Plant Syst Evol (2008) 275:245–255
DOI 10.1007/s00606-008-0080-5
ORIGINAL ARTICLE
Reproductive morphology of the early-divergent grass
Streptochaeta and its bearing on the homologies
of the grass spikelet
M. G. Sajo Æ H. M. Longhi-Wagner Æ
P. J. Rudall
Received: 30 November 2007 / Accepted: 21 July 2008 / Published online: 13 September 2008
Ó Springer-Verlag 2008
Abstract Reproductive morphology and development are
described in the Brazilian grass Streptochaeta spicata, in
order to assess the homologies of the characteristic grass
inflorescence, termed a spikelet, and other reproductive
organs. Streptochaeta possesses some features that are
commonly found in Poaceae, including a well-differentiated embryo. It also possesses some relatively unusual,
presumably derived features, such as non-plumose stigmas,
which indicate that it could be insect-pollinated. It shares
some features with other early-divergent grasses, such as
Pharus, which could represent plesiomorphic conditions
for grasses. The inflorescence unit in Streptochaeta has
been interpreted as a compound branching system or
pseudospikelet. The present data suggest that it is a highly
modified spikelet, with a modified flower borne either on a
different axis to the basal bracts (glumes) or on the same
axis as the basal bracts. The three bracts below the stamens
are interpreted as homologous to the lodicules. The
Streptochaeta spikelet could be considered as morphologically intermediate between the true spikelet of grasses and
reproductive units of close grass relatives.
M. G. Sajo
Depto de Botânica, IB, UNESP, C Postal 199,
Rio Claro, SP 13506-900, Brazil
H. M. Longhi-Wagner
Depto de Botânica, UFRGS, Avenida Bento Gonçalves 9500,
Porto Alegre, RS, Brazil
P. J. Rudall (&)
Jodrell Laboratory, Royal Botanic Gardens, Kew,
Richmond, Surrey TW9 3DS, UK
e-mail: p.rudall@kew.org
Keywords Caryopsis Grass flower Grass spikelet
Inflorescence Scutellum
Introduction
The grass family Poaceae (Gramineae) is arguably the most
species-rich and economically important of all plant families. The monophyly of Poaceae is clearly demonstrated by
the long branch that separates it from related taxa in
molecular cladistic analyses (Briggs et al. 2000; Bremer
2002; Michelangeli et al. 2003), and the family is easily
recognizable by numerous highly characteristic morphological features. In particular, most grasses share a
specialized bracteate partial inflorescence termed a spikelet, each spikelet containing one to many florets with a
reduced or absent perianth (Clifford 1987). The family was
traditionally divided into tribes and subfamilies based
mainly on spikelet morphology, but more recently the
Grass Phylogeny Working Group (GPWG 2001) provided
a synthetic reclassification of grasses based on a combined
phylogenetic analysis of both molecular and morphological
data, which has facilitated re-evaluation of the homologies
of the characteristic grass features. GPWG (2001) recognized 12 monophyletic subfamilies, and subsequently
Sanchez-Ken et al. (2007) added a further subfamily,
Micrairoideae. The three earliest-divergent lineages –
Anomochlooideae (Anomochloa and Streptochaeta), Pharoideae (Pharus) and Puelioideae (Puelia and Guadella) –
are all relatively species-poor, and were previously included in the former subfamily Bambusoideae.
In all grasses except Anomochlooideae, which is sister
to all other Poaceae, the typical spikelet consists of a series
of distichous bracts with the two basal (proximal) set
empty (the glumes) and one to many distal bracts (the
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lemmas). Each lemma subtends a contracted floral axis on
which is borne a palea, two to three lodicules, the
androecium and the gynoecium (Soreng and Davis 1998).
The grass spikelet has been compared with a transformed
stem axis with the glumes and lemmas representing modified leaf sheaths and the palea being a presumed prophyll
subtending each flower (Clifford 1987). The grass flower is
mostly interpreted as a monochlamydeous structure with
only one perianth whorl, the lodicules (Rowlee 1898;
Celakovský 1889; Arber 1929; Page 1951), though
Ambrose et al. (2000) revived a dichlamydeous interpretation suggesting that the palea and possibly also the
lemma have genetic features in common with the outer
perianth whorl.
