Poaceae (Angiosperm Phylogeny)

Extracted from Angiosperm Phylogeny Website - Version xx   Date

http://www.mobot.org/mobot/research/apweb/welcome.html

By P.F. Stevens and E.A. Kellogg

    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,
    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. 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 now species-poor clades, as well as the stem PACCMAD
clade, may have diverged by the end of the Cretaceous (Bouchenak-Khelladi et al.
2010c - but Puelioideae not included).

However, Poinar (2004) proposed that Programinis
burmitis, fossil in the Early Cretaceous of Myanmar some 100-110 million
years before present, was an early bambusoid grass type. Although it has some
vegetative features that are common in Poaceae, it does not have distinctive
features of the family and so is unlikely to be included here (Caroline
Stömberg, pers. comm.; Smith et al. 2010). 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 by the discovery of
well-preserved phytoliths of types to be found in the PACCMAD 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: there are grass pollen and
macrofossils also known from this age), and this would date the origination of
the clade to some 85-80 million years ago. This record, too, 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. 1993). The bottom line is that
dates from these different lines of evidence are apparently irreconcilably in
conflict (Vicentini et al. 2008).

As to more conventional grasses (the [PACCMAD +
BEP] clade), fossil spikelets assignable to them 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 about 55-35
million years ago and the PACCMAD clade rather later some 45-37 million years
ago (see Bouchenak-Khelladi et al. 2010a for other dates; Bouchenak-Khelladi et
al. 2010c suggest (55-)52(-50) and (34-)28(-22) million years respectively).
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.

The Poaceae group of families has been described as
being notably speciose (Magallón & Sanderson 2001), but there is
considerable asymmetry in family size within this clade, with most
species belonging to Poaceae themselves. The second most species-rich family
(Restionaceae) has only some 520 species. Poaceae themselves may be seven times
more speciose than its animal-pollinated sister clade (Kay & Sargent 2009).
But again, even within Poaceae there are three species-poor clades that are
successively immediately sister below the PACCMAD and BEP clades (there are two
more such clades successively sister below the family), so calling the whole
family speciose is an overstatement. If there is a focus on diversification,
this may have occurred within the PACCMAD and BEP clades (see also Linder &
Rudall 2005; Smith et al. 2011; and especially Bouchenak-Khelladi et al. 2010c
for diversification). Such statements 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).

Much has been written on the evolution of
C4 photosynthesis in grasses, e.g. see Kellogg (1999), Giussani et
al. (2001: Paniceae), etc. 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, for a
total of perhaps ca 18 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). 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).
Furthermore, taxa like Miscanthus x giganteus carry out this kind of
photosynthesis under decidedly cooler conditions than is common (Wang et al.
2008). 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; Ingram et al. 2011b for a reversal that wasn't).
Indeed, the level of parallelisms here may be at the amino acid, 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 parallelisms
between grasses and Capparidaceae). 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., and 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.).

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), while 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). 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 probably somewhat under 4,600 species are grasses (Sage et
al. 1999).

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. However, why C4 grasses spread in the way they did is still
not well understood. 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 additional factors that would lead to the increased
occurrence of fires, which would have removed trees - and also nitrogen by
volatilizing it - from some habitats and hence favoured grasses, 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 more susceptibe to fire
(Wedin 1995). Grasses also have dense root masses that would make the
establishment of woody vegetation in grassland difficult. Interestingly, both
origins of and reversals from C4 photosynthesis may be clustered
(Vicentini et al. 2008, for reversals from C4, see also Ibrahim et
al. 2009).

Which of the various factors favoured the initial
expansion of grasslands, and what might cause clustering of origins and losses
of different photosynthetic mechanisms, and which favoured the great spread and
expansion to dominance of late Miocene C4 grasslands, is 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. 1989
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). Recent work suggests that many C4
origins are correlated with a reduction in annual rainfall - indeed, grasslands
transpire less than the woodlands they seem iniitially to have replaced
(Retallack 2001), and 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). 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).

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 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).

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). 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 Oligocene to early Miocene 7-11 million years later (Strömberg 2005),
although grasslands of the Great Plains may be late Oligocene ca 24 millions
year in age and Argentinian grasslands older (Edwards et al. 2010). Some
C4 grasses may have originated in the Oligocene ca 33 million years
ago, but they became diverse - and made a corresponding major contribution to
overall vegetation biomass - only in the late Miocene-early Pliocene 9-8 million
years ago, the process being complete as recently as 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).
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); grasslands seem to have expanded at the expense of woodlands
(Retallack 2001), although 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. What makes grasslands still
more distinctive ecologically is not just the habit of grasses, 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).

A perhaps ecologically related feature of a number
of grasses scattered in different subfamilies is their accumulation of 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, as well as being allelopathic (Frey et al. 1997,
2009); they are very uncommon in other angiosperms (Schullehner et al. 2008).
Sindhu et al. (2008) note that the PACCMAD clade are characterized by a gene
that protects the plant against attack by the the ascomycete Cochliobolus
carbonorum. Finally, leaves of pooid monocots (presumably including sedges)
decompose more slowly than do those of other angiosperms (Cornwell et al. 2008).

There are additional eco-physiological factors to
bear in mind. The dumb-bell shaped stomata of grasses show remarably 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 occut
in other Poales, but are rare in broad-leaved angiosperms. Interestingly,
C4 grasses have roots with long root hairs yet may respond positively
in terms of phosphorus uptake when forming endomycorrhizal associations - long
root hairs and endomycorrhizal associations tend to be thought of as alternative
ways of securing phosphorus supply, etc. (Schweiger et al. 1995 and references).
Finally, it may be worth mentioning that Poaceae, apparently alone in flowering
plants (Römheld 1987), acquire iron through chelation of ferric ions with
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......

There was a Miocene radiation of grazing mammals
(Thomasson & Voorhies 1990) that may be associated with the spread of such
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 to deal
with the wear caused by eating the abrasive grasses (but see below - Sanson
& Heraud 2010); the persistent dead leaves of most grasses may have
decreased their palatability (Antonelli et al. 2010). 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). However, 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 dominated (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. In New Zealand, lacking mammalian herbivores,
Danthonioideae in particular may have tended to become deciduous, increasing
their productivity (Antonelli et al. 2010). 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 seems to me likley that the two are
linked (see also Retallack 2001 for a good summary).

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 can be placed in
ascomycetes-Clavicipitaceae-Balansiae (Clay 1986). 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 its phylogeny and evolution
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 forms, see Rodgers et al. (2009). 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 in fact synthesized by the fungal member of
this association, which could be ca 40 million years old (Schardl et al. 2004).
These loliine alkaloids are primarily active against insects (Schardl et al.
2007; Zhang et al. 2009), and so the presence of endophytes affects 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,
infestation by nematodes, 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; Schardl 2010). Furthermore, the larvae of Phorbia (or
Botanophila) flies live on Epichloë stroma, and the adults
transmit the 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).

Large numbers 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 fungi (Herrera et al. 2009), perhaps aiding in their dispersal.

Bacteria may be endophytes too, 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).

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 Morphini, are common (over
10% of the records); the satyrine group as a whole diverged from other
Nymphalidae some 85 million years ago (Wahlberg et al. 2009), Satyrini
themselves diverging from the rest of the group about 65-55 million years ago
(Peña & Wahlberg 2008; Wahlberg et al. 2009 - age depends on calibration
points used, the position of Satyrini within the satyrine clade differs
greatly). Indeed, larvae of Satyrinae-Satyrini, with some 2,200 species, the
bulk of the clade, almost exclusively eat grasses, and the main lineages within
Satyrini diversified well after the initial divergence of Satyrini and only some
36–23 Myr ago - an age perhaps contemporaneous with the spread of grasses (see
above: Peña et al. 2006; Peña & Wahlberg 2008, dates from a tree where
Satyrini diverge ca 55 million years ago and are not sister to all other
Satyrinae). Galling diptera, especially Cecidomyiidae, are quite common here
(Labandeira 2005); 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 gall formers 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 PACCMAD clade, less commonly
on the BEP clade; Teracrini are also concentrated on Poaceae (Slater 1976). 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).

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).

Poaceae are of course predominantly wind-pollinated
with dangling anthers and protandrous flowers. 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 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. Flowering may occur only every 120
years or so, and after a rather protracted period of reproduction, the plant
dies. 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.
Water often congregates in the hollow stems of bamboos, and a distinctive fauna
lives there (Kitching 2000). Many bamboos are monocarpic - that is, the plants
dies after flowering - and this has profound effects both on the general
vegetation and all organisms dependent on them.

Relationships within Danthonioideae are complex,
and there seems to have been much reticulation 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.

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 clade, and this duplication has been dated to
70-50/73-56 million years before present (Schlueter et al. 2004; The
International Brachypodium Initiative 2010). Soltis et al. (2009) suggest that
diversification in Poaceae may be connected with this genome duplication. It has
been suggested that diversification of the groups including the cereals 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). 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).
Indeed, 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).

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 [PACCMAD + 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 plastid
evolution may have since slowed down; these changes are placed at the level of
Poaceae as a whole, althougfh they might more correctly go at the PACCMAD/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. 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); 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.

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 it. 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...). 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).

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 need confirmation. 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 - here the testa and pericarp
are fused, basically a variant of an achene. Poaceae are noted for their well
developed, lateral embryo with a scutellum - 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).

Some information is taken from Judziewicz and
Soderstrom (1989) and in particular from 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 the series of
inversions in the single copy region and expansion of the inverted repeats of
the chloroplast genome, see Hiratsuka et al. (1989), for C4
photosynthesis, see also Kellogg (1999), for accD gene loss, see Katayama
and Ogihara (1996), for phytoliths and their distribution, see Piperno and
Pearsall (1998), Piperno and Sues (2005) and Piperno (2006), for deletions,
etc., in the 3' end of the mat K gene, see Hilu & Alice (1999), for
loss of introns in chloroplast genome, see Daniell et al. (2008) for references,
and for a summary of genome evolution in the family, see Bennetzen (2007). For
the occurrence of ergot alkaloids, see Gröger and Floss (1998), for the
relationship between genus size, life form and polyploidy, see Hilu (2007a), for
inflorescence development, see Malcomber et al. (2006) and Reinheimer et al.
(2008: Paniceae), 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, see Malahy and Doust
(2009), for aspects of inflorescence morphology, see Perreta et al. (2009), and
for endosperm development, see Sabelli and Larkins (2009). Leseberg and Duvall
(2009) look at plastome-level variation in Poaceae, and Morris and Duvall (2010)
discuss aspects of chloroplast genome evolutiom, focusing on Anomochloa.
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) is a classic 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, see
Soreng and Davis (1998), Kellogg (2000a) and the Grass Phylogeny Working Group
(2001); the first in particular show how difficult it is to be sure of the
position on the tree of many of the characters mentioned above. Duvall et al.
(2010) provide a preliminary tree based on whole chloroplast genomes.
Relationships of the major clades within the PACCMAD and BEP clades are for the
most part unclear, indeed, the position of Poöideae (Hodkinson et al. 2007, and
references; Duvall et al. 2008a) and Ehrhartoideae (Cahoon et al. 2010, as
Oryzoideae) are also not clear in some analyses, however, Duvall et al. (2007)
found strong support for the BEP clade, albeit the taxon sampling was slight
(see also Saarela & Graham 2010; cf. Davis & Soreng 2008; Christin et
al. 2008: BEP clade paraphyletic and immediately basal to the PACCMAD clade).
Ehrhartoideae and Poöideae have weak to moderate support as sister taxa
(Bambusoideae not included: Saski et al. 2007: see also grass Phylogeny Working
Group 2001). Where exactly Streptogyneae are to be placed, whether in
Bambusoideae, Ehrhartoideae, or in a separate subfamily, is unclear (Hisamoto et
al. 2008). In a multi-gene study, Bouchenak-Khelladi et al. (2008) clarified
further relationships in the core Poales, while at the same time questioning
others. Thus Bouchenak-Khelladi et al. (2008) did not find strong evidence for
the monophyly of Anomochlooideae, Streptochaeta possibly being sister to
all other Poaceae; Micrairoideae may 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). The
relationships obtained by Bouchenak-Khelladi et al. (2009) are largely those in
the account above. However, relationships in the PACCMAD clade are particularly
difficult (Saarela & Graham 2010, but sampling).

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 ]] (Peterson et al. 2009);
Peterson et al. (2010a) 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).

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 copies of the gene 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
Quintinar et al. (2007, also Döring et al. 2007; Soreng et al. 2007; Saarela et
al. 2010), for that of Poa, see Gillespie and Soreng (2005), Gillespie et
al. (2009) and Soreng et al. (2010). 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 importamnt appear not to be so - see Romaschenko
et al. (2007, esp. 2008, 2009, 2010; 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), although there has
been considerable recent change in detail. See also the World
Checklist of Monocots for a checklist of grasses; 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 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.

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. 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).

CLASSIFICATION  (APG)

POACEAE Barnhart, nom. cons.//GRAMINEAE
Jussieu, nom. cons. et nom. alt.

(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 cellsconical
to dome-shaped; microhairs bicellular; leaves pseudopetiolate,
supervolute(-plicate), midrib +; two adaxial outer T 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]; ovule single, central, amphitropous or hemianatropous,
crassinucellate, [funicle short], micropyle
endostomal; supernumerary antipodals +; fruit an
achene, the testa closely adherent to pericarp [= caryopsis], hilum long
[reverses]; peripheral layer of endosperm meristematic, embryo lateral,
long, well differentiated,
plumule lateral; 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, intragenomic translocation of chloroplast rpl23 gene.

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 / 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 ]] / 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 ]: (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]: ?

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.

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.

1. Brachyelytreae Ohwi

Stomata subsidiary cells
with parallel sides; n = 11.

