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2 Department of Biology, Colorado State University, Fort Collins, Colorado 80523-1878 USA; 3 EMBRAPA/CENARGEN, Caiza Pastal 02372 Brasilia/DF 70770-900 Brazil; and 4 Pioneer HiBred International, Inc., Johnston, Iowa 50131-1004 USA
Received for publication March 1, 1999. Accepted for publication November 9, 1999.
ABSTRACT
Two recessive male-sterile mutants of maize with similar patterns of pollen abortion were studied. Genetic studies showed that one of the two mutations was allelic with a previously identified male-sterility locus (ms23) and the other mutation was in a newly identified male-sterility locus (ms32). Cytological characterization of homozygous mutants and fertile heterozygous control siblings was performed using brightfield, fluorescence, and electron microscopy. During normal anther development, the final anther wall periclinal division divides the secondary parietal anther wall layer into the middle layer and tapetum, forming an anther with four wall layers. This is followed by differentiation of the tapetal cells into protoplastic binucleate, secretory tissue. In both the ms23 and ms32 mutants, the prospective tapetal layer divided into two layers, termed t1 and t2, forming an anther with five wall layers. Neither the t1 nor the t2 layers differentiated normally into tapetal layers, as determined by examination of cell walls, nucleus number, and cytoplasmic organization. Pollen mother cells aborted after the onset of prophase I of meiosis, suggesting that an early developmental coordination may exist between tapetum and pollen mother cells.
Key Words: maize • male-sterility • microsporogenesis • Poaceae • pollen development • tapetum
Pollen development in higher plants is a cooperative process requiring multiple interactions between the sporophytic plant and the developing male gametophyte. Sporophytic male-sterility results from mutations in genes expressed in diploid tissues that are required in the pollen developmental pathway. Such mutations have been identified in many plant species (Gottschalk and Kaul, 1974
; Kaul, 1988
), and some have been extensively characterized (maize—Beadle, 1932
; Albertsen and Phillips, 1981
; tomato—Rick, 1948
; Gorman and McCormick, 1997
; soybean—Graybosch and Palmer, 1988
; pea—Gottschalk, 1971
; Myers, Gritton, and Struckmeyer 1992
, Nirmala and Kaul, 1995
, and Arabidopsis—Dawson et al., 1993
; Chaudhury et al., 1994
; Peirson et al., 1996
). By comparing pollen development in these mutants with that in normal fertile plants, much can be learned about the cellular events involved in pollen development (Cheng, Greyson, and Walden, 1979
; Greyson, Walden, and Cheng, 1980
; Morton, Lawson, and Bedinger, 1989
; Loukides, Broadwater, and Bedinger, 1995
).
The maize anther is composed of several anther wall layers and of sporogenous tissue that undergoes meiosis to form haploid microspores. The four anther wall layers are the outer epidermis, the endothecium, one middle layer, and an inner wall layer called the tapetum that lines the anther locule. The tapetum is thought to play an important role in pollen development (Pacini, Franchi, and Hesse, 1985
; Chapman, 1987
) because (1) tapetal cells secrete nutritive materials and other substances into the anther locule, including a ß-glucanase that releases the microspore tetrads from their callose wall (Steiglitz, 1977
), (2) male-sterile mutants often have recognizable defects in tapetal structure, and (3) specific ablation of the tapetal cell layer causes male sterility (Goldberg, Beals, and Sanders, 1993
).
The formation of anther wall layers in monocots involves three successive periclinal divisions within the anther primordium (Davis, 1966
). The archesporial cell interior to the epidermis first divides to form the primary parietal layer and primary sporogenous cells; the primary parietal layer then divides to produce the endothecium and secondary parietal layer. The secondary parietal layer then divides periclinally a final time to form the middle wall layer and the inner wall layer that differentiates into the tapetum. Each wall layer expands by anticlinal divisions. In many plant species the tapetum has a dual origin, but in the grasses (Poaceae) the tapetum is derived from a single layer of cells produced by synchronous periclinal divisions entirely surrounding the sporogenous cells (Bhandari and Khosla, 1982
). In maize, the differentiation of the tapetum includes a nuclear division in the absence of cytokinesis, resulting in the formation of binucleate cells (Moss and Heslop-Harrison, 1967
; D'Amato, 1984
). The cytoplasm of tapetal cells becomes dense, rich with mitochondria, plastids, endoplasmic reticulum, Golgi, and vesicles. Cellulosic cell walls are dissolved on the locular and radial faces of the cells to form polar secretory protoplasts. Thus, tapetal differentiation involves coordinated changes in the nucleus, cytoplasm, and cell wall.
