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2Department of Biology, University of Northern Iowa, Cedar Falls, Iowa 50614 USA; 3USDA-ARS, Southern Plains Range Research Station, Woodward, Oklahoma 73801 USA; and 4Department of Biological Sciences, Emporia State University, Emporia, Kansas 66801 USA
Received for publication December 1, 1999. Accepted for publication May 4, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: development • Eastern gamagrass • gynomonoecious mutant • inflorescence • organogenesis • Poaceae • Tripsacum dactyloides.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Mangelsdorf and Reeves, 1939
; Mangelsdorf, 1974
; Galinat, 1983
; Iltis, 1983
; Doebley, 1990
; Wilkes and Goodman, 1995
). Although most current workers favor the hypothesis that maize arose from a teosinte ancestor, the debate gained renewed vigor with a recast of a Mangelsdorf hypothesis that Tripsacum may have played a role in the evolution of maize (Eubanks, 1995, 1997
). Fertile F1 Tripsacum-teosinte hybrid plants, which were derived when Eubanks (1995)
crossed a teosinte (Zea diploperennis) and Tripsacum dactyloides (Eastern gamagrass), produced hybrid inflorescences (ears) with fused, nondisarticulated cupules and reduced glumes. According to Eubanks (1995)
these first-generation hybrid ears exhibit an intermediate morphological stage toward the evolution of the maize ear.
In previous studies by two of us (Orr and Sundberg) we described the development of inflorescences (ears and tassels) in the teosintes (Orr, 1980
; Sundberg and Orr, 1986, 1990
; Orr and Sundberg, 1994a, b
), in primitive wild-type maize (Sundberg, LaFargue, and Orr, 1995
; Sundberg and Orr, 1996
), and in a maize mutant (Orr, Haas, and Sundberg, 1997
). The organogenic observations from these scanning electron microscope (SEM) studies were used to examine the prevailing ideas on the origin of the maize ear: did the maize ear evolve from a pistillate teosinte inflorescence as suggested by the traditional teosinte hypothesis (Beadle, 1939, 1978
; Galinat, 1983, 1985
), or did it evolve by a catastrophic feminization of a staminate inflorescence terminating a primary lateral branch (Iltis, 1983
; Benz and Iltis, 1992
)? Our SEM observations on maize and teosinte disclosed that the controversy appears to be a classic example of what Sattler (1988)
calls a pseudoquestion (cf. Iltis, 1987
). Thus, it is not an either/or question (i.e., was the maize ear derived from a teosinte ear or a teosinte tassel?). Rather, the crucial events of maize ear evolution were derived from a developmental pattern common to all Zea inflorescences (Sundberg and Orr, 1990
; cf. Fig. 25 in Orr and Sundberg, 1994a
): (1) solitary spikelets of teosinte ears result from arrested growth and subsequent abortion of the pedicellate primordia; (2) femaleness in maize and teosinte spikelets is marked by the abortion of the lower florets, whereas maleness in maize and teosinte spikelets is marked by a retention of the lower florets; (3) the development of a two-ranked or four to multiple-ranked (distichy to polystichy) inflorescence could arise from a change in the developmental program that controls the bifurcation of spikelet pair primordia; and (4) a proposed switch from a staminate to a pistillate inflorescence (Iltis, 1983
) may have involved an inflorescence with a male spikelet zone and female spikelet zone (i.e., a bisexual morphological structure).
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hypothesis indicating a possible role of Tripsacum in the origin of the maize ear, it became imperative that the early organogenesis of T. dactyloides bisexual inflorescences be investigated to test the developmental similarity between Zea (maize and the teosintes) and Tripsacum.