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

[Nardeae [Phaenospermateae + The Rest]]: primary inflorescence branches
2-ranked; embryo lacking scutellar cleft, embryonic leaf margins
non-overlapping.

2. Nardeae Koch

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

2/2. Europe.

Synonymy: Nardaceae Martynov

[Phaenospermateae + The Rest]: microhairs 0 (+ - some Stipeae); (stomata
subsidiary cells with parallel sides); n = 7 [chromosomes "large"].

3. Phaenospermateae

21 bp insertion in in
rpl32-trnL; n = 7, 12.

7/11. Central to East Asia, also Australia, Mexico, Balkans, Caucasus;
scatttered.

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

Extracted from Angiosperm Phylogeny Website Version 13, Sep 2013

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

(Aerial branching + [?level]); vesicular-arbuscular mycorrhizae +; 3 desoxyanthocyanins, flavone 5- and C-glycosides, tricin, flavonoid sulphates, (cyanogenic glycosides) +; primary cell wall rich in arabinoxylans, pectin 10³%, xyloglucans lacking fucose; sieve tube plastids also with rod-shaped protein bodies, P-proteins 0; arm and fusoid cells +; cuticle waxes as aggregated rodlets; stomatal subsidiary cells conical to dome-shaped; microhairs bicellular; leaves pseudopetiolate, ligulate, (ligule ± fringed with hairs), with a broad blade, vernation supervolute(-plicate), midrib +; T with two adaxial outer members distinct, abaxial smaller; A centrifixed [?level]; pollen grains central in loculus; gynoecial rudiment annular, (G open in development), stigmas 3[?]; ovule one/flower, central, amphitropous or hemianatropous, micropyle endostomal, funicle short; seed coat closely adherent to pericarp [= caryopsis]; testa not persistent, hilum long; peripheral layer of endosperm meristematic, endosperm hard, embryo lateral, long, well differentiated, cotyledon = scutellum + coleoptile, lateral, plumule terminal, embryonic leaf margins overlapping; radicle 0, collar [epiblast, the ligule of the cotyledon] conspicuous; expansion of the inverted repeat [level?], chloroplast genome with [third!] trnT inversion in the single-copy region, only 17 introns [that in clpP absent], loss ofaccD, ycf1, ycf2 genes, x = 12 [genome duplication; duplication of AP1/FUL genes (= FUL1 and FUL2), etc.], rpoC2 gene insert, rps14 gene to nucleus, pseudogene remaining in mitochondrion, intergenomic translocation of chloroplast rpl23 gene; ADP-glucose pyrophosphorylase in cytosol.

x

707/11,337. Twelve subfamilies below. Worldwide (map: from Vester 1940; Hultén 1961). [Genera List]

Age. Crown group Poaceae are ca 83 m.y.o. (Janssen & Bremer 2004; see also Bremer 2002). Bouchenak-Khelladi et al. (2009, 2010a) suggest that crown grasses are (97-)76(-43) m.y.o.; see also below for estimates of the age of the genome duplication that characterises this clade.

However, Poinar (2004) proposed that Programinis burmitis, found fossil in deposits from the Early Cretaceous of Myanmar some 100-110 m.y.a., represented an early bambusoid grass. To others, it seemed to have some vegetative features that are common in Poaceae, but not the distinctive features of the family and so was unlikely to be included there (Smith et al. 2010). Nevertheless, in a recent more detailed analysis of P. laminatus, Poinar (2011) affirmed that the silica bodies, etc., indeed supported a placement in Poaceae, particularly in Poöideae, so suggesting an age for that subfamily about twice that of other estimates (see below). Although recent estimates of the age of these amber deposits are younger, no earlier than Early Cenomanian at (99.4-)98.8(-98.2) m.y. (Shi et al. 2012), their age is still inconsistent with nearly all estimates of the age of grasses.

The age of grasses (as well as that of other monocot groups, not to mention the animals, both vertebrates and insects, associated with them) is also called into question, although somewhat less dramatically, by the discovery of well-preserved phytoliths of types to be found in the PACMAD and BEP clades in coprolites of sauropod dinosaurs from the Late Cretaceous 67-65 m.y. of central India (Prasad et al. 2005), and this would date the origination of the PACMAD-BEP clade to some 85-80 m.y.a.; such fossils have been identified as Ehrhartoideae-Oryzeae (Prasad et al. 2011). A recent critical analysis of some ages in Poaceae comparing those obtained using or not using these fossils and comparing chloroplast and nuclear data, etc. (Christin et al. 2014), underscores the importance of confirming the identity of these fossils. Indeed, the fossil pollen genusGraminidites occurs widely (but not in Australia) in the Late Cretaceous (Srivastava 2011), even if at least locally not in association with dinosaurs. Although the enigmatic Late Cretaceous mammalian sudamericid gondwanatherians had hypsodont teeth and there is a record of a Cretaceous hadrosaurian dinosaur with carbon isotope ratios that suggests that it might have been eating C₄ plants (Prasad et al. 2005; Bocherens et al. 1994), the origin of C₄ grasses - and most other C₄ plants - is usually put in the middle of the Tertiary (see below). To summarize: Dates from different lines of evidence are apparently irreconcilably in conflict (Vicentini et al. 2008).

1. Anomochlooideae Potzdal

Silica bodies elongated transverse to the long axis of the leaf; microhairs 75-150 µm long [i.e., huge], basal cells constricted part way up; (leaves spiral - Streptochaeta); pseudopetiole with an apical (and basal) pulvinus, midrib projecting on both surfaces, (ligule 0); inflorescence (branches two-ranked? - Anomochloa), cymose, two "bracts" along each branch unit, two more "bracts" below each flower; flowers perfect, protogynous; P 2 (3) + 3; or flowers spirally arrranged along racemose axis, with several spiral "bracts" below each flower, = T, possibly 3 + 3, the latter coriaceous; A (4 - Anomochloa, 3 members of the inner whorl), centrifixed, basally connate, not dangling, anthers ± latrorse, wall with 2 persistent middle layers [Reduced type], endothecium lacking thickenings; (microsporogenesis simultaneous - Streptochaeta); style solid, stigma not plumose; nucellar cap 4-5 cells across [Anomochloa]; (testa lignified, persistent - Anomochloa); embryo small [Anomochloa], (scutellar cleft +), (epiblast +), (embryonic leaf margins not overlapping); 21bp [long] subrepeats in rpoC2 gene insert; n = 11, 18; first seedling leaf lacking blade.

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

Age. Divergence within Anomochlooideae is estimated to have occurred (86-)68(-53) m.y.a. (Bouchenak-Khelladi et al. 2010c).

Synonymy: Anomochloaceae Nakai, Streptochaetaceae Nakai

[Pharoideae [Puelioideae [PACMAD + BEP clades]]] / the spikelet clade: inflorescence without inflorescence bracts, spikelets +, laterally compressed, racemose, pedunculate, with two basal glumes [sterile bracts = spikelet bract + prophyll], flowers two-ranked, plane of symmetry of flower relative to spikelet horizontal; flower protandrous, with lemma and palea [?= bract and 2 adaxial connate outer-whorl T], lodicules 3 [= C/inner whorl T; esp. in staminate flowers], median member adaxial; 1 bp deletion in the 3' end of the mat K gene, loss of rpoC1 gene, 39bp subrepeats in rpoC2 gene insert.

Age. The spikelet clade may have originated in the Late Cretaceous (95-)74(-73) m.y.a. or (83-)67(-55) m.y. (Bouchenak-Khelladi et al. 2009, also 2010a, c.f. 2010c).

2. Pharoideae L. G. Clark & Judziewicz

Inner bundle sheath multi-layered; intercostal epidermis with files of fibres alternating with files of normal long cells; microhairs 0; leaves resupinate, lateral veins oblique; plants monoecious; inflorescence and spikelets with uncinate microhairs; spikelets 1-flowered; (lodicules 0); staminate flowers: A (4-)6, anthers basifixed, latrorse, wall with 2 persistent middle layers [Reduced type], endothecium lacking thickenings [bothPharus]; carpellate flowers: style hollow; micropyle bistomal [Pharus]; (scutellar cleft +), epiblast +; coleoptile [= sheathing base of cotyledon] with blade.

4/13. Pantropical, in forests (map: from Judziewicz 1987; Judziewicz et al. 1999). [Photo - Flower.]

Synonymy: Pharaceae Herter

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

Age. The age of this node may be (76.8-)58(-57.6) m.y.a. or ca 65 m.y.a. (Bouchenak-Khelladi et al. 2010a, c.f. 2010c).

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

Culm hollow; (minute bracts subtending inflorescence branches); spikelets with several flowers, basal flowers staminate or sterile, apical pistillate or perfect; ?lodicules; A 6, ?anther wall; (stigmas 3); embryo small, otherwise unknown; seedling leaf unknown.

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

[PACMAD + BEP clades]: fructan levels low, (benzoxazinoids, ergot alkaloids [latter synthesized by endophytes] +), lignins acylated with p-coumarates or acetate; arm cells 0, fusoid cells 0; transverse veins 0; pseudopetiole 0; flower type?; C/lodicules 2; A 3, opposite K/outer whorl of T; G 2, styles separate; antipodal cells proliferating; scutellar cleft +, epiblast +;, 15 bp insertion in ndhF gene, Helminthosporium carbonum [HC]-toxin reductase gene [Hm1 gene].

Age. Molecular evidence suggests that the [PACMAD + BEP] clade may have begun to diversify (53.8-)51.9(-49) m.y.a. (Wu & Ge 2011: 95% c.i.). Other estimates including Vicentini et al. (2008: (60-)52(-44) m.y.), Bouchenak-Khelladi et al. (2010c: (55-)52(-50) m.y.) are similar, some are a little older - Kim et al. (2009 [MAD members not included]), 67.8-50 m.y., Bouchenak-Khelladi et al. (2010a), (75-)57(-51) m.y., Naumann et al. (2013) about 47.7 or 32.3 m.y., and Z. Peng et al. (2013), 64.5-53.9 m.y., while Bell et al. (2010), at (42-)31, 28(-17) m.y., provide a rather younger age.

Fossil spikelets assignable to this clade are known from the Palaeocene-Eocene boundary, about 55 m.y. before present (Crepet & Feldman 1991).

[Aristidoideae [Panicoideae ]] / PACMAD clade: C₄ photosynthesis prevalent; (ligule of hairs); phytoliths dumb-bell shaped; lemma awned; starch grains compound; mesocotyl internode elongated, epiblast 0, embryonic leaf margins meeting; extension of ndhF gene from the short single copy region into the inverted repeat.

Age. This node may be approximately 45-37 m.y. old, rather younger than the crown-group BEP clade (see Bouchenak-Khelladi et al. 2010a); Bouchenak-Khelladi et al. (2010c) suggest an age of only (34-)28(-22) m.y..

4. Aristidoideae Caro

(Plants annual); (spikelet cylindrical), with one flower; lemma awn trifid, with basal column, or 3 (1); callus pubescent; (scutellar cleft 0); n = 11, 12; germination flap +.

3/365: Aristida (250-290), Stipagrostis (50). Warm temperate, few in Europe.

Age. Stem Aristidoideae date from (38-)29(-9) m.y.a. (sister group?, crown Aristidoideae date from (25.5-)20.3(-15.9) m.y.a. (Bouchenak-Khelladi et al. 2010a; Cerros-Tlatilpa et al. 2011).

[Panicoideae ]: 6 bp insertion in the 3' end of the mat K gene [?whole clade]

5. Panicoideae Link

(Plant annual); (culms branched); (fusoid cells +); microhairs often with slender, elongated thin-walled apical cells [panicoid type]; (mesophyll differentiated into palisade and spongy tissues), (chlorenchyma cells lobed [c.f. arm cells]); culms usually solid; (pseudopetiole +), (midrib complex); (inflorescence bracts +); spikelet 2-flowered, lower flower staminate or sterile [gynoecial cell death caused by Tasselseed2], development basipetal, rachilla 0; plane of symmetry of flower relative to spikelet vertical; ?lemma awned; (style +); (spikelet disarticulation below the glumes); hilum punctate; (epiblast 0), embryonic leaf margins overlapping; starch grains simple; 5 bp insertion in the rpl16 intron; n = (5, 7) 9 [Paniceae], 10 (11, 12, 14); (epiblast +), germination flap +; rps14 pseudogene lost.

212/3316: Paspalum (330), Cenchrus (105: inc. Pennisetum), Andropogon (100), Panicum (100), Dicanthelium (55), Eriachne (40). Tropics to temperate.

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

: ?

[Arundinoideae + Micrairoideae]: (hilum short).

6. Arundinoideae Burmeister

Microhairs with elongated, slender, thin-walled apical cells [panicoid type]; callus pubescent; (embryonic leaf margins overlapping); n = 6, 9, 12.

19/46. Temperate to tropical, hydrophytic to xerophytic.

Synonymy: Arundinaceae Döll

7. Micrairoideae Pilger

(Annual plants); culms solid or hollow; leaves (spirally arranged - Micraira); (lemma awn 0); starch grains simple, embryo small; n = 10; germination flap +; (C₄photosynthesis - Eriachneae).

9/188: Isachne (100), Eriachne (35). Tropics.

[Danthonioideae + Chloridoideae]: lemma bilobed, awned from the sinus; hilum punctate.

8. Danthonioideae Barker & Linder

(Plants annual), with C₃ photosynthetic pathway; (stomata with parallel-sided subsidiary cells)); prophylls bilobed [?distribution]; lemma awn trifid, or 3 awns; lodicules with microhairs; bases of styles well apart; embryo sac with haustorial synergid cells; n = 6, 7, 9.

