Cytoplasmic male sterility in plants with special emphasis on sugar beet

Gabriela Sadzik

doi:10.18778/1730-2366.18.17

Authors

Gabriela Sadzik University of Agriculture in Krakow, Faculty of Biotechnology and Horticulture, Department of Plant Biology and Biotechnology, Poland

DOI:

https://doi.org/10.18778/1730-2366.18.17

Keywords:

Beta vulgaris L., cytoplasmic male sterility, mitochondrial DNA, open reading frame, fertility restorer genes

Abstract

The phenomenon of cytoplasmic male sterility (CMS) in plants is characterized by a disturbance in the development of functional pollen. The cause of this disorder is the incompatibility of the mitochondrial and nuclear genome. Determinants of CMS are found in the mitochondrial genome and are inherited maternally. Nuclear Rf genes are responsible for restoring male fertility in CMS plants most often by posttranscriptional and/or posttranslational activity on mitochondrial gene expression. Two fertility restoring genes have been identified in sugar beet plants, of which Rf1 is the best characterized. It is concluded that the translation product of this gene acts as a molecular chaperone leading to inactivation of a specific mitochondrial protein that is a marker for the CMS trait in sugar beet. The CMS phenomenon is applied in the commercial breeding of hybrid varieties of many crop species. Exploiting heterosis is easier with the knowledge of cytoplasmic (mitochondrial) determinants of sterility and corresponding restorer genes.

Downloads

Download data is not yet available.

References

Andersen, W.R. 1965. Cytoplasmic male sterility in hybrids of Lycopersicon esculentum and Solanum pennelli. Journal of the Minnesota Academy of Science, 32, 93–94.
Google Scholar

Arakawa, T., Ue, S., Sano, C., Matsunaga, M., Kagami, H., Yoshida, Y., Kuroda, Y., Taguchi, K., Kitazaki, Kazuyoshi, K., Kubo, T. 2019. Identification and characterization of a semi-dominant restorer-of-fertility 1 allele in sugar beet (Beta vulgaris). Theoretical and Applied Genetics, 132, 227–240.
Google Scholar

Arakawa, T., Matsunaga, M., Matsui, K., Itoh, K., Kurodaa, Y., Matsuhira, H., Kitazaki, K., Kubo, T. 2020. The molecular basis for allelic differences suggests Restorer-of-fertility 1 is a complex locus in sugar beet (Beta vulgaris L.). BMC Plant Biology, 20, 503.
Google Scholar

Barkan, A., Small, I. 2014. Pentatricopeptide repeat proteins in plants. Annual Review of Plant Biology, 65, 415–442.
Google Scholar

Bino, R.J. 1985. Ultrastructural aspects of cytoplasmic male sterility in Petunia hybrida. Protoplasma, 127, 230–240.
Google Scholar

Bosemark, N.O. 2006. Genetics and breeding. (In:) Draycott, A.P. (ed.), Blackwell, Oxford, pp. 50–88.
Google Scholar

Chen, L., Liu, Y.G. 2014. Male Sterility and Fertility Restoration in Crops. Annual Review of Plant Biology, 65, 579–606.
Google Scholar

Hochholdinger, F., Hoecker, N. 2007. Towards the molecular basis of heterosis. Trends in Plant Science, 12, 427–432.
Google Scholar

Honma, Y., Taguchi, K., Hiyama, H., Yui-Kurino, R., Mikami, T., Kubo, T. 2014. Molecular mapping of restorer-of-fertility 2 gene identified from a sugar beet (Beta vulgaris L. ssp. vulgaris) homozygous for the non-restoring restorer-of-fertility 1 allele. Theoretical and Applied Genetics, 127, 2567–2574.
Google Scholar

Horner, H.T., Rogers, M.A. 1974. A comparative light and electron microscopic study of microsporogenesis in male-fertile and cytoplasmic male-sterile pepper (Capsicum annuum). Canadian Journal of Botany, 3, 435–441.
Google Scholar