The reproductive structures of Anomochlooideae are
highly atypical for Poaceae (Page 1951; Soderstrom 1981;
Judziewicz and Soderstrom 1989). Neither Anomochloa
nor Streptochaeta possesses structures that are clearly
homologous with glumes, lemmas, or paleas, and thus
neither can be described as possessing typical grass spikelets. Each partial inflorescence consist of solitary bisexual
flowers in Anomochloa and bisexual flowers isolated by
multiple bracts in Streptochaeta. Thus, in these two genera
the partial inflorescence is more commonly termed as
‘‘pseudospikelet’’ (Page 1951; Soderstrom 1981; Soreng
and Davis 1998) or a ‘‘spikelet-equivalent’’ (Judziewcz
et al. 1999). In both the genera, the absence of an identifiable palea makes flowers appear terminal on the main
sympodial axis rather than on lateral branches as in other
Poaceae, in which there is a palea in the proximal, adaxial
position on the branch, often interpreted as a prophyll
(Clayton 1990). The pseudospikelet could be interpreted
either as a synapomorphy of Anomochlooideae, or a
plesiomorphy of grasses that is retained in only these two
genera (Judziewicz and Soderstrom 1989).
Further questions remain about the homologies of the
floral organs. The occurrence of lodicules in flowers of
Anomochloa and Streptochaeta is controversial, because
the homologies of the fringe of hairs below the staminal
whorl in Anomochloa and the large, fleshy, lanceolate
bracts in this position in Streptochaeta are not clear
(Soreng and Davis 1998). However, the recent genetic
study of Whipple et al. (2007) with Streptochaeta and two
outgroups provides strong evidence that they are transformed inner tepals or lodicules. Reduction in stamen
number is common in grasses and their close allies, often
due to suppression of nonhomologous stamens (reviewed
by Rudall and Bateman 2004; Rudall et al. 2005). However, Streptochaeta possesses six stamens, as in most
monocots, which probably represents the plesiomorphic
condition in grasses. The ovary and style are unusual in
flowers of Anomochloa and Streptochaeta, and the three
stigmas of Streptochaeta are simple, contrary to the
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M. G. Sajo et al.
plumose condition present in most grasses (Soreng and
Davis 1998).
In this paper, we investigate the reproductive morphology and anatomy of Streptochaeta spicata Schrad. ex Nees,
a herbaceous grass that grows in shaded tropical forests in
Brazil, and one of only three species of Streptochaeta. We
evaluate the existing hypotheses on the homologies of the
Streptochaeta spikelet and floral organs, and compare the
development of anthers, ovary and ovules with those of
other grasses, in the context of ongoing comparative
studies on early-divergent grasses and their allies (Rudall
et al. 2005; Sajo et al. 2007).
Materials and methods
Material was collected from plants in their natural habitat
in Rio Grande do Sul, Brazil, by Hilda Longhi-Wagner.
Vouchers were deposited at the Herbário do Departamento
de Botânica da Universidade Federal do Rio Grande do Sul
(Streptochaeta spicata Schrad.: HLW 9371, 9372, 10087,
10097, 10234, ICN).
Flowers were fixed in formalin-acetic alcohol (FAA)
and stored in 70% ethanol. For light microscopy, flowers
were embedded in paraplast using standard methods (Johansen 1940) and serially sectioned at ca 13 lm thickness
using a rotary microtome. For light microscopy (LM),
sections were mounted onto microscope slides, stained in
safranin and Alcian blue, dehydrated through an ethanol
series to 100% ethanol, transferred to Histoclear, and
mounted in DPX mounting medium (distrene, with dibutyl
phthalate and xylene). Slides were examined using a Leica
DMLB photomicroscope fitted with a Zeiss Axiocam digital camera. For scanning electron microscope (SEM)
examination, fixed spikelets and florets were carefully
dissected in 70% ethanol and then dehydrated in an ethanol
series to 100% ethanol. Then they were dried at critical
point using a Bal-Tec 030 critical point dryer, mounted
onto pin stubs, coated with platinum using an Emitech
K550 sputter coater, and examined using a Hitachi cold
field emission SEM S-4700 at 2 kV.
Observations
Morphology of inflorescence and pseudospikelet
(or spikelet-equivalent)
In Streptochaeta spicata, the inflorescence axis bears several short-pedicellate pseudospikelets arranged more or
less spirally in a 2/5 phyllotaxy. The axis apex is covered
by a tuft of hairs and has an aborted bud in a subapical
position (Fig. 1a–c). Although some authors report the
Floral anatomy in Streptochaeta
247
pseudospikelet, with bract 1 on the left and bract 2 on the
right (Fig. 2d). Bract 3 lies laterally on the left, bract 4 is
adaxially placed, and bract 5 is more or less opposite to
bract 4 and overlapped by it on the right (Fig. 2d). None of
the five basal bracts have axillary buds in pseudospikelets
examined here.
