Preview

Vegetable crops of Russia

Advanced search

Cytoplasmic male sterility in Beta vulgaris L., molecular-genetic mechanisms and application in hybrid breeding (review)

https://doi.org/10.18619/2072-9146-2026-2-28-36

Abstract

Relevance. In the context of the objectives of the Food Security Doctrine of the Russian Federation, breeding and seed production work to develop domestic heterotic hybrids of table beet (Beta vulgaris L. var. conditiva Alef.) is particularly relevant. This review is devoted to a comprehensive analysis of the cytoplasmic male sterility (CMS) trait, both as a technological basis for hybrid breeding in general and as it manifests in Beta vulgaris L., including table beet.

Results. A number of biological features of the reproductive system and traits associated with CMS in table beet are examined. Attention is paid to the tissue-specific manifestation of CMS, associated with mitochondrial dysfunction in the cells of the tapetum the nutrient layer of developing pollen grains leading to impaired male reproductive function. CMS is characterized by maternal inheritance and is molecularly controlled by the interaction of the mitochondrial (determining the sterile phenotype) and nuclear (capable of restoring fertility) genomes. In red beet, the CMS trait is characterized by variability in the degree of pollen sterility. Specific changes in anther color (from pink to brown) and morphology (shrinkage, deformation) serve as informative markers for the visual assessment of sterile phenotypes. This review examines and characterizes the main CMS types in the species Beta vulgaris L. (Owen, G, E) at the molecular genetic level. Each type is associated with a unique structure of chimeric mitochondrial open reading frames (S-orf). Expression of these mitochondrial genes disrupts cellular energy metabolism. Fertility restoration occurs through the action of nuclear restorer genes (Rf), whose products likely suppress or neutralize the action of Sorf. The potential for using molecular markers tightly linked to mitochondrial CMS genes and nuclear Rf genes for marker-assisted selection (MAS) of sterile and fertile forms at the early stages of parental line development is discussed, significantly accelerating the process of producing commercial hybrids.

Conclusion. Deeper research into the molecular basis of CMS and the development of modern breeding technologies based on these studies will provide the scientific and technological foundation for the development of competitive beet vegetable production.

About the Authors

O. A. Blandinskaya
Federal State Budgetary Scientific Institution Federal Scientific Vegetable Center (FSBSI FSVC)
Russian Federation

Olga A. Blandinskaya – Cand. Sci. (Agriculture), Senior Researcher, Laboratory of Molecular Genetics and Cytology

14, Selectsionnaya str., VNIISSOK, Odintsovo district, Moscow region, 143072



S. A. Vetrova
Federal State Budgetary Scientific Institution Federal Scientific Vegetable Center (FSBSI FSVC)
Russian Federation

Svetlana A. Vetrova – Cand. Sci. (Agriculture), Senior Researcher of the Laboratory Molecular Immunological Research

14, Selectsionnaya str., VNIISSOK, Odintsovo district, Moscow region, 143072



E. G. Kozar
Federal State Budgetary Scientific Institution Federal Scientific Vegetable Center (FSBSI FSVC)
Russian Federation

Elena G. Kozar – Cand. Sci. (Agriculture), Senior Researcher of the Laboratory Molecular Immunological Research

14, Selectsionnaya str., VNIISSOK, Odintsovo district, Moscow region, 143072



A. S. Domblides
Federal State Budgetary Scientific Institution Federal Scientific Vegetable Center (FSBSI FSVC)
Russian Federation

Arthur S. Domblides – Dr. Sci. (Agriculture), Chief Researcher, Laboratory of Molecular Genetics and Cytology

14, Selectsionnaya str., VNIISSOK, Odintsovo district, Moscow region, 143072



References

1. Pivovarov V.F. Vegetables of Russia. M., 2006. 816 p. (In Russ.) https://www.elibrary.ru/qkxtmt

2. Clifford T., Howatson G., West D.J., Stevenson E.J. The potential benefits of red beetroot supplementation in health and disease. Nutrients. 2015;7(4):2801-2822. https://doi.org/10.3390/nu7042801

3. Guldiken B., Toydemir G., Memis K.N., Okur S., Boyacioglu D. et al. Home-processed red beetroot (Beta vulgaris L.) Products: Changes in antioxidant properties and bioaccessibility. International Journal of Molecular Sciences. 2016;17(6):858. https://doi.org/10.3390/ijms17060858

4. Sawicki T., Wiczkowski W. The effects of boiling and fermentation on betalain profiles and antioxidant capacities of red beetroot products. Food Chemistry. 2018;259:292-303.

