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Development and Morphogenesis |
2Department of Biology, University of Northern Iowa, Cedar Falls, Iowa 50614 USA; 3Department of Biological Sciences, Emporia State University, Emporia, Kansas 66801 USA
Received for publication April 25, 2003. Accepted for publication September 12, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: development • evolution • inflorescence • maize • organogenesis • Poaceae • teosinte • Zea
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Galinat, 1992
; Iltis, 2000
; Bennetzen et al., 2001
; Benz, 2001
; Matsuoka et al., 2002
), other origin hypotheses are still being considered (Mangelsdorf, 1974
; Bird, 1979
; Wilkes, 1979
; Eubanks, 1995
, 1997
, 2001a
, b
; Provan et al., 1999
; MacNeish and Eubanks, 2000
). Additionally, substantial uncertainty prevails concerning the developmental transformation of a teosinte inflorescence into a maize ear. One view contends that the maize ear evolved from a pistillate inflorescence (Beadle, 1939
, 1978
; Galinat, 1983
, 1985
). A second outlook proposes the ear was derived from a feminized staminate inflorescence that terminated a primary lateral branch (Iltis, 1983
, 2000
; Benz and Iltis, 1992
).
The discovery of Zea diploperennis Iltis, Doebley & Guzman (Iltis et al., 1979
) energized new interest in the origin of the maize ear. Scanning electron microscopy (SEM) studies clarified a developmental pattern common to the ears and tassels of teosinte (Sundberg and Orr, 1986
, 1990
; Sundberg, 1987
; Orr and Sundberg, 1994
), small-eared "primitive" maizes (Sundberg et al., 1995
; Sundberg and Orr, 1996
), cultivated maizes (Cheng et al., 1983
), and eastern gamagrass (Orr et al., 2001
). Although key developmental variations were observed that distinguish Tripsacinae inflorescences among Zea (maize and teosinte) species and between Zea ears and Zea tassels, it was revealed that femininity and masculinity in teosinte and maize were derived from a common developmental background (Orr and Sundberg, 1994
). These investigations also supported a subsequent view that a common mechanism of sex expression operates in the Andropogoneae (Le Roux and Kellogg, 1999
). Moreover, our SEM developmental studies (Sundberg and Doebley, 1990
; Sundberg and Orr, 1996
) were useful in supporting a general tenet of the sexual translocation theory: that terminal tassels (central spikes) of primary lateral branches were converted into maize ears (Iltis, 2000
). We suggested that one or more heterochronic mutations lead from two ranked (distichous) to four-or-more ranked (polystichous) inflorescence.
Recently we extended our SEM studies of inflorescence development to include a high altitude annual teosinte from the Toluca Valley of Mexico (Orr et al., 2002
). This investigation illuminated a multi-authored hypotheses on the origin of maize domestication: our analysis revealed support for the proposal that populations of both lowland Balsas teosinte and highland Chalco teosinte contributed to the origin of maize (Wilkes, 1979
; Galinat, 1992
, 1995
; Eagles and Lothrop, 1994
).
The recent discovery of a new teosinte from Pacific Coastal Nicaragua (Iltis and Benz, 2000
) has sparked yet another opportunity to better understand the origin of the maize ear. This fresh genetic resource occurs at 6–15 m above sea level, a very low elevation for teosinte, and has the unusual ability to grow in 0.4 m of standing or slowly moving water (Iltis and Benz, 2000
). However, it is almost extinct: apparently only two locations remain (6000 plants at one location and 30 plants at another site (R. Bird [emeritus, North Carolina State University], Raleigh, North Carolina, USA, personal communication). This new teosinte offers another opportunity to test our hypothesis that male and female maize inflorescences are derived from a common developmental background. Although the chromosome number of Z. nicaraguensis Iltis & Benz is lacking and the degree of hybridization (if any) between Z. nicaraguensis and Zea mays L. subsp. mays is unknown, developmental studies of Z. nicaraguensis inflorescence development could be useful towards the enhancement of maize growth in water-logged soils (Iltis and Benz, 2000
).
