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Reproductive Biology |
2Department of Botany and Bessey Microscopy Facility, 3USDA Agriculture Research Service and Corn Insects and Crop Genetics Research Unit and Departments of Agronomy and of Zoology/Genetics, Iowa State University, Ames, Iowa 50011 USA
Received for publication May 11, 2001. Accepted for publication August 28, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: cytoplasmic male sterility • Glycine max • Glycine soja • Leguminosae • male cells • mitochondria • pollen • soybean • tapetum
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Hanson and Conde, 1985
; Schnable and Wise, 1998
; Mackenzie and McIntosh, 1999
; Wise et al., 1999a, b
). The CMS genotypes can arise in plants spontaneously, through intergeneric- or interspecific-wide crosses or through recurrent backcrossing of a CMS cytoplasm with a nonrestoring nuclear genome (Shivanna and Sawhney, 1997
). Interaction between the maternally inherited sporophytic genome and the paternally inherited nuclear genome is the suspected cause of the CMS condition leading to degeneration of the mitochondria (He, Lyznik, and Mackenzie, 1995
; Mackenzie and McIntosh, 1999
; Liu et al., 2001
). The mitochondrial genome frequently undergoes extensive rearrangement, which may lead to assembly of unusual, novel, chimeric gene products. The products may be produced in varying copy numbers in individual mitochondria, resulting in a heterogeneous mitochondrial population (Mackenzie and Chase, 1990
).
The CMS systems of Zea mays L. Texas (T)- and USDA (S)-cytoplasms, Brassica, Petunia, Phaseolus vulgaris, Helianthus, and Nicotiana have been investigated at the molecular level (Hanson and Conde, 1985
; Hanson, 1991
; Schnable and Wise, 1998
; Wen and Chase, 1999a, b
; Liu et al., 2001
). Sequences so far identified are mutations in the atp, cox, or nad genes. Ding, Gai, and Yang (1999)
characterized a mutation in a CMS soybean line (NJCMS1A) and its maintainer line (NJCMS1B) possibly associated with the coxI gene.
Published microscopic studies are in agreement with molecular evidence indicating that mitochondrial deterioration in the tapetum occurs prior to degeneration, and in some cases also in the parietal layer (Mackenzie and McIntosh, 1999
; Wise et al., 1999a
). In most studies, deterioration of anther tissues occurs during microsporogenesis either shortly before or after meiosis II (Laser and Lersten, 1972
; Hanson, 1991
; Newton and Gabay-Laughnan, 1998
).
Soybean, like maize, is a major crop worldwide. Several CMS genotypes have been described in soybean (Gai et al., 1995
; Sun, Zhao, and Huang, 1997
; Zhang and Dai, 1997
) but they have not been thoroughly characterized by molecular techniques, and none of the CMS genotypes have been characterized by microscopic techniques. One of the CMS soybean lines (Sun, Zhao, and Huang, 1997
), resulting from an interspecific cross between a wild-type Chinese Glycine max (L.) Merr. and a wild annual G. soja Sieb. and Zucc., is the focus of this microscopic study. The CMS A-line resulting from this cross, as well as two fertility-restored (FR) lines, were subjected to extreme photoperiod and temperature regimes (Smith, Horner, and Palmer, 2001
) to challenge their environmental stability for expression of sterility. The CMS A-line remained completely sterile under all environmental conditions tested and, therefore, prompted further investigation by microscopic methods to determine how its cytology and development compared with CMS taxa from other genera. This microscopic investigation focuses on the changes that occur during microsporogenesis and microgametogenesis under normal as well as three different environmental regimes.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) and two proprietary FR lines were obtained from Pioneer Hi-Bred International (Johnston, Iowa, USA) for this study. The seeds were germinated in pots in growth chambers programmed for three photoperiod/temperature regimes (Smith, Horner, and Palmer, 2001)
. The purpose of these three regimes was to test the three lines for their ability to developmentally maintain fertility or sterility during microsporogenesis and microgametogenesis.