In this work, we describe the organogenic patterns of inflorescence development in the wild type and a gynomonoecious mutant of gamagrass. Although there is no previous organogenic study of inflorescence development in T. dactyloides, an examination of Camara-Hernandez and Gambino's (1992)
structural study of T. dactyloides reveals a single photograph of an early spike-like raceme, and the investigation of Li et al. (1997)
exhibits photographic evidence showing late floret development in the wild type and the gynomonoecious mutant (gsf1) of gamagrass. We use the SEM analysis of T. dactyloides inflorescences to test the hypothesis that both feminity and masculinity in the subtribe Tripsacinae are derived from a common developmental background (Iltis, 1987
; Sundberg and Orr, 1990
; Orr and Sundberg, 1994a
). Recent evidence indicates that SEM developmental studies can shed light on the evolution of floral development in the Andropogoneae (Le Roux and Kellogg, 1999
): similarity in spikelet organogenesis and the formation of unisexual florets indicates a common genetic mechanism for sex determination in the tribe Andropogoneae of Poaceae.
SEM analysis of mutants that perturb wild-type morphogenic patterns has also proved useful in understanding the genetic regulatory logic of maize inflorescence development (Veit et al., 1993
). Recent evidence for a developmental monophyletic trait in the subtribe Tripsacinae was shown for the inflorescences of Zea mays ssp. mays (maize) and its wild relative T. dactyloides (Li et al., 1997
). The developmental acquisition of monoecy in maize and gamagrass requires, respectively, the action of the Tassel seed2 and the Gynomonoecious Sex Form1 genes (Li et al., 1997
). These genes are thought to be orthologous based on restriction fragment length polymorphism mapping (Blakey, Dewald, and Coe, 1994
; Li et al., 1997
). SEM analysis revealed the organogenic pattern by which Tassel seed2 and the Gynomonoecious Sex Form1 genes feminize the inflorescence.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Tripsacum dactyloides or eastern gamagrass, a high-protein forage crop with good resistance to wet soils and drought, also offers seed crop potential (Jackson, Dewald, and Bohlen, 1992
; Jackson and Dewald, 1994
) through an increased feminization of the inflorescence by the gynomonoecious (gsf) mutation (Dewald et al., 1987
), and the development of an apomictic, gynomonecious triploid (Dewald and Kindiger, 1994
).
Tripsacum dactyloides plants, dense vegetative clumps of tillers (shoots), were grown at the USDA, Agricultural Research Service, Southern Plains Range Research Station, Woodward, Oklahoma, USA. During the floral reproductive period the largest and oldest vegetative shoots are induced to flower, and each shoot may generate 1–5 inflorescences (Jackson, 1990
). Preflowering and flowering stems of wild type (WW 1379) and gynomonoecious sex form1 (gsf1) mutants (WW 1582) were harvested weekly during May 1994. Each flowering stem initially produced a terminal (A1), panicle-like inflorescence (Fig. 1). The axis (rachis) of the terminal inflorescence consisted of a distal central spike and a lower, proximal zone of lateral long branches. Each flowering stem also produced axillary (A2), spike-like inflorescences (Fig. 1). This codification of the branching pattern in teosinte inflorescences is illustrated by Sundberg and Orr (1986)
and is comparable to Camara-Hernandez and Gambino (1990)
where they label the terminal teosinte inflorescence A0 with axillary teosinte inflorescences designated A1. This codification scheme also is used with maize inflorescences (Orr, Haas, and Sundberg, 1997
) and is employed to compare maize and teosinte organogenesis (cf. Fig. 25 in Orr and Sundberg, 1994a
). In addition, our codification of Tripsacum inflorescence branching is similar to the terminology used by Camara-Hernandez and Gambino (1992)
to describe the inflorescence of Tripsacum. Terminal (A1) and axillary (A2) inflorescences in various developmental stages were dissected from reproductive stems using an Olympus SZH dissecting microscope and fixed in formalin-acetic acid-alcohol fixative (Jensen, 1962
).
