The processed C‐terminus of AvrRps4 effector suppresses plant immunity via targeting multiple WRKYs

• Published in: Journal of integrative plant biology 2024-08, Vol.66 (8), p.1769-1787
• Main Authors: Nguyen, Quang‐Minh, Iswanto, Arya Bagus Boedi, Kang, Hobin, Moon, Jiyun, Phan, Kieu Anh Thi, Son, Geon Hui, Suh, Mi Chung, Chung, Eui‐Hwan, Gassmann, Walter, Kim, Sang Hee
• Format: Article
• Language: English
• Subjects: Arabidopsis; Arabidopsis - genetics; Arabidopsis - immunology; Arabidopsis - metabolism; Arabidopsis - microbiology; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; AvrRps4; bacterial effector; Bacterial Proteins - genetics; Bacterial Proteins - metabolism; Binding; Cytoplasm; Effector cells; effector‐triggered immunity; Gene Expression Regulation, Plant; Host plants; Hypersensitive response; Immune response; immune response suppression; Immune system; Pathogenesis; Pathogens; Plant cells; Plant Diseases - genetics; Plant Diseases - immunology; Plant Diseases - microbiology; Plant immunity; Plant Immunity - genetics; Promoter Regions, Genetic - genetics; Protein Binding; Proteins; Pseudomonas syringae - pathogenicity; transcription factor; Transcription Factors - genetics; Transcription Factors - metabolism; Virulence; Virulence - genetics; WRKY
• ISSN: 1672-9072; 1744-7909; 1744-7909
• DOI: 10.1111/jipb.13710

ABSTRACT Pathogens generate and secrete effector proteins to the host plant cells during pathogenesis to promote virulence and colonization. If the plant carries resistance (R) proteins that recognize pathogen effectors, effector‐triggered immunity (ETI) is activated, resulting in a robust immune response and hypersensitive response (HR). The bipartite effector AvrRps4 from Pseudomonas syringae pv. pisi has been well studied in terms of avirulence function. In planta, AvrRps4 is processed into two parts. The C‐terminal fragment of AvrRps4 (AvrRps4C) induces HR in turnip and is recognized by the paired resistance proteins AtRRS1/AtRPS4 in Arabidopsis. Here, we show that AvrRps4C targets a group of Arabidopsis WRKY, including WRKY46, WRKY53, WRKY54, and WRKY70, to induce its virulence function. Indeed, AvrRps4C suppresses the general binding and transcriptional activities of immune‐positive regulator WRKY54 and WRKY54‐mediated resistance. AvrRps4C interferes with WRKY54's binding activity to target gene SARD1 in vitro, suggesting WRKY54 is sequestered from the SARD1 promoter by AvrRps4C. Through the interaction of AvrRps4C with four WRKYs, AvrRps4 enhances the formation of homo‐/heterotypic complexes of four WRKYs and sequesters them in the cytoplasm, thus inhibiting their function in plant immunity. Together, our results provide a detailed virulence mechanism of AvrRps4 through its C‐terminus. The processed C‐terminus of AvrRps4 from Pseudomonas syringae targets the Arabidopsis transcription factors WRKY46, WRKY53, WRKY54, and WRKY70, promoting virulence by suppressing WRKY54‐mediated enhanced resistance and WRKY54's transcriptional and binding activities. AvrRps4C induces WRKY‐complex formation and translocates WRKYs to the cytoplasm, thus inhibiting WRKY function in plant immunity.