Anther/bud collection and processing
Young buds as well as open flowers at several stages were collected for viewing with light (LM) and transmission electron microscopy (TEM). Anthers were dissected from the open flowers, whereas flower buds were left intact. All organs were placed into cold (4°C) primary fixative of 3% paraformaldehyde and 3% glutaraldehyde in 0.1 mol/L sodium cacodylate buffer at pH 7.3. Each flower was submersed into a drop of cold primary fixative during dissection of the anthers. If whole buds were fixed, they were cut at the base of the flower and placed in the fixative in a vacuum of 
1.33 Pa for 1–1.5 h, followed by one change of fixative. All samples were kept in the primary fixative at 4°C ranging from 8 h to up to 3 d. In the latter case, the primary fixative was replaced every 24 h. Primary fixation was followed by three 15-min washes in 0.1 mol/L cacodylate buffer, after which the specimens were postfixed in 1% osmium tetroxide in the same buffer for 1–1.5 h at room temperature. The secondary fixative was followed by one 15-min wash in the same buffer and two 15-min washes in distilled water.
Specimens were dehydrated through a graded ethanol series and infiltrated and embedded with Spurr's resin (Electron Microscopy Sciences, Fort Washington, Pennsylvania, USA; hard mixture). One-micrometer-thick cross sections of anthers were cut with glass knives and stained with 1% toluidine blue in 1% borax for 30 sec on a hot plate, rinsed with distilled water, and air dried. Permount (Fisher Scientific, Fair Lawns, New Jersey, USA) was added to the sections and coverslips were placed over them.
Light microscope carbohydrate histochemistry
Representative thick sections were placed on acid-cleaned glass slides, treated in 10% hydrogen peroxide for 30 min to remove the osmium tetroxide, hydrolyzed, and stained with the Periodic-Acid-Schiff's (PAS) technique (Berlyn and Miksche, 1976
). Thick sections were viewed with a Leitz Orthoplan light microscope (Leica Microsystems Inc., Deerfield, Illinois, USA) and photographed using Kodakchrome 64T 35 mm film (Eastman Kodak, Rochester, New York, USA).
Transmission electron microscope
Thin sections of approximately 60–80 nm were cut with a diamond knife and were placed on 300-mesh, uncoated copper grids, or on Formvar-coated, slotted or 50-mesh copper grids. Thin sections for TEM were stained with 20% methanolic uranyl acetate for 30–45 min, rinsed with 50% methanol, rinsed with distilled water, and the water was wicked off. They were counterstained with Reynolds lead citrate (Reynolds, 1963
) for 10–20 min, rinsed with distilled water, and the water was wicked off. The sections were viewed with a JEOL 1200EX TEM (JEOL, Peabody, Massachusetts, USA), and images were recorded on Kodak (Eastman Kodak) SO-163 film.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Anther development in FR plants, under normal growing conditions, followed the standard sequence as described by Laser and Lersten (1972)
, Buntman and Horner (1983)
, and Horner and Palmer (1995)
. Stages in anther development used in this study are according to Horner and Palmer (1995)
.
Light microscopy, anther development
No structural and/or histochemical (carbohydrate) differences were observed among anther tissues (e.g., anther wall layers, tapetum, sporogenous cells, connective tissue, and vasculature) at the sporogenous mass to tetrad stages, and they are not shown. Early- and late-microspore and mid-pollen stages of FR anthers (Figs. 1–3) appear different than CMS anthers at the same stages (Figs. 4–9). In CMS anthers, the first abnormalities in the tapetum were detected during mid- (Fig. 4) to late-vacuolate- (Fig. 5) microspore stages, becoming more distinct in pollen stages (Figs. 6–9). Structural changes in CMS anthers and changes in stain affinity of the tapetum exhibited the following characteristics, sometimes in the same anthers: (1) premature tapetal cell layer degeneration, often first seen in one portion of the tapetum as a darkly stained and later as a collapsed and flattened mass (Figs. 5 and 8, arrowheads); (2) persistence and hypertrophy of the tapetal cell layer (at a stage when FR tapetum displayed degeneration) (Figs. 5 and 6, arrowheads); (3) lightly stained and enlarged tapetal cells (Figs. 5 and 7); (4) inner tangential wall of tapetum persisted until late pollen stages or, if disrupted, tapetal contents could be found dispersed in the locule (Fig. 6); and (5) and premature secondary wall deposition in the endothecial layer (Figs. 7–9, asterisks). Endothecial wall formation in FR anthers occurred during mid- to late-pollen stages (Fig. 3) when the partially degenerated and shrunken tapetum was still visible as an intact cell layer. In CMS anthers, tapetal changes seemed to be associated with premature secondary wall deposition in the endothecial layer and premature pollen formation.