Above the basal node there is a bractless internode
(Fig. 2f) containing four vascular bundles (Fig. 2d) supplying bracts 6–11, which are attached at the
pseudospikelet level that is here termed as the ‘‘flower
node’’ (Fig. 2f, k). At the flower node, bract 6 is on the
adaxial side of the spikelet-equivalent (in the opposite
sector to bract 5) with its back facing the inflorescence axis
(Fig. 2k, m); it bears an extensive awn that becomes
entangled in the hairs of the rachis apex (Fig. 1a, d). At
anthesis, pseudospikelets become entangled by their awns
to the rachis apex and are dispersed together. Bracts 7 and
8 form a whorl, with bract 7 overlaping bract 8 in the
opposite direction to bracts 4 and 5 (compare Fig. 2d and
k). These bracts (7–8) lie on the abaxial side of the
pseudospikelet opposite bract 6, to which they eventually
become basally fused during late development (Fig. 2m).
Above bracts 7–8, three bracts (9–11) form another whorl
and overlap each other to the left in a direction opposite to
bracts 7–8 (compare Fig. 2m and k). The last two whorls
(7–8 and 9–11) are spirally arranged, though the outer one
(7–8) presumably lacks a member.
All bracts at the flower node (6–11) are long (ca 1–2 cm)
and coriaceous, and supplied by many vascular bundles;
they form a hard, more or less tubular structure that surrounds the fertile organs. Fertile organs consist of six
stamens and a single ovary that bears a single solid style
and three non-plumose stigmas (Fig. 2j). Each stamen is
supplied by a single vascular bundle; the ovary bears three
vascular bundles that each pass into one of the stigmas
(Fig. 2l).
Contrary to some previous authors (see ‘‘Discussion’’)
we never found an ‘‘awned palea’’ (bracts 7–8), nor a
‘‘rudimentary palea bract’’ opposite bracts 7–8, nor an
‘‘extra bract’’ above and behind bracts 7–8.
Fig. 1 a SEM entire rachis with two young pseudospikelets and
sterile apical region. b SEM rachis apex with aborted bud in a
subapical position indicated by white arrow. c SEM subapical aborted
bud. d SEM young spikelet. Bracts 6–8 and basal bract 5 numbered
(see Fig. 2b, d). a awn, bb basal bracts. Scale a, d 1 mm; b, c 100 lm
presence of 12 bracts, all pseudospikelets examined here
consisted of 11 bracts that are similar in texture but differ
in size and shape. The pseudospikelet axis (below the basal
node) contains two vascular bundles (Fig. 2c). Bracts 1–5
(the basal bracts, sometimes interpreted as glumes) are
attached to a basal node (Figs. 1d, 2b, d). Bracts 1–2 are
smaller, scale-like and positioned on the adaxial side of the
Pseudospikelet ontogeny (Fig. 3)
The bracts of the basal node are relatively well-developed
at an early stage, while primordia are still initiating at the
flower node (Fig. 3d). At the flower node, bract 6 has a
long tip that will develop into the awn (Fig. 3d). Bracts 9–
11 develop after bracts 7–8, and are followed by the six
stamen primordia, which initiate simultaneously (Fig. 3a–
c). A single whorl of three carpel primordia is also visible
at this time. Bracts 6–11 rapidly enlarge and completely
enclose the reproductive structures (Fig. 3d). The bracts of
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Fig. 2 a. SEM mature spikelet. b SEM five basal bracts attached to
axis, numbered from inside outwards, as in d; remainder of
pseudospikelet removed. c Light micrograph (LM) of transverse
section of axis with two vascular bundles. d LM transverse section of
five basal bracts surrounding the remainder of pseudospikelet. e SEM
basal node. f LM of longitudinal section of pseudospikelet. g SEM
partially dissected developing inflorescence with bracts 7–8 just
starting to envelope reproductive parts. h SEM partially dissected
pseudospikelet showing stamen with short filaments surrounding
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M. G. Sajo et al.