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); storage in 100% acetone; critical-point drying in a Samdri-790 Critical Point Dryer; mounting on a metal stub; and gold-palladium sputter-coating in a Technics Hummer VII sputter coater. Inflorescences were examined with a Hitachi S-570 scanning electron microscope at 20 kV and representative organogenic stages were photographed using Polaroid Type 55 4 x 5 black and white film. The material for histological study was dehydrated in tertiary butyl alcohol (TBA) series, embedded in Paraplast, sectioned at 8 µm, mounted, and stained with safranin-fast green (Jensen, 1962
). Approximately 35 wild- type plants and 25 gsf1 mutant plants were studied. Two inflorescences per plant were often removed for study. More than 85 T. dactyloides inflorescences (50+ wild type; 35+ mutant) were examined and analyzed with SEM. Approximately ten sectioned wild-type T. dactyloides inflorescences were studied with a light microscope. |
RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Francis, 1990
; Jackson, 1990
), will be briefly reviewed here. Eastern gamagrass, a monoecious bunch grass, produces wild-type inflorescences (A1 and A2) with a dorsiventral structure (Fig. 1; Camara-Hernandez and Gambino, 1992
). These inflorescences consist of sessile, solitary female spikelets on the lower (proximal) two-thirds to three-quarters of the rachis and paired staminate spikelets on the upper (distal) portion of the rachis (Francis, 1990
; Camara-Hernandez and Gambino, 1992
). Staminate spikelets contain two functional male florets. Pistillate spikelets, enclosed in a cupulate fruitcase, contain one functional female floret. Both wild-type (A1 and A2) inflorescences are sexually mixed. Generally, there is a transition zone in the rachis between the upper staminate zone and lower pistillate zone that consists of one or two nodes with a solitary, sessile staminate spikelet or an occasional pair of pistillate spikelets (Camara-Hernandez and Gambino, 1992
). Pistillate mutant (gsf1) inflorescences usually have 10–25 more pistillate florets than wild-type inflorescences (Fig. 2). These dorsiventral inflorescences are similar to the wild-type inflorescences in having an upper paired spikelet region and a lower single spikelet region (Jackson, Dewald, and Bohlen, 1992
).
Organogenesis of inflorescences: wild type
Early ontogeny of T. dactyloides inflorescences, both terminal inflorescences (Fig. 1, A1) and spike-like axillary inflorescences (Fig. 1, A2) showed a dorsiventral rachis (Fig. 3). The dorsiventrality was revealed by a flat, adaxial inflorescence surface (Fig. 3) and a convex abaxial surface with distichously arranged branch primordia and paired spikelet primordia (Fig. 4). Occasionally, the dorsiventrality was more evident on the distal part of the inflorescence than in the proximal region.
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Female spikelet development
Inflorescences formed distichously arranged spikelet pair primordia, which divided unequally into paired pedicellate and sessile spikelets (Fig. 27). As mentioned previously, the zone of the inflorescence axis that later developed female spikelets was characterized by the arrest and abortion of pedicellate spikelets during the formation of the outer and inner glumes (Fig. 28). Female spikelets arose from the remaining sessile spikelets (Fig. 28). Each sessile spikelet sequentially developed four bract primordia that were similar to those observed in the male spikelets: outer glume, inner glume, outer lemma, and inner lemma (Fig. 29). Prior to the formation of an inner lemma, a lower floret was initiated in the axis of an outer lemma (Fig. 29). The residual portion of the sessile spikelet meristem became the upper floret primordium (Fig. 29). The upper and the lower florets were separated by the palea of the upper floret (Figs. 30, 31). The palea of the lower floret was formed adjacent and abaxial to the upper palea, and opposite to the two lateral stamen primordia of the lower floret (Fig. 31). At this stage of spikelet organogenesis, the upper floret was developmentally ahead of the lower floret.
