Cytoplasmic male sterility in plants with special emphasis on sugar beet
DOI:
https://doi.org/10.18778/1730-2366.18.17Keywords:
Beta vulgaris L., cytoplasmic male sterility, mitochondrial DNA, open reading frame, fertility restorer genesAbstract
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
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.
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. DOI: https://doi.org/10.1007/s00122-018-3211-6
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. DOI: https://doi.org/10.1186/s12870-020-02721-9
Barkan, A., Small, I. 2014. Pentatricopeptide repeat proteins in plants. Annual Review of Plant Biology, 65, 415–442. DOI: https://doi.org/10.1146/annurev-arplant-050213-040159
Bino, R.J. 1985. Ultrastructural aspects of cytoplasmic male sterility in Petunia hybrida. Protoplasma, 127, 230–240. DOI: https://doi.org/10.1007/BF01276267
Bosemark, N.O. 2006. Genetics and breeding. (In:) Draycott, A.P. (ed.), Blackwell, Oxford, pp. 50–88. DOI: https://doi.org/10.1002/9780470751114.ch4
Chen, L., Liu, Y.G. 2014. Male Sterility and Fertility Restoration in Crops. Annual Review of Plant Biology, 65, 579–606. DOI: https://doi.org/10.1146/annurev-arplant-050213-040119
Hochholdinger, F., Hoecker, N. 2007. Towards the molecular basis of heterosis. Trends in Plant Science, 12, 427–432. DOI: https://doi.org/10.1016/j.tplants.2007.08.005
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. DOI: https://doi.org/10.1007/s00122-014-2398-4
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. DOI: https://doi.org/10.1139/b74-056
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. DOI: https://doi.org/10.1134/S1022795407040023
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.
Kaul, M.L.H. 1988. Male sterility in higher plants. Monographs on Theoretical and Applied Genetics, vol. 10. Springer-Verlag, Berlin-Heidelberg-New York. DOI: https://doi.org/10.1007/978-3-642-83139-3
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. DOI: https://doi.org/10.1007/BF00332225
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. DOI: https://doi.org/10.1111/tpj.12888
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. DOI: https://doi.org/10.1007/s004380051085
Laser, K.D., Lersten, N.R. 1972. Anatomy and cytology of microsporogenesis in cytoplasmic male sterile angiosperms. The Botanical Review, 38, 425–454. DOI: https://doi.org/10.1007/BF02860010
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. DOI: https://doi.org/10.1007/BF00227579
Majewska-Sawka, A., Sadoch, Z. 2003. Cytoplazmatyczna męska sterylność roślin – mechanizmy biologiczne i molekularne. Kosmos, 52, 413–423.
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. DOI: https://doi.org/10.1534/genetics.112.145409
McGrath, J.M., Panella, L. 2018. Sugar Beet Breeding. (In:) Plant Breeding Reviews. Golgman I. (ed.), Wiley, USA, 167–218. DOI: https://doi.org/10.1002/9781119521358.ch5
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. DOI: https://doi.org/10.1093/pcp/pcs069
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. DOI: https://doi.org/10.1105/tpc.1.11.1121
Owen, F.V. 1945. Cytoplasmically inherited male sterility in sugar beet. Journal of Agricultural Research, 71, 423–440.
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. DOI: https://doi.org/10.1007/BF00273922
Rohrbach, U. 1965. Beitrage zum Problem der Pollensterilitat bei Beta voulgaris L. Untersuchungen uber die Ontogenese des Phanotyps. Zeitschrift fur Pflanzeuchtung, 52, 105–104.
Schmitz-Linnerweber, C., Small, I. 2008. Pentatricopeptide repeat proteins, a socket set for organelle gene expression. Trends in Plant Science, 13, 663–670. DOI: https://doi.org/10.1016/j.tplants.2008.10.001
Schnable, P.S., Wise, R.P. 1998. The molecular basis of cytoplasmic male sterility and fertility restoration. Trends in Plant Science, 3, 175–180. DOI: https://doi.org/10.1016/S1360-1385(98)01235-7
Scoles, G.J., Evans, L.E. 1979. Pollen development in male-fertile and cytoplasmic male-sterile rye. Canadian Journal of Botany, 57, 2782–2790. DOI: https://doi.org/10.1139/b79-330
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.
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. DOI: https://doi.org/10.1007/BF00039566
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. DOI: https://doi.org/10.37317/biul-2019-0032
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.
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. DOI: https://doi.org/10.1186/s12863-015-0205-0
Tsaftaris, A.S. 1995. Molecular aspects of heterosis in plants. Physioligia Plantarum, 94, 362–370. DOI: https://doi.org/10.1111/j.1399-3054.1995.tb05324.x
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. DOI: https://doi.org/10.1093/jxb/ert065
Wasiak, M. 2019. Genetyczne podstawy cytoplazmatyczno-jądrowej męskiej sterylności (CMS) u roślin oraz jej wykorzystanie w hodowli. Agronomy Science, 74, 15–30. DOI: https://doi.org/10.24326/as.2019.1.2
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. DOI: https://doi.org/10.37317/biul-2019-0099
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. DOI: https://doi.org/10.1080/07352689.2017.1327762
Downloads
Published
Issue
Section
License

This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