style/stigmas. j SEM pseudospikelet with sterile bracts removed to
show six stamens surrounding style. k LM transverse section of
flower node. l LM transverse section of flower showing six anthers
surrounding solid style. m LM transverse section near the base of
anthetic flower showing bracts 6, 7 and 8 basally fused; bracts 9–11
surrounding ovary with a single ovule. a awn, an anther, bb basal
bracts, bn basal node, fn flower node, in internode, st style/stylodia
(all SEM, except LM in c, d, f, k–m). Scale a, b, e 1 mm, c–f, k–m
100 lm, g, h, j 500 lm
Floral anatomy in Streptochaeta
249
Fig. 3 Pseudospikelet ontogeny (SEM). a–c Successive developmental stages of flower ontogeny, showing six developing stamens
surrounding ovary with three stylodia. Central basal ovule just visible
in a. d Developing inflorescence. e, f Older stages of floral ontogeny
than in a–c. Bracts numbered as in text. s stamen. Scale 100 lm
the basal node grow minimally, whereas the bracts of the
flower node (6–11) grow extensively (Fig. 4b).
Stamen development (Fig. 4)
At early stages male and female parts develop synchronously. When microsporocytes are present inside the
anthers, an ovule primordium is initiating within the ovary
(Fig. 5d). However, the gynoecium enlarges before the
anthers, pushing the three stigmas outside the spikelet
when the anthers are still enclosed at the base (Figs. 2h,
3e–f). The anthers never hang free, as in most grasses.
When the anthers reach the spikelet top, an early fruit is
already developing. Initially, the stamen filaments are short
and free, keeping the anthers inside the spikelet even when
the pollen grains are mature inside the anthers; at this stage,
the three stigmas are outside the spikelet. The filaments
eventually twist together into a tube that elongates and
pushes the anthers to the top of the spikelet (Fig. 4a).
Fig. 4 a Dissected pseudospikelet with anthers just protruding. b
Mature spikelet. a anther, f fused filaments. Scale 1 mm
Ovary and ovule development (Figs. 5, 6)
The ovary is subsessile and fusiform. The ovary wall is of
approximately similar thickness throughout, though at the
point of attachment to the pedicel the ventral side is thicker
than the dorsal (Fig. 5g). The ovary wall consists of 7–8 cell
layers including the outer and inner epidermis (Fig. 5b).
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M. G. Sajo et al.
Fig. 5 Caryopsis development.
a SEM mature caryopsis in
dissected pseudospikelet. b LM
of longitudinal section of ovary
and ovule wall. c LM of
longitudinal section of caryopsis
wall. d LM of longitudinal
section of flower with young
ovule and stamen. e, f LM of
longitudinal section of embryo
sac and micropyle. g LM of
longitudinal section of ovule.
h LM of longitudinal section of
fruit with embryo. a anther, an
antipodals, e embryo, ii inner
integument, n nucellus, o ovule
wall, oi outer integument, ov
ovary wall, sy synergids. Scale
50 lm in a, d, e, g, h; 20 lm in
b, c; 100 lm in f
The single ovule arises in the basal position of the locule
(Fig. 3a) but further growth leads to its curvature, becoming
hemianatropous with its funiculus fused to the dorsal carpel
wall (Fig. 5d). Subsequently, the ovule undergoes gradual
curvature towards the base of the ovary, becoming anatropous at the megagametophyte stage (Fig. 5g). Following
megagametophyte formation, the nucellus enlarges, especially at the chalazal region, where it is massive (Fig. 5g).
At this stage, the region of ovular attachment to the placenta
is more than three-quarters the length of the ovule, and there
is no well-defined funiculus. Both integuments are initiated
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simultaneously (Fig. 5d) and extend beyond the nucellus,
though only the inner integument forms the micropyle
(Fig. 5e). Both integuments are mostly two-layered, though
the outer one becomes two to four-layered on the ventral
side and five-layered at the chalazal end (Fig. 5g).
Inside the ovule primordium, a hypodermal archesporial
cell gives rise directly to the megasporocyte without cutting off parietal cell (the tenuinucellate condition). The
megasporocyte undergoes meiosis to form a tetrad of megaspores. The functional chalazal megaspore develops into
a seven-celled, eight-nucleate megagametophyte with a
Floral anatomy in Streptochaeta
Fig. 6 a SEM mature embryo. b LS mature embryo (LM). c
coleoptile, sc scutellum. Scale 100 lm
globular egg cell, two pear-shaped synergid cells with filiform apparatus (Fig. 5e, f), three antipodal cells (Fig. 5f),
and a central cell with two polar nuclei.
