Phytophthora Disrupts Plant Immunity by Manipulating Nitric Oxide Homeostasis Through GSNOR Inhibition.

Abstract

Nitric oxide (NO), a pivotal redox signaling molecule, coordinates plant development and immune responses through S-nitrosylation-mediated protein modification. While NO-dependent S-nitrosylation fine-tunes immune responses, whether pathogens hijack this process to subvert plant immunity remains unclear. Here it is shown that S-nitrosoglutathione reductase (GSNOR), which maintains NO homeostasis by degrading S-nitrosoglutathione (GSNO), positively regulates tomato resistance to Phytophthora capsici. Active-site mutations in GSNOR abolished its function in plant defense. Remarkably, GSNOR is manipulated by PcRD18, which is an RxLR effector of P. capsici that is involved in virulence of this oomycete pathogen. PcRD18 elevates the cellular NO content and S-nitrosylation levels by dually inhibiting GSNOR activity and promoting its autophagy-mediated degradation via enhanced ATG8c interaction. Structure analysis reveals critical PcRD18-GSNOR interaction interfaces and mutations in these sites of PcRD18 abolish its ability to interact with GSNOR, thereby blocking the effector's ability to elevate NO levels, suppress the reactive oxygen species (ROS) burst, and enhance virulence. GSNOR mutations disrupting PcRD18 binding produced a mutant form of GSNOR enhancing Phytophthora resistance. These findings unveil a pathogen strategy to subvert NO homeostasis through effector-mediated hijacking of GSNOR and suggest that engineering the host-pathogen interface to disrupt the interaction between GSNOR and PcRD18 will enhance crop disease resistance.