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Stigma receptors control intraspecies and interspecies barriers in Brassicaceae

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Listed:
  • Jiabao Huang

    (Shandong Agricultural University
    Shandong Agricultural University)

  • Lin Yang

    (Shandong Agricultural University
    Shandong Agricultural University)

  • Liu Yang

    (Shandong Agricultural University
    Shandong Agricultural University)

  • Xiaoyu Wu

    (Shandong Agricultural University
    Shandong Agricultural University)

  • Xiaoshuang Cui

    (Shandong Agricultural University
    Shandong Agricultural University)

  • Lili Zhang

    (Shandong Agricultural University
    Shandong Agricultural University)

  • Jiyun Hui

    (Shandong Agricultural University
    Shandong Agricultural University)

  • Yumei Zhao

    (Shandong Agricultural University
    Shandong Agricultural University)

  • Hongmin Yang

    (Shandong Agricultural University
    Shandong Agricultural University)

  • Shangjia Liu

    (Shandong Agricultural University
    Shandong Agricultural University)

  • Quanling Xu

    (Shandong Agricultural University
    Shandong Agricultural University)

  • Maoxuan Pang

    (Shandong Agricultural University
    Shandong Agricultural University)

  • Xinping Guo

    (Shandong Agricultural University
    Shandong Agricultural University)

  • Yunyun Cao

    (Shandong Agricultural University
    Shandong Agricultural University)

  • Yu Chen

    (Shandong Agricultural University
    Shandong Agricultural University)

  • Xinru Ren

    (Shandong Agricultural University
    Shandong Agricultural University)

  • Jinzhi Lv

    (Shandong Agricultural University
    Shandong Agricultural University)

  • Jianqiang Yu

    (Shandong Agricultural University
    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
    Shandong Agricultural University)

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.

Suggested Citation

  • 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 & , 2023. "Stigma receptors control intraspecies and interspecies barriers in Brassicaceae," Nature, Nature, vol. 614(7947), pages 303-308, February.
  • Handle: RePEc:nat:nature:v:614:y:2023:i:7947:d:10.1038_s41586-022-05640-x
    DOI: 10.1038/s41586-022-05640-x
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    Cited by:

    1. 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 & Xi, 2023. "A toxin-antidote system contributes to interspecific reproductive isolation in rice," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    2. Keyi Chen & Qiming Wang & Xiaowen Yu & Chaolong Wang & Junwen Gao & Shihao Zhang & Siqi Cheng & Shimin You & Hai Zheng & Jiayu Lu & Xufei Zhu & Dekun Lei & Anqi Jian & Xiaodong He & Hao Yu & Yun Chen , 2024. "OsSRF8 interacts with OsINP1 and OsDAF1 to regulate pollen aperture formation in rice," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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