Skip to main content
Log in

Genetic and cytological analyses of the male sterility mutation induced in a sorghum tissue culture with streptomycin

  • Plant Genetics
  • Published:
Russian Journal of Genetics Aims and scope Submit manuscript

Abstract

Treatment of sorghum callus cultures with 500–1000 mg/l streptomycin led to a high regeneration frequency of plants with complete or partial male sterility (MS), up to 100% of all green regenerants. The induced MS mutation (ms-str) was preserved in the F1 and BC1 progenies and was genetically unstable: many families produced semisterile and fertile revertants, whose progenies again contained semisterile and sterile mutants. The ms-str mutation was maintained through eight generations via selection and self-pollination of semisterile plants. The mutation was inherited as a recessive nuclear mutation in test crosses of sterile plants segregated in the progenies of fertile and semisterile revertants and was expressed only in single cases in a test cross for ms-str transfer through pollen of hybrids with restored male fertility. Recessive nuclear mutations determining a low plant height (dwarfness) and the lack of waxy bloom on the stem and leaves (bloomless) were found in male-sterile plants with the ms-str mutation. Cytological analysis of sterile plants reveal multiple abnormalities at various pollen development stages and in tapetal cells: cytomyxis, defects of chromosome conjugation, distorted cytokinesis in meiotic division II, a lack of tetrad separation, a defective formation of the microspore coat, generation of microspores with two to four nuclei, and the formation of micronuclei and large vacuoles in tapetal cells. A possible transfer of the induced cytoplasmic MS mutation into the nuclear genome and the causes of the high genetic instability are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Kaul M.L.H., Male Sterility in Higher Plants, Berlin: Springer-Verlag, 1988.

    Google Scholar 

  2. Scott, R.J., Spielman, M., and Dickinson, H.G., Stamen Structure and Function, Plant Cell, 2004, vol. 16, pp. 46–60.

    Article  Google Scholar 

  3. McCormick, S., Control of Male Gametophyte Development, Plant Cell, 2004, vol. 16, pp. 142–153.

    Article  Google Scholar 

  4. Ariizumi, T., Hatakeyama, K., Hinata, K., et al., Disruption of the Novel Plant Protein NEF1 Affects Lipid Accumulation in the Plastids of the Tapetum and Exine Formation of Pollen, Resulting in Male Sterility in Arabidopsis thaliana, Plant J., 2004, vol. 39, no. 2, pp. 170–181.

    Article  PubMed  CAS  Google Scholar 

  5. Francis, K.E., Lam, S.Y., and Copenhaver, G.P., Separation of Arabidopsis Pollen Tetrads Is Regulated by QUARTET1, a Pectin Methylesterase Gene, Plant Physiol., 2006, vol. 142, no. 3, pp. 1004–1013.

    Article  PubMed  CAS  Google Scholar 

  6. Chase, C.D and Gabay-Laughnan, S, Cytoplasmic Male Sterility and Fertility Restoration by Nuclear Genes, Molecular Biology and Biotechnology of Plant Organelles, Daniell, H. and Chase, C.D., Eds., Springer-Verlag, 2004, pp. 593–621.

  7. Hanson, M.R. and Bentolila, S., Interactions of Mitochondrial and Nuclear Genes That Affect Male Gametophyte Development, Plant Cell, 2004, vol. 16,suppl., pp. 154–169.

    Article  Google Scholar 

  8. Touzet, P. and Budar, F., Unveiling the Molecular Arms Race between Two Conflicting Genomes in Cytoplasmic Male Sterility?, Trends Plant Sci., 2004, vol. 9, pp. 568–570.

    Article  PubMed  CAS  Google Scholar 

  9. Chetrit, P., Rios, R., De Paepe, R., et al., Cytoplasmic Male Sterility Is Associated with Large Deletions in the Mitochondrial DNA of Two Nicotiana sylvestris Protoclones, Curr. Genet., 1992, vol. 21, pp. 131–137.

    Article  PubMed  CAS  Google Scholar 

  10. Petrov, D.F., Fokina, E.S., and Zheleznova, N.B., Method of Obtaining Cytoplasmic Male Sterility in Maize by Treatment of Seeds with Streptomycin, US Patent 3594152. 1971.

