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Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138-2020
Received for publication December 29, 1997. Accepted for publication August 18, 1998.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: andromonoecy • Andropogoneae • floral development • maize • monoecy • Poaceae • Tripsacum • unisexuality
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Unisexual flowers do not develop the same way in all angiosperms. In some species, both stamen and gynoecial primordia are initiated and then arrested at different stages of development. This mechanism applies in legumes (Tucker, 1992
), Asparagus officinalis L. (Bracale et al., 1991
) and Silene L. (campion, also referred to as =Melandrium Roehl; Ye et al., 1991
), Zea L. (maize), and Tripsacum L. (De Long, Calderón-Urrea, and Dellaporta, 1993
; Dellaporta and Calderón-Urrea, 1994
; Li et al., 1997
). In other species, one or the other sex organ is never initiated. For example, in female flowers of Cannabis sativa L. (Mohan Ram and Nath, 1964
) and in both male and female flowers of the dioecious Mercurialis annua L. (Durand and Durand, 1991
), Spinacia oleracea L. (Sherry, Eckard, and Lord, 1993
), Rumex acetosella L. (Ainsworth et al., 1995
), and Philodendron acutatum Schott (Boubes and Barabé, 1996
) either gynoecial or stamen primordia are initiated, but not both.
Unisexual species have evolved various ways of distributing the unisexual flowers on the plant. Staminate and pistillate flowers can be borne on the same (monoecious) or different (dioecious) plants. Many intermediate forms occur; for example, bisexual and female or male flowers can be produced on the same plant, conditions known as gyno- or andromonoecy, respectively. Where bisexual and male or female plants result, the conditions are known as gyno- or androdioecy (Richards, 1986
). The formation of unisexual flowers is thought to have evolved to promote out-crossing (allogamy) (Stebbins, 1957
) and has evolved independently in many plant species.
Floral development in the monoecious grass Zea mays L. has been studied extensively (Cheng, Greyson, and Walden, 1983
; Sundberg and Orr, 1996
). As in all other grasses, the flowers, or florets, are arranged in spikelets, with each spikelet subtended by a pair of glumes. Maize is a member of the subfamily Panicoideae, in which all spikelets contain two and only two florets. Although most panicoids are either hermaphroditic or andromonoecious, maize is monoecious with unisexual florets borne on separate tassel (staminate) and ear (pistillate) inflorescences. The two florets in each tassel spikelet are staminate. Although the two florets in each ear spikelet are female, the proximal floret aborts during development so that at maturity the ear spikelets contain only one floret each. All floral meristems initiate all floral organs, including stamens and gynoecia. The stamen primordia then cease growth in pistillate (ear) florets, whereas gynoecium development is arrested in staminate (tassel) florets.
The formation of unisexual flowers from a bisexual meristem requires the action of sex determination genes (Dellaporta and Calderón-Urrea, 1993
). Genetic studies in maize have shown that the tasselseed (Ts1, Ts2, and ts5) genes are required for gynoecial abortion (Dellaporta and Calderón-Urrea, 1993
; Irish, Langdale, and Nelson, 1994
; Dellaporta and Calderón-Urrea, 1994
) When ts1 and ts2 are mutated, a complete sex reversal in tassels occurs, causing pistils to develop while stamens are suppressed (Veit et al., 1993
; Irish, Langdale, and Nelson, 1994
; Irish, 1996
, 1997
). The hormone gibberellin is apparently the primary signal that stimulates stamen arrest in ears and possibly mediates stamen suppression in feminized tassels of tasselseed mutants (Irish, 1996
). Genes involved in the gibberellin pathway, such as anther ear and dwarf genes, confer female function, leading to stamen suppression in ear spikelets. When these genes are mutated, stamens develop in ear spikelets (Irish, Langdale, and Nelson, 1994
).