5. Mirmiran P., Houshialsadat Z., Gaeini Z., Bahadoran Z., Azizi F. Functional properties of beetroot (Beta vulgaris) in management of cardiometabolic diseases. Nutrition & Metabolism (London). 2020;17:3. https://doi.org/10.1186/s12986-019-0421-0

6. Decree of the President of the Russian Federation of January 21, 2020 N 20 "On approval of the Doctrine of Food Security of the Russian Federation". URL: http://publication.pravo.gov.ru/Document/View/0001202001210002

7. State Register of Selection Achievements Approved for Use. Volume 1. Plant Varieties. Moscow: Federal State Budgetary Scientific Institution "Gossortkomissiya", 2025. URL: https://gossortrf.ru/registry/gosudarstvennyy-reestr-selektsionnykh-dostizheniy-dopushchennykh-k-ispolzovaniyutom-1-sorta-rasteni/

8. Burenin V.I., Sokolova D.V., Piskunova T.M. The gene pool for table beet breeding (modern aspects of study and use). Proceedings on applied botany, genetics and breeding. 2019;180(3):19-25. (In Russ.) https://doi.org/10.30901/2227-8834-2019-3-19-25 https://www.elibrary.ru/allqrw

9. Krasochkin V.T. Beet. Cultivated flora of the USSR. 1971;19:7-266. (In Russ.)

10. Maletsky S.I. Seed propagation of sugar beet. Encyclopedia of the genus Beta. Biology, genetics, and breeding of beet. Novosibirsk: Sova, 2010. pp. 52-62. (In Russ.)

11. Linnaeus C. Species Plantarum. 1st ed. Stockholm: Lawrence Salvii, 1753.

12. Lange W., Brandenburg W.A., Bock T.S.M. Taxonomy and cultonomy of beet (Beta vulgaris L.). Botanical Journal of the Linnean Society. 1999;130:81-96. https://doi.org/10.1006/bojl.1998.0250

13. Galewski P., McGrath J.M. Genetic diversity among cultivated beets (Beta vulgaris) assessed via population-based whole genome sequences. BMC Genomics. 2020;21:189. https://doi.org/10.1186/s12864-020-6451-1

14. Abu-Ellail F.F.B., Salem K.F.M., Saleh M.M., Alnaddaf L.M., Al-Khayri J.M. Molecular Breeding Strategies of Beetroot (Beta vulgaris ssp. vulgaris var. conditiva Alefeld). Advances in Plant Breeding Strategies: Vegetable Crops. eds. by J.M. Al-Khayri, S.M. Jain, D.V. Johnson. Cham: Springer, 2021. P.119-149. https://doi.org/10.1007/978-3-030-66965-2_4

15. Andrello M., Henry K., Devaux P., Desprez B., Manel S. Taxonomic, spatial and adaptive genetic variation of Beta section Beta. Theoretical and Applied Genetics. 2016;129(2):257-271. https://doi.org/10.1007/s00122-015-2625-7

16. Vavilov N.I. Centers of origin of cultivated plants // Works on applied botany, genetics and breeding. 1926;16(2):3-96. (In Russ.)

17. Krasochkin V.T. Beetroot. Moscow, 1960. 438 p. (In Russ.)

18. Zosimovich V.P. Wild species and origin of cultivated beet. Beet growing. Kyiv. 1940;5:17-44. (In Russ.)

19. Cooke D.A., Scott R.K. The sugar beet crop. London: Chapman and Hall Publishers, 1993. 675 p.

20. Kubota K., Oishi M., Taniguchi E., Akazawa A., Matsui K., Kitazaki K., Toyoda A., Toh H., Matsuhira H., Kuroda Y., Kubo T. Mitochondrial phylogeny and distribution of cytoplasmic male sterility-associated genes in Beta vulgaris. PLOS ONE. 2024;19(8). https://doi.org/10.1371/journal.pone.0308551

21. Dhiman A., Taliadoros D., Stukenbrock E., McGrath M., Emrani N., Jung C. Signatures in domesticated beet genomes pointing at genes under selection in a sucrose-storing root crop. bioRxiv. 2024. Preprint. https://doi.org/10.1101/2024.05.27.596033.