Following fertilization, the primary endosperm nucleus
divides earlier than the zygote (Fig. 5f), and endosperm
development conforms to the ‘‘Nuclear type’’. In the mature
caryopsis the endosperm is large and the embryo is small,
with an extensive free scutellum (Fig. 5h). Both cell layers
of the outer integument and the outer cell layer of the inner
integument become disorganized as the caryopsis enlarges.
The cells of the inner layer of the inner integument enlarge
anticlinally and show deposition of a densely staining
material (Fig. 5c). As the caryopsis enlarges, these cells
become sclerified first at the micropylar region and subsequently all round the seed. Both the outer and the inner
pericarp epidermis remain intact and the cells of its median
layers enlarge periclinally, resulting in a multi-layered tissue that together with the epidermal cells covers the seed
coat, which is formed only by the inner layer of the inner
integument (Fig. 5b–c). The mature caryopsis is enveloped
by the coriaceous lemma, paleas and lodicules (Fig. 5a).
The mature embryo is about one-seventh the length of the
caryopsis and has a large scutellum (Fig. 6). The vascular
supply to the scutellum and embryonic leaves diverges from
the common point and there is no epiblast. The coleoptile is a
conical structure and posses a small opening on the side
away from the scutellum and a small slit on opposite side.
Discussion
Inflorescence and pseudospikelet
morphology – a revised interpretation
Morphologists such as Celakovský (1889), Arber (1929),
Page (1951) and Soderstrom (1981) have postulated
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different hypotheses to interpret the Streptochaeta spikelet
(Fig. 7). Both Arber (1929) and Page (1951) reported
axillary buds on bracts 1–5 (those attached to the basal
node), and concluded that these bracts are fertile and
homologous with the awned bract 6 (the lemma). Page
(1951) also reported a ‘‘rudimentary palea bract’’ opposite
the paleas (bracts 7–8). In two spikelets she found paleas
with a short curled awn, and interpreted these structures as
modified lemmas. She also reported an ‘‘extra bract’’ above
and behind the paleas (bracts 7–8), and regarded the lodicules as homologous to the inner perianth of the flower, a
view later supported by Whipple et al. (2007). Thus, Page
(1951) interpreted the Streptochaeta spikelet as possessing
a basal branch with six potentially fertile bracts. Of these,
bract 6 (the awned bract) subtends a branch that could be
either (1) a complete flower without the anterior member of
the outer perianth (represented by the ‘‘rudimentary palea
bract’’) with the ‘‘extra bract’’ representing either a lemma
or a prophyll (Fig. 7a), or (2) a branch with two sterile
bracts (the paleas, which she reinterpreted as lemmas,
including the ‘‘rudimentary palea bract’’) and a flower
lacking the outer perianth, lemma and prophyll. In this
case, the ‘‘extra bract’’ would be homologous to the lemma
and the spikelet would represent a reduced compound
branching system (Fig. 7b).
Based primarily on Page’s (1951) observations, Soderstrom (1981) agreed that the Streptochaeta spikelet
possesses five fertile bracts that are homologous to each
other and to bract 6 (the lemma), and that bracts 7–8 (the
paleas) and ‘‘the rudimentary palea bract’’ (bract 9) are on a
different axis from bracts 1–6 and bracts 10–12. Assuming
that the branching pattern repeats itself, he suggested that a
flower lacking a perianth is on a different axis subtended by
bract 12; the floral axis would be protected by bracts 10–
12, and the prophyll (palea) and lodicules have been lost
during evolution. Thus, Soderstrom (1981, page 41) interpreted the Streptochaeta spikelet as a ‘‘highly modified
branching system made up of three orders of pseudospikelet’’ (Fig. 7c).
However, contrary to the observations of Arber (1929)
and Page (1951) on the same species – Streptochaeta spicata, we found no axillary buds in the five basal bracts in
any pseudospikelets. Thus, we found no evidence to support the basal node as an inflorescence branch. Also
contrary to Page’s (1951) description, we did not find a
‘‘rudimentary palea bract’’, nor an ‘‘extra bract’’, nor an
awned palea (bracts 7–8) in any spikelets. It is difficult to
explain this significant discrepancy. Page (1951) observed
material from 12 greenhouse-grown plants, of which six
originated from a single collection and the other six from
seeds produced by the first group; thus, the different
structures that she observed could have resulted from an
inherited teratology, possibly representing natural
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M. G. Sajo et al.
