Hydrogen peroxide sensor HPCA1 is an LRR receptor kinase in Arabidopsis

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, Matthew Sima, Suping Chen, Minghua Zhu, Jessica Pei, Douglas M. Johnson, Shan Zhu, Xiaoqiang Cao, Christopher Pei, Zijing Zai, Yihao Liu, Tianyi Liu, Gary B. Swift, Weiguo Zhang, Min Yu, Zhangli Hu, James N. Siedow, Xian Chen and Zhen-Ming Pei ()
Additional contact information
Feihua Wu: Duke University
Yuan Chi: Duke University
Zhonghao Jiang: Duke University
Yuanyuan Xu: Hangzhou Normal University
Ling Xie: University of North Carolina
Feifei Huang: Duke University
Di Wan: Hangzhou Normal University
Jun Ni: Hangzhou Normal University
Fang Yuan: Duke 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
Matthew Sima: Duke University
Suping Chen: Hangzhou Normal University
Minghua Zhu: Duke University Medical Center
Jessica Pei: Duke University
Douglas M. Johnson: Duke University
Shan Zhu: Duke University
Xiaoqiang Cao: Hangzhou Normal University
Christopher Pei: Duke University
Zijing Zai: Duke 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

Nature, 2020, vol. 578, issue 7796, 577-581

Abstract: 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.

Date: 2020
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DOI: 10.1038/s41586-020-2032-3

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