Stigma receptors control intraspecies and interspecies barriers in Brassicaceae

Jiabao Huang, Lin Yang, Liu Yang, Xiaoyu Wu, Xiaoshuang Cui, Lili Zhang, Jiyun Hui, Yumei Zhao, Hongmin Yang, Shangjia Liu, Quanling Xu, Maoxuan Pang, Xinping Guo, Yunyun Cao, Yu Chen, Xinru Ren, Jinzhi Lv, Jianqiang Yu, Junyi Ding, Gang Xu, Nian Wang, Xiaochun Wei, Qinghui Lin, Yuxiang Yuan, Xiaowei Zhang, Chaozhi Ma, Cheng Dai, Pengwei Wang, Yongchao Wang, Fei Cheng, Weiqing Zeng, Ravishankar Palanivelu, Hen-Ming Wu, Xiansheng Zhang, Alice Y. Cheung () and Qiaohong Duan ()
Additional contact information
Jiabao Huang: Shandong Agricultural University
Lin Yang: Shandong Agricultural University
Liu Yang: Shandong Agricultural University
Xiaoyu Wu: Shandong Agricultural University
Xiaoshuang Cui: Shandong Agricultural University
Lili Zhang: Shandong Agricultural University
Jiyun Hui: Shandong Agricultural University
Yumei Zhao: Shandong Agricultural University
Hongmin Yang: Shandong Agricultural University
Shangjia Liu: Shandong Agricultural University
Quanling Xu: Shandong Agricultural University
Maoxuan Pang: Shandong Agricultural University
Xinping Guo: Shandong Agricultural University
Yunyun Cao: Shandong Agricultural University
Yu Chen: Shandong Agricultural University
Xinru Ren: Shandong Agricultural University
Jinzhi Lv: Shandong Agricultural University
Jianqiang Yu: Shandong Agricultural University
Junyi Ding: Shandong Agricultural University
Gang Xu: Shandong Agricultural University
Nian Wang: Shandong Agricultural University
Xiaochun Wei: Henan Academy of Agricultural Sciences
Qinghui Lin: Chinese Academy of Sciences
Yuxiang Yuan: Henan Academy of Agricultural Sciences
Xiaowei Zhang: Henan Academy of Agricultural Sciences
Chaozhi Ma: Huazhong Agricultural University
Cheng Dai: Huazhong Agricultural University
Pengwei Wang: Huazhong Agricultural University
Yongchao Wang: Shandong Yiyi Agricultural Science and Technology Co., Ltd
Fei Cheng: Qingdao Agricultural University
Weiqing Zeng: International Flavors & Fragrances
Ravishankar Palanivelu: University of Arizona
Hen-Ming Wu: University of Massachusetts
Xiansheng Zhang: Shandong Agricultural University
Alice Y. Cheung: University of Massachusetts
Qiaohong Duan: Shandong Agricultural University

Nature, 2023, vol. 614, issue 7947, 303-308

Abstract: Abstract Flowering plants have evolved numerous intraspecific and interspecific prezygotic reproductive barriers to prevent production of unfavourable offspring1. Within a species, self-incompatibility (SI) is a widely utilized mechanism that rejects self-pollen2,3 to avoid inbreeding depression. Interspecific barriers restrain breeding between species and often follow the SI × self-compatible (SC) rule, that is, interspecific pollen is unilaterally incompatible (UI) on SI pistils but unilaterally compatible (UC) on SC pistils1,4–6. The molecular mechanisms underlying SI, UI, SC and UC and their interconnections in the Brassicaceae remain unclear. Here we demonstrate that the SI pollen determinant S-locus cysteine-rich protein/S-locus protein 11 (SCR/SP11)2,3 or a signal from UI pollen binds to the SI female determinant S-locus receptor kinase (SRK)2,3, recruits FERONIA (FER)7–9 and activates FER-mediated reactive oxygen species production in SI stigmas10,11 to reject incompatible pollen. For compatible responses, diverged pollen coat protein B-class12–14 from SC and UC pollen differentially trigger nitric oxide, nitrosate FER to suppress reactive oxygen species in SC stigmas to facilitate pollen growth in an intraspecies-preferential manner, maintaining species integrity. Our results show that SRK and FER integrate mechanisms underlying intraspecific and interspecific barriers and offer paths to achieve distant breeding in Brassicaceae crops.

Date: 2023
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DOI: 10.1038/s41586-022-05640-x

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