This study describes early ear and tassel development in Z. nicaraguensis, Zea section Luxuriantes, and compares the data to patterns of inflorescence development in other members of the genus Zea.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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).
Seeds were sown and placed into a Conviron CMP 3020 plant growth chamber (Conviron, Winnipeg, Manitoba, Canada) under a day/night temperature environment of 24°/18°C and a long-day (LD) photoperiod of 15 h light/9 h dark. When plants reached the eighth ligule (V8) stage of leaf growth, the photoperiod in the growth chamber was changed to a short-day (SD) regime of 8 h light/16 h dark to induce inflorescence formation and promote flowering (Orr and Sundberg, 1994
; Orr et al., 2002
). Photosynthetic photon flux density (PPFD) was maintained at 600–700 µmol · s–1 · m–2 at the top of the leaf canopy during both LD and SD photoperiods. The PPFD was measured twice per week using a LI-COR 185 (LI-COR, Lincoln, Nebraska, USA) equipped with a quantum sensor.
Terminology
Staminate (tassel) inflorescences (A1) of Z. nicaraguensis teosinte terminated the main axis and consisted of a central tassel spike and one or more proximal tassel branches. Pistillate (ear) inflorescences (A2) arose as lateral clusters to the main axis. Each ear cluster was composed of a series of branchlets of higher order (A2, A3, etc.). Each branchlet was tipped by a pistillate inflorescence. This arrangement of Z. nicaraguensis inflorescences is similar to that previously described for other teosintes (Iltis, 2000
). This paper uses a codification for the teosinte branching pattern as illustrated by Sundberg and Orr (1986)
and Orr et al. (2002)
, a scheme also employed with maize inflorescences (Orr et al., 1997
), and was used to compare maize and teosinte organogenesis (cf. Fig. 25, Orr and Sundberg, 1994
). This codification is comparable to that used by Cámara-Hernández and Gambino (1990)
and by Iltis (2000)
for teosinte and maize, except that they labeled the terminal teosinte inflorescence A0 and axillary branchlets of teosinte as A1, A2. The codification of the inflorescence branching pattern in Tripsacum, another member of the Tripsacinae, is similar to the axial designation used in this paper (Orr et al., 2001
).
Zea nicaraguensis tassel inflorescences were harvested from the tip of the primary axis (A1), and the Z. nicaraguensis ear inflorescences were harvested from the tip of the secondary (A2) branchlet or higher order branchlets (A3, A4). Tassel and ear inflorescences in various developmental stages were fixed in formalin-acetic acid-alcohol fixative (Jensen, 1962
), dehydrated in a graded ethanol-acetone series (Liang and Tucker, 1989
), and stored in 100% acetone. Samples were critical-point dried in a Samdri-790 Critical Point Dryer (Tousimis Research, Rockville, Maryland, USA), mounted on a metal stub, and gold-palladium sputter-coated in a Technics Hummer VII sputter coater (Technics, Alexandria, Virginia, USA). Examination and photography of inflorescences was done using an Hitachi S-570 scanning electron microscopy (Hitachi, Tokyo, Japan) at 20 kV.
Inflorescences from 80–90 plants were observed: 40+ tassels (A1 inflorescence) and 45+ ears (A2 inflorescence) were examined at various stages of development. Representative organogenic stages were photographed using Polaroid Type 55 4 x 5 black and white film.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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. Approximately 22 d after germination under short day conditions, Z. nicaraguensis plants reached the V8 stage of leaf development. Beginning approximately 20 d after Z. nicaraguensis plants were transferred to long days, they were periodically harvested and examined for patterns of inflorescence development. Results for Z. nicaraguensis inflorescence development are summarized in Figs. 1–10 (male tassels) and Figs. 11–21 (female ears).
