Stigma receptors control intraspecies and interspecies barriers in Brassicaceae

• Published in: Nature (London) 2023-02, Vol.614 (7947), p.303-308
• Main Authors: Huang, Jiabao, Yang, Lin, Yang, Liu, Wu, Xiaoyu, Cui, Xiaoshuang, Zhang, Lili, Hui, Jiyun, Zhao, Yumei, Yang, Hongmin, Liu, Shangjia, Xu, Quanling, Pang, Maoxuan, Guo, Xinping, Cao, Yunyun, Chen, Yu, Ren, Xinru, Lv, Jinzhi, Yu, Jianqiang, Ding, Junyi, Xu, Gang, Wang, Nian, Wei, Xiaochun, Lin, Qinghui, Yuan, Yuxiang, Zhang, Xiaowei, Ma, Chaozhi, Dai, Cheng, Wang, Pengwei, Wang, Yongchao, Cheng, Fei, Zeng, Weiqing, Palanivelu, Ravishankar, Wu, Hen-Ming, Zhang, Xiansheng, Cheung, Alice Y., Duan, Qiaohong
• Format: Article
• Language: English
• Subjects: 38; 38/77; 38/90; 631/449/2675; 631/449/2679/1489; 82/1; 82/111; 82/58; 82/83; 96; 96/63; 96/95; Brassicaceae; Brassicaceae - genetics; Brassicaceae - metabolism; Breeding; Coat protein; Compatibility; Flowering; Flowering plants; Flowers - metabolism; Humanities and Social Sciences; Hybridization, Genetic; Inbreeding; Inbreeding Depression; Incompatibility; Interspecific; Kinases; Molecular modelling; multidisciplinary; Nitric oxide; Nitric Oxide - metabolism; Oxygen; Phosphotransferases - metabolism; Pistils; Plant Breeding; Plant Proteins - metabolism; Plant reproduction; Plant reproductive structures; Plants (botany); Pollen; Pollen - metabolism; Pollination; Protein B; Proteins; Reactive oxygen species; Reactive Oxygen Species - metabolism; Receptors; Science; Science (multidisciplinary); Self-Fertilization; Self-incompatibility; Species Specificity; Stigma; Stigmas (botany)
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/s41586-022-05640-x

Flowering plants have evolved numerous intraspecific and interspecific prezygotic reproductive barriers to prevent production of unfavourable offspring 1 . Within a species, self-incompatibility (SI) is a widely utilized mechanism that rejects self-pollen 2 , 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 pistils 1 , 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 stigmas 10 , 11 to reject incompatible pollen. For compatible responses, diverged pollen coat protein B-class 12 – 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. A signalling mechanism ensuring intraspecies and interspecies reproductive barriers in flowering plants is uncovered.