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

9. Chloridoideae Beilschmied

Plants tolerate drought, high saline conditions; C₄ PCK subtype (phosphoenolpyruvate carboxykinase) + (0); microhairs with ± hemispherical and thick-walled apical cells the same thickness as the long base cell, latter with internal membranes and secretory [chloridoid type], also panicoid type; embryo with an epiblast; 4 bp insertion in the rpl16 intron; n = (6-8) 9, 10.

130/1721: Eragrostis (300), Muhlenbergia (155), Sporobolus (160), Chloris (55). Tropical to warm temperate, more or less dry environments especially in Africa and Australia.

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

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

Age. Bouchenak-Khelladi et al. (2009, 2010a, c) suggested that the BEP clade began to diversify at the end of the Palaeocene about 53 m.y.a., while Magallón et al. (2013) gave a much younger age of around 38.5 m.y.. Wu and Ge (2011) offer an age of (53.8-)51.9(-50) m.y., and Z. Peng et al (2013) an age of ca 48.6 m.y.; (16-)15, 12(-11) m.y. is the age in Wikström et al. (2001).

10. Ehrhartoideae Link

(Silica bodies elongated transverse to the long axis of the leaf); (arm cells + - Oryzeae), (fusoid cells +); (longitudinal walls of epidermal cell straight); (microhairs 0); (ligule a ring of hairs); flowers perfect or not; spikelet with two basal sterile florets, apical floret fertile; A (1-)6, style branches separate almost from the very base; n = (10, 15); (first seedling leaf lacking blade - Oryzeae), (roots at scutellar node - Ehrharta).

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

Synonymy: Ehrhartaceae Link, Oryzaceae Berchtold & J. Presl

[Bambusoideae + Poöideae]: ?

Age. Wu and Ge (2011) suggested that this node was some (51.6-)47(-40.8) m.y. old, while in Z. Peng et al (2013) the age was ca 47.8-46.9 m.y..

11. Bambusoideae Luersson

Woody; culm branched, development biphasic, lignification and branch development in 2^nd phase; fusoid cells +,arm cells +, strongly asymmetrically invaginated; microhairs with elongated, slender, thin-walled cap cells [panicoid type]; (multiple buds per node); leaves pseudopetiolate, blade deciduous, articulated, culm leaves different from the others, largely sheaths, outer ligule +; flowering synchronized, plants monocarpic; (inflorescence bracts +); lodicules 3, vascularized; A (2-)6(-140), (basally connate), (endothecial cells with ± U-shaped thickenings); (stigmas 1-3); (ovules ategmic, unitegmic); (fruit a berry); first seedling leaf without blade; much polyploidy.

116/2123. Tropical to temperate, often in forests (map: see Judziewicz et al. 1999; Sungkaew et al. 2009).

Age. Crown-group Bambusoideae diversified some (48-)29(-26) m.y.a. in the middle Oligocene (Bouchenak-Khelladi et al. (2009, 2010a, c); Wu and Ge (2011) dated the separation of Phyllostachys and Bambusa to (35.6-)22.5(-9) m.y.a..

The actual age of this clade may be more towards the upper end of the molecular estimates, since the earliest fossils ascribed to the subfamily, the small-leaved Chusquea oxyphylla, are Eocene (Frenguelli & Parodi 1941; see also L. Wang et al. 2013).

11a. Arundinarieae Ascherson & Graebner

Culms hollow, branch development basipetal; midrib complex; n = 24.

26/533: Fargesia (60), Sasa (40-60), Phyllostachys (55), Arundinaria (50). More or less temperate E. U.S.A., eastern Asia, also Africa, scattered, ± montane.

11b. Bambuseae Dumortier

Rhizomes massive; branch development acropetal or bidirectional; midrib complex; n = (10), 20, (22), 23, 24, etc. [x = 10, 12]

84-101/1470. Chusquea (200), Bambusa (120), Merostachys (50), Schizostachyum (50). Tropical to (warm) temperate.

Synonymy: Bambusaceae Berchtold & J. Presl, Parianaceae Nakai

11c. Olyreae Martinov

± Herbaceous; culm development uniphasic, branching slight; epidermal silica cells usu. with cross-shaped silica bodies in the costal zone and crenate [olyroid] silica bodies in the intercostal zone [not Buergersiochloa]; blade not articulated, culm leaves not very different from the others, outer ligule 0; flowering rarely synchronized and monocarpic; plant monoecious; spikelets unisexual, dimorphic, one-flowered, often dorsiventrally compressed, rachilla extension 0; (lodicules 0); n = 7, 9, 10, 11, (12).

21/120 Pariana (35). Central and South America and Africa, also New Guinea (Buergersiochloa).

Synonymy: Olyraceae Berchtold & J. Presl

12. Poöideae Bentham

Temperate habitats, (plants annual); Epichloë endophytes pervasive; aerial branching at most rare; fructose oligosaccharides in stem; root epidermal cell division forming trichoblast/atrichoblast pair asymmetric; longitudinal walls of epidermal cells straight [?level]; culms hollow; lemma usually with 5 nerves, (awned); lodicules at most slightly vascularized; style branches separate almost from the very base; (postament +); (endosperm with some non-starch soluble storage polysaccharides); embryo small; n = (2, 4-13); duplication of the ß-amylase gene.

177/3850. Largely North Temperate.

12A. Brachyelytreae Ohwi

Stomata subsidiary cells with parallel sides; n = 11.

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

[Nardeae [Phaenospermateae + The Rest]]: primary inflorescence branches 2-ranked [primary branches from two orthostichies]; embryo lacking scutellar cleft,embryonic leaf margins non-overlapping.

12B. Nardeae Koch

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

2/2. Europe.

Synonymy: Nardaceae Martynov

[Phaenospermateae + The Rest]: microhairs 0 (+ - some Stipeae); (stomata subsidiary cells with parallel sides)

12 C. Phaenospermateae

21 bp insertion in in rpl32-trnL; n = 7, 12.

7/11. Central to East Asia, also Australia, Mexico, Balkans, Caucasus; scattered.

12 D. The Rest [some characters not quite at right level; more phylogenetic resolution needed]: fructan concentration often high; style solid [Triticum]; primary inflorescence branches usu. 2-ranked; n = 7, chromosomes "large".

169/3833: Festuca (470: inc. Lolium), Poa (200), Stipa (300), Calamagrostis (230), Agrostis (220), Elymus (150), Bromus (100), Anthoxanthum (50). Largely North Temperate.

Synonymy: Aegilopaceae Martynov, Agrostidaceae Berchtold & J. Presl, Alopecuraceae Martynov, Anthoxanthaceae Link, Avenaceae Martynov, Bromaceae Berchtold & J. Presl, Chaeturaceae Link, Coeleanthaceae Pfeiffer, Cynosuraceae Link, Echinariaceae Link, Festucaceae Sprengel, Glyceriaceae Link, Holcaceae Link, HordeaceaeBerchtold & 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-blade 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 often 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 it has paired spikelets.

Evolution. Divergence & Distribution. The family may have originated in Africa (Bouchenak-Khelladi et al. 2010c) or South America (Bremer 2002) - either way, on Gondwanan continents.

The Poaceae group of families has been described as being notably speciose (Magallón & Sanderson 2001), but there is considerable asymmetry in clade size within this larger clade, with the great majority of species belonging to Poaceae themselves, which may be seven times more speciose than their animal-pollinated sister clade (Kay & Sargent 2009: surely a stunning underestimate?). Even within Poaceae there are three species-poor clades that are successively immediately sister below the PACMAD and BEP clades (to add to the two to three more such clades successively sister below the family). Thus any foci of diversification are likely to be found within the PACMAD and BEP clades (c.f. Linder & Rudall 2005; Smith et al. 2011; and especially Bouchenak-Khelladi et al. 2010c). However, diversification estimates depend on clade ages, and there are major problems here (Christin et al. 2014); until these ages stabilize, it is difficult to worry too much about diversification here... Burleigh et al. (2006) suggest that by some measures Poaceae do show a notable shift (increase) in complexity.

With the above caveats in mind, Hodkinson et al. (2008) discuss increases of diversification rates in Poaceae in the context of a supertree; there seems to have been one increase when true spikelets developed, at the Puelioideae node, etc. (see also Bouchenak-Khelladi et al. 2010c). The age of the PACMAD/BEP node is broadly in line with that of the age of a genome duplication in Poaceae estimated at 70-50 m.y.a. (Blanc & Wolfe 2004; Schlueter et al. 2004; Paterson et al. 2004; Kim et al. 2009). Schranz et al. (2012) thought that there was a lag time between this genome duplication and subsequent diversification increases, but they thought that the two might be linked; the evolution of the PACMAD and the BEP clades are associated with other shifts in diversification rates (Bouchenak-Khelladi et al. 2010c).

Ecology and diversification has been examined at finer levels and in various groups. Thus the herbaceous habit and annual life cycle appear to be correlated with species richness (Salamin & Davies 2004; Smith & Donoghue 2008), however, the speciose Bambusoideae are woody. Poöideae are largely temperate; C₄ photosynthesis has arisen many times in the PACMAD clade, and clades with C₄ photosynthesis tend to be more speciose than their sister clades with C₃ photosynthesis; Chloridoideae tolerate drought and saline conditions particularly well; etc..

Much diversification in crown Aristidoideae is considerably younger than the (25.5-)20.3(-15.9) m.y. crown age (Bouchenak-Khelladi et al. 2010a; Cerros-Tlatilpa et al. 2011, q.v. for other estimates). Linder et al. (2013) discussed the distribution of the largely austral Danthonioideae; they thought that the main variables were the distance between suitable areas and their extent, but not wind direction, extent of water gaps, etc., while Linder et al. (2014) emphasized topographic activity/heterogeneity ad drivers of radiation. The very diverse Old World members of Arundinarieae are a mere 15 m.y.o.. and tropical Old and New World bamboos may have diverged 24.8-40.2 m.y.a. (Burke et al. 2012: c.f. other ages there). Within Poöideae-Stipeae, Romaschenko et al. (2014) found evidence of genomes from clades extinct in the area in which some of their hybrid descendents could be found.

Ecology & Physiology. For good summaries of the ecology of grasses and grasslands, see Coupland (1993a, b), White et al. (2000) and Gibson (2009). The global extent of contemporary grassland, including savanna, is 52.5x10⁶km², or somewhere between 41-56x10⁶ km², that is, 31-43% of the total land surface area (excluding Greenland and Antarctica: Gibson 2009)). Other estimates are lower, ca 20% of the earth's surface (Hall et al. 2000; Sabelli & Larkins 2009), the figures depending in part on the definitions of grassland, savanna and forest. Grasses in the Great Plains alone cover slightly over 3x10⁶ km², the Campos Cerrado ca 2x10⁶ km² - see also the map, where rather virulent green = more or less pure grassland, and olive green = communities with trees and shrubs as well as substantial grass (map: from endpapers in Coupland 1993a, b; esp. White et al. 2000, Map 1, for more details; see also Clade Asymmetries).

Grasses and C₄ photosynthesis.

There have been suggestions that C₄ photosynthesis persisted through the Mesozoic (Keeley & Rundel 2003 for literature). However, its appearance in clades of extant angiosperms is a Tertiary phenomenon. All told, only 7,500 species of flowering plants have the C₄ photosynthetic syndrome, and of these about 4,500 are grasses, where they make up about three quarters of the almost 5,900 species of the PACMAD clade (Sage et al. 1999, 2012; Grass Phylogeny Working Group II 2011). For a summary of C₄ photosynthesis, see Sage et al. (2012) and Kellogg (2013).

Within grasses, there has been massive parallelism in the acquisition of C₄ photosynthesis, with some 22-24 separate origins of this feature in the PACMAD clade (e.g. Kellogg 2000; Roalson 2011: 12-19 transitions; Christin et al. 2008a, 2009 b; Vicentini et al. 2008; Cerros-Tlatilpa & Columbus 2009 and Christin & Besnard 2009 [both Aristidoideae]; Grass Phylogeny Working Group II 2011; Sage et al. 2011, 2012; Morrone et al. 2012). Interestingly, both origins of and reversals from C₄ photosynthesis may be clustered, although reversals are not very common (Vicentini et al. 2008; for reversals, see also Ibrahim et al. 2009). The relatively uncommon C₄ PCK subtype (phosphoenolpyruvate carboxykinase) may be basal in Chloridoideae, being subsequently lost and reacquired (Christin et al. 2009b; Christin et al. 2010a: reversals; Ingram et al. 2011b: a reversal that wasn't). A few intermediates in which there is C₂ photosynthesis are known from the family (Monson & Rawsthorne 2000; Bauwe 2011 for references).

The adoption of C₄ photosynthesis is associated with well-known anatomical changes, such as closer spacing of the veins, the development of a sheath of chloroplast-rich cells around the vascular bundles, etc., i.e., the Kranz anatomical syndrome, although the control of this is particularly poorly understood (Kellogg 2013; see Pengelly et al. 2011 for vein spacing; Sack & Scoffoni 2013 for literature suggesting that this potentiated the repeated evolution of C₄ grasses). The mechanisms of C₄ photosynthesis and the anatomies associated with it are very variable in Panicoideae, and C₄ photosynthesis may have evolved up to eight times there alone (Kellogg 2000; Giussani et al. 2001; Christin et al. 2007a, 2009a). Although anatomy has been used to characterize subtypes of C₄ photosynthesis, the correlation of anatomy and photosynthetic pathway may not be that good (Ingram 2010), and the typology needs to be revisited (E. A. Kellogg, pers. comm.).