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Light microscopy, temperature and photoperiod treatments
Elevated temperatures of 32°C light/24°C dark and a floral induction period of 13 h light/11 h dark (Smith, Horner, and Palmer, 2001)
accelerated the abortive process in CMS anthers. In contrast, cooler temperatures of 25°C light/15°C dark and a constant photoperiod of 14 h light/10 h dark (Smith, Horner, and Palmer, 2001
) slowed down the abortive process.
At elevated temperatures, CMS anthers demonstrated a faster rate of tissue maturation and degradation (Figs. 10–12). The effects of the increased rate were apparent as vacuolation of the tapetum started soon after meiosis II. Ultimately, the pollen grains aborted, sometime after the early pollen stage (Figs. 11 and 12).
The cool temperature/continuous photoperiod treatment induced the opposite results (Figs. 13–15). Although no viable pollen grains or seeds were produced from CMS plants, anthers showed some pollen grains that were minimally filled with reserves (Fig. 15); no cross-pollinations were conducted with the FR plants. Personal communication with H. Sun (Jilin Academy of Agricultural Sciences, Gongzhuling, Jilin Province, Chinca) indicated that no CMS pollen grains germinated under any conditions tested). The overall developmental process, however, was similar to that described for FR anthers, including tapetal degeneration (Figs. 14 and 15).
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Beginning approximately at late-microspore to early-pollen stages, progressive differences between FR and CMS anthers became apparent. The FR anthers showed an overall increase in PAS-positive staining in pollen grains, which was due to accumulation of small granular material (Fig. 18). At the latest CMS pollen stage observed (Fig. 21), staining of anther wall cells also decreased, and very few PAS-positive-staining starch granules could be found near the connective tissue of the filament.
Transmission electron microscopy, development
No differences in ultrastructure were detected between CMS and FR anthers from plants grown under normal conditions. However, the onset of degradation in CMS anthers varied, beginning as early as the early-microspore stage or as late as the late-microspore stage. In general, differences in organelle structure first became discernible at mid-microspore stage and persisted throughout later development.
From early- to late-microspore stages, mitochondria in the tapetum of CMS anthers displayed a structural disorganization/degradation of the inner membrane, and/or an enlargement of cristae, forming large internal lacunae (Figs. 23a–e and 29). Concurrent with mitochondrial deterioration in the tapetum, about mid- to late-microspore stages, whorls of endoplasmic reticulum (ER) were seen; the most extreme of these were large, densely wound ER coils (Fig. 23a). The whorls of CMS tapetal ER sometimes encircled vacuoles and/or electron-dense material (presumably lipid bodies) (Fig. 23a) and, although the ER was in close association with many ribosomes, no microbodies were associated with these whorls. However, microbodies were associated with CMS ER in anthers at the very onset of formation of the ER whorls (Fig. 22a–c). In contrast, in FR anthers the tapetum displayed normal, parallel arrays of ER (Fig. 24) and microbodies. Mitochondria of FR anthers (Fig. 24) appeared normal in tapetal cells. At approximately mid- to late-microspore stages, tapetal plastids of FR anthers contained many discrete bodies of electron-dense material (Figs. 25, 27, 28; arrowheads).
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In FR anthers, tapetal degeneration was not seen until the pollen grains were almost completely engorged. Figures 27 and 30 show portions of the tapetum and a pollen grain at mid- to late-pollen stages, respectively, with electron-opaque and electron-dense bodies.
The pollen exine appeared similar in thickness between CMS and FR anthers, but seemed to be initiated and completed much earlier in CMS anthers and had only a rudimentary intine (Fig. 32). In FR anthers, pollen wall formation was completed relatively late, at very late pollen stage, after tapetal degeneration (Fig. 30), and appeared to have a thicker intine.
