae, see Tyrell et al. (2009).

Within Ehrhartoideae, the relationships of Oryzeae have been much studied (Guo & Ge 2005; L. Tang et al. 2010 and references); for diversification within Oryza, see Zou et al. (2008). The first seedling leaf of Oryzeae does not have a lamina.

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 of (many) Poöideae. One of the gene copies breaks down starch into fermentable sugars in the endosperm, while the other is more broadly expressed in the plant, as it is in other Poaceae (Mason-Gamer 2005). For the expansion of the inverted repeat in Poöideae at the SSC/IRa boundary, see Saski et al. (2007). Soreng and Davis (2000) outlined relationships in Poöideae. Within Poöideae, a number of taxa show complex reticulating patterns of relationships; for those in Triticeae in particular, see G. Petersen et al. (2006a) and Mason-Gamer (2008) and references. For relationships and morphology in Phaenospermateae (inc. Duthieae), see Schneider et al. (2011); Phaenosperma itself is a very distinct grass previously included in Bambusoideae. For a phylogeny of Poeae, which should now include Aveneae, see Grebenstein et al. (1998), Quintinar et al. (2007, also Döring et al. 2007; Soreng et al. 2007; Saarela et al. 2010, 2011; Gillespie & Soreng 2011), for that of Poa, see Gillespie and Soreng (2005), Gillespie et al. (2009) and Soreng et al. (2010, 2011). See also Gillespie et al. (2008, 2010) for relationships in Poinae, Quintanar et al. (2010) for Koeleriinae, Essi et al. (2008) for relationships around Briza, and Consaul et al. (2010) for polyploid speciation in Puccinellia. For a phylogeny of Stipeae in which Macrochloa may be sister to the rest of the tribe and there are later parallel diversifications in the Old and New Worlds - characters traditonally thought to be phylogenetically important appear not to be so - see Romaschenko et al. (2007, esp. 2008, 2009, 2010, 2011; Jacobs et al. 2008; Barkworth et al. 2008), for New World Stipeae, see Ciadella et al. (2010: but sampling). Winterfeld (2006) discussed cytogenetic evolution, mainly in the old Aveneae. Inda et al. (2008a) discuss the biogeography of Loliinae, which seems to have involved multiple dispersal events from a centre in the Mediterranean region over the last ca 13 million years. There are several papers on Poooideae in Aliso 23: 335-471. 2008. which should also be consulted, and see Schneider et al. (2009) for relationships within the whole subfamily.

Classification. For the basic classification of the family, see the Grass Phylogeny Working Group (2001, 2011); there may be further change in detail, but the main outline now seems clear. For a provisional checklist of the family, see World Checklist of Monocots; Grassworld, moderated by B. K. Simon, has just started up; Watson and Dallwitz (1992b onwards) includes generic treatments, etc.

Peterson et al. (2010) provide a detailed suprageneric classification of Chloridoideae (see also Columbus et al. 2010 for Muhlenbergia), while Sánchez-Ken and Clark (2010) outline a tribal classification for a Panicoideae in the broad sense that now include Centothecoideae. Setaria (Panicoideae) will have to be dismembered (Kellogg et al. 2009), Panicum itself is getting pulverized, perhaps overly much so, (e.g. Sede et al. 2008, 2009b; Zuloaga et al. 2010); Panicum s.l. has about 500 species, s. str. ca 100 species, while Dicanthelium has about 55 species - see e.g. Zuloaga et al. (2007). Cenchrus is to include Pennisetum (Chemisquy et al. 2010) and Muhlenbergia is also to be slightly expanded (Peterson et al. 2010b). 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 generic delimitation in the temperate bamboos, see Peng et al. (2008), in the palaeotropical woody bamboos, see Yang et al. (2008b) and in Bambusa and its relatives, see Yang et al. (2010). There are also generic problems in Bambusoideae-Arundinarieae (Zeng et al. 2010) and -Bambuseae-Arthrostylidiinae (Tyrell et al. 2009); Chusquea must include Neurolepis (Fisher et al. 2009). Schneider et al. (2009) ouline tribal limits within Poöideae. For generic limits around Piptatherum, see Romaschenko et al. (2011). For a catalogue of New World Poöideae, see Soreng et al. (2003). Hybridisation, introgression, and polyploidy are rife in Poöideae-Triticeae (e.g. G. Petersen et al. 2006a; Mason-Gamer 2008), which include a number of important grain genera such as Triticum, Hordeum, etc. Genera are certainly not monophyletic here, but are based on different genome combinations that are (hopefully) correlated with morphological variation (Dewey 1984; Löve 1984); Barkworth (2000) summmarises the history of the classification of this group (see also Goncharov 2011 for taxonomic confusion in Triticum).

Apparently the earliest name for Chloridoideae is Chondrosoideae Link, which is a sort of resurrection name - Googling it (as of 3.vii.2007) returned only Thorne and Reveal (2007), apparently the only people to have used it for some time, and about 42,100 returns for Chloridoideae. Two cheers for priority!

Botanical Trivia. A typical sheep consumes more than 10kg of silica phytoliths per year (Baker et al. 1959) - and current work suggests that this may affect its teeth very little (Sanson et al. 2007).

Woody bamboos, for example Chusquea, may have a hundred or so branches at a node, produced by a combination of multiple buds and axillary shoots with very short internodes, all nodes producing branches (see e.g. Judziewicz et al. 1999).

Thanks. I am very grateful to E. A. Kellogg for discussions about the evolution of this family.

Unassigned Synonymy: Asperellaceae Link, Coeleanthaceae Pfeiffer, Echinariaceae Link, Ophiuraceae Link