The numerous acquisitions of C₄ photosynthesis within the PACMAD clade perhaps reflect an underlying change that faciltated subsequent "independent" acquisitions of the pathway (Grass Phylogeny Working Group II 2011: gene duplication not involved; Williams et al. 2012; see Marazzi et al. 2012). These parallelisms may even be at the level of particular amino acids being substituted, similar changes occurring independently in the phosphoenolpyruvate carboxylase gene in grasses (Christin et al. 2007a, esp. b, 2009a). Indeed, a mutation to serine at position 780 seems to have occurred in all plants with C₄ photosynthesis (Bläsing et al. 2000; see also Brown et al. 2011 for C₄ parallelisms between grasses and Capparidaceae; Grass Phylogeny Working Group II 2011), and functionally important parallelisms are also found in rbcL (Christin et al. 2008b). John et al. (2014) also discuss extensive parallelism in C₄ grasses. Lateral transfer of genes may also have been involved in putting together C₄ pathways. The sequential transfer of genes over a period of millions of years from quite unrelated grasses, perhaps via movement of genes from pollen of a grass that lands on the stigma of a plant that it cannot pollinate, may explain the nature of the C₄ pathway in Allopteropsis (Panicoideae). No other genes seem to be involved, and a taxon embedded in the clade has ordinary C₃photosynthesis (Christin et al. 2012). This is difficult to get one's head around...

Christin et al. (2013) have suggested particular anatomical changes that facilitated the transition to C₄ photosynthesis in grasses. They suggest that veins - or at least bundle sheaths - became closer in the common ancestor of the PACMAD + BEP clade - and a high proportion of vascular bundle sheath tissue facilitated this transition (for venation densities, ca 5.1 vs 10.6mm mm^-2 in C vs C₄ plants, see Ueno et al. 2006). C₄ photosynthesis did not develop in the BEP clade, because the outer bundle sheath cells subsequently became smaller, but it did in the PACMAD clade because they became larger (although they were sometimes lost there, but then the inner sheath cells became dramatically larger). Finally, mesophyll cells were sometimes lost in the PACMAD clade (Christin et al. 2013). In a less elaborate analysis, Griffiths et al. (2012) suggested that bundle sheath proliferation had begun before any change in vein densities.

Grasslands, Fire and Forests.

This discussion applies both to C₄ grasses and to the more cold tolerant grasses, most of which are C₃; the evolution of cold tolerance per se is discussed later.

Understanding the ecological relationship between grasslands and woodland over time is important since the two differ greatly in associated flora and fauna and in their effects on the biosphere. Poaceae may initially have been forest dwellers (e.g. Bouchenak-Khelladi et al. 2010a, c: Puelioideae not included; Givnish et al. 2010b), although most Bambusoideae are secondarily woody (3 m or more tall) and forest dwellers. Most or all of the species-poor largely forest-dwelling basal clades had diverged by the end of the Cretaceous; diversification of the PACMAD/BEP clade, largely consisting of plants growing in more open habitats, is probably entirely Tertiary in age (but see above for caveats about dates).

The factors that favoured the initial development of grasslands, caused the clustering of origins and losses of different photosynthetic mechanisms, and were involved in the great spread and expansion to dominance of late Miocene C₄ grasslands, remain unclear (see also Tipple & Pagani 2007; Jacobs et al. 1999; Sage & Kubien 2003; Fox & Koch 2004; Osborne & Beerling 2006; Bond 2008; Westhoff & Gowick 2010) and will be still less clear if some of the older clade ages are confirmed (Christin et al. 2014). Some combination of temperature, low atmospheric CO₂ concentration, fire and water stress is now emphasized (Bond et al. 2003; Edwards & Still 2008; Vincentini et al. 2008; Edwards 2009; Strömberg & McInerney 2011; Christin et al. 2011b; Kellogg 2013). There was a decline - perhaps quite rapid - in atmospheric CO₂ concentration ca 30 m.y.a. in the Oligocene (Pagani et al. 2005; Zachos et al. 2008; Gerhart and Ward 2010; Arakaki et al. 2011) perhaps caused by the activities of ectomycorrhizal plants (L. L. Taylor et al. 2009; see above). Temperatures in the late Miocene were also decreasing (Arakaki et al. 2011). Indeed, grasslands may be very sensitive to changing climates, in some reconstructions of the effect of the current increase in CO₂ in the atmosphere, the spread of C₃ grasslands is quite extensive (e.g. Collatz et al. 1998; Hall et al. 2000; Knapp & Smith 2001). Of course, the initial move of grasses from woodlands to open habitats and their much more recent dominance may have quite different precipitating causes.

S. H. Taylor et al. (2010) and Ripley et al. (2010) compared the ecophysiology of C₃ and C₄ grasses, the latter sometimes being more sensitive to drought and recovering more slowly from it. C₄ grasses, grasslands and savanna may be favoured in environments with some combination of high temperatures and low CO₂ concentrations. When stomata close in plants with C₄ photosynthesis transpiration losses are reduced, so mitigating the effect of temperature and water stress, however, carbon fixation is not necessarily reduced and damaging photorespiration is avoided, so mitigating the negative effects of the decrease in CO₂ concentration (Morgan et al. 2011; Sage et al. 2012). Interestingly, taxa like Miscanthus x giganteus carry out C₄ photosynthesis under decidedly cooler conditions than is common (Wang et al. 2008), while the C₃ Lolium perennecan also tolerate water stress (Holloway-Phillips & Brodribb 2010, see below). Declining CO₂ concentrations may also have made trees less competitive (Pagani et al. 2009). Many C₄ origins seem to be correlated with a reduction in annual rainfall, and grasslands transpire less than the woodlands they may have replaced (Retallack 2001). Increasing temperature, open habitats, and perhaps especially decreasing precipitation would all increase water stress, although by no means all C₄ grasses are drought tolerant (e.g. Edwards & Still 2007, esp. 2008; Edwards et al. 2007; Edwards 2009). In a compartive study, Pinto et al. (2014) found that C₄ grasses used nitrogen and water more effectiently that C₃ or C₃-C₄ intermediates in low (glacial) CO₂ concentrations.

The amount and persistence of litter in grasslands may be an important factor in their success. Grasslands accumulate litter very easily, and there is a negative correlation between silicon concentration - especially high in annual grasses - and rate of leaf decomposition (Cook & Leishman 2011b). The relatively low nitrogen content in grass litter, especially the litter of C₄ grasses, also means that it decomposes slowly and accumulates (Wedin 1995; Pérez-Harguindeguy et al. 2000: Bromeliaceae could be similar!; Cornelissen et al. 2001; decomposition fast, Chapin & Körner 1995, but comparison with mosses). Leaves of poöid monocots (presumably including sedges) decompose more slowly than do those of other angiosperms (Cornwell et al. 2008).

Thus grasslands are particularly flammable because of litter accumulation (Scheiter et al. 2012; Sage et al. 2012); certainly, charcoal from fires has become abundant since the Late Miocene about 10 m.y.a. (Bond & Scott 2010). The high flammability of dry grasses, disturbance by grazers, and windiness are among the factors, many related, that would lead to the increase of fires and further spread of grasslands (Retallack 2001; Woodward et al. 2004; Bond & Scott 2010). Scheiter et al. (2012) see an interaction between increased temperatures, favouring C₄ grasses, relatively low atmospheric CO₂, favouring the invasion of C₃ grassland by C₄ grasses, and fire, allowing the expansion of grassland and also the development of savanna, with its shade intolerant and fire-resistant trees. Since grasses have their perennating parts underground, they are not harmed by fire, while burning suppresses woodland by kiling fire-susceptible trees; nitrogen is also volatilized and lost. Both would favour grasses: The habitat was opened, and C₄grasses in particular have a reduced requirement for photosynthetic enzymes and so a lower nitrogen requirement (Wedin 1995). (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.) The dense - and sometimes remarkably deep - root masses of grasses also make the establishment of woody vegetation in grassland difficult (D'Antonio & Vitousek 1992); the seedling/young plant stage is critical here (Bond & Midgley 2000). Bond et al. (2005) estimated that if there were no fires, about 52% of C₄ grassland and 41% of C₃ grassland would revert to forest; of the latter, over half would be dominated by gymnosperms. A further wrinkle is that fires may have increased over the last 50,000 years because of the widespread extinction of megaherbivores by humans and/or climate (Lorenzen et al. 2011; Gill 2013). However, in North America, at least, McInerney et al. (2011) suggest that the late Neogene expansion of C₄ grasses was at the expense of C₃grasses rather than of woody vegetation, while with decreasing temperatures survival of tree seedlings in the forest-grassland transition is increased (Will et al. 2013).

Some vegetation simulations show circum-Arctic grasslands early in the Tertiary (Shellito & Sloan 2006), although this is unlikely. Palaeosol and other evidence suggests that grassland grasses began diversifying in the Eocene (e.g. Bouchenak-Khelladi & Hodkinson 2011), and the grasses involved are mostly caespitose bunch grasses (Retallack 2013). Although some grasslands may have been developing in the Oligocene, they did not become widespread until far later. Most open habitat grasses, probably C₃, appear in the Middle Eocene ca 42 m.y.a., and may have become locally dominant (Strömberg 2011); they diversified taxonomically in North America in the early Oligocene ca 34 m.y.a. (Strömberg 2005). Evidence from palaeosols suggest that grasslands in the Great Plains may be late Oligocene in age (ca 24 m.y. old), although some Argentinian grasslands may be older, Eocene in age (Retallack 1997b; Edwards et al. 2010). From the examination of phytolith assemblages, grass-dominated open habitats in Patagonia did not develop before ca 18.5 m.y.a., and it was open-habitat C₃ poöid grasses that were dominant then (Strömberg et al. 2011).

C₄ grasses may have originated in the Oligocene ca 33 m.y.a., and C₄ photosynthesis is known from grasses from the Early to Middle Miocene in both the Great Plains and Africa, some 25-12.5 m.y.a. (e.g. Ehleringer 1997 and references; Christin et al. 2008a, 2011b). However, such grasses made a major contribution to overall vegetation biomass - only in the late Miocene 9-8 m.y.a., the process being complete as recently as the late Pliocene 3-2 m.y.a. (Bouchenak-Khelladi et al. 2009, 2014; Edwards et al. 2010; Strömberg & McInerney 2011; McInerney et al. 2011 for North America; Strömberg et al. 2011: South America; Arakaki et al. 2011; Sage et al. 2012). Thus there is a pronounced lag at both global and local scales between the initial evolution and diversification of grasses that carry out C₄ photosynthesis and their ecological expansion (e.g. Strömberg & McInerney 2011) - a lag of over 20 m.y.. The extensive Brazilian Cerrado, savanna vegetation with flammable C₄ grasses and plants, a number woody, that have become adapted to a fire regime, developed only within the last (10-)5 m.y. (Pennington et al. 2006b; Simon et al. 2009; Simon & Pennington 2012). Indeed, the Neogene has been called the age of grasses (c.f. Palaeos).

Grasslands affect the biosphere because the total C sequestration grasslands is greater than that of the forests they in many cases they seem to have replaced, with a shift in the sequestration pattern from above-ground parts to the soil (McGuire et al. 1992; Retallack 2001). Some Oligocene palaeosols approach mollisols, a soil type known only from the Tertiary and uniquely associated with grasslands (Retallack 1997b). Short sod grassland (the grasses are mostly rhizomatous) with shallow soils may have appeared in the early Miocene ca 20 m.y.a. in relatively warmer and wetter (400< mm/yconditions (Retallack 2001, 2013). Tall sod grasslands made up mostly of C₄ grasses and with deeper soils appeared in the late Miocene ca 7-5 m.y.a. in areas with up to 750 mm annual precipitation, and it was these grasslands that had true mollisols. In their fullest development, mollisols are dark and deep (the carbon-rich layer may be 1 m or so); carbon is mixed with rounded clods of clay 2-3 mm across, they are nutrient-rich, with carbonate and easily-weathered minerals, and are densely permeated by grass roots (Retallack 1997b). Grassland soils are notably moister than corresponding woodland soils, with increased weathering, yet somewhat paradoxically grasslands support a drier climate, transpiration being relatively low. Woodlands have a higher albedo and transpire more, so their soil is drier (Retallack 2001, 2013).

To conclude. The relationships between C₃ and C₄ grasses, temperature, trees, moisture, atmospheric CO₂ concentration and fire are complex and dynamic. Grasslands and savanna currently cover about 40% of the land surface of the globe, about half that area being within the tropics (Gibson 2009 for references). The global distribution of C₄vegetation, which of course includes more than just grasslands, has been estimated at ca 18.8 x 10⁶ km², somewhat over 15% of the total (Still et al. 2003). All told C₄photosynthesis accounts for about 23-28% of terrestrial gross primary productivity, although the biomass of C₄ plants is only ca 5% of the global total (Still et al. 2003: GPP = 35.3 vs 114.7 Pg C yr^-1, simulated biomass, leaf, wood, root = 18.6 vs 389.3 Pg C; Ito & Oikawa 2004; see also Lloyd & Farquhar 1994; Ehleringer et al. 1997; Retallack 2001). Another estimate suggests that grasslands in general - both C₃ and C₄ species - currently account for 11-19% of net primary productivity on land (Hall et al. 2000). Estimates of the proportion of below-ground biomass in grasslands is as high as 80-95% (Dormaar 1992) accounting for 10-30% of global soil carbon storage (Hall et al. 2000); Gibson (2009) estimated as much as ca 33% total C storage - 650-810 Gt, broadly in line with the estimates in Retallack (2013). Overall, grasslands can be considered a long-term carbon and water sink, and one of the consequences of their activities is long-term global cooling (Retallack 2001, 2013).

What makes grasslands and savannas still more distinctive ecologically is not just the abundance of grasses and their distinctive growth habit, but that relatively fewspecies of grasses are ecologically dominant in any one place, and most of these seem to be C₄ grasses; of the some 11,300 species of grasses, only some 600 species dominate ecologically in grasslands and savanna, and most of these are C₄ photosynthesizers (Edwards et al. 2010). Finally, although C₄ grasses in particular may have first appeared in the Oligocene ca 33 m.y.a. and began tp diversify soon after, they made a major contribution to overall vegetation biomass only in the late Miocene 9-8 m.y.a.. It was then that grasslands began to spread rapidly, the process being complete as recently as the late Pliocene 3-2 m.y.a. (e.g. Bouchenak-Khelladi et al. 2009, 2014; Edwards et al. 2010; Strömberg & McInerney 2011; McInerney et al. 2011; Strömberg et al. 2011; Arakaki et al. 2011; Sage et al. 2012)

Grasses, Grasslands, Herbivory and the Silicon Cycle.