The maize gene tasselseed2 (ts2), orthologous to the gene gynomonoecious sexform1 (gsf1) in Tripsacum dactyloides (Li et al., 1997
), is the only sex-determination gene cloned to date (De Long, Calderón-Urrea, and Dellaporta, 1993
). It encodes a short-chain alcohol dehydrogenase, possibly using gibberellin or a steroid-like molecule as a substrate (De Long, Calderón-Urrea, and Dellaporta, 1993
; Irish, 1996
). The gene product appears directly or indirectly to induce cell death leading to organ abortion. In the gynoecium of the wild-type staminate (tassel) florets, TS2 is expressed as the gynoecium forms a gynoecial ridge (De Long, Calderón-Urrea, and Dellaporta, 1993
). This correlates with cessation of gynoecial development and also with breakdown of nuclei in subepidermal cells (Calderón-Urrea, 1996
). This developmental pattern has been found in both Zea and its sister genus Tripsacum (Li et al., 1997
), which is also monoecious.
Zea and Tripsacum are two of 
100 genera in the tribe Andropogoneae, a tribe that makes up about half of the grass subfamily Panicoideae. Throughout the subfamily, the spikelets are two flowered. The proximal floret is consistently reduced and at anthesis is either sterile or male, whereas the distal floret is generally hermaphroditic. This unique spikelet structure was thought to be evidence of the monophyly of the subfamily (Kellogg and Campbell, 1987
), a hypothesis that has been supported by every molecular phylogenetic study to date (summarized by Kellogg, 1998
). Within this monophyletic subfamily, the Andropogoneae are also monophyletic based on phylogenetic analysis of morphological data (Kellogg and Watson, 1993
), and sequence data from granule-bound starch synthase I (GBSSI; Mason-Gamer, Weil, and Kellogg, 1998
) and NADH dehydrogenase (ndhF; R. E. Spangler, B. Zaitchick, E. T. Russo, and E.A. Kellogg, unpublished data, Harvard University). All members of the tribe share not only the characteristic paired florets of the subfamily, but also paired spikelets, with one spikelet sessile and the other pedicellate (Fig. 1). The two spikelets, each with two florets, define a set of four florets; these may differ in their development and in their sex expression (Fig. 2). In most Andropogoneae the distal floret of the sessile spikelet is hermaphroditic, whereas the proximal floret is sterile; this appears to be the derived condition in the tribe (B. Zaitchik, unpublished data, Harvard University). Most commonly in these species, the distal floret of the pedicellate spikelet is male and the proximal floret is sterile, making the entire plant andromonoecious.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Several plants were studied per accession. Multiple inflorescences per plant (minimum of ten, often more) were fixed for scanning electron microscopy (SEM) or embedding. These covered a range of developmental stages. To determine the length of anthers and aborting gynoecia of Bothriochloa bladhii, measurements were made from microscopic slides of sectioned material, while the anther length of all other studied species was determined by measuring whole anthers under a dissecting microscope. Five samples were measured per species.
Developing inflorescences were dissected and fixed for 12 h in 4% paraformaldehyde in phosphate-buffered saline (PBS), pH 7.0. Tissue was stored at 4°C in 70% ethanol. For paraffin wax embedding, material was dehydrated in an alcohol series and replaced by an ethanol: Hemo De (Fisher) series before being infiltrated with paraffin wax kept at 59°C. Wax blocks were cooled on ice and sectioned at 6–7 µm. Slides were stained in aqueous 0.1% toluidine blue. To determine whether cell death or nuclear abortion occurred during the formation of unisexual spikelets a 0.01% DNA-specific fluorochrome 4'6 Diamidino-2-phenylindole (DAPI) was used (Vergne et al., 1987). The stained material was studied and photographed using an Olympus BX60 microscope fitted with epifluorescence optics, exciting filters, UV (420
) barrier filter, and a 12 V, 100 WHAL halogen bulb. Light microscope photographs were taken using 160T Kodak film.