22. Vega A., Oravec M., Goldman I.L. Phenotypic, genetic, и population structure analysis offer insights into the genetic architecture of root shape in Beta vulgaris. Horticulture Research. 2025;12. https://doi.org/10.1093/hr/uhaf201

23. Goldman I.L., Navazio J.P. Table Beet. Vegetables I. Eds. by J. Prohens, F. Nuez. New York, NY: Springer, 2008. P.219-238. (Handbook of Plant Breeding; vol. 1). https://doi.org/10.1007/978-0-387-30443-4_7

24. Boudry P., Mörchen M., Saumitou-Laprade P., Vernet Ph., Van Dijk H. The origin and evolution of weed beets: consequences for the breeding and release of herbicide-resistant transgenic sugar beets. Theoretical and Applied Genetics. 1993;87:471-478. https://doi.org/10.1007/BF00215093

25. Bartsch D., Lehnen M., Clegg J., Pohl-Orf M., Schuphan I., Ellstrand N.C. Impact of gene flow from cultivated beet on genetic diversity of wild sea beet populations. Molecular Ecology. 1999;8:1733-1741. https://doi.org/10.1046/j.1365-294x.1999.00769.x

26. Andrello M., Henry K., Devaux P., Verdelet D., Desprez B., Manel S. Insights into the genetic relationships among plants of Beta section Beta using SNP markers. Theoretical and Applied Genetics. 2017;130:1857- 1866. https://doi.org/10.1007/s00122-017-2929-x

27. Sandell F.L., Stralis-Pavese N., McGrath J.M. et al. Genomic distances reveal relationships of wild and cultivated beets. Nature Communications. 2022;13(2021). https://doi.org/10.1038/s41467-022-29676-9

28. Felkel S., Dohm J., Himmelbauer H. Genomic variation in the genus Beta based on 656 sequenced beet genomes. Scientific Reports. 2023;13:7322. https://doi.org/10.1038/s41598-023-35691-7

29. Schnable P.S., Wise R.P. The molecular basis of cytoplasmic male sterility and fertility restoration. Trends in Plant Science. 1998;3:175-180.

30. Bentolila S., Alfonso A.A., Hanson M.R. A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proceedings of the National Academy of Sciences of the United States of America. 2002;99:10887-10892. https://doi.org/10.1073/pnas.102301599

31. Chase C.D. Cytoplasmic male sterility: a window to the world of plant mitochondrial-nuclear interactions. Trends in Genetics. 2007;23(2):81-90. https://doi.org/10.1016/j.tig.2006.12.004

32. Gaborieau L., Brown G.G., Mireau H. The Propensity of Pentatricopeptide Repeat Genes to Evolve into Restorers of Cytoplasmic Male Sterility. Frontiers in Plant Science. 2016;7:1816. https://doi.org/10.3389/fpls.2016.01816

33. Xu F., Yang X., Zhao N., Hu Z., Mackenzie S., Zhang M., Yang J. Exploiting sterility and fertility variation in cytoplasmic male sterile vegetable crops. Horticulture Research. 2022;9: https://doi.org/10.1093/hr/uhab039

34. Ren W., Si J., Chen L., Fang Z., Zhuang M., Lv H., Wang Y., Ji J., Yu H., Zhang Y. Mechanism and Utilization of Ogura Cytoplasmic Male Sterility in Cruciferae Crops. International Journal of Molecular Sciences. 2022;23:9099. https://doi.org/10.3390/ijms23169099