  11. Burton, G.W. and Hanna, W.W., Stable Cytoplasmic Male-Sterile Mutants Induced in Tift 23DB1 Pearl Millet with Mitomycin and Streptomycin, Crop Sci., 1982, vol. 22, no. 3, pp. 651–652.

    CAS  Google Scholar 

  12. Jan, C.C. and Rutger, J.N., Mitomycin C-and Streptomycin-Induced Male Sterility in Cultivated Sunflower, Crop Sci., 1988, vol. 28, no. 5, pp. 792–795.

    CAS  Google Scholar 

  13. Kinoshita, T., Takahashi, M., and Mikami, T., Cytoplasmic Mutation of Male Sterility Induced by Chemical Mutagens in Sugar Beet, Proc. Jpn. Acad., Ser. B, 1982, vol. 58, no. 10, pp. 312–322.

    Google Scholar 

  14. Davydenko, O.G., Nechromosomnye mutatsii (Extrachromosomal Mutations), Minsk: Nauka i Tekhnika, 1984.

    Google Scholar 

  15. Doudican, N.A., Song, B., Shadel, G.S., and Doetsch, P.W., Oxidative DNA Damage Causes Mitochondrial Genomic Instability in Saccharomyces cerevisiae, Mol. Cell. Biol., 2005, vol. 25, no. 12, pp. 5196–5204.

    Article  CAS  Google Scholar 

  16. Elkonin, L.A. and Tyrnov, V.S., Studying Genetic Control of Cytoplasmic Male Sterility in Plants: State of the Problem and Current Approaches, Russ. J. Genet., 2000, vol. 36, no. 4, pp. 347–358.

    CAS  Google Scholar 

  17. Elkonin, L.A. and Milovanova, T.N., Induction of Male Sterility Mutations by Streptomycin Treatment of Sorghum Tissue Cultures, Int. Sorghum Millet Newslett., 1995, vol. 36, pp. 76–77.

    Google Scholar 

  18. El’konin, L.A., Modifications of Plant Reproductive System by Means of in Vitro Culture Methods (with the Example of Sorghum), Extended Abstract of Doctoral (Biol.) Dissertation, St. Petersburg: Inst. Plant Ind., 1999, p. 48.

    Google Scholar 

  19. Elkonin, L.A., Tyrnov, V.S., Papazyan, N.D., and Ishin, A.G., Culture of Sorghum Somatic Tissue: Phytohormonal Regulation of Morphogenesis, Fiziol. Rast., 1986, vol. 33, no. 3, pp. 504–512.

    CAS  Google Scholar 

  20. Lakin, G.F., Biometriya (Biometrics), Moscow: Vysshaya Shkola, 1990.

    Google Scholar 

  21. Sarma, N.P. and Patnaik, A., Streptomycin Induced Nuclear and Cytoplasmic Chloroplast Mutations in Rice, Indian J. Exp. Biol., 1982, vol. 20, pp. 177–178.

    CAS  Google Scholar 

  22. Gallili, S., Fromm, H., Aviv, D., et al., Ribosomal Protein S12 as a Site for Streptomycin Resistance in Nicotiana plumbaginifolia, Mol. Gen. Genet., 1989, vol. 218, no. 2, pp. 289–292.

    Article  Google Scholar 

  23. Yeh, K.C., To, K.Y., Sun, S.W., et al., Point Mutations in the Chloroplast 16S rRNA Gene Confer Streptomycin Resistance in Nicotiana plumbaginifolia, Curr. Genet., 1994, vol. 26, no. 2, pp. 132–135.

    Article  CAS  Google Scholar 

  24. Rasmussen, A.K., Chatterjee, A., Rasmussen, L.J., and Singh, K.K., Mitochondria-Mediated Nuclear Mutator Phenotype in Saccharomyces cerevisiae, Nucleic Acids Res., 2003, vol. 31, no. 14, pp. 3909–3917.

    Article  CAS  Google Scholar 

  25. Imamura, Y., Yukawa, M., Kimura, K., et al., Fredericamycin A Affects Mitochondrial Inheritance and Morphology in Saccharomyces cerevisiae, Boisci. Biotechnol. Biochem., 2005, vol. 69, no. 11, pp. 2213–2218.

