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A natural gene drive system confers reproductive isolation in rice

Chaolong Wang; Jian Wang; Jiayu Lu; Yehui Xiong; Zhigang Zhao; Xiaowen Yu; Xiaoming Zheng; Jing Li; Qibing Lin; Yulong Ren; Yang Hu; Xiaodong He; Chao Li; Yonglun Zeng; Rong Miao; Mali Guo; Bosen Zhang; Ying Zhu; Yunhui Zhang; Weijie Tang; Yunlong Wang; Benyuan Hao; Qiming Wang; Siqi Cheng; Xiaojuan He; Bowen Yao; Junwen Gao; Xufei Zhu; Hao Yu; Yong Wang; Yan Sun; Chunlei Zhou; Hui Dong; Xiaoding Ma; Xiuping Guo; Xi Liu; Yunlu Tian; Shijia Liu; Chunming Wang; Zhijun Cheng; Ling Jiang; Jiawu Zhou; Huishan Guo; Liwen Jiang; Dayun Tao; Jijie Chai; Wei Zhang; Haiyang Wang; Chuanyin Wu; Jianmin Wan.

Cell, 2023, IF 64.50

DOI: 10.1016/j.cell.2023.06.023

ABSTRACT:

Hybrid sterility restricts the utilization of superior heterosis of indica-japonica inter-subspecific hybrids. In this study, we report the identification of RHS12, a major locus controlling male gamete sterility in indica-japonica hybrid rice. We show that RHS12 consists of two genes (iORF3/DUYAO and iORF4/JIEYAO) that confer preferential transmission of the RHS12-i type male gamete into the progeny, thereby forming a natural gene drive. DUYAO encodes a mitochondrion-targeted protein that interacts with OsCOX11 to trigger cytotoxicity and cell death, whereas JIEYAO encodes a protein that reroutes DUYAO to the autophagosome for degradation via direct physical interaction, thereby detoxifying DUYAO. Evolutionary trajectory analysis reveals that this system likely formed de novo in the AA genome Oryza clade and contributed to reproductive isolation (RI) between different lineages of rice. Our combined results provide mechanistic insights into the genetic basis of RI as well as insights for strategic designs of hybrid rice breeding.



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