Science China Life Sciences

, Volume 62, Issue 6, pp 737–743 | Cite as

Molecular mechanisms of hybrid sterility in rice

  • Yongyao Xie
  • Rongxin Shen
  • Letian ChenEmail author
  • Yao-Guang LiuEmail author
Review From CAS & CAE Members


Hybrid sterility presents a major bottleneck in hybrid crop breeding and causes postzygotic reproductive isolation in speciation. Here, we summarize the current understanding of the genetics of rice hybrid sterility and highlight new advances in deciphering the molecular basis of the major genetic loci for hybrid sterility in rice. We also discuss practical strategies for overcoming reproductive barriers to utilize hybrid vigor in inter-specific and inter-subspecific hybrid rice breeding.

speciation reproductive isolation heterosis hybrid sterility rice 



This work was supported by grants from the Key Research Program of Guangzhou Science Technology and Innovation Commission (201707020016), the National Natural Science Foundation of China (31471564, 31701499) and the China Postdoctoral Science Foundation (2018M630955).


  1. Bateson, W. (1909). Heredity and variation in modern lights. In Darwin and Modern Science. Seward AC, ed. (Cambridge: Cambridge University Press), pp. 85–101.Google Scholar
  2. Chen, J., Ding, J., Ouyang, Y., Du, H., Yang, J., Cheng, K., Zhao, J., Qiu, S., Zhang, X., Yao, J., et al. (2008). A triallelic system of S5 is a major regulator of the reproductive barrier and compatibility of indica-japonica hybrids in rice. Proc Natl Acad Sci USA 105, 11436–11441.CrossRefGoogle Scholar
  3. Chen, L., and Liu, Y.G. (2014). Male sterility and fertility restoration in crops. Annu Rev Plant Biol 65, 579–606.CrossRefGoogle Scholar
  4. Chen, L., Zhao, Z., Liu, X., Liu, L., Jiang, L., Liu, S., Zhang, W., Wang, Y., Liu, Y., and Wan, J. (2011). Marker-assisted breeding of a photoperiod-sensitive male sterile japonica rice with high cross-compatibility with indica rice. Mol Breed 27, 247–258.CrossRefGoogle Scholar
  5. Cheng, S.H., Zhuang, J.Y., Fan, Y.Y., Du, J.H., and Cao, L.Y. (2007). Progress in research and development on hybrid rice: a super-domesticate in China. Ann Bot 100, 959–966.CrossRefGoogle Scholar
  6. Dobzhansky, T. (1937). Genetics and the Origin of Species (New York: Columbia University Press).Google Scholar
  7. Garavito, A., Guyot, R., Lozano, J., Gavory, F., Samain, S., Panaud, O., Tohme, J., Ghesquière, A., and Lorieux, M. (2010). A genetic model for the female sterility barrier between Asian and African cultivated rice species. Genetics 185, 1425–1440.CrossRefGoogle Scholar
  8. Guo, J., Xu, X., Li, W., Zhu, W., Zhu, H., Liu, Z., Luan, X., Dai, Z., Liu, G., Zhang, Z., et al. (2016). Overcoming inter-subspecific hybrid sterility in rice by developing indica-compatible japonica lines. Sci Rep 6, 26878.CrossRefGoogle Scholar
  9. Huang, X., Kurata, N., Wei, X., Wang, Z.X., Wang, A., Zhao, Q., Zhao, Y., Liu, K., Lu, H., Li, W., et al. (2012). A map of rice genome variation reveals the origin of cultivated rice. Nature 490, 497–501.CrossRefGoogle Scholar
  10. Ikehashi, H., and Araki, H. (1987). Screening and genetic analysis of wide-compatibility in F1 hybrids of distant crosses in rice, Oryza Sativa L. Tech Bull Tarc 2, 231–241.Google Scholar