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Each spikelet pair primordium gave rise to a pair of spikelets, pedicellate and sessile (Fig. 2). Thus, two ranks of spikelet pair primordia gave rise to four rows of spikelets. The two rows of sessile spikelets were adjacent to one another along the abaxial surface (Fig. 2). Each spikelet (pedicellate and sessile) meristem produced in series first (outer) and second (inner) glumes (Fig. 3) and first (outer) lemma (Fig. 3) and second (inner) lemma (Fig. 4). A lower floret formed in the axis of the outer lemma, and the terminal meristem of the spikelet became the upper floret (Fig. 4). The upper and lower florets of each spikelet were separated by an upper palea (Fig. 5). Thus, each upper floret was bracketed by an inner lemma and a palea (upper). At this stage of development the lower floret did not exhibit a palea (lower) and was developmentally behind the upper floret. The upper floret formed two lateral stamen primordia (Fig. 5) followed by the initiation of the third stamen primordia in the adaxial position (Fig. 6). The final primordium produced on the upper floret was the ovary wall ring meristem (gynoecial ridge) on the adaxial surface (Fig. 7). Although the lower floret was developmentally behind the upper floret, the pattern of organogenesis in the lower floret was a mirror image of the upper floret (Figs. 7, 8). For example, the third stamen primordium and the ovary wall ring meristem were initiated abaxial to the ovary (Fig. 7). The lower palea was the final primordium to appear on the lower floret (Fig. 8). Two lodicules were initiated at the base of the lower floret (Figs. 8, 9). Concomitant with anther development in the upper floret gynoecial growth was arrested and the organ aborted (Fig. 9). Abortion of the gynoecium also was observed in the lower floret.
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Ear
Development of the A2 inflorescence began when the vegetative meristem (Fig. 11) elongated into the transition stage (Fig. 12) and subsequently initiated two ranks (distichous) of branch primordia (Figs. 13, 14) along the rachis. All branch primordia functioned as spikelet pair primordia (Figs. 13, 14): each gave rise to a pair of spikelets, pedicellate and sessile (Fig. 14). As in the tassel, the spikelet pairs were shifted abaxially on the axis such that the sessile spikelets were adjacent (Figs. 14, 15, 16).
Each spikelet primordium produced in acropetal succession outer (first) and inner (second) glumes (Figs. 15, 16). Development of the pedicellate spikelet was arrested after the formation of the inner glume and usually prior to the initiation of the outer (first) lemma in the sessile spikelet (Figs. 15, 16). Lateral growth of the outer glume of the sessile spikelet enveloped the arrested pedicellate spikelet (Fig. 15). Sessile spikelet development continued with the formation of the outer (first) lemma (Fig. 15) followed by the formation of the inner (second) lemma (Fig. 16).
The lower floret meristem of the sessile spikelet was initiated on the rachilla in the axil of the lower lemma, and the upper floret developed at the terminus of the rachilla (Figs. 17, 18). Next, an upper palea was initiated in a lateral abaxial position on the upper floret (Fig. 18). Subsequently, two lateral stamen primordia formed on the upper floret (Fig. 19), and later a third stamen primordium developed in the adaxial position (Fig. 19). The residual portion of the upper floret meristem formed an ovary ring wall (Fig. 20), which ultimately encloses the ovule (Fig. 21). Both upper and lower florets produced androecial and gynoecial primordium, but the lower floret was developmentally behind the upper floret (Figs. 20, 21). Eventually both the androecial and gynoecial tissues were aborted (data not shown) in the lower floret, leaving the sessile spikelet with a single floret. However, a lower palea was formed on the rachilla adjacent to the upper palea (Fig. 21) prior to the arrested development of the lower floret. The enlargement of the rachis flaps both crushed the aborted pedicellate spikelet and partially enveloped the sessile spikelet (Figs. 19–21).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Orr and Sundberg, 1994
; Sundberg et al., 1995
; LeRoux and Kellogg, 1999; Pizzolato and Sundberg, 1999
; Kellogg, 2000
; Orr et al., 2001
). In addition, archaeological studies (Bird, 1994
; Benz, 2001
), molecular plant genetics (Doebley, 1990
; Buckler et al., 1997
; Provan et al., 1999
; Matsuoka et al., 2002
), and taxonomic investigations (Bird, 1978
; Doebley and Iltis, 1980
; Iltis and Doebley, 1980
) have all contributed to an understanding of the evolutionary history of maize and maize inflorescences. The primary aim of this study was to describe inflorescence development in a newly discovered teosinte, Z. nicaraguensis—a teosinte that is very rare and is notable for its ability to thrive in a habitat of standing or slow moving water (Iltis and Benz, 2000
).