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Transition zone
Dissection of a sessile spikelet in the transition zone of some inflorescences revealed development of both upper and lower florets with androecial tissues. Also, some inflorescences displayed a spikelet in the transition zone with ovary development in both the upper and lower floret. The occurrence of these variants has been observed in mature Tripsacum inflorescences (Camara-Hernandez and Gambino, 1992
).
Organogenesis of inflorescences: mutant
The gynomonoecious sex form1 (gsf1) inflorescence mutant of T. dactyloides will be briefly reviewed here. The gynomonoecious sex form1 is a feminizing, recessive mutation that increases the pistillate condition of spikelets by blocking pistil abortion in distal staminate spikelets and floret abortion in proximal pistillate spikelets of A1 and A2 inflorescences (Dewald et al., 1987
). Thus, mature gsf1 inflorescences bear paired, bisexual spikelets along the distal part of the rachis and single spikelets with two pistillate florets along the proximal part of the rachis (Fig. 2). The central part of the inflorescence rachis bears spikelets containing two feminized florets with rudimentary stamens.
The early organogenic stages in all gsf1 inflorescences were identical to those of wild-type Eastern gamagrass inflorescences. Distichously arranged spikelet pair primordia were formed acropetally along a dorsiventral inflorescence (Figs. 35, 36). Spikelet pair primordia at the base of A1 inflorescence produced long branches (Fig. 35). All other spikelet pair primordia on A1 and A2 inflorescence produced a pair of spikelet primordia, pedicellate and sessile (Fig. 36). Each spikelet formed an outer and inner glume (Fig. 37). Development of the pedicellate spikelets was arrested and the spikelet size greatly reduced after the formation of the outer and inner glumes (Figs. 37 and 38, x's).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Cheng, Greyson, and Walden, 1983
; Sundberg and Orr, 1996
) and wild-type teosinte plants (Sundberg and Orr, 1986, 1990
; Orr and Sundberg, 1994a
).
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; Camara-Hernandez and Gambino, 1992
) and wild- type maize (Bonnett, 1953
), the sessile spikelet is a branch of the pedicellate. While both pairs of spikelets continued development along the distal portion of the rachis, pedicellate spikelets were aborted in the proximal (pistillate) region of the rachis (Fig. 52). This pattern of paired spikelet formation and subsequent abortion of the pedicellate spikelets is similar to a previous report (Camara-Hernandez and Gambino, 1992
) showing a single SEM observation of gamagrass. In fact, this organogenic pattern is common to annual (Sundberg and Orr, 1990
) and perennial (Sundberg and Orr, 1986
; Orr and Sundberg, 1994a
) teosintes, but not maize (Cheng, Greyson, and Walden, 1983
; Stevens et al., 1986
; Sundberg et al., 1995
; Sundberg and Orr, 1996
). Although maize produces spikelet pair primordia that divide to produce paired spikelets, subsequent abortion of the pedicellate spikelet to produce solitary mature spikelets does not occur in either modern (Cheng, Greyson, and Walden, 1983
; Stevens et al., 1986
), or land race (Sundberg, LaFargue, and Orr, 1995
; Sundberg and Orr, 1996
) maize ear formation. According to Galinat (1983, 1985)
, the production of pedicellate spikelets (i.e., restoration of a paired spikelet condition) in the evolution of the maize ear from the teosinte ear was likely to involve a modified function of the Pd gene. If we assume a functional change in the Pd gene terminated the abortion event in the pedicellate spikelets in a pure pistillate teosinte ear, or in the pistillate portion of a mixed inflorescence of either teosinte or Tripsacum, a paired spikelet condition would result.