For SEM, inflorescences were fixed in 4% glutaraldehyde in 0.025 mol/L phosphate buffer (pH 7.0) and dehydrated in an alcohol series. Material was critical point dried with CO2 and coated with 40/60-gold/palladium alloy. Samples were studied with an Amray 1000 SEM at 10 kV, and photographed using a Polaroid camera.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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. The species were strikingly similar to each other from the time of spikelet initiation through floral organ initiation. The development of unisexual florets was also uniform. Differences appeared both early in development, in inflorescence structure and sequence of spikelet pair primordium (SPP) maturation, and later in development, after gynoecial ridge formation, in glume elongation and sex expression. The gynoecial ridge, as defined by Cheng and Pareddy (1994)
, is the stage at which the ovary begins to extend upwards around the nucellus, giving the appearance of an "egg" (the nucellus) in an "egg cup" (the ovary).
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In contrast to the disparate patterns of early inflorescence development, initiation and early development of spikelets are strikingly uniform. In all studied species, differentiation of the SPP involves formation of two unequally sized spikelet primordia, the pedicellate spikelet (PS) being developmentally more advanced than the sessile spikelet (SS). SPP differentiation may be either basipetal or acropetal. Spikelet development starts with initiation of an outer glume (OG) followed by an inner glume (IG) after which an outer (OL) and inner lemma (IL) are initiated, respectively (Figs. 4, 7, 10, 13). Subsequently, a floral meristem is visible by the inner or second lemma (IL) only (Figs. 5, 8, 11, 14, 31). The OL corresponds to the proximal floret, which in the studied species is sterile. Despite diligent investigation of material dissected for SEM (Figs. 5, 8, 11, 14) or sectioned (Fig. 31), we found no evidence that floral organs ever initiated in this position. One palea is initiated opposite the IL surrounding the meristem of the distal floret (Fig. 1). We refer to this as a unifloral spikelet, to contrast with the bifloral spikelets of maize and Tripsacum where both florets develop (Fig. 1).
Floral development
Although the PS develops more rapidly than the SS at first, initiation of floral organ primordia in the PS and SS occurs simultaneously, except in Heteropogon contortus, in which the SS initiates floral primordia first (Fig. 14). In each floret, three stamen primordia are initiated first, two on the lateral flanks of the meristem and one abaxially. Thereafter a gynoecial primordium forms (Figs. 5, 8, 11, 14). Just after floral primordium initiation, the gynoecial primordia in both spikelets appear to be slightly bigger than the stamen primordia. Two lodicules are initiated in a whorl outside the bases of the anther primordia (Figs. 17, 19, 20, 22, 25, 26). The gynoecial primordium elongates faster on the side of the IL, producing a gynoecial ridge, surrounding an obvious nucellus (Figs. 15, 18, 21, 24). As the gynoecial ridge initiates, the tips of the developing anther locules are at approximately the same height as the gynoecial ridge in both PS and SS (Fig. 15, 18, 21, 24). In Hyparrhenia hirta and Heteropogon contortus, the floral parts of the PS (staminate) are covered with at least the outer glume soon after gynoecial ridge formation whereas in the SS (hermaphroditic) glume elongation is delayed, leaving floral parts exposed (Table 1; Figs. 18, 24) . In Coelorachis aurita, in which both PS and SS produce a single hermaphroditic flower and are thus identical in sex expression, glumes envelop both flowers more or less simultaneously, before gynoecial ridge formation (Fig. 15). By the time of anthesis the floral parts of all spikelets in all species are completely enveloped in glumes and the elongated pedicels of PS spikelets are clearly visible. In some species, the IL of hermaphroditic (Hyparrhenia hirta, Bothriochloa bladhii) or female (Heteropogon contortus) sessile spikelets elongates to form an awn, which is detectable after gynoecial ridge initiation (Figs. 18, 24).