In this report we describe two male-sterile mutations of maize with an unusual phenotype; both produce a five-layered anther wall after a fourth periclinal division. The "extra" cells formed by this division do not undergo any of the differentiation events in normal tapetal cells. Pollen mother cells appear to be normal in structure and enter prophase I of meiosis but then abort, resulting in male-sterility.
MATERIALS AND METHODS
Materials
Plants were grown either in glasshouses at Colorado State University or in fields at the Agricultural Research, Development and Education Center in Fort Collins. The ms23 mutant was from stocks derived from the originally described spontaneous male-sterile mutation (West and Albertsen, 1985
). Two other male-sterile mutants, ms*-SB29 and ms*-SB131, were from a series of Robertson's Mutator-containing families segregating for male-sterility as identified by lack of anther exertion. Young spikelets were collected from immature tassels at 2–3 d intervals from the mid-portion of tassels from plants segregating 1:1 for male-sterile:male-fertile plants. Samples were placed on ice in polypropylene tubes containing 0.5 mL 0.15 mol/L NaCl. For each mutant, multiple plants were sampled to assure collection of a series of developmental stages of both heterozygous fertile and homozygous male-sterile anthers. Young and old anthers from a spikelet were squashed on glass slides and observed with a dissection microscope to assess the pollen developmental stage. Selected anthers were fixed and processed for microscopy. Sampling was performed from four separate plantings, two in the field and two in the greenhouse. More than three samples of each representative stage were examined from each planting. A portion of the tassel was left intact on sampled plants for examination and scoring for anther exertion at anthesis. Plants had to be sacrificed to obtain the very young ms23 anthers in Figs. 1 and 2, but because the line used consistently produced tillers, it was possible to determine fertility or sterility.
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. DNA was subjected to restriction digestion, gel electrophoresis, and DNA blotting. Approximately 60 restriction fragment length polymorphism (RFLP) markers, evenly dispersed throughout the genome, were used to screen the DNA blots. Genetic linkage was confirmed by using a DNA blot comprising ms*-SB29 male-sterile individuals that was hybridized with the polymorphic markers.
Allelism
A series of allelic crosses were made among the three male-sterile mutants and the available maize male-sterile mutants using the homozygous male-sterile plants (msms) as female and known heterozygotes (Msms) as pollen donors. Crosses between ms23 and ms*-SB131, performed in either direction (ms23 plants as male or female) produced male-sterile plants in the next generation in the predicted 1:1 ratio, with 25/51 plants exhibiting a male-sterile phenotype. Crosses between ms*-SB29 and all of the available maize male-sterile mutants produced no sterile plants (Table 1).
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) for 7 min, and examined with a JEOL 2000EXII transmission electron microscope. For cellulose fluorescence, thick sections were incubated for 2 h in 0.1% aqueous Calcofluor White (MR2) and rinsed with water. Slides were examined for fluorescence, using a 360–370 nm excitation filter, a 400 nm dichroic mirror, and a 420 nm barrier filter.
RESULTS
Initial results
Two recessive male-sterile mutants (ms*-SB29 and ms*-SB131) from maize lines containing the Robertson's Mutator transposable element system (Chandler and Hardeman, 1992
) were identified. In homozygous mutants, young anthers having sporogenous cells and three newly formed, cytoplasmically dense anther wall layers (stage IIa according to Greyson, Walden, and Cheng, 1980
) appear to be identical to those of control heterozygotes (Figs. 1, 2). However, in slightly older anthers from homozygous mutant plants (four wall layers, no callose in the sporogenous tissue, stage IIb) the innermost cell layer undergoes an additional periclinal cell division (Figs. 6, 9), resulting in five anther wall layers by stage III, central callose (Figs. 7, 10). The extra cell division results in similar-sized "t1" and "t2" daughter cells (e.g., Fig. 9). Both cells become vacuolate, with thin strands of cytoplasm (Figs. 7, 10); the inner "t2" cells elongate, becoming finger-like projections extending into the anther locule (Figs. 8, 11). By examining light micrographs such as that shown in Fig. 8, we initially thought that further divisions commonly occurred to produce additional cell layers. However, both Calcofluor WhiteMR2 staining of cell walls (see Fig. 15) and TEM analysis (data not shown) indicated that most commonly only five wall layers were formed, with thin strands of cytoplasm giving the impression of the presence of extra cells in light micrographs. Rarely (one cell observed in 50 sections), mitotic chromosomes can be seen in the "t2" cell (data not shown). In homozygous sterile plants, pollen mother cells abort prior to completing meiosis (Figs. 8, 11, also see below). In normal anthers from heterozygous sibling plants, pollen mother cells undergo meiosis to form meiotic dyads and tetrads (Fig. 5).
