A bacterial kinase phosphorylates OSK1 to suppress stomatal immunity in rice

Shanzhi Wang,Xiu-Fang Xin,Zhao-Qing Luo,Shuai Li,Dayong Li,Yanping Wang,Sheng Yang He,Shuang Zhou,Jiaqing Xu,Qian Li,Jiyang Wang,Wenxian Sun

doi:10.1038/s41467-021-25748-4

Abstract

The Xanthomonas outer protein C2 (XopC2) family of bacterial effectors is widely found in plant pathogens and Legionella species. However, the biochemical activity and host targets of these effectors remain enigmatic. Here we show that ectopic expression of XopC2 promotes jasmonate signaling and stomatal opening in transgenic rice plants, which are more susceptible to Xanthomonas oryzae pv. oryzicola infection. Guided by these phenotypes, we discover that XopC2 represents a family of atypical kinases that specifically phosphorylate OSK1, a universal adaptor protein of the Skp1-Cullin-F-box ubiquitin ligase complexes. Intriguingly, OSK1 phosphorylation at Ser53 by XopC2 exclusively increases the binding affinity of OSK1 to the jasmonate receptor OsCOI1b, and specifically enhances the ubiquitination and degradation of JAZ transcription repressors and plant disease susceptibility through inhibiting stomatal immunity. These results define XopC2 as a prototypic member of a family of pathogenic effector kinases and highlight a smart molecular mechanism to activate jasmonate signaling.

Highlights

The Xanthomonas outer protein C2 (XopC2) family of bacterial effectors is widely found in plant pathogens and Legionella species
XopC2 defines a novel family of bacterial effector kinases
XopC2 is not matched with any identified protein kinase from primary sequence alignment, the predicted secondary structure of XopC2 shows a similarity to the canonical protein kinase A (PKA)

Summary

Introduction

The Xanthomonas outer protein C2 (XopC2) family of bacterial effectors is widely found in plant pathogens and Legionella species. OSK1 phosphorylation at Ser[53] by XopC2 exclusively increases the binding affinity of OSK1 to the jasmonate receptor OsCOI1b, and enhances the ubiquitination and degradation of JAZ transcription repressors and plant disease susceptibility through inhibiting stomatal immunity. These results define XopC2 as a prototypic member of a family of pathogenic effector kinases and highlight a smart molecular mechanism to activate jasmonate signaling. Xanthomonas spp. secrete two classes of type III effectors, transcription activator-like (TAL) and non-TAL effectors, into host cells[17]. Vesicatoria targets a cell size regulator gene upa[20] to induce hypertrophy of plant mesophyll cells to promote infection[21]

Methods

Results

Conclusion