A toxin-antidote system contributes to interspecific reproductive isolation in rice

Shimin You, Zhigang Zhao, Xiaowen Yu, Shanshan Zhu, Jian Wang, Dekun Lei, Jiawu Zhou, Jing Li, Haiyuan Chen, Yanjia Xiao, Weiwei Chen, Qiming Wang, Jiayu Lu, Keyi Chen, Chunlei Zhou, Xin Zhang, Zhijun Cheng, Xiuping Guo, Yulong Ren, Xiaoming Zheng, Shijia, Nature Communications, 14. 2023.

Breakdown of reproductive isolation facilitates flow of useful trait genes into crop plants from their wild relatives. Hybrid sterility, a major form of reproductive isolation exists between cultivated rice (Oryza sativa) and wild rice (O. meridionalis, Mer). Here, we report the cloning of qHMS1, a quantitative trait locus controlling hybrid male sterility between these two species. Like qHMS7, another locus we cloned previously, qHMS1 encodes a toxin-antidote system, but differs in the encoded proteins, their evolutionary origin, and action time point during pollen development. In plants heterozygous at qHMS1, ~ 50% of pollens carrying qHMS1-D (an allele from cultivated rice) are selectively killed. In plants heterozygous at both qHMS1 and qHMS7, ~ 75% pollens without co-presence of qHMS1-Mer and qHMS7-D are selectively killed, indicating that the antidotes function in a toxin-dependent manner. Our results indicate that different toxin-antidote systems provide stacked reproductive isolation for maintaining species identity and shed light on breakdown of hybrid male sterility.