Ivanow, M.K., Dymshits, G.M. 2007. Cytoplasmic male sterility and restoration of pollen fertility in higher plants. Russian Journal of Genetics, 43, 354–368.
Google Scholar

Jańska, H., Wołoszyńska, M. 1996. Molekularne podstawy cytoplazmatycznej męskiej sterylności u roślin wyższych. (In:) Postępy biochemii. Zielińska Z. (ed.), Polskie Towarzystwo Biochemiczne, Warszawa, 253–259.
Google Scholar

Kaul, M.L.H. 1988. Male sterility in higher plants. Monographs on Theoretical and Applied Genetics, vol. 10. Springer-Verlag, Berlin-Heidelberg-New York.
Google Scholar

Kennel, J.C., Pring, D.R. 1989. Initiation and processing of atp6, T-urf13 and ORF221 transcripts from mitochondrial of T cytoplasm maize. Molecular Genetics and Genomics, 216, 16–24.
Google Scholar

Kitazaki, K., Arakawa, T., Matsunaga, M., Yui-Kurino, R., Matsuhira, H., Mikami, T., Kubo, T. 2015. Post-translational mechanisms are associated with fertility restoration of cytoplasmic male sterility in sugar beet (Beta vulgaris). The Plant Journal, 83, 290–299.
Google Scholar

Kubo, T., Nishizawa, S., Mikami, T. 1999. Alterations in organization and transcription of the mitochondrial genome of cytoplasmic male sterile sugar beet (Beta vulgaris L.). Molecular and General Genetics, 262, 283–290.
Google Scholar

Laser, K.D., Lersten, N.R. 1972. Anatomy and cytology of microsporogenesis in cytoplasmic male sterile angiosperms. The Botanical Review, 38, 425–454.
Google Scholar

Majewska-Sawka, A., Rodriguez-Garcia, M.I., Nakashima, H., Jassem, B. 1993. Ultrastructural expression of cytoplasmic male sterilityin sugar beet (Beta vulgaris L.). Sexual Plant Reproduction, 6, 22–32.
Google Scholar

Majewska-Sawka, A., Sadoch, Z. 2003. Cytoplazmatyczna męska sterylność roślin – mechanizmy biologiczne i molekularne. Kosmos, 52, 413–423.
Google Scholar

Matsuhira, H., Kagami, H., Kurata, M., Kitazaki, K., Matsunaga, M., Hamaguchi, Y., Hagihara, E., Ueda, M., Harada, M., Muramatsu, A., Yui-Kurino, R., Taguchi, K., Tamagake, H., Mikami, T., Kubo, T. 2012. Unusual and typical features of a novel restorer-of-fertility gene of sugar beet (Beta vulgaris L.). Genetics, 192, 1347–1358.
Google Scholar

McGrath, J.M., Panella, L. 2018. Sugar Beet Breeding. (In:) Plant Breeding Reviews. Golgman I. (ed.), Wiley, USA, 167–218.
Google Scholar

Nakamura, T., Yagi, Y., Kobayashi, K. 2012. Mechanistic insight into pentatricopeptide repeat proteins as sequence-specific RNA-binding proteins for organellar RNAs in plants. Plant and Cell Physiology, 53, 1171–1179.
Google Scholar

Nivison, H.T., Hanson, M.R. 1989. Identification of a mitochondrial protein associated with cytoplasmic male sterility in petunia. The Plant Cell, 1, 1121–1130.
Google Scholar

Owen, F.V. 1945. Cytoplasmically inherited male sterility in sugar beet. Journal of Agricultural Research, 71, 423–440.
Google Scholar

Pruitt, K.D., Hanson, M.R. 1991. Transcription of the Petunia mitochondrial CMS-associated Pcf locus in male sterile and fertility-restored lines. Molecular Genetics and Genomics, 227, 348–355.
Google Scholar