Fig. 7 Different interpretations
of Streptochaeta pseudospikelet
(see text). a, b Page (1951)
described several features that
were not observed here,
including axillary buds on
bracts 1–5, a ‘‘rudimentary
palea bract’’ (rpb) opposite
bracts 7–8, an ‘‘extra bract’’
above bracts 7–8 and awned
bracts 7–8. She interpreted bract
6 as subtending either a a
complete flower without the
anterior member of the outer
perianth (represented by the
rpb), or b a branch with two
sterile bracts (including the rpb)
and a flower. c. Soderstrom
(1981) proposed that a flower
lacking a perianth is in a
different axis subtended by
bract 12. d, e. Our observations
suggest two further
interpretations, in both of which
bracts 1–5 of the basal node
represent glumes. d A modified
flower is borne on a different
axis to the basal bracts, in the
axil of bract 6 (the awned one).
Bracts 7–8 represent the outer
perianth with a missing
member, and bracts 9–11
represent the inner perianth.
This agrees with Celakovsky’s
(1889) interpretation. e As in d,
except the flower is borne on the
same axis as the basal bracts,
but on a different node. rpb
rudimentary palea bract
variation. Our wild-collected material from several distantly located plants lacked such ‘‘abnormal’’ structures.
Furthermore, we found no pseudospikelets with more than
11 bracts, despite reports of 12 bracts by some authors
(Judziewicz et al. 1999; Whipple and Schmidt 2006;
Whipple et al. 2007).
Our observations show that bract 6 (the awned bract)
belongs, together with bracts 7–11, to a different node from
the basal bracts (1–5), and is irrigated by the same vascular
complex as the reproductive parts. Regarding ovule
attachment, bract 6 always lies opposite the free side of the
ovule, like the lemma in other grasses, though bract 6 is
adaxial, contrary to the abaxial lemma of other grasses. In
contrast to a ‘‘true’’ grass spikelet, with a single palea on
the same side of the ovule attachment, the Streptochaeta
pseudospikelet has two bracts in this position (bracts 7–8).
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Although with a missing adaxial member, bracts 7–8
overlap each other in a clockwise spiral that lies in the
opposite direction to the basal node bracts 4–5. Above
bracts 7–8, bracts 9–11 also form a whorl overlapping each
other in a counter-clockwise direction. The same arrangement (spirally overlapping whorls) of bracts 7–8 and 9–11
(in the same spiral) suggests that these two alternating
cycles are borne on a different branch to the basal bracts
(1–5), and lie in the axil of bract 6, though earlier ontogenetic stages are necessary to confirm this.
Our results suggest two further interpretations for the
Streptochaeta pseudospikelet. In both the cases, bracts 1–5
of the basal node represent glumes; they are empty as are
the glumes of grasses. (1) The Streptochaeta pseudospikelet contains a modified flower that is borne on a different
axis to the basal bracts (1–5), in the axil of a lemma (the
Floral anatomy in Streptochaeta
awned bract 6). Bracts 7–8 represent the outer perianth
with a missing member, and bracts 9–11 represent the inner
perianth (Fig. 7d). (2) Alternatively, the Streptochaeta
pseudospikelet contains a modified flower that is borne on
the same axis as the basal bracts (1–5), but on a different
node. Bracts 6–8 representing the outer perianth members,
and bracts 9–11 the inner perianth members (Fig. 7e). In
both the cases the abaxial prophyll is missing.
Our first (preferred) model (Fig. 7d) agrees with Celakovský’s (1889) interpretation of the Streptochaeta
spikelet. The second (Fig. 7e) agrees with Ambrose et al.’s
(2000) interpretation of the grass lodicules as modified
petals, and paleas and lemma as modified sepals. In either
case, the Streptochaeta pseudospikelet is not a compound
structure and cannot be termed a pseudospikelet as defined
by Soderstrom (1981). Our interpretations of the Streptochaeta pseudospikelet are consistent with derivation of the
grass flower from an ancestral monocot flower with a perianth containing two whorls of tepals, perhaps similar to the
perianths of Joinvillea or Ecdeiocolea (Rudall et al. 2005),
though this became highly modified with the origin of
grasses (Zanis 2007). The highly condensed grass spikelet
compares with the condensed pseudanthial inflorescences of
other anemophilous Poales (Linder and Rudall 2005).
