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

• Published in: Nature communications 2024-09, Vol.15 (1), p.7891-19, Article 7891
• Main Authors: Duan, Yuhang, Wang, Zhaoyun, Fang, Yuan, Pei, Zhangxin, Hu, Hong, Xu, Qiutao, Liu, Hao, Chen, Xiaolin, Luo, Chaoxi, Huang, Junbin, Zheng, Lu, Chen, Xiaoyang
• Format: Article
• Language: English
• Subjects: 13/89; 38/32; 631/250/2519; 631/326/193/2544; 631/326/421; 631/449/2169/2673; Degradation; Disease Resistance - genetics; False smut; Fungal Proteins - genetics; Fungal Proteins - metabolism; Gene Expression Regulation, Plant; Gene silencing; Host plants; Host-Pathogen Interactions - immunology; Humanities and Social Sciences; Hypocreales - genetics; Hypocreales - pathogenicity; Immune response; Kinases; MAP kinase; multidisciplinary; Oryza - genetics; Oryza - immunology; Oryza - microbiology; Oryza sativa; Pathogens; Phosphorylation; Plant Diseases - immunology; Plant Diseases - microbiology; Plant growth; Plant immunity; Plant Immunity - genetics; Plant Proteins - genetics; Plant Proteins - metabolism; Plant resistance; Plants, Genetically Modified; Proteasome 26S; Proteasomes; Protein kinase C; Protein Kinases - genetics; Protein Kinases - metabolism; Protein Serine-Threonine Kinases - genetics; Protein Serine-Threonine Kinases - metabolism; Reactive oxygen species; Reactive Oxygen Species - metabolism; Receptors; Rice; Science; Science (multidisciplinary); Target recognition; Ubiquitin; Ustilaginoidea virens; Virulence
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-52204-w

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. The Ustilaginoidea virens effector UgsL is shown to interact with receptor kinase OsSRF3. OsSRF3 positively regulates immunity in rice and UgsL mediates its degradation, thereby inhibiting the activation of OsBAK1–OsSRF3-mediated immune responses in rice.