Abstract
Male sterility is an important trait in rice for hybrid rice (Oryza sativa) breeding. However, the factors involved in dominant male sterility are largely unknown. Here, we identified a gene from Sanming dominant genic male sterile rice, named Sanming dominant male sterility (SMS), and reported that an epi-allele of this locus contributes to male sterility. Segregation analysis attributed dominant male sterility to a single locus, SMS, which we characterized using a male-sterile near isogenic line (NIL) of rice cultivar 93-11. The SMS locus was heterozygous in the male-sterile 93-11 NIL, containing an epi-allele identical to that in 93-11, and an epi-allele identical to that in rice cultivar Nipponbare, which we refer to as SMS9 and SMSN, respectively. SMS9 is silent and hyper-methylated, whereas SMSN is expressed and hypo-methylated in the 93-11 NIL. Overexpressing SMSN led to male sterility. Mutations in SMS rescued the male sterility of the 93-11 NIL. Interestingly, we observed the duplication of SMSN in Nipponbare, but did not observe the duplication of SMS9 in 93-11. Together, these findings suggest that the reduced methylation and enhanced expression of the SMSN epi-allele in the 93-11 NIL is responsible for its role in conferring dominant male sterility.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Cai, D., Zhang, Z., Zhao, L., Liu, J., and Chen, H. (2023). A novel hybrid seed production technology based on a unilateral cross-incompatibility gene in maize. Sci China Life Sci 66, 595–601.
Cheng, S.H., Cao, L.Y., Zhuang, J.Y., Chen, S.G., Zhan, X.D., Fan, Y.Y., Zhu, D.F., and Min, S.K. (2007). Super hybrid rice breeding in China: achievements and prospects. J Integr Plant Biol 49, 805–810.
Deng, X.J., and Zhou, K.D. (1994). Study on fertility transition and inheritance of the lower temperature thermo-sensitive dominant male-sterile rice “8987” (in Chinese). J Sichuan Agric Univ 12, 376–382.
Ding, J., Lu, Q., Ouyang, Y., Mao, H., Zhang, P., Yao, J., Xu, C., Li, X., Xiao, J., and Zhang, Q. (2012). A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice. Proc Natl Acad Sci USA 109, 2654–2659.
Ding, Y., Wang, X., Su, L., Zhai, J.X., Cao, S.Y., Zhang, D.F., Liu, C.Y., Bi, Y.P., Qian, Q., Cheng, Z.K., et al. (2007). SDG714, a histone H3K9 methyltransferase, is involved in Tos17 DNA methylation and transposition in rice. Plant Cell 19, 9–22.
Dong, N.V., Subudhi, P.K., Luong, P.N., Quang, V.D., Quy, T.D., Zheng, H. G., Wang, B., and Nguyen, H.T. (2000). Molecular mapping of a rice gene conditioning thermosensitive genic male sterility using AFLP, RFLP and SSR techniques. Theor Appl Genet 100, 727–734.
Fan, Y., Yang, J., Mathioni, S.M., Yu, J., Shen, J., Yang, X., Wang, L., Zhang, Q., Cai, Z., Xu, C., et al. (2016). PMS1T, producing phased small-interfering RNAs, regulates photoperiod-sensitive male sterility in rice. Proc Natl Acad Sci USA 113, 15144–15149.
Fang, X., Sun, X., Yang, X., Li, Q., Lin, C., Xu, J., Gong, W., Wang, Y., Liu, L., Zhao, L., et al. (2021). MS1 is essential for male fertility by regulating the microsporocyte cell plate expansion in soybean. Sci China Life Sci 64, 1533–1545.
Fukagawa, N.K., and Ziska, L.H. (2019). Rice: importance for global nutrition. J Nutr Sci Vitaminol 65, S2–S3.
He, H., Peng, X., Gong, H., Zhu, C., and Ye, G. (2006). Fertility behaviour of rice (Oryza sativa) lines with dominant male sterile gene and inheritance of sterility and fertility restoration. Field Crops Res 98, 30–38.
He, L., Huang, H., Bradai, M., Zhao, C., You, Y., Ma, J., Zhao, L., Lozano-Durán, R., and Zhu, J.K. (2022). DNA methylation-free Arabidopsis reveals crucial roles of DNA methylation in regulating gene expression and development. Nat Commun 13, 1335.
