Skip to main content
Log in

Molecular mechanisms of hybrid sterility in rice

  • Review
  • From CAS & CAE Members
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

Abstract

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.

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

  • Bateson, W. (1909). Heredity and variation in modern lights. In Darwin and Modern Science. Seward AC, ed. (Cambridge: Cambridge University Press), pp. 85–101.

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen, L., and Liu, Y.G. (2014). Male sterility and fertility restoration in crops. Annu Rev Plant Biol 65, 579–606.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dobzhansky, T. (1937). Genetics and the Origin of Species (New York: Columbia University Press).

    Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Muller, H.J. (1942). Isolating mechanisms, evolution, and temperature. Biol Symp 6, 71–125.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oka, H.I. (1957). Genic analysis for the sterility of hybrids between distantly related varieties of cultivated rice. J Genet 55, 397–409.

    Article  Google Scholar 

  • Oka, H. (1974). Analysis of genes controlling F1 sterility in rice by the use of isogenic lines. Genetics 77, 521–534.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ouyang, Y., and Zhang, Q. (2013). Understanding reproductive isolation based on the rice model. Annu Rev Plant Biol 64, 111–135.

    Article  CAS  PubMed  Google Scholar 

  • Ouyang, Y. (2016). Progress of indica-japonica hybrid sterility and wide-compatibility in rice (in Chinese). Chin Sci Bull 61, 3833–3841.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Ouyang, Y., and Zhang, Q. (2018). The molecular and evolutionary basis of reproductive isolation in plants. J Genet Genomics 45, 613–620.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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: https://doi.org/10.1038/S41467-019-10488-3.

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan, L. (2014). Development of hybrid rice to ensure food security. Rice Sci 21, 1–2.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

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).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Letian Chen or Yao-Guang Liu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xie, Y., Shen, R., Chen, L. et al. Molecular mechanisms of hybrid sterility in rice. Sci. China Life Sci. 62, 737–743 (2019). https://doi.org/10.1007/s11427-019-9531-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11427-019-9531-7

Navigation