Nature Communications (Sep 2024)

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,
  • Xiaoyang Chen

DOI
https://doi.org/10.1038/s41467-024-52204-w
Journal volume & issue
Vol. 15, no. 1
pp. 1 – 19

Abstract

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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.