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), produced segregating 1:1 male-sterile:male-fertile plants in the next generation (25 sterile/51plants). ms*-SB131 is therefore allelic with ms23 and is henceforth called ms23-SB131. Crosses of all described male-sterile mutants of maize with ms*-SB29 produced no sterile plants (Table 1); therefore ms*-SB29 is a newly identified male sterility locus, henceforth called ms32.
Bulk segregant analysis of the ms32 mutation revealed polymorphism with RFLP markers UMC131 and UMC139 on the long arm of chromosome 2. Subsequent genotype analysis of the male-sterile individuals with UMC131 and UMC139 showed 17 (42.5%) and 10 (25%) recombinant alleles, respectively, out of 40 alleles total. Both markers having recombinant individuals in common suggests that the ms32 gene maps distally to UNC139 on the long arm of chromosome 2. The male-sterile mutant ms23 had been previously shown to map to the long arm of chromosome 3 by the use of AB-interchanges (Albertsen, 1988
). Thus, while the phenotypes of the ms23 and ms32 mutants are very similar, the two genes are unlinked.
Cells produced by auxiliary cell division do not differentiate
Anthers in mutant plants were examined to determine whether the two cell layers closest to the sporogenous cells ("t1" and "t2") underwent any of the known cellular events that mark normal tapetal cell differentiation. First, anther sections were stained with Calcofluor White MR2 to test for the presence of a cellulose cell wall, as shown in Figs. 12–15. In the anthers of heterozygous, fertile sibling plants, cellulose-containing cell walls surrounding tapetal cells disappear during meiosis and are completely gone at the tetrad stage (Figs. 12, 13). In contrast, the "t1" and '"t2" cell layers in mutant plants retain their cellulose cell walls, even after pollen mother cell abortion (Figs. 14, 15).
All anther cell types from mutant plants were inspected with transmission electron microscopy (TEM) to determine whether any unusual subcellular features could be observed (Figs. 16–19). The epidermis, endothecium, and middle layer in anthers from sterile mutant plants were similar to those from anthers of fertile heterozygous sibling plants. After pollen mother cells had aborted, epidermal cells become highly vacuolated and acquire a ridged, cutinized surface, as do epidermal cells in normal anthers. Endothecial cells elongate normally, becoming rectangular, and accumulate starch granules. The middle layer remains undifferentiated, with a few starch granules. Only the tapetal cells varied significantly between fertile and sterile plants. The tapetal cells in heterozygous sibling control plants have a characteristically dense cytoplasm, with numerous organelles and two nuclei (Figs. 16, 17). In contrast, the "t1" and "t2" cell layers in mutant plants contain a large vacuole and are quite similar in structure to the parenchyma-like middle layer cells (Figs. 18, 19). Examination of serial and longitudinal sections of the "t1" and t2" layers failed to detect any binucleate cells. Thus, the auxiliary anther cells formed in mutant plants had none of the distinguishing nuclear, cytoplasmic, or cell wall features of differentiated tapetal cells.
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In the nucleus of the pollen mother cells in sterile plants, chromosomes are condensed and synaptonemal complexes—structures found only in meiotic prophase I—are observed (Figs. 24, 25). In cross sections, the components of the synaptonemal complexes were measured as follows: lateral elements—50 nm; central region—100 nm; central element—40 nm. These values are typical for maize synaptonemal complexes (Gillies, 1973
).
DISCUSSION
Much can be learned about normal development by ablation of genes specifically required for a developmental process. We have described two unlinked genes, identified as recessive male-sterile mutants, required for normal pollen development: a new allele of ms23 (ms23-SB131) and ms32, representing a new male-sterility locus. In the homozygous condition, both mutations cause the inner parietal layer of the developing anther to undergo a supernumerary division to form an anther wall with five, rather than the normal four cell layers. The resulting cells do not differentiate a functional tapetum and pollen mother cells abort prior to completion of meiosis. The "t1" and "t2" cells retain their cellulose cell walls, become vacuolate, and are uninucleate. It is significant that although the primary defect appears to be in tapetal cell differentiation, the meiocytes are affected as well. While the essential role of a highly secretory tapetum in microspore development after meiosis is widely accepted, an earlier role for the tapetum in pollen development is less established and is supported by our results.