35. Bohra A., Tiwari A., Pareek S., Joshi R., Naik S., Kumari K., Verma R., Parihar A., Patil P.G., Dixit G.P. Past and future of cytoplasmic male sterility and heterosis breeding in crop plants. Plant Cell Reports. 2025;44(2):33. https://doi.org/10.1007/s00299-024-03414-5

36. Ivanov M.K., Dymshits G.M. Cytoplasmic male sterility and restoration of pollen fertility in higher plants. Russian journal of genetics. 2007;43(4):354-368. https://doi.org/10.1134/S1022795407040023 https://www.elibrary.ru/lksjxd

37. Laser K.D., Lersten N.R. Anatomy and cytology of microsporogenesis in cytoplasmic male sterile angiosperms. The Botanical Review. 1972;38:425- 454.

38. Kalia P., Mangal M., Singh S., Chugh C., Mishra S., Chaudhary S., Shivpratap. Morphological and molecular changes on cytoplasmic male sterility (CMS) introgression in Asiatic carrot (Daucus carota L.). Planta. 2019;250:507-518. https://doi.org/10.1007/s00425-019-03185-4

39. Hanson M.R., Bentolila S. Interactions of mitochondrial and nuclear genes that affect male gametophyte development. The Plant Cell. 2004;16(S1):154-169.

40. Wasiak M. Genetyczne podstawy cytoplazmatyczno-jądrowej męskiej sterylności (CMS) u roślin oraz jej wykorzystanie w hodowli. Agronomy Science. 2019;74:15-30.

41. Rohrbach U. Beitrage zum Problem der Pollensterilitat bei Beta voulgaris L. Untersuchungen uber die Ontogenese des Phanotyps. Zeitschrift fur Pflanzeuchtung. 1965;52:105-124.

42. Majewska-Sawka A., Rodriguez-Garcia M.I., Nakashima H., Brown G.G. Ultrastructural expression of cytoplasmic male sterility in sugar beet (Beta vulgaris L.). Sexual Plant Reproduction. 1993;6:22-32. https://doi.org/10.1007/BF00227579

43. Fedorova M., Vetrova S., Kozar E. Phenotypic features of cms in seedbearing plants of red beet. Vegetable crops of Russia. 2011;(3):18-23. (In Russ.) https://doi.org/10.18619/2072-9146-2011-3-18-23 https://www.elibrary.ru/ozmdrd

44. Vetrova S.A., Kozar E.G., Fedorova M.I. Morphobiological features of generative organs of fertile and sterile table beet plants and their variability as a result of self-pollination (review). Vegetable crops of Russia. 2023;(3):16-23. (In Russ.) https://doi.org/10.18619/2072-9146-2023-3-16-23 https://www.elibrary.ru/nheyte

45. Vetrova S.A., Kozar E.G., Fedorova M.I. Acceleration of the breeding process to create a linear material of red beet. Vegetable crops of Russia. 2019;(1):29-36. (In Russ.) https://doi.org/10.18619/2072-9146-2019-1-29-36 https://www.elibrary.ru/fhksep

46. Kaul M.L.H. Male sterility in higher plants. Monographs on Theoretical and Applied Genetics. Vol. 10. Berlin; Heidelberg; N.Y.: Springer, 1988. 1005 p.

47. Budar F., Pelletier G. Male sterility in plants: occurrence, determinism, significance and use. Comptes Rendus de l'Académie des Sciences - Series III - Sciences de la Vie. 2001;324:543-550.

48. Kubo T., Kitazaki K., Matsunaga M., Kagami H., Mikami T. Male sterilityinducing mitochondrial genomes: how do they differ? Critical Reviews in Plant Sciences. 2011;30:378-400.

49. Anisimova I.N. Structural and functional organization of genes inducing and suppressing cytoplasmic male sterility in plants. Genetics. 2020;56(11):1239-1249. https://doi.org/10.31857/s0016675820110028(In Russ.) https://www.elibrary.ru/zxyiud

50. Satoh M., Kubo T., Mikami T. The Owen mitochondrial genome in sugar beet (Beta vulgaris L.): Possible mechanisms of extensive rearrangements and the origin of the mitotype-unique regions. Theoretical and Applied Genetics. 2006;113:477-484.