The arrest and abortion of the pedicellate spikelets in the proximal portion of the inflorescence result in single spikelets (Fig. 1). Each of the functional paired and single spikelet primordia developed additional primordia (outer glume, inner glume, outer lemma, lower floret, inner lemma, upper floret, and palea) in a pattern that is similar to modern maize (Cheng, Greyson, and Walden, 1983
), primitive maize (Sundberg, LaFargue, and Orr, 1995
; Sundberg and Orr, 1996
) and the teosintes (Sundberg and Orr, 1986, 1990
; Orr and Sundberg, 1994a
). Both the upper and lower floret primordia produced three stamens and an ovary. The organogenic pattern of upper and lower floret development in wild-type T. dactyloides also was similar to that of maize and the teosintes (Cheng, Greyson, and Walden, 1983
; Sundberg and Orr, 1986, 1990
; Orr and Sundberg, 1994a
; Sundberg, LaFargue, and Orr, 1995
). A similar conclusion is offered in regard to stamen abortion in the proximal (pistillate) portion of the inflorescence and ovary abortion in the distal (staminate) portion of the Eastern gamagrass inflorescence (Fig. 52). The arrested development of the lower florets in sessile spikelets of T. dactyloides, located proximal to the transition zone, was similar to the abortion of the lower floret on the entire A2 axis of a pure pistillate inflorescences in maize, Z. perennis (Orr and Sundberg, 1994a
), Z. mexicana, Z. parviglumis (Sundberg and Orr, 1990
), and Z. diploperennis (Sundberg and Orr, 1986
). Thus, this study shows that a common pattern of inflorescence organogenesis is exhibited by both Zea and Tripsacum, subtribe Tripsacinae. This supports the proposal that virtually all the Andropogonoid grasses share a common pattern of inflorescence development (Francis, 1990
).
While maize and most teosintes usually develop pure A2 pistillate inflorescences, wild-type T. dactyloides usually develops sexually mixed inflorescences on A2 axes similar to a pattern of mixed inflorescence development observed for the A2 axis of Z. diploperennis (Sundberg and Orr, 1986
). Interestingly, in wild-type T. dactyloides the pistillate condition in the proximal region of the rachis developed similarly to the A2 pure female inflorescences of Z. mexicana and Z. parviglumis (Sundberg and Orr, 1990
) and Z. perennis (Orr and Sundberg, 1994a
). Also, A2 inflorescences of the teosinte, Z. parviglumis, sometimes will exhibit a sexual mixed condition that is derived following an organogenic pattern observed in T. dactyloides and Z. diploperennis (Orr, unpublished data). These observations demonstrate the potential of sexually mixed (distal male spikelet zone and a proximal female spikelet zone) T. dactyloides A2 axes to develop an inflorescence with only female spikelets. This potential is partially realized by a seasonal increase in the number of nodes supporting female spikelets (L. L. Jackson, personal communication, University of Northern Iowa). A feminizing potential is realized in the gamagrass pistillate mutant gsf1. Our results support the proposal of Iltis (1983, 1987)
that a maize ear evolved at the tip of a lateral A2 branch through a switch in sexuality from staminate to pistillate. However, it is speculated that such a lateral A2 sexual transmutation was not sudden and catastrophic (Iltis, 1983, 1987
), but that a sexually mixed inflorescence was ancestral to the maize ear (Sundberg and Orr, 1986
; Sundberg, 1987
).