The phenotype of these mutants appears to be unique, but there are some similarities with known male-sterile mutants that affect normal tapetal differentiation. In the ms9 male-sterile mutant of maize, plasma membranes are elaborated between two tapetal nuclei in 20% of the tapetal cells in sterile plants (Greyson, Walden, and Cheng, 1980
). However, this occurs at stage III (central callose stage), later than we observe divisions (stage IIb), and no cell walls appear to develop at the site of the new membrane in ms9 plants. In ms9, the primary defect appears to be in pollen mother cells, which accumulate abnormal, darkly staining bodies. The tapetal cells of the ms2 male-sterile mutant of soybean retain their cellulose cell walls, but tapetal differentiation is initiated, and meiosis is completed prior to abortion of microspores (Graybosch and Palmer, 1985
). In the ms5 male-sterile mutant of tomato, tapetal cells on the abaxial side of the anther do not differentiate normally, possibly due to the presence of excess sporogenous cells (Rick, 1948
). In the stamenless-2 mutant of tomato, differentiated tapetal cells undergo an additional division in some parts of the anther (Sawhney and Bhadula, 1988
), and in one type of cytoplasmic male sterility in Brassica napus, a proliferation of differentiated tapetal cells occurs (Grant, Beversdorf, and Peterson, 1986
). A male-sterile mutant of Cucurbita maxima has a phenotype most similar to that of ms23 and ms32 of maize in that there is a uniform bilayer of tapetal cells in the anther locule (Francis and Bemis, 1970
). However, it appears that in this case the division to form a tapetal bilayer occurs during meiosis, after tapetal differentiation.
Both of the genes identified by these mutations are sporophytic, i.e., genes expressed in diploid cells. It is possible that either or both of the genes encode a factor(s) regulating cell division number in the secondary parietal or tapetal cell layers. The extra cell division in both mutants occurs at the four-layer precallose stage IIb (Figs. 6, 9). This is earlier than the normal nuclear division in tapetal cells that leads to a binucleate state, which in maize occurs during pachytene of the first meiotic division (Moss and Heslop-Harrison, 1967
). The extra divisions to produce t1 and t2 are complete by the time the meiocytes are surrounded by callose (Figs. 7, 10). Therefore, we tentatively conclude that the divisions seen in both of these mutants represent extra cell divisions rather than the lack of inhibition of cytokinesis after normal nuclear division in tapetal cells. Future cloning of the affected genes, with careful gene expression studies, will clarify this issue.
The primary defect in these mutants appears to be the absence of a differentiated tapetum. In both alleles of ms23, and in ms32 mutants, the pollen mother cells initiate, but do not complete, meiosis. Thus, the mutant phenotypes described here may result from interference with intercellular communication in the developing anther prior to meiosis. It is possible that the ms23 and ms32 genes are expressed in sporogenous cells, rather than in the secondary parietal cells or tapetal cells. It is thought that sporogenous cells may play a role in the differentiation of tapetal tissue. In many plant species the tapetum has a dual origin (Boke, 1949
; Esau, 1965
). In these cases, the "outer" tapetum is derived from the successive periclinal divisions of subepidermal cells, whereas the "inner" tapetum (closest to the vascular tissue in the filament) differentiates from the connective cell layer adjoining the sporogenous cells. This is suggestive of an inductive role for the sporogenous cells in forming at least the inner tapetum. Although in the Poaceae the entire tapetum appears to be derived from periclinal division of cells surrounding the sporogenous cells (Bhandari and Khosla, 1982
), an inductive activity in the sporogenous cells or PMC could still be important for tapetal differentiation in the grasses.
Both the ms32 allele and the ms23-SB131 allele reported here are derived from Robertson's Mutator lines of maize. This transposable element system has been used successfully to isolate genes by transposon tagging (Chandler and Hardeman, 1992
; Walbot, 1992
). Maize transposable elements have been used to tag and then isolate male-sterility genes in both Arabidopsis (Aarts et al., 1993
) and maize (Albertsen, Fox, and Trimnell, 1993
). Future cloning, sequencing, and localization of expression of the ms23 and ms32 genes will be critical in distinguishing between the above models for the roles of these genes in regulating tapetal cell division and differentiation.
FOOTNOTES
1 The authors thank Dr. Steve Stack, Dr. Lorinda Anderson, and John Anderson for suggestions and critical reading of the manuscript, and the Agricultural Research Development and Education Center for field space and management. This work was supported by USDA NRI grants, number 95-37300-1576 and number 97-1380-04. 
5 Author for correspondence (e-mail: bedinger{at}lamar.colostate.edu
)
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