51. Budar F., Berthomé R. Cytoplasmic male sterilities and mitochondrial gene mutations in land plants. Plant Mitochondria. Ed. by D.C. Logan. Oxford: Blackwell Publishing, 2007. P.278-307.

52. Chase C.D., Babay-Laughnan S. Cytoplasmic male sterility and fertility restoration by nuclear genes. Molecular Biology and Biotechnology of Plant Organelles. Eds. by H. Daniell, C.D. Chase. Dordrecht: Kluwer Academic publisher, 2004. P.593-622.

53. Owen F.V. Cytoplasmically inherited male-sterility in sugar beets. Journal of Agricultural Research. 1945;71:423-440.

54. Bosemark N.O. Genetics and breeding. Sugar beet. Ed. by A.P. Draycott. Oxford: Blackwell, 2006:50-88.

55. Saumitou-Laprade P., Rouwendal G.J.A., Cuguen J., Krens F.A., Michaelis G. Different CMS sources found in Beta vulgaris ssp. maritima: mitochondrial variability in wild populations revealed by a rapid screening procedure. Theoretical and Applied Genetics. 1993;85:529-535.

56. Mikami T., Kishima Y., Sugiura M., Kinoshita T. Organelle genome diversity in sugar beet with normal and different sources of male sterile cytoplasms. Theoretical and Applied Genetics. 1985;71:166-171.

57. Yamamoto M.P., Kubo T., Mikami T. The 5′-leader sequence of sugar beet mitochondrial atp6 encodes a novel polypeptide that is characteristic of Owen cytoplasmic male sterility. Molecular Genetics and Genomics. 2005;273:342-349. https://doi.org/10.1007/s00438-005-1140-y

58. Ducos E., Touzet P., Boutry M. The male sterile G cytoplasm of wild beet displays modified mitochondrial respiratory complexes. The Plant Journal. 2001;26:171-180. https://doi.org/10.1046/j.1365-313x.2001.01017.x

59. Meyer E.H., Lehmann C., Boivin S., Brings L., De Cauwer I., Bock R. et al. CMS-G from Beta vulgaris ssp. maritima is maintained in natural populations despite containing an atypical cytochrome c oxidase. Biochemical Journal. 2018;475:759-773. https://doi.org/10.1042/BCJ20170527

60. Katsura N., Itoh K., Matsuhira H., Kuroda Y., Kubo T., Kitazaki K. Two cytoplasmic male sterility phenotypes in beet (Beta vulgaris L.): implications of their simultaneous onset and divergent paths. Euphytica. 2023;219:96. https://doi.org/10.1007/s10681-023-03244-8

61. Yamamoto M.P., Shinada H., Onodera Y., Komaki C., Mikami T., Kubo T. A male sterility-associated mitochondrial protein in wild beets causes pollen disruption in transgenic plants. The Plant Journal. 2008;54:1027- 1036. https://doi.org/10.1111/j.1365-313X.2008.03473.x

62. Jańska H., Wołoszyńska M. Molekularne podstawy cytoplazmatycznej męskiej sterylności u roślin wyższych. Postępy biochemii. Z. Zielińskiej. Warszawa: Polskie Towarzystwo Biochemiczne, 1996. P.253-259.

63. Hanson M.R., Pruitt K.D., Nivison H.T. Male sterility loci in plant mitochondrial genes. Oxford Surveys in Plant Molecular and Cellular Biology. 1989;6:61-85.

64. Song J., Hedgcoth C. Influence of nuclear background on transcription of a chimeric gene (orf256) and coxI in fertile and cytoplasmic male sterile wheats. Genome. 1994;37:203-209.

65. Nakamura T., Yagi Y., Kobayashi K. Mechanistic Insight into Pentatricopeptide Repeat Proteins as Sequence-Specific RNA-Binding Proteins for Organellar RNAs in Plants. Plant and Cell Physiology. 2012;53(7):1171-1179. https://doi.org/10.1093/pcp/pcs069

66. Schmitz-Linnerweber C., Small I. Pentatricopeptide repeat proteins, a socket set for organelle gene expression. Trends in Plant Science. 2008;13:663-670. https://doi.org/10.1016/j.tplants.2008.10.001

67. Barkan A., Small I. Pentatricopeptide repeat proteins in plants. Annual Review of Plant Biology. 2014;65:415-442.

68. Chen L., Liu Y.-G. Male sterility and fertility restoration in crops. Annual Review of Plant Biology. 2014;65:579-606.