There are also suggestions that C₄ grasses in particular, grasslands in general, and grazing are connected (e.g. Retallack 2013). Thus Bouchenak-Khelladi and Hodkinson (2011) thought that there were "adaptive coevolutionary processes" (unspecified) going on between grass and grazer. However, C₄ plants tend to be less attractive to herbivorous animals because of their lower nitrogen concentration and greater amount of fibrous tissue - they have more sclerenchyma because their veins are closer (Caswell et al. 1973; Schoonhoven et al. 2005 for references: Taylor et al. 2010 suggested that the N content of C₃ and C₄ grasses was similar). The persistent dead leaves of most grasses may also decrease their general palatability to grazers (Antonelli et al. 2010). Be this as it may, diversification of grazers began in the Oligocene ca 35 m.y.a. and there was a Miocene radiation of grazing mammals (Thomasson & Voorhies 1990; MacFadden 1997; Retallack 2001; Keeley & Rundel 2003) that has been linked to the spread of prairie and savanna grasses (see also Cerling et al. 1997; Bouchenak-Khelladi et al. 2009, 2010a: considerable detail and many dates; Mihlbachler et al. 2011). Most extant grazers eat C₄ plants, but C₃ grazers, now uncommon, were found in a diversity of ecosystems before 7 m.y.a. (MacFadden 1997). Grazing mammals evolved hypsodont or hypselodont dentition, the former teeth with high crowns, enamel extending below the gum lines, and short roots, and the latter, ever-growing teeth, both apparently to deal with the wear caused by eating the abrasive grasses with their complex silica bodies.

However, tooth enamel seems to be harder than the silica encountered in grasses (Sanson et al. 2007), although surprisingly little is known about the mechanics of tooth action (Sanson 2006). It is probably dust particles, likely to be more numerous in food eaten by a grazer than by a browser, that are the most abrasive element in the food ingested (e.g. Kay and Covert 1983). Bouchenak-Khelladi et al. (2009) noted that the density of silica bodies in the leaf epidermis seems to have increased in a number of grass groups, perhaps as a defence against herbivory, however, Sanson and Heraud (2010) suggested that the silica there might not be in crystalline form and so would not cause wear on the enamel of mammalian teeth. But silica bodies do affect the feeding behaviour of at least some smaller herbivores, both mammals and insects, even if they are not the immediate "cause" of hypsodonty in mammalian teeth (for rabbits, see Cotterill et al. 2007). Higher silica in grasses decreases the amount of nitrogen taken up by both armyworm (Spodoptera exempta) larvae and voles (Microtus), and in the former in particular there are long-term negative effects on the growth of the caterpillar, perhaps via damage to the larval midgut. Moreover, the mandibles of armyworm larvae, made out of chitin, are worn down by silica, and it is well known that grass tissues produced after attack by a herbivore (but not after comparable purely mechanical damage) have an increased silica concentration and are less attractive to the animals (see Schoonhoven et al. 2005; Massey & Hartley 2006, 2009; Massey et al. 2007b).

The relationship between silica, herbivory, and the mechanical protection of plant tissues is clearly not straightforward. Although prairie grasses expanded in Nebraska in the Early Miocene ca 23 m.y.a., hypsodont ungulates were already around by then (Strömberg 2004, 2006; Mihlbacher et al. 2011). Massive diversification of North American ungulates is largely a Miocene phenomenon, Bovidae and Cervidae starting to diversify by at least 26 m.y.a. (Bouchenak-Khelladi et al. 2009), and herbivores that are now specialists on C₄ grasses seem to have evolved before those grasses came to dominate ecosystems (Edwards et al. 2010). Grazers in South America appeared earlier than in North America, ca 50 m.y.a., and were pervasive" there by the Oligocene ca 35 m.y.a. (MacFadden 1997, esp. p. 185), probably eating C₃ plants. Establishing connections between the evolution and rise to dominance of grasses in some ecosystems and the evolution of grazing animals and of hypsodonty needs more work; it is likely that the two are linked, but not at such a simplistic level as high SiO₂ = hypsodonty (see also Retallack 2001 for a summary); similarly, Bouchenak-Khelladi and Hodkinson (2011) noted that hypsodonty has been gradually increasing for 20 m.y., but there is no documentation of the comparable spread of grasslands.

Of course, silica is not the only defence that grasses have (Massey et al. 2007a), for instance, they vary in toughness and may contain noxious metabolites, sometimes because of their association with endophytes (see above). In some grasses defence against herbivores is mediated by the production of volatile mono- and sesquiterpenes which can, for example, attract nematodes (to attack Diabrotica - the chrysomelid corn root-worm - larvae) or parasitic wasps (to attack caterpillars) (Degenhardt 2009).

There is a further ecological dimension of silica and grazing. Silica becomes mobilized during digestion, particularly during digestion by ruminants because grasses stay in the gut for a long time, and hence there is a massive mobilization of silica in grazed grasslands. The spread of grasses in the Miocene and the increased activity of herbivores may have increased the flux of silica into fresh waters, so sparking the Early Miocene increase of diatomite (diatomaceous earth, kieselguhr) deposits and diamtom diversity in fresh waters; the cell walls (frustules) of diatoms are made up of silica (Kidder & Gierlowski-Kordesch 2005; Vandevenne et al. 2013). Whether diatom growth in the sea was stimulated is unclear, certainly, marine diatom diversity peaked at the Eocene/Oligocene boundary well before the spread of grasslands (Rabosky, D. L., & Sorhannus 2009), after that period the calcite compensation depth (the depth below which calcite dissolves) considerably increased, with calcium carbonate nanofossil ooze replacing siliceous radiolarian ooze (Coxall et al. 2005; Tripati et al. 2005) in connection with the developing ice caps.

Other.

There are other aspects of the eco-physiology of Poaceae to take into account.

1. Hydraulic Conductance. Woody bamboos, some 1,300 species, can grow to 30 m tall or more, and may live for 100 years before flowering; palms and bamboos are the two major woody monocot clades. Given that there is no secondary thickening in bamboos, how the vascular tissue of these plants remained functional was unclear. However, Cao et al. (2012 and references) found that in the bamboos they studied root pressure was sufficient to drive water the entire height of the plant; root pressure and plant height were strongly correlated. This would help in the repair of embolisms in the xylem.

In the poöid Lolium perenne, leaf hydraulic conductance may decrease during the day, with cavitation presumably occuring, yet photosynthetic rates may stay high, the stomata remaining open. The plant was able to recover from quite extreme daytime hydraulic dysfunction, although here root pressure seemed not to be involved (Holloway-Phillips & Brodribb 2010). It will be interesting to see how widespead such behaviour is in the family.

2. Cold Tolerance. The ecological success of Poaceae is not just because some adopted C₄ photosynthesis. Cooler temperate grasslands in the northern hemisphere are dominated by Poöideae, all of which are C₃ grasses. Thus although about 16% of all species growing in Quebec and Labrador north of 54^o N are Cyperaceae, Poaceae, all members of Poöideae, are next at 11% (Escudero et al. 2012). Poöideae have a complex relationship between freezing tolerance, day length, vernalization, and flowering (e.g. Edwards 2009; Edwards & Smith 2010; Dhillon et al. 2010). Core Poöideae evolution may be linked with the cooling at the beginning of the Oligocene ca 33-27 m.y.a. (Strömberg 2005; Sandve et al. 2008; c.f. Christin et al. 2014), gene families implicated in low temperature-induced stress response expanding prior to Poöideae diversification (Sandve & Fjellheim 2010); the genes seem to have been under positive selection (Vigeland et al. 2013: clades downstream from Brachypodium not examined). Proteins that inhibit ice recrystallization are known from the group (Sidebottom et al. 2000; Tremblay et al. 2005; Sandve et al. 2010). Furthermore, low levels of fructan - specifically levans - accumulation have been noted in many Poaceae, but notably high levels are found only in Poöideae, although not in taxa of the "basal" pectinations like Nardus, Stipa and Phalaridinae (Smouter & Simpson 1989; Hendry 1993; Pollard & Cairns 1991). Fructans may enable Poöideae that accumulate them to survive drought or frost better, and they have been implicated in stabilizing cell membranes at low temperatures (Livingston et al. 2009; Sandve & Fjellheim 2010). The establishment of vernalization requirements may have contributed to the diversification of Poöideae (Preston & Kellogg 2008), although how widely they occur outside the subfamily is unclear. Finally, the development of theEpichloë/Poöideae relationship may have been involved in the spread of Poöideae from shady to sunny open habitats in the predominantly cool-season climates that they favor (Kellogg 2001), the mutualism aiding the plant's defences against herbivores and drought (Schardl et al. 2008; Schardl 2010).

Other grasses also tolerate cooler condition, including the more northerly temperate bamboos (Bambusoideae: Arundinarieae) and the austral Danthonioideae. In the latter, evolution of cold tolerance is estimated to have begun ca 25 m.y.a. during the late Oligocene in Africa (Humphreys & Linder 2013; see also Linder et al. 2013). The two species of Danthonioideae studied (Chionochloa) seemed to tolerate cold conditions by controlling ice nucleation (Wharton et al. 2010).

3. Stomatal Opening. The dumb-bell shaped stomata of grasses show remarkably rapid stomatal movements, very much faster than those few other stomata have been examined (Franks & Farquhar 2006; Haworth et al. 2011). However, since the stomata of quite a number of other Poales are similar, it is unclear if they are a major component of the ability of grasses to spread as climates became drier at the end of the Eocene (Hetherington & Woodward 2003).

4. Roots. Much goes on in grass roots. Prominent rhizosheaths - mucilage from root cap cells, soil particles, bacteria, etc., all anchored to root hairs - occur in many Poaceae (McCulley 1995), especially those growing in drier conditions, although the distribution of such roots is poorly known. They are found in other Poales, but are apparently rare in broad-leaved angiosperms. Interestingly, C₄ grasses have roots with long root hairs yet may respond positively in terms of phosphorus uptake when forming endomycorrhizal associations - long root hairs and endomycorrhizal associations tend to be thought of as alternative ways of securing phosphorus supply, etc. (Schweiger et al. 1995 and references). Some crops, including maize and wheat, show a substantial uptake of nitrogen from bacteria that are either in the rhizosphere are are endophytic (Santi et al. 2013). Finally, Poaceae, apparently alone in flowering plants (Römheld 1987), acquire iron through chelation of ferric ions with non-protein amino acid siderophores which are then taken up by the roots; iron (and zinc) are commonly limiting trace elements in alkaline soils (Schmidt 2003; Kraemer et al. 2006). Interestingly, ectomycorrhizal plants, also noted for dominating the communities in which they occur, also produce siderophores.

5. Allelopathic Reactions. Some Poaceae have allelopathic reactions with other plants, Sorghum roots producing a quinone (an oxygen-substituted aromatic compound) andFestuca roots meta-tyrosine, a non-protein amino acid (Bertin et al. 2007). Benzoxazinoids, cyclic hydroxamic acids, are largely restricted to Poaceae, and are found in both Panicoideae and Poöideae. They confer resistance to fungi, insects (volatilized, they attract wasps parasitizing herbivorous insects), and even herbicides, and are also allelopathic, but less so to other grasses than other plants (Frey et al. 1997, 2009; Gierl & Frey 2001; Sicker et al. 2000: ecological role; Dick et al. 2012; Schullehner et al. 2008: non-grasses).

6. Salt Tolerance. Poaceae such as Spartina and Puccinellia are major elements of salt marshes. The C₄ Spartina (Chloridoideae) is a particularly prominent component of temperate salt marshes where it dominates large areas; there has been past hybridisation in the genus, and hybridization also occurs between introduced and native species, some of the products (like S. anglica) being very invasive (Srong & Ayres 2013). Salt tolerance in grasses is quite widespread, and two thirds of the species are also C₄ plants (Flowers & Colmer 2008). Some 200+ species are involved, and weak salt tolerance - tolerance of salinity up to ca 80mM NaCl - has evolved some 76 times (Bennett et al. 2013). Euhalophytes, tolerating at least 200mM NaCl, about half the salinity of sea water, have evolved some 43 times, and in both cases the clades involved are young and small; A number of grasses in different subfamilies accumulate glycine betaines and other compounds commonly associated with allowing plants to grow in saline conditions (Rhodes & Hanson 1993). Bambuseae (sic) and Danthonioideae are notable for lacking even weak halophytes (Bennett et al. 2013).

7. Bamboos and Dominance. Woody bamboos tend to colonize forest gaps and edges and can dominate in the canopy and understory of both temperate and tropical forests, particularly in mountainous regions. They play a very important role in forest dynamics; monocarpic flowering (see below) allows broad-leaved angiosperms to become established ina reas where they grew. Even herbaceous bamboos (Olyreae) may dominate understory vegetation (Bamboo Phylogeny Group 2012b for details and references). Note, however, that although bamboos are the second most important woody monocot clade (after palms), they do not appear in the very top ranks of any of the important ecological traits studied by Cornwell et al. 2014).

8. Fungus Attack. Sindhu et al. (2008) suggested that the whole PACMAD/BEP clade can be characterized by a gene that protects the plant against toxins produced by the ascomycete Cochliobolus (anamorph Helminthosporium) carbonum; they describe the gene as "a guardian of the grass family" (ibid.; p. 1766). This gene could be an apomorphy of the whole clade, but its wider distribution in monocots is unknown.

