Ca2+ sensor-mediated ROS scavenging suppresses rice immunity and is exploited by a fungal effector

• Published in: Cell 2021-10, Vol.184 (21), p.5391-5404.e17
• Main Authors: Gao, Mingjun, He, Yang, Yin, Xin, Zhong, Xiangbin, Yan, Bingxiao, Wu, Yue, Chen, Jin, Li, Xiaoyuan, Zhai, Keran, Huang, Yifeng, Gong, Xiangyu, Chang, Huizhong, Xie, Shenghan, Liu, Jiyun, Yue, Jiaxing, Xu, Jianlong, Zhang, Guiquan, Deng, Yiwen, Wang, Ertao, Tharreau, Didier, Wang, Guo-Liang, Yang, Weibing, He, Zuhua
• Format: Article
• Language: English
• Subjects: Ca2+-sensor; catalase; disease resistance; E3 ubiquitin ligases; fungal effector; Life Sciences; natural variation; Phytopathology and phytopharmacy; reactive oxygen species; rice immunity; ROD1; structural mimicry; Vegetal Biology
• ISSN: 0092-8674; 1097-4172
• DOI: 10.1016/j.cell.2021.09.009

Plant immunity is activated upon pathogen perception and often affects growth and yield when it is constitutively active. How plants fine-tune immune homeostasis in their natural habitats remains elusive. Here, we discover a conserved immune suppression network in cereals that orchestrates immune homeostasis, centering on a Ca2+-sensor, RESISTANCE OF RICE TO DISEASES1 (ROD1). ROD1 promotes reactive oxygen species (ROS) scavenging by stimulating catalase activity, and its protein stability is regulated by ubiquitination. ROD1 disruption confers resistance to multiple pathogens, whereas a natural ROD1 allele prevalent in indica rice with agroecology-specific distribution enhances resistance without yield penalty. The fungal effector AvrPiz-t structurally mimics ROD1 and activates the same ROS-scavenging cascade to suppress host immunity and promote virulence. We thus reveal a molecular framework adopted by both host and pathogen that integrates Ca2+ sensing and ROS homeostasis to suppress plant immunity, suggesting a principle for breeding disease-resistant, high-yield crops. [Display omitted] •Rice ROD1 suppresses immunity via catalase activation and ROS scavenging•ROD1 is a Ca2+-sensor fine-tuned by ubiquitination-mediated protein degradation•Natural ROD1 variants influence indica and japonica rice immunity•The fungal effector AvrPiz-t exploits the ROD1 cascade to promote virulence ROD1 encodes a Ca2+ sensor to suppress rice immunity by promoting ROS scavenging. The fungal effector AvrPiz-t structurally mimics ROD1 and shares the same ROS-elimination cascade to suppress rice immunity and promote virulence.