Unisex inflorescences
We observed that Z. nicaraguensis plants developed pure male and pure female flowers in different inflorescences. However, every flower of every functional spikelet in Z. nicaraguensis initiated organs of the opposite sex. This is similar to other teosintes (Orr and Sundberg, 1994
; Orr et al., 2002
), cultivated maize (Bonnett, 1953
; Cheng et al., 1983
; Stevens et al., 1986
) and landrace maize (Sundberg et al., 1995
). Although most maize and teosinte plants usually develop pure (unisexual) inflorescences, a mixed (bisexual) condition, more typical of Tripsacum dactyloides (L.) L. (Orr et al., 2001
), has been observed in some teosintes: Z. diploperennis plants (Sundberg and Orr, 1986
), and occasionally Z. parviglumis plants, exhibit an atypical sexual mixed condition in the A2 inflorescence (Orr et al., 2001
). Interestingly, Z. parviglumis (Doebley, 1990
; Bennetzen et al., 2001
), Z. diploperennis (Eubanks, 1995
, 1997
), and Tripsacum (Eubanks, 1997
, 2001a
, b
) have all been proposed progenitors of domesticated maize. A mixed sexual condition was not observed in the development of the A2 inflorescence of Z. nicaraguensis. Thus, our data are in agreement that the formation of a pure sexual inflorescence (staminate or pistillate) typifies the usual development pattern of teosinte inflorescences (Orr and Sundberg, 1994
). However, this developmental agreement does not exclude the possibility that the maize ear evolved from a sexual mixed (bisexual) inflorescence (Weatherwax, 1916
; Sundberg and Orr, 1986
; Sundberg, 1987
). Notably, both sexes can occur in the same maize inflorescence (Montgomery, 1906
; Weatherwax, 1916
; Dellaporta and Calderon-Urrea, 1994
).
Spikelets and florets
Our observations of Z. nicaraguensis inflorescence development are entirely concordant with the hypothesis that both maleness and femaleness in the genus Zea (teosinte and maize), subtribe Tripsacinae (Poaceae, Andropogoneae), were derived from a common developmental pathway (Orr and Sundberg, 1994
). Moreover, the development of Z. nicaraguensis inflorescences substantiates a view that all andropogonoid grasses exhibit a common pattern of inflorescence development (Francis, 1990
). Tassels and ears of Z. nicaraguensis are morphologically indistinguishable early in their development, except for the proximal long branches of the tassel. In Z. nicaraguensis distichously arranged branch primordia (spikelet pair primordia) gave rise to a pair of spikelets (pedicellate and sessile) along the central rachis of A1 inflorescences and A2 inflorescences. This is consistent with inflorescence development in other teosintes (Orr and Sundberg, 1994
; Orr et al., 2001
), the lateral long branches of maize tassels (Bonnett, 1953
; Cheng et al., 1983
; Sundberg et al., 1995
; Sundberg and Orr, 1996
), and eastern gamagrass (Orr et al., 2001
). Nevertheless, the distichous arrangement of spikelet pair primordia in Z. nicaraguensis inflorescences was inconsistent with the polystichous pattern of spikelet pair primordia in the maize ear and the central rachis of the maize tassel.