9. Phloem transport. Some sieve tubes, especially in the cross-veins in the leaves, that are adjacent to the xylem lack companion cells, are notably thick-walled, and are symplastically isolated from "normal" sieve tubes. They seem to be involved in short distance transport of not very concentrated sugars (Botha 2013). They are quite common in grasses, and probably evolved well before 7-5 m.y.a. (c.f. Botha 2013); although their distribution in other monocots is unclear, they are also reported from Cyperaceae.

10. Other. For the role of the leaf sheath in supporting the stem, particularly the region with the intercalary meristem, see Kempe et al. (2013 and references). The pattern of evolution of the Rp1 disease resistance gene family in the PACMAD/BEP clade is complex (Luo et al. 2010). At least some species of Micraira (Micrairoideae) are resurrection plants (Sanchez-Ken et al. 2007).

Bacterial/Fungal Associations. Ascomycete clavicipitaceous endophytes are widely distributed among grasses (Clay 1990: review; Leuchtmann 1992: distribution and host specificity of grass endophytes; Schardl 2010; Rodriguez et al. 2009: endophytes in general); the association could be ca 40 m.y. old (Schardl et al. 2004). Some 30% or more Poöideae are involved in these associations, and there is both horizontal and in particular vertical transmission of the fungus. One of the most important fungi involved is Epichloë(Clavicipitaceae), a systemic endophyte restricted to Poöideae; Neotyphodium is its asexual stage, perhaps representing hybrids of Epichloë species (Roberts et al. 2005; Moon et al. 2005; Rodgers et al. 2009: patterns of infection of the two forms). These hybrid fungi may even increase the competitive ability of the host grass under stressful conditions (Saari & Faeth 2012), although under some conditions they severely reduce sexual reproduction (Oberhofer et al. 2013: both greenhouse experiments). The larvae ofPhorbia (or Botanophila) flies live on Epichloë stroma, and the adults transmit the fungal spermatia in a fashion analogous to insect pollination of flowers (Bultman 1995). Indeed,Epichloë synthesizes unique compounds that specifically attract the flies (Steinebrunner et al. 2008) and which may also be toxic to other fungi that secondarily invade the fungal stromata (Schiestl et al. 2006). However, the equilibrium of such relationships can easily be disturbed (Eaton et al. 2010). For details of the phylogeny and evolution of the endophyte association see Schardl (1996, 2002, 2010), Craven et al. (2001), Clay and Schardl (2002), Jackson (2004: possible codivergence), and Gentile et al. (2005).

Clavicipitaceae-Balansiae (Clay 1986; White et al. 2003: review) are now included in Hypocreales, the old Clavicipitaceae having been split up. Hypocreales include many insect pathogens, plant parasites, and especially parasites of other fungi, but also yeast-like obligate symbionts (of leaf hoppers). There has been widespread cross-kingdom host switching (e.g. Vega et al. 2009; Kepler et al 2012). Hypocreales may ancestrally have been plant parasites, although the immediate ancestor of grass endophytes may have been an insect pathogen (e.g. Spatafora et al. 2007; Vega et al. 2009). Some fungi like Metarhizium robertsii may even be both endophyte and insect pathogen (e.g. Sasan & Bidochka 2012).

The endophyte-grass relationship is usually described as being one of mutualism, although this may sometimes, at least, not be so (see Saikkonen et al. 1998; Gundel et al. 2006; Ren & Clay 2009), indeed, the more that is found out about the relationship, the more complex it appears to be. These endophytic fungi synthesize a diversity of secondary metabolites (Spatafora et al. 2007). Four groups of "grass" alkaloids are synthesized by Epichloë: Indole diterpenes, loliine (1-aminopyrrolizidines), peramine, and the ergot (ergolines) alkaloids (Fleetwood et al. 2007). Loliines are primarily active against insects (Schardl et al. 2007; Zhang et al. 2009). Endophytes that are insect pathogens may also be antagonistic to plant pathogens (Vega et al. 2009 and references). Furthermore, the presence of endophytes affects both the palatability of grasses to herbivores and of their seeds to granivorous birds (Madej & Clay 1991), animals eating the infected material sometimes not thriving at all. The level of aphid infestation and that of their parasites and parasitoids is also affected (Omacini et al. 2001), as is the infestation of the plant by nematodes, insect herbivory (Tanaka et al. 2005), the resistance of the plant to the effects of water stress (Hahn et al. 2007), and even the pattern and rate of decomposition of dead grass (Lemmons et al. 2005; see also Popay & Rowan 1994; Schardl 2010). Fungal endophytes may also affect root growth and root hair production (Sasan & Bidochka 2012). It has recently been suggested that some of these endophyte-mediated affects can be co-opted for developing improved strains of forage grasses (Gundel et al. 2013).

Many other species of apparently symptomless endophytes (= class 3 endophytes: Rodriguez et al. 2009) are also found in Poaceae, but little is known about their interactions with their hosts. Márquez et al. (2007) noted that only when the endophytic fungus (Curvularia) was infected with a virus was Dicanthelium lanuginosum, the host of the fungus, able to grow in volcanically-heated soils, suggesting the complexity of such relationships, while Marks and Clay (2007) discuss growth rate of endophyte-infected and -free plants under various conditions. Some root-associated endophytic fungi (class 4) are also coprophilic (Herrera et al. 2009), perhaps aiding in their dispersal. For fungal records - very numerous and diverse - on grasses, see Tang et al. (2007); there are at least 1933 species of fungi known from bamboos alone.

Bacteria, too, may be endophytic in grasses, and several bacterial endophytes are implicated in fixing one third to one fifth of the nitrogen needed by sugarcane in Brazil - the bacteria include Gluconacetobacter (alpha-Proteobacteria) and Herbaspirillum and Burkholderia (ß-Proteobacteria) (de Carvalho et al. 2011), for Burkholderia, see also Fabaceae, Rubiaceae, etc.. A wide variety of bacteria have been isolated from the roots of Chrysopogon zizanioides (vetiveria) where they are implicated in the synthesis of terpenoids, etc., in the prized essential oils that the plant produces (del Guidice et al. 2008).

Parasitic rusts and smuts are common on Poaceae, and those on Bambusoideae and Poöideae are particularly distinctive (Savile 1979b); two thirds of Ustilaginales (smuts) - close to 600 species - are found on Poaceae (Kukkonen & Timonen 1979; Stoll et al. 2003). Some seventy species of Berberis are alternate hosts (the aecial stage) for the basidiomycete Puccinia graminis, the black stem rust of wheat and other grain crops in Poöideae; this species (or complex) infects some 77 genera of mostly poöid grasses (Abbasi et al. 2005 and references).

Cyclic hydroxamic acids are widely distributed in the family and confer resistance against a variety of fungal and insect pathogens (Frey et al. 1997); for protection against toxins produced by the ascomycete Cochliobolus carbonum, see Sindhu et al. (2008), also above.

Plant/Animal Interactions. Despite the silica bodies mentioned above, as well as alkaloids and other defences, caterpillars of nymphalid butterflies, in particular the browns, Satyrini, and related tribes like Morphini, Melantinini, etc., are common on Poaceae. Satyrinae as a whole diverged from other Nymphalidae some 80-85 m.y.a. (or perhaps at the K/T boundary: Heikkilä et al. 2011; see also Peña et al. 2011), but the main clades within it did not diverge until the later Palaeocene. Other subtribes of Satyrinae are also found on commelinid monocots, sometimes also including grasses, but none has more than 110 species, compared to the some 2,200 species of Satyrinae-Satyrini.

Satyrini larvae almost exclusively eat grasses, where they are the only common grazing insects. Stem Satyrini may be about 65-55 m.y. old, and the crown group is later Eocene, some (47.8-)41.8, 36.6(-31.5) m.y. (Peña & Wahlberg 2008; Wahlberg et al. 2009; Peña et al. 2006, 2011: age depends on calibration points, position of Satyrini varies), perhaps contemporaneous with the initial spread of grasses (Peña et al. 2006, 2011; Peña & Wahlberg 2008). Although the move of satyrine butterflies from forests to more open environments where grasses are so abundant, not grass feeding per se, may have helped spur their diversification (Peña et al. 2011), diversification has also occurred in Satyrini of more forested habitats. Thus caterpillars of the largely western South American subtribe Pronophilina, with well over 400 named species (?600 species total), are largely bamboo feeders that eat Chusquea. They are most diverse in the Andes just below the cloud forest-páramo transition at ca 3050-3250 m altitude, but some species are found in the páramo itself, where Swallenochloa and some other bamboos grow (Pyrcz et al. 2009; Casner & Pyrcz 2010; Sklenár et al. 2011). Only a few Pronophilina are found in comparable forests in east Brazil and Central America.

Galling dipterans, especially Cecidomyiidae, are quite common in grasses (Labandeira 2005). Cecidomyiid gall midges, notably Mayatiola (M. destructor is the Hessian fly), grow on Poöideae in North America (Gagné 1989). Shoot flies (Diptera-Chloropidae) form galls on monocots, especially grasses, but they are also simple herbivores and have other life styles (de Bruyn 2005). Chinch bugs (Hemiptera-Lygaeidae-Blissinae) have been most commonly observed on members of the PACMAD clade, less commonly on the BEP clade; the lygaeid Teracrini are also concentrated on Poaceae (Slater 1976). Poaceae provide food for both adults (as pollen) and larvae (as roots) of Chrysomelidae-Galerucinae-Luperini-Diabrotica beetles (Jolivet & Hawkeswood 1995).

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

Pollination Biology & Seed Dispersal. Poaceae are predominantly wind-pollinated and usually have protandrous flowers with dangling anthers. However, some forest-dwelling grasses, especially Bambusoideae-Olyreae, small plants of the forest floor in the New World, are pollinated by insects (Soderstrom & Calderón 1971: Parinari, Olyra).Streptochaeta may also be animal pollinated, since it lacks a plumose stigma and its anthers do not dangle; the flowers are protogynous (Sajo et al. 2008). Lodicules, modified members of the inner tepal whorl, help in the opening of the staminate or perfect flowers; they may be absent from carpellate flowers (see Sajo et al. 2007; Reinheimer & Kellogg 2009 for references). There is considerable variation in flower type in the family (see e.g. Le Roux & Kellogg 1999; Chuck 2010 for the development of unisexual flowers).

The caryopsis is often described as being the distinctive fruit type of Poaceae; it is a variant of an achene in which the testa and pericarp are fused. However, the fruit proper is rarely the dispersal unit (but c.f. the fleshy-fruited Alvimia - Bambusoideae), and there is a variety of diaspores and dispersal mechanisms in the family (e.g. Werker 1997). Dispersal is quite often by animals, attracted by structures like elaiosomes (Davidse 1987), while a variety of hooks and spikes attach other diaspores to passing animals (Centotheca is a good example). Wind-dispersal is quite common, for example, Andropogon has long hairs on the awns, while Spinifex and a few other genera are tumbleweeds. Awns can aid in both wind and animal dispersal, while the surface microstructure on awns, minute retrose bristles, may cause the achene to become "planted" in the ground (Elbaum et al. 2007; Humphreys et al. 2010b) or to move along the surface (Kulic et al. 2009; see also Davidse 1987). This is by a ratchet principle similar to that which operates when you put an entire inflorescence of Hordeum up your sleeve and you walk along; the inflorescence migrates up your arm and sometimes also down your back. Despite the apparent advantages of having an awn, this has been lost several times in Danthonioideae, at least, perhaps in association with the adoption of the annual habit where passive burial of seeds suffices (Humphreys et al. 2010b).

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

Vegetative Variation. Woody bamboos, for example Chusquea, may have a hundred or so branches at a node, borne in a fan-like arrangement. They are produced by a combination of multiple buds and axillary shoots with very short internodes, all nodes producing branches (see e.g. McClure 1973; Judziewicz et al. 1999; Tyrrell et al. 2012).

Genes & Genomes. Genome evolution in Poaceae has been particularly active. Comparisons of expressed sequence tags, etc., suggest that the genomes of Poaceae are much more different from the genome of Allium (Asparagales-Asparagaceae-Allioideae) than the genome of Allium is from that of Arabidopsis (Brassicales-Brassicaceae: Kuhl et al. 2004).

As in other groups, genome duplication is thought to have played a major role in the evolution of the family. A duplication of the whole genome in a clade that includes at least Zea, Oryza, Hordeum and Sorghum, i.e. the PACMAD/BEP clade, has been dated to ca 70/70-66/70-50/73-56/50-40 m.y. (Goff et al. 2002; Paterson et al. 2004; X. Wang et al. 2005; Schlueter et al. 2004; International Brachypodium Initiative 2010). Yockteng et al. (2013) date duplication of SEPALLATA genes here to around 82-58.2 m.y.. Although Vandepoele et al. (2003) think that this may be an aneuploidy event, duplication of the whole genome is the favoured hypothesis, with x = 5 -> x = 10 (polyploidy) -> x = 12 (two interchromosomal translocations and fusions) in the ancestor of the PACMAD/BEP clade, with much subsequent rearrangement, chromosome number reduction, etc. (Bennetzen 2007; Salse et al. 2008, 2009a, b; Bolot et al. 2009; Abrouk et al. 2010; Murat et al. 2010). (Hilu [2004] suggested that the base chromosome number for the whole family might be x = 11.) X = 12 is still found in rice (Oryza), for example, while x = 10 in Panicoideae. Certainly one or more rounds of genome duplication have occurred, with subsequent independent reductions in chromosome numbers (Schnable et al. 2009; Abrouk et al. 2010 and references). Within Poöideae there have been independent reductions in chromosome number from n = 12, for example, Brachypodium has n = 5 (International Brachypodium Initiative 2010; Murat et al. 2010).