  11. Kate, S., Kosaka, H. and Hara S. (1928). On the affinity of rice varieties as shown by fertility of hybrid plants. Bull Sci Fac Agric Kyushu Univ 3, 132–147.Google Scholar
  12. Kitamura, E. (1962). Genetics studies on sterility observed in hybrids between distantly related varieties of rice (Oryza sativa L.). Bull Chgoku Agri Exp Sta Ser A 8, 141–205.Google Scholar
  13. Koide, Y., Onishi, K., Nishimoto, D., Baruah, A.R., Kanazawa, A., and Sano, Y. (2008). Sex-independent transmission ratio distortion system responsible for reproductive barriers between Asian and African rice species. New Phytol 179, 888–900.CrossRefGoogle Scholar
  14. Koide, Y., Ogino, A., Yoshikawa, T., Kitashima, Y., Saito, N., Kanaoka, Y., Onishi, K., Yoshitake, Y., Tsukiyama, T., Saito, H., et al. (2018). Lineage-specific gene acquisition or loss is involved in interspecific hybrid sterility in rice. Proc Natl Acad Sci USA 115, E1955–E1962.CrossRefGoogle Scholar
  15. Kubo, T., Takashi, T., Ashikari, M., Yoshimura, A., and Kurata, N. (2016). Two tightly linked genes at the hsa1 locus cause both F1 and F2 hybrid sterility in rice. Mol Plant 9, 221–232.CrossRefGoogle Scholar
  16. Long, Y., Zhao, L., Niu, B., Su, J., Wu, H., Chen, Y., Zhang, Q., Guo, J., Zhuang, C., Mei, M., et al. (2008). Hybrid male sterility in rice controlled by interaction between divergent alleles of two adjacent genes. Proc Natl Acad Sci USA 105, 18871–18876.CrossRefGoogle Scholar
  17. Mi, J., Li, G., Huang, J., Yu H, Zhou, F., Zhang, Q., Ouyang, Y., and Mou, T. (2016). Stacking S5-n and f5-n to overcome sterility in indica-japonica hybrid rice. Theor Appl Genet 129, 563–575.CrossRefGoogle Scholar
  18. Mizuta, Y., Harushima, Y., and Kurata, N. (2010). Rice pollen hybrid incompatibility caused by reciprocal gene loss of duplicated genes. Proc Natl Acad Sci USA 107, 20417–20422.CrossRefGoogle Scholar
  19. Muller, H.J. (1942). Isolating mechanisms, evolution, and temperature. Biol Symp 6, 71–125.Google Scholar
  20. Nguyen, G.N., Yamagata, Y., Shigematsu, Y., Watanabe, M., Miyazaki, Y., Doi, K., Tashiro, K., Kuhara S., Kanamori, H., Wu, J., et al. (2017). Duplication and loss of function of genes encoding RNA polymerase III subunit C4 causes hybrid incompatibility in rice. G3 7, 2565–2575.CrossRefGoogle Scholar
  21. Oka, H.I. (1957). Genic analysis for the sterility of hybrids between distantly related varieties of cultivated rice. J Genet 55, 397–409.CrossRefGoogle Scholar
  22. Oka, H. (1974). Analysis of genes controlling F1 sterility in rice by the use of isogenic lines. Genetics 77, 521–534.Google Scholar
  23. Ouyang, Y., and Zhang, Q. (2013). Understanding reproductive isolation based on the rice model. Annu Rev Plant Biol 64, 111–135.CrossRefGoogle Scholar
  24. Ouyang, Y. (2016). Progress of indica-japonica hybrid sterility and wide-compatibility in rice (in Chinese). Chin Sci Bull 61, 3833–3841.Google Scholar
  25. Ouyang, Y., Li, G., Mi, J., Xu, C., Du, H., Zhang, C Xie, W., Li, X., Xiao, J., Song, H., et al. (2016). Origination and establishment of a trigenic reproductive isolation system in rice. Mol Plant 9, 1542–1545.CrossRefGoogle Scholar
  26. Ouyang, Y., and Zhang, Q. (2018). The molecular and evolutionary basis of reproductive isolation in plants. J Genet Genomics 45, 613–620.CrossRefGoogle Scholar