Sex expression (see Fig. 2 and Table 2)
Three sex distribution modes were found. (1) Bisexual florets are formed in both PS and SS of Coelorachis aurita (Figs. 16, 17). Floral organ primordia give rise to bisexual PS and SS with an androecium composed of tetralocular stamens and a gynoecium consisting of a single ovary with separate style branches and stigmas. (2) The andromonoecious condition is found in Hyparrhenia hirta (Figs. 19, 20, 29, 30) and in Bothriochloa bladhii (Figs. 22, 23). The SS of both species is bisexual (Figs. 19, 22), whereas gynoecial development in the PS does not proceed beyond the development of a gynoecial ridge (Figs. 20, 23). Prior to anther dehiscence the approximate anther locule length : gynoecial length in staminate florets of Hyparrhenia hirta is 2100:92 µm. In Bothriochloa bladhii, the anthers elongate slightly above the aborting gynoecium after which growth ceases; in this case the anther locule length:gynoecial length ratio is 96:54 µm, just before anther dehiscence. (3) Monoecy occurs in Heteropogon contortus. The PS throughout the inflorescence and the SS in the proximal part of the inflorescence are staminate (Fig. 26). In the awned SS in the distal part of the inflorescence, however, stamen primordia are arrested after anther initiation, resulting in pistillate spikelets (Fig. 25).
Sex expression in Paniceae
In the tribe Paniceae, from which the Andropogoneae are derived, spikelets occur singly, rather than in pairs. In Panicum repens, the one representative of Paniceae included in this study, two florets develop per spikelet (Fig. 1), rather than one as in the Andropogoneae species studied here. These florets are both initially hermaphroditic, but the gynoecium in the lower (proximal) floret stops developing after the formation of a gynoecial ridge (Figs. 35, 36). Thus the basic pattern of male flower formation is similar to that in the Andropogoneae.
Cell death
To determine the cellular changes associated with gynoecial arrest, we studied sectioned material stained with toluidine blue and with DAPI, a fluorescent stain that stains intact nuclei. Early in development, florets of all species had cells that appeared densely cytoplasmic in light microscopy and nuclei that fluoresced brightly with DAPI under UV light. In hermaphroditic florets, cells of both stamens and gynoecia continued to maintain cytoplasmic contents and brightly staining nuclei during development (Figs. 27, 28). In developing male florets, however, after gynoecial ridge formation, cells in the subepidermal layers of the gynoecium lose their cytoplasm (Figs. 29, 33) and nuclei (Figs. 30, 34); note, however, that cell walls remain intact (cf. Figs. 29, 33).
Loss of cytoplasm and of nuclei occurred in every staminate flower investigated after gynoecial ridge formation. Because this included multiple flowers in multiple plants, and several accessions of four species, we think it unlikely that the histological pattern is simply an artifact of sectioning. We think it more likely that these species exhibit a controlled cell death pathway, similar to that described by Calderón-Urrea (1996)
for gynoecial arrest in the maize tassel.
The only female florets studied were in the SS of Heteropogon contortus. In these, arrested anthers did not show nuclear breakdown with DAPI (Figs. 31, 32). This indicates that cessation of growth need not be correlated with cell death.
Although we also observed nuclear degeneration in the gynoecia of male florets in Panicum repens, the pattern of abortion was somewhat different from that in the Andropogoneae. In the Andropogoneae gynoecial breakdown is apparent in a longitudinal section through the center of the gynoecium where the gynoecial ridges are clearly visible (Figs. 29, 30, 33, 34). In Panicum, on the other hand, cell death occurs in the outer few cell layers at the base the of gynoecium, being first visible in a tangential section where the gynoecial ridges are not in the plane of the section (Figs. 37, 38). No gynoecial breakdown could be found in a longitudinal section through the center of the gynoecium in Panicum (Figs. 35, 36).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Sundberg and Orr, 1996
). In the maize ear and the central axis of the tassel, however, the distichous condition persists only for the first few nodes before the phyllotaxy changes to polystichous, producing more than two rows of SPP along the inflorescence axis (Sundberg and Orr, 1996)
.
Inflorescence development from SPP differentiation to the sequence of floral bracts and floral organ primordia initiation is strikingly similar among all Andropogoneae studied here, as well as maize and Tripsacum (Cheng, Greyson, and Walden, 1983
; Dellaporta and Calderón-Urrea, 1994
; Irish, 1996
). In all cases the PS is more advanced in development than the SS at SPP differentiation and the floral bracts (glumes, lemmas) and floral organ primordia initiate in exactly the same sequence.