Soltis et al. (2009) suggested that diversification in Poaceae might be connected with this genome duplication, and the development of a cytosolic ADPglucose phosphorylase, perhaps unique to this clade, has been associated with it (Comparot-Moss & Denyer 2009), however, diversification of the groups including the cereals may have occurred ca 20 m.y. later (Paterson et al. 2004; c.f. International Brachypodium Initiative 2010). For a possible relationship between genus size, life form and polyploidy, see Hilu (2007).

Whatever the cause, there has been very extensive duplication of genes - API, AG and SEP families, but not genes of the AP3 lineage (Zahn et al. 2005a; see also Saski et al. 2007 for other duplications in the family). Malcomber and Kellogg (2005) suggest that there has been duplication of LOFSEP genes within Poaceae, while the duplication ofAP1/FUL gene, apparently in stem-group Poaceae, may be involved in the evolution of the spikelet (Preston & Kellogg 2006). Developmental gene duplication and subsequent functional divergence seem to have played a very important role in allowing the development of the baroque diversity of inflorescences in the family (Malcomber et al. 2006; Zanis 2007; see also Doust & Kellogg 2002; Reinheimer & Vegetti 2008). For the evolution of the NADP-malate dehydrogenase gene following its duplication, see Rondeau et al. (2005).

There are other important and more recent duplication events involving hybridization. Thus a genome duplication/hybridization in the ancestor of Zea has been dated to ca 4.8. m.y. (Swigonová et al. 2004) - the two ancestors may have diverged ca 11.9 (Swigonová et al. 2004) or 20.5 m.y.a. (Gaut & Doebley 1997). The over 500 species of temperate bamboos form a clade that is descended from an allotetraploid ancestor (Triplett et al. 2011). Z. Peng et al. (2013) suggest that genome dupication occurred in the ancestor of the giant bamboo Phyllostachys heterocycla (P. edulis) 11.5-7.7 m.y.a.. The complex relationships within Danthonioideae may be connected with extensive past hybridizations (Pirie et al. 2008, 2009).

There has been very substantial genome evolution in grasses, with that in Triticeae being particularly accelerated (Luo et al. 2009; see also Messing & Bennetzen 2008; Salse et al. 2009a). Indeed, Triticeae (Poöideae) are notorious for the extent and complexity of the reticulating relationships that they show (Jacob & Blattner 2006; G. Petersen et al. 2006a; Mason-Gamer 2008; Meimberg et al. 2009; Sun & Komatsuda 2010; Fan et al. 2013: Elymus s.l. and the Y genome; Martis et al. 2013: rye), subsequent polyploidy, chromosome duplication, genome re-arrangement and introgression complicating the picture. Many Triticeae have massive genomes in part because of changes in base chromosome number (Jakob et al. 2004). Winterfeld (2006) discussed cytogenetic evolution, mainly in Aveneae (= Poöeae). In general, genome size varies considerably and at least in part independently of chromosome number, both increasing and decreasing (Caetano-Anollés 2005; Smarda et al. 2008; Schnable et al. 2009).

There has also been substantial evolution in the chloroplast genome (Leseberg & Duvall 2009; Guisinger et al. 2010 for literature), although details on where on the tree (and so when) particular changes occurred await more extensive sampling in Poales and "basal" Poaceae; the rate of plastid evolution may have since slowed down. These rate changes are placed at the level of Poaceae as a whole above, although they might more correctly be put at the PACMAD/BEP node... Morris and Duvall (2010) discuss aspects of chloroplast genome evolutiom, focusing on Anomochloa. For a series of inversions in the single copy region and expansion of the inverted repeat at the single copy-inverted repeat boundary, see Hiratsuka et al. (1989) and Saski et al. (2007). For accD gene loss, see Katayama and Ogihara (1996), for deletions, etc., in the 3' end of the mat K gene, see Hilu & Alice (1999), for loss of introns in chloroplast genome, see Daniell et al. (2008) for references.

The mitochondrial coxII.i3 intron has developed a moveable element-like sequence (Albrizio et al. 1994), but there is a fair bit of variation in other monocots, too. Transposable elements, Mutator-like elements (MULEs), seem to have moved fairly recently by lateral transfer between rice, East Asian bamboos, and a number of Panicoideae-Andropogoneae (Diao et al. 2006), while Stowaway Miniature Inverted repeat Transposable Elements (MITEs) are common in the BEP clade, especially in Poöideae (Minaya et al. 2013).

Economic Importance. Glémin and Bataillon (2009) take a comparative viewpoint and look at how grasses in general have evolved under domestication. Sang (2008) noted that single genes are involved in a number of major morphological transitions in the domestication of grains, such as the development of non-shattering rhachises; the genes may be quite different in unrelated species.

Among the C₃ domesticates, several are Poöideae-Triticeae, which include important grain genera such as Triticum (wheat), Hordeum (barley) and Secale (rye) (see above for genome evolution in this group). Wheat (mostly Triticum aestivum - Poöideae), which provides one fifth of the calories eaten by humans, began to be domesticated ca 10,000 years ago; see Israel Journal of Plant Sciences 55(3-4). 2007, for an entry into the literature on domestication, also Fuller (2007), Baum et al. (2009: haploid genomes) and Carver (2009: general). Most domesticated forms are polyploid, and genome plasticity in connection with this polyploidy has been implicated of the success of wheat in cultivation (Dubcovsky & Dvorak 2007). For the domestication of barley (Hordeum vulgare), see Fuller (2007), Pourkheirrandish and Komatsuda (2007) and Azhaguvel and Komatsuda (2007).

Another major C₃ grain is rice. For a phylogeny of Oryzeae (Ehrhartoideae), 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).

Sorghum and Zea (Panicoideae) are among the important C₄ grain genera. The domestication of maize seems to have occurred in seasonal tropical forests in southwestern Mexico, perhaps the Balsas valley, some 8,700 years 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 the domestication of pearl millet (Pennisetum glaucum), see Fuller (2007), and for that of sorghum (Sorghum spp.), see Dillon et al. (2007). For the domestication of sugarcane (Saccharum officinarum) in New Guinea, see Dillon et al. (2007) - note that Sorghum bicolor and Saccharum officinarumcan be hybridized (e.g. Nair 1999).

Chemistry, Morphology, etc. Because of their great economic importance, many aspects of grass morphology, anatomy, cytology, etc., have been surveyed over the years. By no means all of these really useful early surveys are cited below, although most are easily traceable in the literature.

The primary cell wall hemicellulose and pectin polysaccharides of grasses are very different from those of other seed plants, both in overall composition and particularities of the composition of the xyloglucans (O'Neill & York 2003), and the polysaccharides are less branched than those elsewhere - but overall sampling is very poor. Hatfield et al. (2009) discuss acylation of lignin in grasses, and Boerjan et al. (2003) note that grasses in particular have a variety of minor lignin monomer units; p-coumarate units are usually terminal pendant units in grasses (Ralph 2009; see also Petrik et al. 2014). There is evidence that ADP-glucose pyrophosphorylase, involved in starch synthesis, is very largely present in the cytosol, not in the plastids, in the endosperm of members of the PACMAD/BEP clade in grasses. It occurs in plastids in the starch-storing organs of other seed plants, probably even including the starchy endosperm of other commelinid monocots, but the sampling here, too, is poor (Beckles et al. 2001; Comparot-Moss & Denyer 2009).

Whether or not the division resulting in the trichoblast/atrichoblast pair in roots is asymmetric (Poöideae) or not, and, if it is symmetric, whether or not subsequent development of the two cells is the same, both vary (Kim & Dolan 2011). The sampling is poor, with no species from the basal pectinations and only one species each in Ehrhartoideae and Bambusoideae examined (Row & Reeder 1957: exceptions are no longer so; Kim & Dolan 2011). Poaceae have a nodal vascular plexus (Arber 1919), but I have no idea as to its general distribution and significance. Microhair variation in the family is extensive and of some use in delimiting major groups (Liphschitz & Waisel 1974; Amarasinghe & Watson 1988, 1990; Liu et al. 2010; Oli et al. 2012). Ligule variation is also extensive: Anomochlooideae are sometimes described as lacking a ligule (Judziewicz & Clark 2008, q.v. for other characters), or the ligule is described as being a ring of hairs. The leaf blades of Neurolepis (Bambusoideae) may be up to 4 m long.

Pharus has a number of features in common with Anomochlooideae, perhaps because they are both plants of the forest floor (Sajo et al. 2007, 2012). Its numerous distinctive features need to be integrated with the tree, but whether other members of the subfamily are similar is unknown, and Puelioideae are also very poorly known (see also Judziewicz & Clark 2008; Kellogg 2013).

For inflorescence morphology, see Kellogg et al. (2013). The grass palea, which is often bicarinate, has often been interpreted as being prophyllar/bracteolar in nature, monocots commonly having bicarinate prophylls. However, in this scenario bracteoles would probably have had to be regained, since the immediate outgroups to Poaceae lack them.

For summaries of floral development in grasses, see Ciaffi et al. (2011); see also Rudall and Bateman (2004) and Ronse de Craene (2010). In early studies of gene expression, the palea and perhaps even lemma appeared to be calycine in nature while the lodicules were corolline (Ambrose et al. 2000); A-type genes are expressed in both the palea and lemma (Whipple & Schmidt 2006). General comparative morphology might suggest that the lemma is a bract and the palea represents two connate tepals of the outer whorl; if the lemma is a perianth member, then loss of bracts is an apomorphy for all or most of Poaceae. The tepaloid nature of the lodicules is relatively uncontroversial (see Sajo et al. 2007; Reinheimer & Kellogg 2009; Yoshida 2012).

Understanding the flowers of Streptochaeta and Anomochloa presents a challenge (see also Judziewicz & Soderstrom 1989). Flowers of Streptochaeta can be interpreted as having an outer perianth whorl of two (adaxial) members - c.f. the single, bicarinate palea (there are sometimes three members in this outer whorl), and an inner perianth whorl of three members - c.f. the lodicules. The three stamens common in grass flowers would then be those opposite the three members of the outer perianth whorl (see Whipple & Schmidt 2006; Preston et al. 2009; Reinheimer & Kellogg 2009 for further details). If Ecdeicoleaceae and Joinvilleaceae are sister taxa (Marchant & Briggs 2006) and given the likelihood that the flowers of Anomochloa are sui generis, the floral morphology of Streptochaeta may be plesiomorphic for the family, or aspects of it are apomorphies for the genus. Sajo et al. (2008) suggested that the flowers of Streptochaeta could be interpreted in more or less conventional terms, with a whorl of three rather coriaceous "bracts" being equivalent to lodicules and two adaxial "bracts" outside this perhaps representing the palea (although the structure interpreted as being a lemma was also adaxial...). Sajo et al. (2011, esp. 2012: floral structure assumed rather than demonstrated) described the flowers of Anomochloa as having glumes, palea and lemma (bracteoles, prophylls respctively), lodicules, etc.; there is basically a single carpel, although there are vascular traces to three. The flowers of Ecdeicolea in particular are notably monosymmetric, with the two adaxial tepals of the outer whorl larger and keeled, and comparable differentiation in the outer perianth whorl occurs in Xyridaceae (q.v.); these are likely to be parallelisms.

It is difficult to 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, straight ovules. Although ovules both with and without parietal tissue 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, i.e., the ovules are tenuinucellate. 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) suggested that the persistent part of the seed coat was tegmic, and he sometimes showed the exotegmen in particular as having quite large cells, or quite thick walls, during development.

Poaceae are noted for their well developed, lateral embryo with a scutellum, coleoptile, coleorhiza, and mesocotyl (Tillich 2007). The scutellum is the distinctively-shaped haustorial part of the single cotyledon of other monocots (= the haustorial cotyledonary hyperphyll if one wants to be technical), and the coleoptile is the sheathing base of the cotyledon, the scutellum and coleoptile originating on the same side of the embryo (Kaplan 1997: 1 ch. 5; Takacs et al. 2012). The mesocotyl could be an elongating nodal region or a structure that represents (part of) the hypocotylar region to which the cotyledonary stalk is adnate, while the coleorhiza may be part of the hypocotylar region. The "radicle" is endogenous in origin, and is a lateral root; Poaceae thus lack a radicle proper, and so are homorhizic... (Kaplan 1997: 1 ch. 4, 5). Alpha prolamin genes, involved in the synthesis of seed storage proteins, evolved in Panicoideae-Andropogoneae 26-21 m.y.a. (Xu & Messing 2008).

See Kellogg (2014) for a comprehensive account of the family. Arber (1934) remains a classic treatment, and Chase (1964) an introduction; see also the Grass Phylogeny Working Group (2001, 2011); McClure (1966) gives an account of bamboos (see also the Bamboo Phylogeny Group 2012b for a summary), Bell and Bryan (2008) a good general treatment of grass morphology.

For the occurrence of ergot alkaloids, see Gröger and Floss (1998), for cell wall composition; see Fincher (2009), for non-starch soluble storage polysaccharides in the seed and fructans in vegetative parts, see MacLeod and McCorquodale (1958) and Meier and Reid (1982), for anatomy, see Metcalfe (1960), for C₄ photosynthesis, see also Kellogg (1999), for phytoliths and their distribution, see Piperno and Pearsall (1998), Piperno and Sues (2005) and Piperno (2006). For inflorescence morphology and development, see Vegetti and Anton (1996), Vegetti and Weberling (1996 and references: classical approach), Perreta et al. (2009) and Thompson and Hake (2009), for floral/spikelet evolution, see Yuan et al. (2009) and Thompson et al. (2009), for aerial branching, Malahy and Doust (2009), for a quantitative analysis of the hitherto supposedly taxonomically rather uninformative pollen, see Mander et al. (2013), for the style of Triticum, see Li and You (1991), for embryo variation, see Reeder (1957), for proliferating antipodal cells, Anton and Cocucci (1984) and Wu et al. (2011), for endosperm and its development, see Olsen (2007) and Sabelli and Larkins (2009), and for the morphology of starch grains in the endosperm, see Shapter et al. (2008).