Huang, T., Wang, Y., Ma, B., Ma, Y., and Li, S. (2007). Genetic analysis and mapping of genes involved in fertility of Pingxiang dominant genic male sterile rice. J Genet Genomics 34, 616–622.
Ikram, A.U., Zhang, F., Xu, Z., Li, E., Xue, G., Wang, S., Zhang, C., Yang, Y., Su, Y., and Ding, Y. (2022). Chromatin remodeling factors OsYAF9 and OsSWC4 interact to promote internode elongation in rice. Plant Physiol 188, 2199–2214.
Jeong, H.J., and Jung, K.H. (2015). Rice tissue-specific promoters and condition-dependent promoters for effective translational application. J Integr Plant Biol 57, 913–924.
Lang, N.T., Subudhi, P.K., Virmani, S.S., Brar, D.S., Khush, G.S., Li, Z., and Huang, N. (1999). Development of PCR-based markers for thermosensitive genetic male sterility gene tms3(t) in rice (Oryza Sativa L.). Hereditas 131, 121–127.
Lee, D.S., Chen, L.J., and Suh, H.S. (2005). Genetic characterization and fine mapping of a novel thermo-sensitive genic male-sterile gene tms6 in rice (Oryza sativa L.). Theor Appl Genet 111, 1271–1277.
Lei, D., Jian, A., Huang, X., Liu, X., Chen, L., Bai, W., Cheng, S., He, X., Xiong, Y., Yu, X., et al. (2023). Anther-specific expression of OsRIP1 causes dominant male sterility in rice. Plant Biotechnol J 21, 1932–1934.
Lin, S.C., and Yuan, L.P. (1980). Hybrid rice breeding in China. In: Innovative Approaches to Rice Breeding: Selected Papers form the 1979 International Rice Research Conference International Rice Research Institute. Los Banos.
Liu, X., Shangguan, Y., Zhu, J., Lu, Y., and Han, B. (2013). The rice OsLTP6 gene promoter directs anther-specific expression by a combination of positive and negative regulatory elements. Planta 238, 845–857.
Lopez, M.T., Toojinda, T., Vanavichit, A., and Tragoonrung, S. (2003). Microsatellite markers flanking the tms2 gene facilitated tropical TGMS rice line development. Crop Sci 43, 2267–2271.
Luo, D., Xu, H., Liu, Z., Guo, J., Li, H., Chen, L., Fang, C., Zhang, Q., Bai, M., Yao, N., et al. (2013). A detrimental mitochondrial-nuclear interaction causes cytoplasmic male sterility in rice. Nat Genet 45, 573–577.
Lynch, M. (2002). Gene duplication and evolution. Science 297, 945–947. Magadum, S., Banerjee, U., Murugan, P., Gangapur, D., and Ravikesavan, R. (2013). Gene duplication as a major force in evolution. J Genet 92, 155–161.
Ni, F., Qi, J., Hao, Q., Lyu, B., Luo, M.C., Wang, Y., Chen, F., Wang, S., Zhang, C., Epstein, L., et al. (2017). Wheat Ms2 encodes for an orphan protein that confers male sterility in grass species. Nat Commun 8, 15121.
Panchy, N., Lehti-Shiu, M., and Shiu, S.H. (2016). Evolution of gene duplication in plants. Plant Physiol 171, 2294–2316.
Peng, X., Wang, K., Hu, C., Zhu, Y., Wang, T., Yang, J., Tong, J., Li, S., and Zhu, Y. (2010). The mitochondrial gene orfH79 plays a critical role in impairing both male gametophyte development and root growth in CMS-Honglian rice. BMC Plant Biol 10, 125.
Si, F., Luo, H., Yang, C., Gong, J., Yan, B., Liu, C., Song, X., and Cao, X. (2023). Mobile ARGONAUTE 1d binds 22-nt miRNAs to generate phasiRNAs important for low-temperature male fertility in rice. Sci China Life Sci 66, 197–208.
Sun, C., Hu, Z., Zheng, T., Lu, K., Zhao, Y., Wang, W., Shi, J., Wang, C., Lu, J., Zhang, D., et al. (2017). RPAN: rice pan-genome browser for ~3000 rice genomes. Nucleic Acids Res 45, 597–605.
Tang, S., Yang, C., Wang, D., Deng, X., Cao, X., and Song, X. (2022). Targeted DNA demethylation produces heritable epialleles in rice. Sci China Life Sci 65, 753–756.