Most discussion in the literature has focused on species of Zea and Tripsacum, in which both distal and proximal florets initiate in all spikelets even though the proximal floret is aborted in the maize ear. The spikelets are thus bifloral. This is not the case for most species of Andropogoneae, which resemble the species described here in having unifloral spikelets. Within a unifloral spikelet, we have found no evidence that the palea or floral organs of the proximal floret ever initiate; the floret is represented only by an empty lemma.
Andropogoneae species may have only hermaphroditic florets (e.g., Coelorachis), or be andromonoecious, with SS bisexual and PS male (e.g., Bothriochloa, Hyparrhenia), or monoecious (e.g., Heteropogon contortus, Zea, Tripsacum) (Fig. 2). The distribution of unisexual florets on the plant differs among the monoecious taxa. In Heteropogon contortus the PS throughout the inflorescence and the proximal SS are staminate, whereas the distal SS are pistillate. This contrasts with the more familiar patterns of maize and Tripsacum. In all inflorescences of Tripsacum, the distal two-thirds to three-quarters bear paired, bifloral staminate spikelets. The proximal spikelets are unpaired with one functional pistillate floret (Dewald et al., 1987
; Li et al., 1997
). In maize, unisexual florets are borne in separate inflorescences. All spikelets are paired. The tassel has bifloral staminate florets. Both florets in the ear are pistillate but the proximal floret aborts during development so that at maturity the ear spikelets are solitary (Cheng, Greyson, and Walden, 1983
; Dellaporta and Calderón-Urrea, 1994
; Irish, 1996
).
Among species of Andropogoneae, we found no obvious correspondence between the size of floral organ primordia and their developmental fate. At the differentiation of floral organ primordia, the stamen initials in our species consistently appear to be slightly smaller than gynoecial initials in PS and SS, whether the floret is destined to become hermaphroditic or male. (Note, however, that we did not quantify primordium size, so some subtle differences may have been undetected.) In maize, at the same developmental stage the floral organ primordia destined for abortion are smaller. Maize ears have smaller stamen primordia while the gynoecial primordia in tassels are smaller (Irish and Nelson, 1993
). Irish and co-workers conclude that the difference in floral organ primordium size indicates a critical stage at which sex determination occurs (Irish and Nelson, 1989
, 1993
). Sex expression might occur later in our species than in maize and therefore the size of floral primordia destined for abortion is not affected.
In some species studied here, glume morphology correlates with sex expression as in maize (Irish, Langdale, and Nelson, 1994
) and Tripsacum. At the initiation of floral primordia, floral organs are either exposed or enveloped by glumes (Table 1). The male florets (PS) of Hyparrhenia hirta and Heteropogon contortus are covered by glumes at gynoecial ridge formation, while the floral primordia in female florets (SS) of Heteropogon contortus and hermaphroditic SS of Hyparrhenia hirta and Bothriochloa bladhii are exposed. By anthesis, however, floral parts in PS and SS of all species are always enveloped by glumes. In the maize tassel (male), glumes envelop florets by the time floral organ primordia differentiate, while the glumes of ear florets (female) do not enclose spikelets (Irish, Langdale, and Nelson, 1994
). The glumes of tasselseed2 mutants, with feminized tassel spikelets, encircle but do not enclose the florets (Irish and Nelson, 1993
; Irish, Langdale, and Nelson, 1994
). Thus sex determination genes in maize and possibly in some Andropogoneae influence the elongation of glumes. Our results suggest that this may apply to the entire tribe.
Sex determination in maize influences other traits such as inflorescence axis diameter, and length of vegetative internodes proximal to inflorescences (Dellaporta and Calderón-Urrea, 1993
; Irish, 1996
). The inflorescence axis of the ear increases in diameter, while the vegetative internodes proximal to the ear inflorescence fail to elongate. These traits are associated with ear development, however, and do not occur in the species studied here. These traits were apparently selected for during the domestication of maize and are therefore not an attribute of natural selection (Doebley, Stec, and Hubbard, 1997
).