    Article  CAS  Google Scholar 

  26. Fischel-Ghodsian, N., Mitochondrial Mutations and Hearing Loss: Paradigm for Mitochondrial Genetics, Am. J. Hum. Genet., 1998, vol. 62, no. 1, pp. 15–19.

    Article  PubMed  CAS  Google Scholar 

  27. Selimoglu, E., Aminoglycoside-Induced Ototoxicity, Curr. Pharm. Des., 2007, vol. 13, no. 1, pp. 119–126.

    Article  PubMed  CAS  Google Scholar 

  28. Adams, K.L. and Palmer, J.D., Evolution of Mitochondrial Gene Content: Gene Loss and Transfer to the Nucleus, Mol. Phylogenet. Evol., 2003, vol. 29, no. 3, pp. 380–395.

    Article  PubMed  CAS  Google Scholar 

  29. Odintsova, M.S. and Yurina, N.P., Genomics and Evolution of Cellular Organelles, Russ. J. Genet., 2005, vol. 41, no. 9, pp. 957–967.

    Article  CAS  Google Scholar 

  30. Ueda, M., Tsutsumi, N., and Kadowaki, K., Translocation of a 190-kb Mitochondrial Fragment into Rice Chromosome 12 Followed by the Integration of Four Retrotransposons, Int. J. Biol. Sci., 2005, vol. 1, no. 3, pp. 110–113.

    PubMed  CAS  Google Scholar 

  31. Dorogova, N.V. and Shamina, N.V., Cytokinesis in Higher Plant Cells, Tsitologiya, 1994, vol. 36, nos. 9–10, pp. 899–915.

    Google Scholar 

  32. Dawe, R.K., Meiotic Chromosome Organization and Segregation in Plants, Annu. Rev. Plant. Physiol. Plant Mol. Biol., 1998, vol. 49, pp. 371–395.

    Article  PubMed  CAS  Google Scholar 

  33. Zhang, C., Guinel, F.C., and Moffatt, B.A., A Comparative Ultrastructural Study of Pollen Development in Arabidopsis thaliana Ecotype Columbia and Male-Sterile Mutant apt1-3, Protoplasma, 2002, vol. 219, nos. 1–2, pp. 59–71.

    Google Scholar 

  34. Hirochika, H., Retrotransposons of Rice: Their Regulation and Use for Genome Analysis, Plant Mol. Biol., 1997, vol. 35, nos. 1–2, pp. 231–240.

    Article  PubMed  CAS  Google Scholar 

  35. Kaeppler, S.M., Kaeppler, H.F., and Rhee, Y., Epigenetic Aspects of Somaclonal Variation in Plants, Plant. Mol. Biol., 2000, vol. 43, pp. 179–188.

    Article  PubMed  CAS  Google Scholar 

  36. Mckenzie, N., Wen, L.-Y., and Dale, P.J., Tissue-Culture Enhanced Transposition of the Maize Transposable Element Dissociation in Brassica oleracea var. italica, Theor. Appl. Genet., 2002, vol. 105, no. 1, pp. 23–33.

    Article  PubMed  CAS  Google Scholar 

  37. Ferguson, L.R. and von Borstel, R.C., Induction of the Cytoplasmic ‘Petite’ Mutation by Chemical and Physical Agents in Saccharomyces cerevisiae, Mutat. Res., 1992, vol. 265, no. 1, pp. 103–148.

    PubMed  CAS  Google Scholar 

  38. Elkonin, L.A., Tsvetova, M.I., Nosova, O.N., and Leshko, E.V., Male Sterility and Multiple Genetic Instabilities in Sorghum Lines Regenerated from Callus Cultures Treated by Ethidium Bromide, Abstr. Int. Congress Plant Tissue Cult. Biotechnol., Beijing, 2006, p. 120.

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to L. A. Elkonin.

Additional information

Original Russian Text © L.A. Elkonin, M.I. Tsvetova, 2008, published in Genetika, 2008, Vol. 44, No. 5, pp. 663–673.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Elkonin, L.A., Tsvetova, M.I. Genetic and cytological analyses of the male sterility mutation induced in a sorghum tissue culture with streptomycin. Russ J Genet 44, 575–583 (2008). https://doi.org/10.1134/S1022795408050104

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1022795408050104

Keywords

Navigation