  27. Qian, Q., Guo, L., Smith, S.M., and Li, J. (2016). Breeding high-yield superior quality hybrid super rice by rational design. Nat Sci Rev 3, 283–294.CrossRefGoogle Scholar
  28. Shen, R., Wang, L., Liu, X., Wu, J., Jin, W., Zhao, X., Xie, X., Zhu, Q., Tang, H., Li, Q., et al. (2017). Genomic structural variation-mediated allelic suppression causes hybrid male sterility in rice. Nat Commun 8, 1310.CrossRefGoogle Scholar
  29. Tang, H., Xie, Y., Liu, Y.G., and Chen, L. (2017). Advances in understanding the molecular mechanisms of cytoplasmic male sterility and restoration in rice. Plant Reprod 30, 179–184.CrossRefGoogle Scholar
  30. Xie, Y., Xu, P., Huang, J., Ma, S., Xie, X., Tao, D., Chen, L., and Liu, Y.G. (2017a). Interspecific hybrid sterility in rice is mediated by OgTPR1 at the S1 locus encoding a peptidase-like protein. Mol Plant 10, 1137–1140.CrossRefGoogle Scholar
  31. Xie, Y., Niu, B., Long, Y., Li, G., Tang, J., Zhang, Y., Ren, D., Liu, Y.G., and Chen, L. (2017b). Suppression or knockout of SaF/SaM overcomes the Sa-mediated hybrid male sterility in rice. J Integr Plant Biol 59, 669–679.CrossRefGoogle Scholar
  32. Xie, Y., Tang, J., Xie, X., Li, X., Huang, J., Fei, Y., Han J., Chen, S., Tang, H., Zhao, X., et al. (2019). An asymmetric allelic interaction drives allele transmission bias in interspecific 1 rice hybrids. Nat Commun, doi:
  33. Yamagata, Y., Yamamoto, E., Aya, K., Thanda Win, K., Doi, K., Ito, T., Kanamori, H., Wu, J., Matsumoto, T., Matsuoka, M., et al. (2010). Mitochondrial gene in the nuclear genome induces reproductive barrier in rice. Proc Natl Acad Sci USA 107, 1494–1499.CrossRefGoogle Scholar
  34. Yang C, Chen Z, Zhuang C et al. Genetic and Physical Fine-Mapping of the Sc Locus Conferring Indica-Japonica Hybrid Sterility in Rice (Oryza sativa L.). Chin Sci Bull, 2004, 16: 1718–1721.Google Scholar
  35. Yang, J., Zhao, X., Cheng, K., Du, H., Ouyang, Y., Chen, J., Qiu, S., Huang, J., Jiang, Y., Jiang, L., et al. (2012). A killer-protector system regulates both hybrid sterility and segregation distortion in rice. Science 337, 1336–1340.CrossRefGoogle Scholar
  36. Yu, Y., Zhao, Z., Shi, Y., Tian, H., Liu, L., Bian, X., Xu, Y., Zheng, X., Gan, L., Shen, Y., et al. (2016). Hybrid sterility in rice (Oryza sativa L.) involves the tetratricopeptide repeat domain containing protein. Genetics 203, 1439–1451.CrossRefGoogle Scholar
  37. Yuan, L. (2014). Development of hybrid rice to ensure food security. Rice Sci 21, 1–2.CrossRefGoogle Scholar
  38. Yu, X., Zhao, Z., Zheng, X., Zhou, J., Kong, W., Wang, P., Bai, W., Zheng, H., Zhang, H., Li, J., et al. (2018). A selfish genetic element confers non-Mendelian inheritance in rice. Science 360, 1130–1132.CrossRefGoogle Scholar

Copyright information

© Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.State Key Laboratory for Conservation and Utilization of Subtropical Agro-BioresourcesSouth China Agricultural UniversityGuangzhouChina
  2. 2.Guangdong Provincial Key Laboratory of Protein Function and Regulation in Agricultural OrganismsSouth China Agricultural UniversityGuangzhouChina
  3. 3.Key Laboratory of Plant Functional Genomics and Biotechnology of Guangdong Provincial Higher Education InstitutionsSouth China Agricultural UniversityGuangzhouChina
  4. 4.College of Life SciencesSouth China Agricultural UniversityGuangzhouChina

Personalised recommendations