The formation of unisexual florets in studied Andropogoneae species, maize (Cheng, Greyson, and Walden, 1983
; Sundberg and Orr, 1996
), and Tripsacum (Dewald et al., 1987
; Li et al., 1997
) is uniform. All florets initiate both pistil and stamen primordia. In florets destined to be male, cell death occurs in the subepidermal layers of the gynoecium after the formation of a gynoecial ridge, as shown by the loss of cytoplasm and of nuclei stained by DAPI. We consider this to be evidence of a programmed cell death pathway. The cells of aborting pistils in the maize tassel become highly vacuolated (Cheng, Greyson, and Walden, 1983
; Dellaporta and Calderón-Urrea, 1994
) and lose free ribosomes and other organelles (Cheng, Greyson, and Walden, 1983
). While we have not investigated the ultrastructure of cells in male florets of other Andropogoneae species, our data suggest that the same processes documented in maize may occur throughout the tribe.
The pattern of cell death observed in Panicum is different from that seen in Andropogoneae. It is observed clearly only in the gynoecium of the proximal male floret and thus appears to be associated with gynoecial abortion. Cell death in the gynoecium of Panicum occurs in different cell layers than the Andropogoneae. While the genetic signal, and the time of its expression, may be the same in Panicum as in Andropogoneae, the pattern of cell death suggests that there may be subtle differences in the timing or location of gene activity.
Unisexual florets destined to be female do not show any nuclear breakdown, but stamen growth ceases after anther initiation. Our data on Heteropogon contortus suggest that it is like maize in this respect. Stamens in both florets of maize ear spikelets abort (Dellaporta and Calderón-Urrea, 1994
; Irish, 1996
). Ultrastructural studies on aborting anthers reveal increased vacuolation and loss of cytoplasmic organelles in the maize anthers (Cheng, Greyson, and Walden, 1983
). The ways in which pistil and stamen cells abort differ. This is consistent with the genetic data, which indicate that the elimination of these organs may be under the control of different genetic pathways.
The formation of unisexual florets from a bisexual meristem requires the action of sex determination genes. These genes have been identified in maize and Tripsacum by the analysis of mutants that disrupt the normal sex expression program (Dellaporta and Calderón-Urrea, 1993
). tasselseed2 (= gsf1) orthologues are the only sex determination genes cloned to date in any flowering plant (De Long, Calderón-Urrea, and Dellaporta, 1993
; Lebel-Hardenack and Grant, 1997
). Pistil abortion in maize correlates with the expression of tasselseed2 in the subepidermal cell layers of pistils before abortion. The gsf1 mutation blocks pistil abortion in the distal staminate spikelets as well as the lower florets of the proximal pistillate spikelets (Li et al., 1997
) and thus has feminizing effects similar to the tasselseed genes in maize. By RFLP (restriction fragment length polymorphism) mapping and by using intergeneric hybrids in a complementation test, Li et al. (1997)
were able to demonstrate that ts2 and gsf1 are orthologous. Many aspects of floral development correlate among the studied species, Tripsacum, and maize, so we infer that the genetic and molecular basis for the sex determination may be similar.
Male flowers are formed by a cell death pathway in all members of the Panicoideae studied to date. The subfamily was first recognized as a group by Robert Brown (1810)
on the basis of the paired florets with the proximal one reduced. If gynoecial reduction in proximal florets is caused by the same mechanism that creates male flowers elsewhere in the subfamily, as is suggested by our results for Panicum, then we have identified the basis of an important systematic character first identified nearly 200 years ago. Furthermore, if the cell death pathway can be shown to correlate with expression of ts2, then we may have identified the genetic basis of the subfamilial synapomorphy.
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FOOTNOTES |
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2 Present address: Biology Department, Boston College, 140 Commonwealth Avenue, Chestnut Hill, Massachusetts 02167-3811.
3 Present address: Department of Biology, University of Missouri-St. Louis, 8001 Natural Bridge Road, St. Louis, Missouri 63121.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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