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Hydrogen peroxide sensor HPCA1 is an LRR receptor kinase in Arabidopsis

Author

Listed:
  • Feihua Wu

    (Duke University
    Duke University
    Shenzhen University
    Hangzhou Normal University)

  • Yuan Chi

    (Duke University
    Hangzhou Normal University
    Zhejiang University)

  • Zhonghao Jiang

    (Duke University
    Duke University
    Shenzhen University)

  • Yuanyuan Xu

    (Hangzhou Normal University)

  • Ling Xie

    (University of North Carolina)

  • Feifei Huang

    (Duke University
    Shenzhen University)

  • Di Wan

    (Hangzhou Normal University)

  • Jun Ni

    (Hangzhou Normal University)

  • Fang Yuan

    (Duke University
    Hangzhou Normal University)

  • Xiaomei Wu

    (Hangzhou Normal University)

  • Yanyan Zhang

    (Hangzhou Normal University)

  • Li Wang

    (University of North Carolina)

  • Rui Ye

    (Duke University)

  • Benjamin Byeon

    (Duke University)

  • Wenhua Wang

    (Duke University)

  • Shu Zhang

    (Hangzhou Normal University
    Zhejiang University)

  • Matthew Sima

    (Duke University
    Shenzhen University)

  • Suping Chen

    (Hangzhou Normal University)

  • Minghua Zhu

    (Duke University Medical Center)

  • Jessica Pei

    (Duke University
    Emory University)

  • Douglas M. Johnson

    (Duke University)

  • Shan Zhu

    (Duke University
    Hangzhou Normal University)

  • Xiaoqiang Cao

    (Hangzhou Normal University)

  • Christopher Pei

    (Duke University)

  • Zijing Zai

    (Duke University
    Shenzhen University)

  • Yihao Liu

    (Duke University)

  • Tianyi Liu

    (Duke University)

  • Gary B. Swift

    (Duke University)

  • Weiguo Zhang

    (Duke University Medical Center)

  • Min Yu

    (Foshan University)

  • Zhangli Hu

    (Shenzhen University)

  • James N. Siedow

    (Duke University)

  • Xian Chen

    (University of North Carolina)

  • Zhen-Ming Pei

    (Duke University
    Duke University)

Abstract

Hydrogen peroxide (H2O2) is a major reactive oxygen species in unicellular and multicellular organisms, and is produced extracellularly in response to external stresses and internal cues1–4. H2O2 enters cells through aquaporin membrane proteins and covalently modifies cytoplasmic proteins to regulate signalling and cellular processes. However, whether sensors for H2O2 also exist on the cell surface remains unknown. In plant cells, H2O2 triggers an influx of Ca2+ ions, which is thought to be involved in H2O2 sensing and signalling. Here, by using forward genetic screens based on Ca2+ imaging, we isolated hydrogen-peroxide-induced Ca2+ increases (hpca) mutants in Arabidopsis, and identified HPCA1 as a leucine-rich-repeat receptor kinase belonging to a previously uncharacterized subfamily that features two extra pairs of cysteine residues in the extracellular domain. HPCA1 is localized to the plasma membrane and is activated by H2O2 via covalent modification of extracellular cysteine residues, which leads to autophosphorylation of HPCA1. HPCA1 mediates H2O2-induced activation of Ca2+ channels in guard cells and is required for stomatal closure. Our findings help to identify how the perception of extracellular H2O2 is integrated with responses to various external stresses and internal cues in plants, and have implications for the design of crops with enhanced fitness.

Suggested Citation

  • Feihua Wu & Yuan Chi & Zhonghao Jiang & Yuanyuan Xu & Ling Xie & Feifei Huang & Di Wan & Jun Ni & Fang Yuan & Xiaomei Wu & Yanyan Zhang & Li Wang & Rui Ye & Benjamin Byeon & Wenhua Wang & Shu Zhang & , 2020. "Hydrogen peroxide sensor HPCA1 is an LRR receptor kinase in Arabidopsis," Nature, Nature, vol. 578(7796), pages 577-581, February.
  • Handle: RePEc:nat:nature:v:578:y:2020:i:7796:d:10.1038_s41586-020-2032-3
    DOI: 10.1038/s41586-020-2032-3
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    Cited by:

    1. Tuo Ji & Lihua Zheng & Jiale Wu & Mei Duan & Qianwen Liu & Peng Liu & Chen Shen & Jinling Liu & Qinyi Ye & Jiangqi Wen & Jiangli Dong & Tao Wang, 2023. "The thioesterase APT1 is a bidirectional-adjustment redox sensor," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    2. Mervin Chun-Yi Ang & Jolly Madathiparambil Saju & Thomas K. Porter & Sayyid Mohaideen & Sreelatha Sarangapani & Duc Thinh Khong & Song Wang & Jianqiao Cui & Suh In Loh & Gajendra Pratap Singh & Nam-Ha, 2024. "Decoding early stress signaling waves in living plants using nanosensor multiplexing," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    3. Du-Hwa Lee & Ho-Seok Lee & Min-Soo Choi & Katarzyna Parys & Kaori Honda & Yasumitsu Kondoh & Jung-Min Lee & Natalie Edelbacher & Geon Heo & Balaji Enugutti & Hiroyuki Osada & Ken Shirasu & Youssef Bel, 2024. "Reprogramming of flagellin receptor responses with surrogate ligands," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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