For general information on Bambusoideae, see Clark (1997), Judziewicz et al. (1999), and Judziewicz and Clark (2008), for foliar epidermis, see H.-Q. Yang et al. (2008a); for pollen in Chloridoideae, see Liu et al. (2004: not much variation). For Micrairoideae, see Sánchez-Ken et al. (2007).

Phylogeny. General. For overviews of the phylogeny of the family, see Kellogg (2000a, 2014) and the Grass Phylogeny Working Group (2001, 2011); Duvall et al. (2010) provide a preliminary tree based on whole chloroplast genomes, and Ruhfel et al. (2014) looked at the genomes of some 35 taxa, the general relationships they found being those discussed below. Zhang and Clark (2000) restricted the limits of Bambusoideae to those accepted here; most taxa in what is now the basal grade of Poaceae have been included in bamboos at one time or another. In a multi-gene study, Bouchenak-Khelladi et al. (2008) did not find strong evidence for the monophyly of Anomochlooideae, Streptochaetapossibly being sister to all other Poaceae; Micrairoideae might not be monophyletic, Isachne not having a fixed position; there was support for a sister relationship between Danthonioideae and Chloridoideae (see also Pirie et al. 2008); and Streptogyna might be sister to the whole PACCMAD clade - and it lacks the possible synapomorphies of that clade (Bouchenak-Khelladi et al. 2008; see also Bouchenak-Khelladi et al. 2009; Hisamoto et al. 2008). Relationships of the major clades within the PACCMAD (as it used to be called) and BEP clades were initially for the most part unclear. Thus the relationships of Poöideae (Hodkinson et al. 2007; Duvall et al. 2008a) and Ehrhartoideae (Cahoon et al. 2010, as Oryzoideae) are unclear in some analyses (see also Saarela & Graham 2010; c.f. Davis & Soreng 2008; Christin et al. 2008a: BEP clade paraphyletic and immediately basal to the PACCMAD clade). Relationships in the PACCMAD clade remained particularly difficult (Saarela & Graham 2010: sampling). However, the Grass Phylogeny Working Group II (2011) have found strong support for many of the relationships in the PACMAD (as it is now called) and BEP clades, although support for the first two branches in the PACMAD clade is still only weak.

Duvall et al. (2007) had found strong support for the BEP clade, albeit the taxon sampling was slight (see also Grass Phylogeny Working Group 2001); relationships between the three subfamilies were initially uncertain (e.g. Hisamoto et al. 2008). Peng et al. (2010: 43 genes, only 10 taxa) found strong support for the relationships [E [B + P]] (ML and Bayesian analyses) and even stronger support for the relationships [B [E + P]] (neighbour joining), but the analyses of Wu and Ge (2011: 76 genes, 22 taxa; see also Bouchenak-Khelladi et al. 2008; Kelchner & the Bamboo Phylogeny Group 2013) supported the former set of relationships, and these are followed here. However, Blaner et al. (2014) found that Brachelytrum moved outside Poöideae in analyses using nuclear rather than chloroplast data.

Panicoideae. For discussions of the relationships - close and becoming ever more entwined - between Panicoideae and the old Centothecoideae, see Duvall et al. (2008a) and especially Sánchez-Ken and Clark (2008); the two are to be combined (Sánchez-Ken & Clark 2010; Teerawatananon et al. 2012). For relationships within Paniceae, see Zuloaga et al. (2000), Gómez-Martínez and Culham (2000) and Morrone et al. (2010, esp. 2012), for the bristle clade of Paniceae, see Doust et al. (2007), and those withinPanicum itself, see Aliscioni et al. (2003) and Sede et al. (2008), within Pennisetum, in which Cenchrus is embedded, see Donadío et al. (2009) and Chemisquy et al. (2010), and within Setaria, see Kellogg et al. (2009); see also Sede et al. (2009) for two new genera. Salariato et al. (2010) examined relationships within Melinidae, particularly fromn the point of view of inflorescence evolution. Ng'uni et al. (2010) looked at relationships with Sorghum, and López and Morrone adjusted the limits of Axonopus. For the phylogeny of Andropogoneae, see Kellogg (2000c) and Mathews et al. (2002), and for that of Paspalum, basically monophyletic, see Rua et al. (2010). Finally, for more information on relationships within Panicoideae, including those of some of its constituent genera, see papers in Aliso 23: 503-562. 2008.

Chloridoideae. Peterson et al. (2009, 2010a, 2011) suggest that relationships are something like [Centropodieae ]]. Eragrostis and Sporobolus may be polyphyletic, while Muhlenbergia is paraphyletic, but there are a number of well supported (and with morphology, too) clades (Peterson et al. 2010b; Columbus et al. 2010); Leptochloa is polyphyletic (Peterson et al. 2012). For a morphological phylogenetic analysis of the subfamily, see Liu et al. (2005), for other relationships, see papers in Aliso 23: 565-614. 2008.

Danthonioideae. For a phylogeny of the Pentaschistis group, also character evolution there, see Galley & Linder (2007), for relationships in the subfamily as a whole, see Barker et al. (2007a), Pirie et al. (2008) and Cerros-Tlatilpa et al. (2011). Some relationships within Danthonioideae are reticulating (Pirie et al. 2008, 2009).

Ehrhartoideae. The relationships of Oryzeae have been much studied (Guo & Ge 2005; L. Tang et al. 2010 and references); for diversification within Oryza itself, see Zou et al. (2008). The position of Streptogyna remains unclear, but it may be close to Ehrhartoideae.

Bambusoideae. See the Bamboo Phylogeny Group (2012b) for a summary of phylogenetic work on the subfamily; Burke et al. (2012) looked at relationships and timings based on analysis of whole plastid genomes. Clark and Triplett (2006) discussed relationships within the subfamily, previously divided into the woody Bambuseae and the herbaceous Olyreae. The woody temperate bamboo group may be sister to the rest of the subfamily; the monotypic Buergersiochloa, from New Guinea, is sister to the rest of the herbaceous Olyreae, which are plants of the New World (e.g. Kellogg & Watson 1993; W. Zhang & Clark 2000; Bouchenak-Khelladi 2008). Sungkaew et al. (2009; five plastid genes; Kelchner & the Bamboo Phylogeny Group 2013) retrieved the relationships [Arundinarieae [Olyreae [Neotropical (strictly) Bambuseae + Paleotropical & Austral Bambuseae]]] and map the distributions of each of these groups. However, Kelchner and the Bamboo Phylogeny Group (2013) noted that the position of Olyreae in particular was not secure, and it might be sister to the rest of the subfamily. For a phylogeny of the woody bamboos, see Clark et al. (2008: resolution poor), of neotropical woody bamboos, see Clark et al. (2008) and Fisher et al. (2009), of palaeotropical woody bamboos, see H.-Q. Yang et al. (2008b: resolution o.k., baccate fruit arose in parallel), ofBambusa and its relatives, see J. B. Yang et al. (2010) and Goh et al. (2010), of Dendrocalamus, see Sungkaew et al. (2010), of temperate bamboos, see Peng et al. (2008), and of Bambuseae-Arthrostylidiinae, see Tyrrell et al. (2009, 2012). Disentangling relationships in Arundinarieae is proving difficult. Zeng et al. (2010) found rather little resolution despite sequencing ca 9,000 base pairs. The extent of the problem has been confirmed: The Phyllostachys clade that was recovered in plastid analyses was pulverised into 24 bits in nuclear gene analyses; hybridization is involved (Y.-X. Zhang et al. 2012; see also H.-M. Yang et al. 2013). For hybridization in the ancestor of temperate bamboos, see Triplett et al. (2011), and for hybridization in paleotropical bamboos, see Goh et al. (2013).

Poöideae. There are several papers on Poöideae in Aliso 23: 335-471. 2008; see also Soreng and Davis (2000) and Schneider et al. (2009) for relationships within the whole subfamily. For the ndhF gene, structural features of chloroplast and nuclear genomes, etc., and the phylogeny of Poöideae, see Davis and Soreng (2008). It is not certain the the duplication of the ß-amylase gene is an apomorphy here; one of the gene copies breaks down starch into fermentable sugars in the endosperm, while the other is more broadly expressed in the plant, as it is in other Poaceae (Mason-Gamer 2005). For relationships and morphology in Phaenospermateae (inc. Duthieae), see Schneider et al. (2011); Phaenosperma itself is a very distinct plant previously included in Bambusoideae. For a phylogeny of Poeae, which should now include Aveneae, see Grebenstein et al. (1998), Quintinar et al. (2007, also Döring et al. 2007; Soreng et al. 2007; Saarela et al. 2010, 2011; Gillespie & Soreng 2011), for that of Poa, see Gillespie and Soreng (2005), Gillespie et al. (2009) and Soreng et al. (2010, 2011). See also Gillespie et al. (2008, 2010) for relationships in Poinae, Quintanar et al. (2010) for those in Koeleriinae, Essi et al. (2008) for relationships around Briza, and Consaul et al. (2010) for polyploid speciation in Puccinellia. For a phylogeny of Stipeae, see Romaschenko et al. (2007, esp. 2008, 2009, 2010, 2011, 2012; Jacobs et al. 2008; Barkworth et al. 2008): Macrochloa may be sister to the rest of the tribe and there are parallel diversifications in the Old and New Worlds, so characters traditonally thought to be phylogenetically important appear not to be so. For New World Stipeae, see Ciadella et al. (2010: sampling). 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 m.y. A number of taxa show complex reticulating patterns of relationships; for those in Triticeae, see G. Petersen et al. (2006a), Mason-Gamer (2008), Sun and Komatsuda (2010) and Fan et al. (2013) and references. For the Anthoxanthum/Hierochloë (Phalarideae) problem, the resolution of which also depends on understanding patterns of hybridization, see Pimentel et al. (2013), while in Stipeae, Romaschenko et al. (2014) disentangled relationships in which old hybridization was again involved.

Classification. The Grass Phylogeny Working Group (2001: a few small taxa remained unplaced in subfamilies, 2011) outlined the basic classification of the family; there have been further changes in detail, but the main outline now seems clear. Watson and Dallwitz (1992b onwards) includes generic treatments, etc., and a more current account is to be found in Kellogg (2014).

Peterson et al. (2010) provide a detailed suprageneric classification of Chloridoideae (see also Columbus et al. 2010: Muhlenbergia; Peterson et al. 2012: Leptochloa and relatives, 2014: some Cynodonteae). Sánchez-Ken and Clark (2010) outline a tribal classification for Panicoideae s.l. (including Centothecoideae), while Morrone et al. (2012) provide a comprehensive classification of Paniceae and their immediate relatives. Setaria will have to be dismembered (Kellogg et al. 2009). Panicum itself is getting pulverized, perhaps overly much so (Lizarazu et al. 2014 and references); Panicum s.l. has about 500 species, s. str. ca 100 species, while Dicanthelium has about 55 species (Zuloaga et al. 2007). Cenchrus is to include Pennisetum (Chemisquy et al. 2010). Linder et al. (2010) offer a subfamilial classification of Danthonioideae; generic limits are difficult there and there has been some confusing hybridization (Pirie et al. 2009; Humphreys et al. 2010a).

For a suprageneric classification of Bambusoideae, see the Bamboo Phylogeny Group (2012a, b). Generic limits in Bambusoideae are proving especially problematic. For generic delimitation in the temperate bamboos, see Peng et al. (2008); the whole clade is descended from an allotetraploid ancestor, and, complicating the issue, there has been hybridization since (Triplett & Clark 2010; Triplett et al. 2011). There are also generic problems in Bambusoideae-Arundinarieae (Zeng et al. 2010) and -Bambuseae-Arthrostylidiinae (Tyrrell et al. 2009, 2012); Chusquea must include Neurolepis (Fisher et al. 2009).

Schneider et al. (2009) outlined tribal limits within Poöideae. For generic limits around Piptatherum, see Romaschenko et al. (2011). For a catalogue of New World Poöideae, see Soreng et al. (2003). Genera are certainly not monophyletic in Triticeae, but are based on different genome combinations that are (hopefully) correlated with morphological variation (Dewey 1984; Löve 1984); Barkworth (2000) summmarises the history of the classification of this group (see also Goncharov 2011 for taxonomic confusion in Triticum; Fan et al. 2013 for Elymus s.l.).

Apparently the earliest name for Chloridoideae was Chondrosoideae Link (Thorne & Reveal 2007), a sort of resurrection name - Googling it (as of 3.vii.2007) returned only Thorne and Reveal themselves, apparently the only people to have used it for some time, and about 42,100 returns for Chloridoideae. However, the name Chloridoideae has since been used by Reveal himself (2012). Chondrosoideae was clearly something of a false alarm, but priority is a very unhelpful tool in such situations.

Given all the ongoing work in the family, web-based lists are much to be desired, so Grassworld, which has just started up, may be preferred over GrassBase and the lists dependent on it like the World Checklist of Monocots. The need is to stay current with all the changes that are being proposed; Vorontsova and Simon (2012) estimated that 10-20% of the species names will need to have been changed by the time all the phylogenetic rearrangements going on in the family are complete. Here, as elsewhere, the temptation is to chip off small monophyletic taxa from a paraphyletic residue; synthesis will be needed.

Botanical Trivia. A typical sheep consumes more than 10kg of silica phytoliths per year (Baker et al. 1959), yet this may affect its teeth very little (Sanson et al. 2007).

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

References

Extracted from Angiosperm Phylogeny references compiled by Peter Stevens by BKS on 01 July 2014

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Amarasinghe, V., & Watson, L. 1988. Comparative ultrastructure of microhairs in grasses. Bot J. Linnean Society 98: 303-319.

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