69. 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. Unusual and typical features of a novel restorer-of-fertility gene of sugar beet (Beta vulgaris L.). Genetics. 2012;192(4):1347-1358. https://doi.org/10.1534/genetics.112.145409

70. Pillen K., Steinrücken G., Herrmann R.G., Jung C. An extended linkage map of sugar beet (Beta vulgaris L.) including nine putative lethal genes and the restorer gene X. Plant Breeding. 1993;111:265-272.

71. Hjerdin-Panagopoulos A., Kraft T., Rading I.M., Tuvesson S., Nilson N.O. Three QTL regions for restoration of Owen CMS in sugar beet. Crop Science. 2002;42:540-544.

72. Honma Y., Taguchi K., Hiyama H., Yui-Kurino R., Mikami T., Kubo T. Molecular mapping of restorer-of-fertility 2 gene identified from a sugar beet (Beta vulgaris L. ssp. vulgaris) homozygous for the non-restoring restorer-offertility 1 allele. Theoretical and Applied Genetics. 2014;127:2567-2574. https://doi.org/10.1007/s00122-014-2398-4

73. Hagihara E., Itchoda N., Habu Y., Iida S., Mikami T., Kubo T. Molecular mapping of a fertility restorer gene for Owen cytoplasmic male sterility in sugar beet. Theoretical and Applied Genetics. 2005;111:250-255.

74. Arakawa T., Matsunaga M., Matsui K., Nagano A.J., Honma Y., Kitazaki K. et al. The molecular basis for allelic differences suggests Restorer-of-fertility 1 is a complex locus in sugar beet (Beta vulgaris L.). BMC Plant Biology. 2020;20:503. https://doi.org/10.1186/s12870-020-02721-9

75. Arakawa T., Sugaya H., Katsuyama T., Honma Y., Matsui K., Matsuhira H. et al. How did a duplicated gene copy evolve into a restorer-of-fertility gene in a plant? The case of Oma1. Royal Society Open Science. 2019;6(11). https://doi.org/10.1098/rsos.190853190853

76. Kitazaki K., Arakawa T., Matsunaga M., Yui-Kurino R., Matsuhira H., Mikami T., Kubo T. Post-translational mechanisms are associated with fertility restoration of cytoplasmic male sterility in sugar beet (Beta vulgaris). The Plant Journal. 2015;83:290-299. https://doi.org/10.1111/tpj.12888

77. Schondelmaier J., Jung C. Chromosomal assignment of the nine linkage groups of sugar beet (Beta vulgaris L.) using primary trisomics. Theoretical and Applied Genetics. 1997;95:590-596.

78. Biancardi E., McGrath J.M., Panella L.W., Lewellen R.T., Stevanato P. Sugar Beet. Root and Tuber Crops. Ed. by J. Bradshaw. New York, NY: Springer, 2010:173-219. (Handbook of Plant Breeding; vol. 7). https://doi.org/10.1007/978-0-387-92765-7_6

79. Karakotov S.D., Apasov I.V., Nalbandyan A.A., Vasilchenko E.N., Fedulova T.P. Modern issues of sugar beet (Beta vulgaris L.) hybrid breeding. Vavilov journal of genetics and breeding. 2021;25(4):394-400. (In Russ.) https://doi.org/10.18699/VJ21.043 https://www.elibrary.ru/xcrkxe


Review

For citations:


Blandinskaya O.A., Vetrova S.A., Kozar E.G., Domblides A.S. Cytoplasmic male sterility in Beta vulgaris L., molecular-genetic mechanisms and application in hybrid breeding (review). Vegetable crops of Russia. 2026;(2):28-36. (In Russ.) https://doi.org/10.18619/2072-9146-2026-2-28-36

Views: 183

JATS XML


Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.


ISSN 2072-9146 (Print)
ISSN 2618-7132 (Online)