Bracts 7–8 were interpreted as halves of a single structure (the paleas) by Arber (1929). However, they originate
from different primordia and are supplied by separate
vasculature, though they eventually fuse to each other and
to the lemma at later developmental stages. Paleas and
lemmas are novel structures found only in grasses and have
been interpreted as sepals or prophylls (Clifford 1987),
though their homology to leaves, bracts, or perianth organs
in other monocots remains uncertain (Arber 1929; Cocucci
and Anton 1988; Rudall et al. 2005; Zanis 2007).
Contrary to most grasses, in which the lodicules are
scalelike and function in opening up the floret (Clayton and
Renvoize 1986), in Streptochaeta there are three coriaceous structures in the position of the lodicules. We
interpret these as homologous to the inner tepals, in
agreement with the Whipple et al. (2007)’s data, and with
the interpretation postulated for different grasses (Celakovský 1889; Rowlee 1898; Arber 1929; Page 1951;
Judziewicz and Soderstrom 1989; Ambrose et al. 2000;
Rudall et al. 2005). We interpret the basal bracts of the
Streptochaeta spikelet as glumes. The term ‘‘glume’’ is
defined as a sterile bract at the base of the spikelet (GPWG
2001), and interpreted as a modified leaf sheath. Most
grasses bear only two glumes, being abaxial, adaxial or
lateral according to the grass group. In Streptochaeta there
are five glumes spirally arranged on the basal node of the
spikelet, the first two being attached adaxially.
The inflorescence of Streptochaeta is determinate as in
other grasses (Kellogg 2001). Its axis bears an aborted bud
253
that is probably subapical, though we cannot rule out the
possibility that it is a displaced apical bud. The Streptochaeta inflorescence probably originates in the same way as
the inflorescence of Andropogoneae – Coelorachis aurita
and Heteropogon contortus (Le Roux and Kellogg 1999), in
which the inflorescence meristem gives rise to a single axis.
However, spikelet development in Streptochaeta does not
entirely conform to the patterns in Andropogoneae (Le
Roux and Kellogg 1999) or Pharus (Sajo et al. 2007), in
which the glumes are very young when the reproductive
parts are initiated. In Streptochaeta the glumes (bracts 1–5)
are completely formed at this stage.
Gynoecium morphology
The ovary of Streptochaeta closely resembles that of other
grasses, including the early-divergent grass Pharus, in
possessing a unilocular ovary supplied by three vascular
bundles (Sajo et al. 2007). In both Streptochaeta and
Pharus the ovary is initiated as three separate primordia,
thus supporting Philipson’s (1985) conclusion that the
grass gynoecium is pseudomonocarpellary. However,
Streptochaeta differs from Pharus in possessing a ‘‘solid’’
style with a stylar transmitting tissue, as in many other
grasses (e.g. Arber 1934; Li and You 1991), rather than a
‘‘hollow’’ style as in Pharus and many other Poales,
including Ecdeiocolea (Rudall et al. 2005). Since solid
styles are relatively uncommon in Poales (though present
in Flagellaria; Rudall, personal observation), the presence
of a solid style could be a significant synapomorphy for
grasses, though optimization could be ambiguous at the
basal node.
Ovule and embryo sac
The length of ovule integuments varies between different
species of Poaceae. In Streptochaeta both the integuments
grow beyond the nucellus but only the inner forms the
micropyle, whereas in some Bambusoideae and Ehrhartoideae the outer integument encloses at most two-thirds of
the ovule (Bhanwra 1988; Bhanwra et al. 2001). Unitegmic
and ategmic ovules occur in some Bambusoideae (Hari
Gopal and Mohan Ram 1987). In Streptochaeta, the outer
integument degenerates after fertilization, and the inner
layer of the inner integument shows deposition of darkstaining material, as in Pharus (Sajo et al. 2007) and some
Arundinoideae, Pooideae, and Chloridoideae (Bhanwra
1988). This layer produces a mechanical coat as the caryopsis develops.
As in the early-divergent grass Pharus (Sajo et al. 2007),
the ovule is basal at early stages, and becomes anatropous
at the megagametophyte stage. It is tenuinucellate, as in
many other Poaceae and Poales (Aulbach-Smith and Herr
123
254
1984; Rudall 1997; Sajo et al. 2004) and the nucellus
epidermis on the micropylar region undergoes periclinal
divisions, as described for some grasses (Bhanwra et al.
1991, 2001). Streptochaeta also possess the plesiomorphic
condition of three antipodals, in contrast to many other
grasses, in which antipodals are proliferated.