Pollen degeneration in CMS anthers followed a pattern similar to that in the tapetum. The mitochondrial inner membranes appeared to have degenerated (Fig. 32). Plastids and cytoplasm (Fig. 31) displayed very little spherical electron-dense material. Ultimately, plastids in CMS pollen manifested an undulating outer membrane (Fig. 31, arrowhead). At late-pollen stage, there were large cytoplasmic vacuoles and unstructured, densely staining material (Fig. 32, asterisks) that was not confined to the dense bodies. The CMS pollen cytoplasm was filled with degenerated organelles, and cell debris (not shown). In contrast, FR pollen grains gradually filled first with opaque and later with electron-dense material, which made them fully engorged at the late-pollen stage. Mitochondria and plastids remained intact (Fig. 33).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Lee, Gracen, and Earle, 1979
; Wise et al., 1999a
). These variations were found in different anthers, in different locules of the same anther, and in the same locule in some anthers.
The PAS-staining procedure for water-insoluble carbohydrates showed a similar staining pattern in CMS and FR soybean anthers at the end of meiosis II. Although carbohydrates were detected in CMS microspores early in development, little or no PAS-positive material was discernible from the middle or parietal layer later. The TEM observations indicated that mitochondrial degeneration had begun by this time. After endothecial wall formation and microspore mitosis in the CMS line, PAS-positive material was minimal in pollen grains. In contrast, FR anthers showed that the pattern of staining progressed inwards from anther walls and vascular strands to pollen grains. Abnormal carbohydrate metabolism in male-sterile anthers has been found repeatedly in CMS and genic male-sterile systems in many plants (Artschwager, 1947
; Fukasawa, 1962
; Kini, Seetharam, and Joshi, 1994
), and this appears to be the case with the CMS soybean in our study.
Endothecial wall formation in FR anthers occurred normally when the pollen grains were filling. In CMS anthers, endothecial wall formation occurred earlier, during late-microspore to early-vacuolate pollen stages. By this latter stage pollen grains were arrested. From TEM results, CMS mitochondria at this developmental stage were already in varying degrees of degeneration, which is similar to the degeneration observed in maize under these conditions (Wen and Chase, 1999a, b
). These differences in development, ultrastructure, and carbohydrate localization between CMS and FR anthers indicated a connection among the events of mitochondrial degeneration, endothecial wall formation, microspore mitosis, and carbohydrate influx, and utilization. This association has been noticed in anthers of different plant species (De Fossard, 1969
; Horner and Rogers, 1974
; Chauhan, 1979
; Chauhan and Kinoshita, 1980a, b
).
The heterogeneous mitochondrial population in CMS anthers, in general, varied in size and degree of degradation at different times in development. Microscopic studies by Warmke and Lee (1977)
, Bino (1985)
, Hack et al. (1991)
, and Majewska-Sawka et al. (1993)
identified mitochondrial membrane deterioration at meiosis II, or shortly thereafter, in tapetum and microspores of T-CMS maize and sugar beet. Such mitochondrial degeneration also has been found in diverse vegetative tissues under hypoxic or anoxic stress (Morisset, 1983
; Davies, Kenworthy, and Mocquot, 1987
; Vartapetian, Snkchian, and Generozova, 1987
; Vartapetian and Zakhmilova, 1990
; Vartapetian and Poljakova, 1994
), in conjunction with concentric whorls of ER. Both structural aberrations have been reported in excised tomato roots (Morisset, 1983
), in pea roots (Couée et al., 1992
), wheat seedlings (Vartapetian and Zakhmilova, 1990
), maize seedlings (Vartapetian, Snkchian, and Generozova, 1987
), rice shoots (Couée et al., 1992
), in a variety of fruits (Asker and Davies, 1985
), and Brugmansia pollen tubes (Walles and Han, 1998
). Vartapetian, Snkchian, and Generozova (1987)
and Davies, Kenworthy, and Mocquot (1987)
suggested that the concentric arrangement of ER was the result of a low cell-energy status, in which the concentric whorls represent a more stable configuration of the ER that requires less energy than the extended arrangement. The literature concerning anoxia studies and knowledge from bioenergetics (Harold, 1986
), together with the microscopic evidence from our study, indicates that degradation of the inner mitochondrial membrane mimics anoxia.
