Cytological Investigation of Pollen Development in Sorghum Line with Male Sterility Induced by Sodium Ascorbate in Tissue Culture

Marina I. Tsvetova, Lev A. Elkonin

Department of Biotechnology, Agricultural Research Institute for South-East Region, Saratov, Russia..

DOI: 10.4236/ajps.2013.47A1002                

Abstract

Investigation of male sterility mutations is an effective approach for identification of genes involved in anther and pollen development. The comparison of “cytological phenotypes” of newly induced mutants with phenotypes determined by already known genes favors elucidation of genetic control of diverse microsporo- and gametogenesis stages. In this paper, we describe pollen development in the grain sorghum line Zh10-asc1 with mutation of male sterility. This line was obtained from callus culture treated by sodium ascorbate. A wide spectrum of abnormalities in microsporogenesis have been found, such as cytomixis, chromosomal laggards, chromosome disjunction, adhesion of chromosomes, disturbed cytokinesis, and others. In tapetum, the cells with one nucleus, with unequal nuclei, and with micronuclei have been observed. During pollen grain (PG) maturation abnormalities in starch accumulation and delay of development often took place. In mature anthers, a variety of pollen grain types have been revealed: fertile, of irregular shape, incompletely filled with starch, PGs delayed at the uni-nucleate or bi-nucleate gametophyte stages, with partially or fully degenerated contents, and with abnormal coloration. Variation in spectrum and the frequency of disturbances between the flowers of one and the same plant have been revealed. The reasons for significant genetic and epigenetic instability are discussed.

Keywords

Male Sterility; Microsporogenesis; Sodium Ascorbate; In Vitro Mutagenesis; Genetic Instability; Sorghum bicolor (L.) Moench