Embryo and endosperm
The highly differentiated grass embryo possesses a prominent outgrowth termed a scutellum, which is normally
interpreted as a modified cotyledon (Fig. 6). The scutellum
is apparently unique to grasses, and is absent from related
taxa such as Ecdeiocolea (Rudall et al. 2005). All grasses
possess a scutellum, including other early-divergent taxa
such as Anomochloa (Judziewicz and Soderstrom 1989)
and Pharus (Sajo et al. 2007). In Streptochaeta the embryo
is highly differentiated, and possesses a small cleft between
the scutellum and the coleorhiza but lacks a distinct epiblast, as in the panicoid embryo type in Reeder’s (1957)
classification. However, there is no distinct elongation
between the point of divergence of the scutellum bundle
and the coleoptile, so in this respect it resembles Reeder’s
(1957) festucoid embryo type. The coleoptile possesses a
small opening on the side away from the scutellum and a
small slit on the opposite side (Fig. 6). The first opening is
probably the point through which the first leaf of the plumule protrudes at germination. The second opening could
represent the marginal attachment of the coleoptile, though
Reeder (1953) suggested that the coleoptile is not closed,
and homologised it to a leaf.
Conclusions
Streptochaeta possesses some features that are commonly
found in Poaceae, such as a female gametophyte of the
Polygonum type, nuclear endosperm and a well-differentiated embryo, and also some unusual (presumably derived)
features. For example, in contrast to most wind-pollinated
grasses, which have a reduced perianth and plumose stigmas, Streptochaeta possesses non-plumose stigmas,
suggesting that it could be insect-pollinated, as suggested
by Soderstrom and Calderón (1971) for some other tropical
herbaceous grasses. The stamens mature before the
gynoecium in most Poales, contrasting with the protogynous condition in Streptochaeta.
Streptochaeta also shares some features with Pharus
(Sajo et al. 2007), perhaps representing the plesiomorphic
conditions in these early-divergent grasses. For example,
the gynoecium in Streptochaeta initiates as three primordial
carpels, and is therefore clearly a pseudomonocarpellary
structure, as in Pharus, supporting the hypothesis that even
123
M. G. Sajo et al.
when monolocular at maturity, the gynoecium of some
grasses retains features of a tricarpellary ancestry (Philipson
1985; Rudall et al. 2005), though this feature is difficult to
distinguish in some relatively derived grasses (Maze et al.
1971, Le Roux and Kellogg 1999). The basal position of the
ovule early in ontogeny in Streptochaeta is unusual within
Poaceae, but resembles the condition in Pharus.
Finally, Streptochaeta differs from other grasses in that
its inflorescence unit lacks structures clearly homologous
to glumes, lemma and palea, and is commonly interpreted
as a compound branching system or pseudospikelet (Page
1951; Soderstrom 1981). We found no evidence supporting
Page and Soderstrom’s interpretation, and regard the
Streptochaeta unit as a spikelet, as in other grasses,
although it is highly modified. It could represent either a
modified flower on the same axis as the basal bracts
(glumes), or a modified flower on a different axis to the
glumes. The spikelet in Streptochaeta and Anomochloa has
been described as lacking lodicules and petals (Soderstrom
1981; Soreng and Davis 1998; GPWG 2001; Kellogg 2001;
Zanis 2007), but we agree with the interpretation of
Whipple and Schmidt (2006) and Whipple et al. (2007) that
the three bracts below the stamens are homologous to the
lodicules and correspond to the inner tepal whorl of outgroups. In Anomochloa, a ring of hairs in the position of the
lodicules could represent modified lodicules (Arber 1929),
though more detailed study of its spikelet is needed to
clarify this controversial interpretation. The Streptochaeta
spikelet possesses two bracts below the lodicules (or inner
tepals), and in the same arrangement as them. These two
bracts (7–8) together with the awned bract 6 could represent an outer tepal whorl, in which case fusion of bracts 7–
8 would produce the single palea typical of a true grass
spikelet. In this respect the Streptochaeta spikelet could be
considered as morphologically intermediate between the
true spikelets of grasses and reproductive units of close
grass relatives.
Acknowledgments We thank two anonymous reviewers for their
detailed comments on the manuscript. MGS acknowledges funding
from the Kew Latin American Fellowship Program and the Royal
Society to support her visit to the Jodrell Laboratory, Royal Botanic
Gardens, Kew, where this research was carried out. Both MGS and
HLW received a fellowship from CNPq, which is gratefully
acknowledged.
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