In the early stages of mitochondrial degeneration in CMS soybean anthers, at the onset of appearance of ER whorls, microbodies were associated with the ER but were later excluded from the tight whorls. Although mitochondrial degeneration seemed to be the initial dysfunction, malfunction or absence of microbodies could further depress the energy level in the tapetum by impeding detoxification of hydrogen peroxide, beta-oxidation, and gluconeogenesis. Microbodies (depending upon their function in a particular tissue) are known to carry out a variety of metabolic processes (Huang, 1998
). The current concept of microbody biogenesis postulates that matrix enzymes are encoded by nuclear genes, synthesized on free polyribosomes, and post-translationally exported into already-formed cell "ghosts" (Huang, 1998
). For this to occur, however, ATP must be available (Huang, 1998
). The lack of water-insoluble carbohydrates, presence of ER whorls, as well as mitochondria with degraded inner membranes, indicated a lack of ATP in the CMS tapetum, which could account for the absence of microbodies. De Bellis et al. (1989)
found that rice coleoptile peroxisomes under anoxia were present in reduced numbers, had depressed enzyme activity, and that their organelle matrices appeared less dense.
During microsporogenesis and early microgametogenesis the tapetum is a tissue with high-energy demand. In maize, a forty-fold increase in the number of mitochondria in tapetal tissue occurred at the time of pollen development (Lee and Warmke, 1979
), which is an indication of the need for a high rate of aerobic respiration and energy turnover. Although mitochondria in all tissues of CMS soybean anthers were of the same genetic constitution, the effects of impaired mitochondria were only expressed in tissues of concentrated high-energy demand. Results from tobacco pollen grain fermentation experiments (Bucher, Brändle, and Kuhlemeier, 1994
; Bucher et al., 1995
; Tadege and Kuhlemeier, 1997
; op den Camp and Kuhlemeier, 1997
), and from the studies by Vartapetian, Snkchian, and Generozova (1987)
, Vartapetian and Zakhmilova (1990)
, and Vartapetian and Poljakova (1994)
on anoxia/hypoxia suggested that the availability of sugar, and not oxygen, was controlling the flux through the fermentation pathway. When sucrose supply was low, or there was a high demand from sinks, the TCA cycle was preferred over the fermentation pathway because it supplies more energy. In CMS soybean anthers, sugar availability was abundant at meiosis, before tapetal degradation but after mitochondrial degradation sugar flux appeared to be less abundant, as evidenced by the low PAS staining. As a consequence, energy production by both pathways could be depressed or halted.
In a CMS line Ding, Gai, and Yang (1999)
showed that the aberrant mitochondrial sequence is associated with the coxI gene. Given previous molecular research on mitochondrial genome mutations (Laughnan and Gabay-Laughnan, 1983
; Hanson and Conde, 1985
; Newton, 1988
; Hanson, 1991
; Janska and Mackenzie, 1993
; Mackenzie, 1996
; Newton and Gabay-Laughnan, 1998
; Mackenzie and McIntosh, 1999
), as well as microscopic evidence, it is possible that in the tapetum of CMS soybean anthers, mitochondrial chimeric sequences resulting from aberrant mitochondrial-nuclear interactions may have disrupted gene products needed for normal cell energy production. This possibility is becoming clearer as more studies dealing with restorer genes are completed (Liu et al., 2001)
.
In CMS soybean, mitochondrial breakdown differed between tapetum and pollen grains. In the latter, cristae typically appeared swollen and developed large inner lacunae. Some tapetal mitochondria also exhibited such changes. The swollen appearance of mitochondria in the pollen grains and tapetum resembled that of leaf mitochondria from Arabidopsis thaliana L. mutants, in which the heteromeric acetyl Coa-carboxylase (ACCase) biotin carboxyl carrier protein (BCCP) subunit was eliminated (H. R. Qian, B. L. Fatland, and E. S. Wurtele, Iowa State University, personal communication).
Even though the tapetum has other functions than supplying nutrients for developing microspores and pollen grains (Hesse and Hess, 1993
; Pacini and Franchi, 1993
; Rudramuniyappa and Manure, 1993
), nutrition of pollen grains is certainly important. If this function is not fulfilled, because of premature tapetal shutdown and disintegration, then CMS male cells show signs of starvation. In addition, the extreme temperature/photoperiod treatments either hastened or slowed down the shutdown and disintegration of the tapetum but did not reverse sterility. This indicates that the CMS line is stable and useful under a range of environments. Thus, the possibility of mitochondrial dysfunction in both the gametophytic microspores and pollen grains and the sporophytic tapetum is supported by evidence from our LM and TEM results that show a lack of pollen grain reserves, premature cell degeneration, and ultimately male sterility.