An organogenic comparison of the gsf1 mutant to the wild type (Fig. 52) revealed an abnormal fate of A1 and A2 inflorescence development in the mutant. The lower floret branches in sessile, pistillate spikelets of the gsf1 mutant were not aborted, and the sex of the paired spikelets switched from unisexual, staminate florets to either unisexual pistillate florets or bisexual florets. No other variation from the wild-type pattern (Fig. 52) was observed in this study. However, cupule morphology of mature mutant inflorescences varies from the wild type (Dewald et al., 1987
). Although the pattern of inflorescence organogenesis in Zea mays subsp. mays is perturbed in several mutants (Veit et al., 1993
), mutant alteration of inflorescence development in other members (teosintes) of the genus Zea is lacking. The first nonmaize mutant known to affect inflorescence development in the Maydeae, gsf1, was observed in the genus Tripsacum (Dewald and Dayton, 1985
; Dewald et al., 1987
). The effect of gsf1 is similar to the maize mutant ts2. Both mutants not only suppressed pistil abortion in staminate spikelets, but also permit development of the lower florets in single, sessile spikelets. The gsf1 mutant inflorescence gains extra florets in the lower sessile spikelets and shifts the pattern of sex expression in the upper, paired spikelets. According to Irish (1997)
some genes controlling sex determination in Zea spikelets also control branching pattern (e.g., ramosa1, branched silkless, and unbranched mutants of maize). However, our results do not indicate that branching pattern and sex determination are associated in the development of T. dactyloides inflorescences. In gamagrass, Gsf1 activity obviously does not exclusively control sex determination in paired, sessile-pedicellate spikelets, but also determines the fate of lower florets in the single, sessile spikelets. Understanding the relationship between the determinacy of floret meristems and sex determinacy in Eastern gamagrass inflorescences might eventually enhance the reproductive versatility of Eastern gamagrass and also contribute to a phylogenetic analysis of the tribe Andropogoneae.
Two of us (Orr and Sundberg) have addressed the origin of the maize ear by studying inflorescence development in members of the genus Zea, land race maize, and the teosintes. One significant result of these SEM comparative assessments of wild-type T. dactyloides inflorescences is that maize and teosinte share a common pattern of development (see Fig. 25 in Orr and Sundberg, 1994a
). The organogenic pattern observed in the A2, sexually mixed inflorescence of wild-type T. dactyloides (Fig. 52) is significant in regard to assessing the origin of the maize ear. There is a growing notion that a sexually mixed inflorescence may have been an ancestor to the modern maize ear. Some believe that a sexually mixed inflorescence similar to T. dactyloides or Z. diploperennis may have preceded the unisexual, pistillate inflorescences of modern maize (Benz and Iltis, 1992
), while others believe the sexually mixed inflorescence of Tripsacum may be ancestral to modern maize ears (Wilkes, 1979
; Eubanks, 1995
). Both of these theories allow that a sexually mixed inflorescence may have preceded the pure pistillate inflorescence of modern maize. A renewed interest in the possible contribution of T. dactyloides alleles in the origin of the maize ear was stimulated by a genetic cross between T. dactyloides and Z. diploperennis (Eubanks, 1995
). The fertile hybrids of this cross revealed hybrid inflorescences (ears) with reduced glumes and fused, nondisarticulating cupules. These hybrid pistillate inflorescences resembled the "wild maize" of Mangelsdorf (1974)
. This led Eubanks (1995)
to hypothesize that back crosses among Tripsacum— diploperennis hybrids to parental species may have provided an ancestral genetic resource for human selection in the domestication of the maize ear. Although the Eubanks hypothesis is inconsistent with molecular evidence (Doebley, 1990
; Hilton and Gaut, 1998
), developmental data are in agreement with a possible hybrid origin in the evolution of the maize ear. Our study shows that the pattern of pistillate development in T. dactyloides inflorescences is similar to development exhibited in maize and the teosintes.
The inflorescence development pattern in Zea and Tripsacum supports the idea that a common pattern of inflorescence organogenesis arose prior to the evolutionary divergence of Tripsacum and Zea 
4.5–4.8 mya (Hilton and Gaut, 1998
). It will be interesting to examine this evolutionary divergence model with genes that target inflorescence development in the Poaceae. Interestingly, molecular analysis of the T. dactyloides gsf1 gene and the maize ts2 gene revealed that pistillate abortion in the staminate region of a Tripsacum gamagrass inflorescence is homologous to that in the staminate maize tassel (Li et al., 1997
). Perhaps a further examination of the maize indeterminate spikelet1 inflorescence architectural gene (Chuck, Meeley, and Hake, 1998
) also will test the evolutionary divergence hypothesis.
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FOOTNOTES |
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5 Author for correspondence (e-mail: orr{at}uni.edu
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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