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	K. Kitada, N. Kurata, H. Satoh and T. Omura, “Genetic Control of Meiosis in Rice, Oriza sativa L. Classification of Meiotic Mutants Induced by MNU and Their Cytogenetical Characteristics,” Japan Journal of Genetics, Vol. 58, No. 3, 1983, pp. 231-240. doi:10.1266/jjg.58.231
[2]	I. N. Golubovskaya, “Meiosis in Maize: Mei Genes and Conception of Genetic Control of Meiosis,” Advances in Genetics, Vol. 26, 1989, pp. 149-192. doi:10.1016/S0065-2660(08)60225-4
[3]	W. Z. Cande, I. N. Golubovskaya, C. J. R. Wang and L. Harper, “Meiotic Genes and Meiosis in Maize,” In: J. L. Bennetzen and S. Hake, Eds., Handbook of Maize, Vol. II, 2009, pp. 353-375. doi:10.1007/978-0-387-77863-1_18
[4]	A. P. Caryll, H. J. Gareth and F. C. H. Franklin, “Dissecting Plant Meiosis Using Arabidopsis thaliana Mutants,” Journal of Experimental Botany, Vol. 54, Plant Reproduction Biology, Special Issue, 2003, pp. 25-38.
[5]	E. V. Deineko, A. A. Zagorskaya and V. K. Shumny, “T-DNA Induced Mutants in Transgenic Plants,” Russian Journal of Genetics, Vol. 43, No. 1, 2007, pp. 5-17. doi:10.1134/S1022795407010012
[6]	M. Borg, L. Brownfield and D. Twell, “Male Gametophyte Development: A Molecular Perspective,” Journal of Experimental Botany, Vol. 60, No. 5, 2009, pp. 1465-1478. doi:10.1093/jxb/ern355
[7]	Z. A. Wilson and D. B. Zhang, “From Arabidopsis to Rice, Pathways in Pollen Development,” Journal of Experimental Botany, Vol. 60, No. 5, 2009, pp. 1479-1492. doi:10.1093/jxb/erp095
[8]	S. Fujii and K. Toriyama, “Genome Barriers between Nuclei and Mitochondria Exemplified by Cytoplasmic Male Sterility,” Plant Cell Physiology, Vol. 49, No. 10, 2008, pp. 1484-1494. doi:10.1093/pcp/pcn102
[9]	L. A. Elkonin and M. I. Tsvetova, “Genetic and Cytological Analyses of the Male Sterility Mutation Induced in a Sorghum Tissue Culture with Streptomycin,” Russian Journal of Genetics, Vol. 44, No. 5, 2008, pp. 575-583. doi:10.1134/S1022795408050104
[10]	L. A. Elkonin, G. A. Geraschenkov, M. I. Tsvetova and N. A. Rozhnova, “Genetic Variation in a Sorghum Line with Multiple Genetic Instability Induced with Ethidium Bromide in an in Vitro Culture,” Russian Journal of Genetics, Vol. 46, No. 7, 2010, pp. 805-815. doi:10.1134/S1022795410070057
[11]	V. K. Voinikov, Yu. M. Konstantinov and V. I. Negruk, “Genetic Functions of Plant Mitochondria,” Nauka, Sib. Branch, Novosibirsk, 1991.
[12]	R. Milczarek, J. Klimek and L. Zelewski, “The Effects of Ascorbate and Alpha-Tocopherol on the NADPH-Dependent Lipid Peroxidation in Human Placental Mitochondria,” Molecular Cell Biochemistry, Vol. 210, No. 1-2, 2000, pp. 65-73. doi:10.1023/A:1007007213846
[13]	T. Sen, N. Sen, G. Tripathi, U. Chatterjee and S. Chakrabarti, “Lipid Peroxidation Associated Cardiolipin Loss and Membrane Depolarization in Rat Brain Mitochondria,” Neurochemistry International, Vol. 49, No. 1, 2006, pp. 20-27. doi:10.1016/j.neuint.2005.12.018
[14]	J. H. Song, S. H. Shin, W. Wang and G. M. Ross, “Oxidative Stress Induced by Ascorbate Causes Neuronal Damage in an in Vitro System,” Brain Research, Vol. 895, No. 1-2, 2001, pp. 66-72. doi:10.1016/S0006-8993(01)02029-7
[15]	C. Wan, S. Li, L. Wen, J. Kong, K. Wang and Y. Zhu, “Damage of Oxidative Stress on Mitochondria during Microspores Development in Honglian CMS Line of Rice,” Plant Cell Reports, Vol. 26, No. 3, 2007, pp. 373-382. doi:10.1007/s00299-006-0234-2
[16]	A. T. Hoye, J. Davoren, P. Wipf, M. P. Fink and V. E. Kagan, “Targeting mitochondria,” Accounts of Chemical Research, Vol. 41, No. 1, 2008, pp. 87-97. doi:10.1021/ar700135m
[17]	S. S. Gill and N. Tuteja, “Reactive Oxygen Species and Antioxidant Machinery in Abiotic Stress Tolerance in Crop Plants,” Plant Physiology and Biochemistry, Vol. 48, No. 12, 2010, pp. 909-930. doi:10.1016/j.plaphy.2010.08.016