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FOOTNOTES |
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4 Author for reprint requests (tel: 515-294-8635; fax: 515-294-1337; hth{at}iastate.edu
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Asker H. D. D. Davies 1985 Mitochondrial aldehyde dehydrogenase from higher plants. Phytochemistry 24: 689-693[CrossRef][ISI]
Berlyn G. P. J. P. Miksche 1976 Botanical microtechnique and cytochemistry. Iowa State University Press, Ames, Iowa, USA
Bino R. J. 1985 Ultrastructural aspects of cytoplasmic male sterility in Petunia hybrida. Protoplasma 127: 230-240[CrossRef][ISI]
Bucher M. K. A. Brander S. Sbicego T. Mandel C. Kuhlemeier 1995 Aerobic fermentation in tobacco pollen. Plant Molecular Biology 28: 739-750[CrossRef][ISI][Medline]
Bucher M. R. Brändle C. Kuhlemeier 1994 Ethanolic fermentation in transgenic tobacco expressing Zymomonas mobilis pyruvate decarboxylase. EMBO Journal 13: 2755-2763[ISI][Medline]
Buntman D. J. H. T. Horner Jr 1983 Microsporogenesis of normal and male sterile (ms3) mutant soybean (Glycine max). Scanning Electron Microscopy II: 913-922
Chauhan S. V. S. 1979 Development of endothecium in relation to tapetal behaviour in some male sterile plants. Phytomorphology 29: 245-251
Chauhan S. V. S. T. Kinoshita 1980a Anther ontogeny in genic, cytoplasmic and chemically induced male sterile plants. Japanese Journal of Breeding 30: 117-124[ISI]
Chauhan S. V. S. T. Kinoshita 1980b Morphological and histochemical studies on pollen degeneration in cytoplasmic male-sterile sugar beet (Beta vulgaris L. var. saccharifera). Journal of the Faculty of Agriculture Hokkaido University 59: 323-331
Couée I. S. Defontaine J.-P. Carde A. Pradet 1992 Effects of anoxia on mitochondrial biogenesis in rice shoots. Plant Physiology 98: 411-421
Davies D. D. P. Kenworthy B. Mocquot 1987 The effects of anoxia on the ultrastructure of pea roots. In R. M. M. Crawford [ed.], Plant life in aquatic and amphibious habitats, 265–277. Blackwell Scientific Publications, Oxford, UK
De Bellis L. N. Rascio L. Pistelli A. Alpi 1989 Peroxisomes in rice coleoptiles grown in air and in anoxia. Botanica Acta 102: 129-133[ISI]
De Fossard R. A. 1969 Development and histochemistry of the endothecium in the anthers of in vitro grown Chenopodium rubrum L. Botanical Gazette 130: 10-22[CrossRef]
Ding D. J. Gai J. Yang 1999 Comparative restriction patterns and RFLP analyses of mitochondria DNA between cytoplasmic-nuclear male sterile line NJCMS1A and its maintainer NJCMS1B of the soybean. In H. E. Kauffman [ed.], Proceedings World Soybean Research Conference VI, 435. Superior Printing, Champaign, Illinois, USA
Fukasawa H. 1962 Biochemical mechanism of pollen abortion and other alterations in cytoplasmic male-sterile wheat. Proceedings of the Second Wheat Genetics Symposium, April 8–9,Seiken Zihô, Report of the Kihara Institute for Biological Research, Yokohama, Japan, 13: 107–111
Gai J. Z. Cui D. Ji Z. Ren D. Ding 1995 A report on the nuclear cytoplasmic sterility from a cross between two soybean cultivars. Soybean Genetics Newsletter 22: 55-58
Hack E. C. Lin H. Yang H. T. Horner 1991 T-urf13 protein from mitochondria of Texas male-sterile maize (Zea mays L.): its purification and submitochondrial localization, and immunogold labeling in anther tapetum during microsporogenesis. Plant Physiology 95: 861-870
Hanson M. R. 1991 Plant mitochondrial mutations and male sterility. Annual Review of Genetics 25: 461-486[CrossRef][ISI][Medline]
