Hydrogen peroxide sensor HPCA1 is an LRR receptor kinase in Arabidopsis

First author: Feihua Wu; Affiliations: Duke University (杜克大学): Durham, USA

Corresponding author: Zhen-Ming Pei

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 cues. 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.

过氧化氢（H2O2）是单细胞生物和多细胞生物中一类主要的活性氧物质，在生物响应外界的环境胁迫或内部的信号时在细胞外产生。H2O2通过水通道膜蛋白进入细胞，并通过共价修饰胞质蛋白来调控胞内的信号转导和细胞学进程。然而，细胞表面是否存在对H2O2的感知受体仍然还不清楚。在植物细胞中，H2O2能够诱导钙离子的内流，该过程往往被认为参与了H2O2的感知和信号转导。本文中，通过基于钙离子成像进行的正向遗传学筛选，作者分离到了一个过氧化氢诱导的钙离子增加突变体hpca，并且鉴定了HPCA1蛋白是一个富含亮氨酸重复的受体激酶，属于一个先前未鉴定的亚家族，特征是胞外结构域有额外的一对半胱氨酸残基。HPCA1定位于质膜，H2O2可通过对其胞外的两个半胱氨酸残基进行共价修饰，从而激活该蛋白，导致HPCA1的自磷酸化。HPCA1介导保卫细胞中 H2O2诱导的钙离子通道激活，并且对于气孔的闭合是必需的。本文的发现有助于鉴定植物胞外的H2O2感知是如何与植物响应多种外界胁迫以及内部信号相关联的，并且对于未来以增强适应性为方向的作物设计提供了重要线索。

通讯：Zhen-Ming Pei (https://biology.duke.edu/people/zhen-ming-pei)

个人简介：1985年，兰州大学，学士；1990年，复旦大学，硕士；1993年，上海植物生理研究所，博士。

研究方向：拟南芥中外源钙离子以及一氧化氮的信号级联。

doi: https://doi.org/10.1038/s41586-020-2032-3

Journal: Nature

Published date: February 19, 2020