[18]	M. I. Tsvetova, L. A. Elkonin and O. V. Ukolova, “Investigation of Tapetal Cells by Means of Squash Technique,” Botanicheskiy Zhurnal, Vol. 91, No. 7, 2006, pp. 969-974.
[19]	R. K. Dawe, “Meiotic Chromosome Organization and Segregation in Plants,” Annual Review of Plant Physiology. Plant Molecular Biology, Vol. 49, 1998, pp. 371-395. doi:10.1146/annurev.arplant.49.1.371
[20]	A. M. Bhatt, C. Listen, T. Page, P. Fransz, K. Findlay, G. H. Jones, H. G. Dickinson and C. Dean, “The DIF1 Gene of Arabidopsis Is Required for Meiotic Chromosome Segregation and Belongs to the REC8/RAD21 Cohesion Gene Family,” Plant Journal, Vol. 19, No. 4, 1999, pp. 463-472. doi:10.1046/j.1365-313X.1999.00548.x
[21]	N. V. Shamina, “Diagnosticum of Abnormalities of Plant Meiotic Divisions,” Tsitologia, Vol. 48, No. 6, 2006, pp. 486-494.
[22]	K. W. Wolfe and Q. Liu, “The Maize Mutant polymitotic Affects Cell Cycle Events during Microspore Development,” Planta, Vol. 210, No. 1, 1999, pp. 27-33. doi:10.1007/s004250050650
[23]	S. Y. Rhee and C. R. Somerville, “Tetrad Pollen Formation in quartet Mutants of Arabidopsis thaliana Is Associated with Persistence of Pectic Polysaccharides of the Pollen Mother Cell Wall,” Plant Journal, Vol. 15, No. 1, 1998, pp. 79-88. doi:10.1046/j.1365-313X.1998.00183.x
[24]	S. Y. Rhee, E. Osborne, P. D. Poindexter and C. R. Somerville, “Microspore Separation in the quartet 3 Mutants of Arabidopsis Is Impaired by a Defect in a Developmentally Regulated Polygalacturonase Required for Pollen Mother Cell Wall Degradation,” Plant Physiology, Vol. 133, No. 3, 2003, pp. 1170-1180. doi:10.1104/pp.103.028266
[25]	T. Ariizumi and K. Toriyama, “Genetic Regulation of Sporopollenin Synthesis and Pollen Exine Development,” Annual Review of Plant Biology, Vol. 62, 2011, pp. 437-460. doi:10.1146/annurev-arplant-042809-112312
[26]	M. C. Albersten and R. L. Phillips, “Developmental Cytology of 13 Genetic Male Sterile Locy in Maize,” Canadian Journal of Genetics and Cytology, Vol. 23, No. 2, 1981, pp. 195-208.
[27]	P. Bedinger, “The Remarkable Biology of Pollen,” Plant Cell, Vol. 4, No. 8, 1992, pp. 879-887.
[28]	J. F. Pedersen, S. R. Bean, D. L. Funell and R. A. Graybosch, “Rapid Iodine Staining Techniques for Identifying the Waxy Phenotype in Sorghum Grain and Waxy Genotype in Sorghum Pollen,” Crop Science, Vol. 44, No. 3, 2004, pp. 764-767.
[29]	J. F. Pedersen, S. R. Bean, R. A. Graybosch, S. H. Park and M. Tilley, “Characterization of Waxy Grain Sorghum Lines in Relation to Granule-Bound Starch Synthase,” Euphytica, Vol. 144, No. 1-2, 2005, pp. 151-156. doi:10.1007/s10681-005-5298-5
[30]	B. K. McClintock, “Further Studies of Gene-Control Systems in Maize,” Carnegie Institute of Washington. Yearbook, Vol. 62, 1963, pp. 486-493.
[31]	C. F. Weil, S. Marillonnet, B. Burr and S. R. Wessler, “Change in State Wx-m5 Allele of Maize Are Due to Intragenic Transposition of Ds,” Genetics, Vol. 130, No. 1, 1992, pp. 175-185.
[32]	T. Ito, N. Nagata, Y. Yoshiba, M. Ohme-Takaqi, H. Ma and K. Shinozaki, “Arabidopsis Male Sterility1 Encodes a PHD-Type Transcription Factor and Regulates Pollen and Tapetum Development,” Plant Cell, Vol. 19, No. 11, 2007, pp. 3549-3562. doi:10.1105/tpc.107.054536
[33]	C. Yang, G. Vizcay-Barrena, K. Conner and Z. A. Wilson, “Male Sterility1 Is Required for Tapetal Development and Pollen Wall Biosynthesis,” Plant Cell, Vol. 19, No. 11, 2007, pp. 3530-3548. doi:10.1105/tpc.107.054981
[34]	J. Zhu, G. Zhang, Y. Chang, X. Li, J. Yang, X. Huang, Q. Yu, H. Chen, T. Wu and Z. Yang, “AtMYB103 Is a Crucial Regulator of Several Pathways Affecting Arabidopsis Anther Development,” Science Сhina. Life Science, Vol. 53, No. 9, 2010, pp. 1112-1122.
[35]	H. A. Phan, S. Iacuone, S. F. Li and R. W. Parish, “The MYB80 Transcription Factor Is Required for Pollen Development and the Regulation of Tapetal Programmed Cell Death in Arabidopsis thaliana,” Plant Cell, Vol. 23, No. 6, 2011, pp. 2209-2224. doi:10.1105/tpc.110.082651