Hanson M. R. M. F. Conde 1985 Functioning and variation of cytoplasmic genomes: lessons from cytoplasmic-nuclear interactions affecting male fertility in plants. International Review of Cytology 94: 213-265[CrossRef]
Harold F. M. 1986 The vital force: a study of bioenergetics. W. H. Freeman, New York, New York, USA
He S. A. Lyznik S. Mackenzie 1995 Pollen fertility restoration by nuclear gene Fr in cms bean: nuclear-directed alteration of a mitochondrial population. Genetics 139: 955-962[Abstract]
Hesse M. M. W. Hess 1993 Recent trends in tapetum research: a cytological and methodological review. Plant Systematics and Evolution (Supplement) 7: 127-145
Horner H. T., Jr. M. A. Rogers 1974 A comparative light and electron microscopic study of microsporogenesis in male-fertile and cytoplasmic male-sterile pepper (Capsicum annuum). Canadian Journal of Botany 52: 435-441
Horner H. T. R. G. Palmer 1995 Mechanisms of genic male sterility. Crop Science 35: 1527-1535
Huang A. H. C. 1998 Plant peroxisomes: discovery and current advances. In S. D. Kung and S. F. Yang [eds.], Discoveries in plant biology, vol. 2, 189–201. World Scientific Publishing, Singapore
Janska H. S. A. Mackenzie 1993 Unusual mitochondrial genome organization in cytoplasmic male sterile common bean and the nature of cytoplasmic reversion to fertility. Genetics 135: 869-879[Abstract]
Kini A. V. A. Seetharam S. S. Joshi 1994 Mechanism of pollen abortion in cytoplasmic male sterile line of sunflower. Cytologia 59: 121-124
Laser K. D. N. R. Lersten 1972 Anatomy and cytology of microsporogenesis in cytoplasmic male sterile angiosperms. Botanical Review 38: 425-454
Laughnan J. R. S. Gabay-Laughnan 1983 Cytoplasmic male sterility in maize. Annual Review of Genetics 17: 27-48[CrossRef][ISI][Medline]
Lee S.-L. J. V. E. Gracen E. D. Earle 1979 The cytology of pollen abortion in c-cytoplasmic male-sterile corn anthers. American Journal of Botany 66: 656-667[CrossRef][ISI]
Lee S.-L. J. H. E. Warmke 1979 Organelle size and number in fertile and T-cytoplasmic male-sterile corn. American Journal of Botany 66: 141-148[CrossRef][ISI]
Liu F. X. Cui H. T. Horner H. Weiner P. S. Schnable 2001 Mitochondrial aldehyde dehydrogenase activity is required for male fertility in maize. Plant Cell 13: 1063-1078
Mackenzie S. 1996 Cytoplasmic genetics in the legumes (Fabaceae), with special reference to soybean. In D. P. S. Verma and R. C. Shoemaker [eds.], Soybean: genetics, molecular biology and biotechnology, 57–68. CAB International, Wallingford, UK
Mackenzie S. A. C. D. Chase 1990 Fertility restoration is associated with loss of a portion of the mitochondrial genome in cytoplasmic male-sterile common bean. Plant Cell 2: 905-912
Mackenzie S. L. McIntosh 1999 Higher plant mitochondria. Plant Cell 11: 571-585
Majewska-Sawka A. M. I. Rodriguez-Garcia H. Nakashima B. Jassen 1993 Ultrastructural expression of cytoplasmic male sterility in sugar beet (Beta vulgaris L.). Sexual Plant Reproduction 6: 22-32[ISI]
Morisset C. 1983 Effects of energetic shortage upon the ultrastructure of some organelles, in excised roots of Lycopersicum esculentum cultivated in vitro. I. Reversible structural modifications of the endoplasmic reticulum. Cytologia 48: 349-362[ISI]
Newton K. J. 1988 Plant mitochondrial genomes: organization, expression and variation. Annual Review of Plant Physiology and Plant Molecular Biology 39: 503-532[CrossRef][ISI]
Newton K. J. S. J. Gabay-Laughnan 1998 Abnormal growth and male sterility associated with mitochondrial DNA rearrangements in plants. In K. K. Singh [ed.], Mitochondrial DNA mutations in aging, disease and cancer, 365–381. Springer Verlag, New York, New York, USA