In the central spike of most tassels of Z. nicaraguensis all four rows of spikelets develop into a four-rowed inflorescence. In the ear the pedicellate spikelets abort leaving only two-rowed inflorescence. This developmental pattern is exhibited in other teosinte ears (Sundberg and Orr, 1990
; Orr and Sundberg, 1994
; Orr et al., 2002
) and the inflorescences of eastern gamagrass (Cámara-Hernández and Gambino, 1992
; Orr et al., 2001
). Pedicellate spikelets did not abort in small-eared "primitive" maize (Sundberg et al., 1995
; Sundberg and Orr, 1996
) nor do they in cultivated maizes (Cheng et al., 1983
; Orr et al., 1997
). We found no evidence of an aberrant restoration of pedicellate spikelets in Z. nicaraguensis that would support our previous morphological hypothesis (Sundberg and Orr, 1990
) that a termination of pedicellate spikelet abortion in a female, A2 teosinte inflorescence would result in paired spikelets—a condition similar to that found in a female A2 maize ear (Bonnett, 1953
). However, this putative developmental event (i.e., restoration of a paired spikelet condition) was deemed crucial in the evolution of the maize ear (Galinat, 1983
, 1985
).
The subsequent development of nonabortive spikelet primordia and florets in both male and female Z. nicaraguensis inflorescences was consistent with the hypothesis that a common mechanism exists for sex determination in the tribe Andropogoneae (Le Roux and Kellogg, 1999
). Zea nicaraguensis developed additional primordia chronometrically—outer glume, inner glume, outer lemma, lower floret, inner lemma, upper floret, and palea—in a sequential pattern. This pattern of spikelet development, the pattern of arrested and aborted development of lower florets in A2 sessile spikelets, and the development of stamen and ovule primordia in all functional spikelets was similar to other teosintes (Orr and Sundberg, 1994
; Orr et al., 2002
), small-eared "primitive" maize (Sundberg et al., 1995
; Sundberg and Orr, 1996
), cultivated maizes (Cheng et al., 1983
; Stevens et al., 1986
), and eastern gamagrass (Orr et al., 2001
). Furthermore, the key variations (Orr et al., 2001
) that differentiate teosinte inflorescences from maize inflorescences and Zea ears from Zea tassels were observed in Z. nicaraguensis. Thus, the development of functional spikelets and florets in Z. nicaraguensis was consistent with the hypothesis that development of femininity and masculinity in the genera Zea and Tripsacum were derived from a common pattern of inflorescence development. In fact, this pattern may have arisen prior to the evolutionary divergence of Zea and Tripsacum more than 4.5 million years ago (Hilton and Gaut, 1998
). Results from our studies in teosinte and "primitive" and cultivated maize are consistent with the idea that genes orchestrating the inflorescence developmental pathway in teosinte have been largely conserved in maize.
Orthostichies
A definitive characteristic of teosintes is a distichous inflorescence (Evans and Grover, 1940
; Orr and Sundberg, 1994
; Iltis, 2000
; Lauter and Doebley, 2002
). This characteristic distinguishes teosinte from the polystichous arrangement found in maize (Cheng et al., 1983
; Stevens et al., 1986
; Sundberg et al., 1995
; Sundberg and Orr, 1996
). In the 80–90 Z. nicaraguensis male (A1) and female (A2) inflorescences that we examined all exhibited a distichous (two-rank) condition, except for two male tassels that developed four ranks (polystichous) of spikelet pair primordia along the axis of the central spike (Fig. 10). This atypical polystichous arrangement of spikelet pair primordia observed in two Z. nicaraguensis tassels is consistent with a polystichous condition observed in some high-altitude Toluca teosinte inflorescences (Orr et al., 2002
). This four-rank orthostichy is characteristic for small-eared "primitive" maize (Sundberg et al., 1995
; Sundberg and Orr, 1996
), and is characteristic of the polystichous condition in maize ears and in the central spike of maize tassels (Iltis, 1983
; Galinat, 1985
).