Rohrbach, U. 1965. Beitrage zum Problem der Pollensterilitat bei Beta voulgaris L. Untersuchungen uber die Ontogenese des Phanotyps. Zeitschrift fur Pflanzeuchtung, 52, 105–104.
Google Scholar

Schmitz-Linnerweber, C., Small, I. 2008. Pentatricopeptide repeat proteins, a socket set for organelle gene expression. Trends in Plant Science, 13, 663–670.
Google Scholar

Schnable, P.S., Wise, R.P. 1998. The molecular basis of cytoplasmic male sterility and fertility restoration. Trends in Plant Science, 3, 175–180.
Google Scholar

Scoles, G.J., Evans, L.E. 1979. Pollen development in male-fertile and cytoplasmic male-sterile rye. Canadian Journal of Botany, 57, 2782–2790.
Google Scholar

Sofi, P.A., Rather, A.G., Wani, S.A. 2007. Genetic and molecular basis of cytoplasmic male sterility in maize. Communications in Biometry and Crop Science, 2, 49–60.
Google Scholar

Song, J., Hedgcoth, C. 1994. A chimeric gene (orf256) is expressed as protein only in cytoplasmic male-sterile lines of wheat. Plant Molecular Biology, 26, 535–539.
Google Scholar

Stojałowski, S., Orłowska, M., Bienias, A., Myśków, B., Tomczak, P., Wesołowski, W., Szklarczyk, M., Brukwiński, W., Banaszak, K., Hanek, M., Krysztrofik, R., Zając, M. 2019. Poszukiwanie wspólnych mechanizmów dziedziczenia płodności roślin z cytoplazmą CMS-C oraz cytoplazmą CMS-Pampa. Biuletyn Instytutu Hodowli i Aklimatyzacji Roślin, 286, 151–154.
Google Scholar

Święcicki, W.K., Surma, M., Koziara, W., Skrzypczak, G., Szukała, J., Bartkowiak-Broda, I., Zimny, J., Banaszak, Z., Marciniak, K. 2011. Nowoczesne technologie w produkcji roślinnej – przyjazne dla człowieka i środowiska. Polish Journal of Agronomy, 7, 102–112.
Google Scholar

Tan, Y., Xu, X., Wang, C., Cheng, G., Li, S., Liu, X. 2015. Molecular characterization and application of a novel cytoplasmic male sterility-associated mitochondrial sequence in rice. BMC Medical Genetics, 16, 45.
Google Scholar

Tsaftaris, A.S. 1995. Molecular aspects of heterosis in plants. Physioligia Plantarum, 94, 362–370.
Google Scholar

Wang, Z.W., Wang, C., Gao., L., Mei S.Y., Zhou, Y., Xiang, C.P., Wang, T. 2013. Heterozygous alleles restore male fertility to cytoplasmic male-sterile radish (Raphanus sativus L.), a case of overdominance. Journal of Experimental Botany, 64, 2041–2048.
Google Scholar

Wasiak, M. 2019. Genetyczne podstawy cytoplazmatyczno-jądrowej męskiej sterylności (CMS) u roślin oraz jej wykorzystanie w hodowli. Agronomy Science, 74, 15–30.
Google Scholar

Wolko, J., Dobrzycka, A., Bosianowski, J. 2019. Ocena efektu heterozji cech struktury plonu mieszańców pojedynczych i mieszańców trójliniowych rzepaku (Brassica napus L.). Biuletyn Instytutu Hodowli i Aklimatyzacji Roślin, 287, 21–22.
Google Scholar

Zhiwen, C., Nan, Z., Shuangshuang, L., Corrinne, E. G., Hushuai, N., Wendel, J.F., Jinping, H. 2017. Plant mitochondrial genome evolution and cytoplasmic male sterility. Critical Reviews in Plant Sciences, 36, 55–69.
Google Scholar