op den Camp R. G. L. C. Kuhlemeier 1997 Aldehyde dehydrogenase in tobacco pollen. Plant Molecular Biology 35: 355-365[CrossRef][ISI][Medline]
Pacini E. G. G. Franchi 1993 Role of the tapetum in pollen and spore dispersal. Plant Systematics and Evolution (Supplement) 7: 1-11
Reynolds E. S. 1963 The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. Journal of Cell Biology 17: 208-212
Rudramuniyappa C. K. A. R. Manure 1993 A review on histochemical aspects of microsporogenesis in angiosperms. In C. P. Malik [ed.], Advances in pollen-spore research: XX, 173–251. Today and Tomorrow's Printers and Publishers, New Delhi, India
Schnable P. S. R. P. Wise 1998 The molecular basis of cytoplasmic male sterility and fertility restoration. Trends in Plant Science 3: 175-180
Shivanna K. R. V. K. Sawhney 1997 Pollen biotechnology for crop production and improvement. Cambridge University Press, Cambridge, UK
Smith M. B. H. T. Horner R. G. Palmer 2001 Temperature and photoperiod effects on sterility in a cytoplasmic male-sterile soybean. Crop Science 41: 702-704
Sun H. L. Zhao M. Huang 1997 Cytoplasmic-nuclear male sterile soybean line from interspecific crosses between G. max and G. soja. In B. Napompeth [ed.], Soybean feeds the world, 1994 Proceedings World Soybean Research Conference V, 99–102. Kasetsart University Press, Bangkok, Thailand
Tadege M. C. Kuhlemeier 1997 Aerobic fermentation during tobacco pollen development. Plant Molecular Biology 35: 343-354[CrossRef][ISI][Medline]
Vartapetian B. B. L. I. Poljakova 1994 Blocking of anaerobic protein synthesis destabilizes dramatically plant mitochondrial membrane ultrastructure. Biochemistry and Molecular Biology International 33: 405-410[ISI][Medline]
Vartapetian B. B. H. H. Snkchian I. P. Generozova 1987 Mitochondrial fine structure in imbibing seeds and seedlings of Zea mays L. under anoxia. In R. M. M. Crawford [ed.], Plant life in aquatic and amphibious habitats, 205–223. Blackwell Scientific, Oxford, UK
Vartapetian B. B. N. A. Zakhmilova 1990 Ultrastructure of wheat seedling mitochondria under anoxia and postanoxia. Protoplasma 156: 39-44[CrossRef][ISI]
Walles B. S. P. Han 1998 Development of the rough endoplasmic reticulum in incompatible pollen tubes of Brugmansia suaveolens (Solanaceae). International Journal of Plant Sciences 159: 738-743[CrossRef]
Warmke H. E. S.-L. J. Lee 1977 Mitochondrial degeneration in Texas cytoplasmic male-sterile corn anthers. Journal of Heredity 68: 213-222
Wen L. C. D. Chase 1999a Pleiotropic effects of a nuclear restorer-of-fertility locus on mitochondrial transcripts in male-fertile and S male-sterile maize. Current Genetics 35: 521-526[CrossRef][ISI][Medline]
Wen L.-Y. C. D. Chase 1999b Mitochondrial gene expression in developing male gametophytes of male-fertile and S male-sterile maize. Sexual Plant Reproduction 11: 323-330[CrossRef][ISI]
Wise R. P. C. R. Bronson P. S. Schnable H. T. Horner 1999a The genetics, pathology, and molecular biology of T-cytoplasm male sterility in maize. Advances in Agronomy 65: 79-130[ISI]
Wise R. P. K. Gobelman-Werner D. Pei C. L. Dill P. S. Schnable 1999b Mitochondrial transcript processing and restoration of male fertility in T-cytoplasm maize. Journal of Heredity 90: 380-385
Zhang L. O. Dai 1997 Selection of cytoplasmic-nuclear male-sterile soybean line W931A. Scientia Agricultura Sinica 30: 90-91
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