Wan, C., Li, S., Wen, L., Kong, J., Wang, K., and Zhu, Y. (2007). Damage of oxidative stress on mitochondria during microspores development in Honglian CMS line of rice. Plant Cell Rep 26, 373–382.
Wang, B., Xu, W.W., Wang, J.Z., Wu, W., Zheng, H.G., Yang, Z.Y., Ray, J. D., and Nguyen, H.T. (1995). Tagging and mapping the thermo-sensitive genic male-sterile gene in rice (Oryza sativa L.) with molecular markers. Theoret Appl Genet 91–91, 1111–1114.
Wang, K., Gao, F., Ji, Y., Liu, Y., Dan, Z., Yang, P., Zhu, Y., and Li, S. (2013). ORFH79 impairs mitochondrial function via interaction with a subunit of electron transport chain complex III in Honglian cytoplasmic male sterile rice. New Phytol 198, 408–418.
Xia, C., Zhang, L., Zou, C., Gu, Y., Duan, J., Zhao, G., Wu, J., Liu, Y., Fang, X., Gao, L., et al. (2017). A TRIM insertion in the promoter of Ms2 causes male sterility in wheat. Nat Commun 8, 15407.
Xu, C., Xu, Y., Wang, Z., Zhang, X., Wu, Y., Lu, X., Sun, H., Wang, L., Zhang, Q., Zhang, Q., et al. (2023). Spontaneous movement of a retrotransposon generated genic dominant male sterility providing a useful tool for rice breeding. Natl Sci Rev 10, nwad210.
Yamaguchi, Y., Ikeda, R., Hirasawa, H., Minami, M., and Ujihara, A. (1997). Linkage analysis of thermosensitive genic male sterility gene, tms-2 in rice (Oryza sativa L.).. Japan J Breed 47, 371–373.
Yang, Z.M., Xie, X.F., Huang, X.B., Wang, F.Q., Tong, Z.J., Duan, Y.L., Lan, T., and Wu, W.R. (2012). Mapping of Sanming dominant genic male sterility gene in rice. Hereditas 34, 615–620.
Yi, P., Wang, L., Sun, Q., and Zhu, Y. (2002). Discovery of mitochondrial chimeric-gene associated with cytoplasmic male sterility of HL-rice. Chin Sci Bull 47, 744–747.
Yuan, L.P. (2014). Development of hybrid rice to ensure food security. Rice Sci 21, 1–2.
Zhang, X., Yazaki, J., Sundaresan, A., Cokus, S., Chan, S.W.L., Chen, H., Henderson, I.R., Shinn, P., Pellegrini, M., Jacobsen, S.E., et al. (2006). Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126, 1189–1201.
Zhou, H., Zhou, M., Yang, Y., Li, J., Zhu, L., Jiang, D., Dong, J., Liu, Q., Gu, L., Zhou, L., et al. (2014). RNase ZS1 processes UbL40 mRNAs and controls thermosensitive genic male sterility in rice. Nat Commun 5, 4884.
Zhu, X.D., and Rutger, J. (2000). Identification of dominant male sterile mutants in rice (Oryza sativa L.) (in Chinese). Acta Agric Nucl Sin 14, 279–283.
Zilberman, D., Gehring, M., Tran, R.K., Ballinger, T., and Henikoff, S. (2007). Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 39, 61–69.
Acknowledgements
This work was supported by the Global Select Project (DJK-LX-2022007) of the Institute of Health and Medicine, Hefei Comprehensive National Science Center, the Key Research and Development Projects in Anhui Province (2023n06020035, 202104b11020008), the University Synergy Innovation Program of Anhui Province (GXXT-2019-033), the National Natural Science Foundation of China (U19A2021, 32230017), the Anhui Province Major Special Project for Improving Seed Production, and the Strategic Priority Research Program “Molecular Mechanisms of Plant Growth and Development” of the Chinese Academy of Sciences (XDB27030203). We thank Mr. Yangwen Qian (Changzhou. Wimi Biotechnology Co., Ltd., China) for generating transgenic plants.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Compliance and ethics The author(s) declare that they have no conflict of interest.
Electronic Supplementary Material
Rights and permissions
About this article
Cite this article
Yang, Y., Zhang, C., Li, H. et al. An epi-allele of SMS causes Sanming dominant genic male sterility in rice. Sci. China Life Sci. 66, 2701–2710 (2023). https://doi.org/10.1007/s11427-023-2457-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11427-023-2457-7