A secreted fungal laccase targets the receptor kinase OsSRF3 to inhibit OsBAK1–OsSRF3-mediated immunity in rice

Yuhang Duan, Zhaoyun Wang, Yuan Fang, Zhangxin Pei, Hong Hu, Qiutao Xu, Hao Liu, Xiaolin Chen, Chaoxi Luo, Junbin Huang, Lu Zheng () and Xiaoyang Chen ()
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Yuhang Duan: Anhui Agricultural University
Zhaoyun Wang: Anhui Agricultural University
Yuan Fang: Anhui Agricultural University
Zhangxin Pei: Wuhan Institute of Landscape Architecture
Hong Hu: Huazhong Agricultural University
Qiutao Xu: Guangxi University
Hao Liu: Huazhong Agricultural University
Xiaolin Chen: Huazhong Agricultural University
Chaoxi Luo: Huazhong Agricultural University
Junbin Huang: Huazhong Agricultural University
Lu Zheng: Huazhong Agricultural University
Xiaoyang Chen: Anhui Agricultural University

Nature Communications, 2024, vol. 15, issue 1, 1-19

Abstract: Abstract The identification effector targets and characterization of their functions are crucial for understanding pathogen infection mechanisms and components of plant immunity. Here, we identify the effector UgsL, a ustilaginoidin synthetase with a key role in regulating virulence of the rice false smut fungus Ustilaginoidea virens. Heterologous expression of UgsL in rice (Oryza sativa) enhances plant susceptibility to multiple pathogens, and host-induced gene silencing of UgsL enhances plant resistance to U. virens, indicating that UgsL inhibits rice immunity. UgsL interacts with STRUBBELIG RECEPTOR KINASE 3 (OsSRF3). Genome editing and overexpression of OsSRF3 demonstrate that OsSRF3 plays a pivotal role in the resistance of rice to multiple pathogens. Remarkably, overexpressing OsSRF3 enhances resistance without adversely affecting plant growth or yield. We show that BRASSINOSTEROID RECEPTOR-ASSOCIATED KINASE 1 (OsBAK1) interacts with and phosphorylates OsSRF3 to activate pathogen-triggered immunity, inducing the mitogen-activated protein kinase cascade, a reactive oxygen species burst, callose deposition, and expression of defense-related genes. UgsL interferes with the phosphorylation of OsSRF3 by OsBAK1. Furthermore, UgsL mediates OsSRF3 degradation by facilitating its association with the ubiquitin-26S proteasome. Our results reveal that OsSRF3 positively regulates immunity in rice and that UgsL mediates its degradation, thereby inhibiting the activation of OsBAK1–OsSRF3-mediated immune pathways.

Date: 2024
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DOI: 10.1038/s41467-024-52204-w

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