The leucine-rich repeat receptor kinase QSK1 is a novel regulator of PRR-RBOHD complex and is employed by the bacterial effector HopF2_Ptoto modulate plant immunity

Yukihisa Goto, Yasuhiro Kadota, Malick Mbengue, Jennifer D Lewis, Hidenori Matsui, Noriko Maki, Jan Sklenar, Paul Derbyshire, Arisa Shibata, Yasunori Ichihashi, David S. Guttman, Hirofumi Nakagami, Takamasa Suzuki, Frank L.H. Menke, Silke Robatzek, Darrell Desveaux, Cyril Zipfel, Ken Shirasu

Abstract

Plants detect pathogens using cell-surface pattern recognition receptors (PRRs) like EFR and FLS2, which recognize bacterial EF-Tu and flagellin, respectively. These PRRs, belonging to the leucine-rich repeat receptor kinase (LRR-RK) family, activate the production of reactive oxygen species via the NADPH oxidase RBOHD. The PRR-RBOHD complex is tightly regulated to prevent unwarranted or exaggerated immune responses. However, certain pathogenic effectors can subvert these regulatory mechanisms, thereby suppressing plant immunity. To elucidate the intricate dynamics of the PRR-RBOHD complex, we conducted a comparative co-immunoprecipitation analysis using EFR, FLS2, and RBOHD. We identified QSK1, an LRR-RK, as a novel component of the PRR-RBOHD complex. QSK1 functions as a negative regulator of PRR-triggered immunity (PTI) by downregulating the abundance of FLS2 and EFR. QSK1 is targeted by the bacterial effector HopF2_Pto, a mono-ADP ribosyltransferase, resulting in the reduction of FLS2 and EFR levels through both transcriptional and transcription-independent pathways, thereby inhibiting PTI. Furthermore, HopF2_Ptoreduces transcript levels ofPROSCOOPgenes encoding important stress-regulated phytocytokines and their receptor MIK2. Importantly, HopF2_Ptorequires QSK1 for its accumulation and virulence functions within plants. In summary, our results provide novel insights into the mechanism by which HopF2_Ptoemploys QSK1 to desensitize plants to pathogen attack.

One Sentence Summary

QSK1, a novel component in the plant immune receptor complex, downregulates these receptors and phytocytokines, and is exploited by bacterial effector HopF2_Ptoto desensitize plants to pathogen attack.