Implications for maize inflorescence evolution
Although we do not understand the mechanism for the polystichous phenotype expressed in our Z. nicaraguensis population of tassels, one possibility is that it resulted from an altered expression of a major gene locus (Doebley and Stec, 1991
). An alternative perspective is that environmental stress can bring out unsuspected genetic potential in teosinte (Iltis, 1983
). A third option is maize-teosinte hybridization, which reveal hidden genetic potential for morphological traits in teosinte populations (Lauter and Doebley, 2002
). A final potential mechanism is that polystichous inflorescences in teosinte populations arise from maize introgression into teosinte (Orr et al., 2002
). Although we cannot rule out the possibility that maize alleles introgressed into the Z. nicaraguensis population sometime in the past, we think it is unlikely. The Cayanlipe collection site of Z. nicaraguensis is within a "gallery forest on a broad, flat, seasonally flooded lowlands island" (Iltis and Benz, 2000
, p. 386), and there was not a maize plant for miles (B. Benz, Texas Wesleyan University, personal communication). Furthermore, prior to 1954 the road from northwest Nicaragua to southern Honduras did not exist, and accordingly, there was very little habitation in the area where Z. nicaraguensis was growing (Robert Bird, Raleigh, North Carolina, USA, personal communication). Our results indicate the presence of a novel, polystichous inflorescence phenotype in this teosinte population. Although one of the morphologically invariant traits between teosinte and maize is phyllotaxy (distichous in teosinte and polystichous in maize), the Z. nicaraguensis population at the Cayanlipe collection site apparently contains heretofore hidden gene(s) that regulate the expression of polystichy.
Conclusions and perspectives
The patterns of inflorescence developmental in a newly discovered teosinte, Z. nicaraguensis, was revealed in this study and compared to inflorescence development in other teosintes, maize and gamagrass. The results were consistent with our hypothesis that both femininity and masculinity share a common mechanism of inflorescence development in Zea and Tripsacum and likely throughout the Poaceae. Our observations also were in accord with a putative common mechanism of sex determination in the Andropogoneae (Le Roux and Kellogg, 1999
).
Interestingly, our results revealed a novel inflorescence phenotype. We suggest this novel phenotypic variation raises the possibility that the domestic evolution of polystichy in maize inflorescences was enabled by the infrequent polystichous phenotypic in teosinte. Indeed, introgression of teosinte genes into races of maize is recognized in Mexico (Bird, 1979
; Wilkes, 1979
; Matsuoka et al., 2002
). However, the polystichous phenotype in Z. nicaraguensis raises a putative, but intriguing, view that the polystichous condition in maize may be more than a domestication query in regard to the evolution of the maize ear. Could polystichy in the maize ear have evolved from a genetic potential in the andropogonoid grasses as a whole? In light of this question, perhaps we should determine the existence, if any, of a possible relationship of distichy in the Andropogoneae to polystichy in the sister clade Paniceae.
Current thinking favors a hypothesis that teosintes are progenitors of cultivated maize (Doebley, 1990
; Galinat, 1992
; Iltis, 2000
; Benz, 2001
; Matsuoka et al., 2002
) and thus a potentially important source of germplasm for the improvement of cultivated maize. Observations of spikelet and floret development in our study revealed a pattern of inflorescence development similar to other teosintes and maize. This indicates that inflorescence development in Z. nicaraguensis plants, whose seed was derived from plants grown in flooded/waterlogged soils, is very stable. This is quite interesting since it is now evident that maize plants grown in waterlogged soils incur significant changes in gene expression (Subdaiah and Sachs, 2003
), photosynthetic capacity (Drew and Lauchli, 1985
), and axillary ear meristems growth (Lejeune and Bernier, 1996
). Zea nicaraguensis, noteworthy for its tolerance to a waterlogged environment and now for its stable expression of a reproductive pathway, could be a useful source of germplasm for maize breeding.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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