Chloroplastic ROS bursts initiate salicylic acid biosynthesis in plant immunity

Abstract

Chloroplasts are essential centers of signal integration and transduction in plants. They are involved in the biosynthesis of primary and specialized metabolites, including salicylic acid (SA), a key defense phytohormone synthesized via the conserved chorismate biosynthetic pathway. However, the identity of the signal(s) that ultimately triggers SA induction in chloroplasts upon perception of a biotic threat has remained elusive. Here, we provide evidence of a functional link between chloroplast-derived reactive oxygen species (cROS) and SA production. We observe that inhibiting ROS bursts generated from photosystem II during plant immune activation completely abrogates the induction of SA synthesis in response to immunity-inducing signals, without affecting SA-independent immune responses. Indeed, time course analyses show that the induction of SA marker genes parallels that of cROS production during an immune response. Consistent with this, preventing cROS induction is sufficient to nullify the immune protection normally conferred by activating immunity prior to an infection. Analyses of transcriptomes and photosynthetic efficiency show that two conserved effectors from the phytopathogen Pseudomonas syringae, HopM1 and AvrE1, redundantly disrupt photosynthesis and cROS bursts. These effects reduce SA accumulation and are mediated via the impact of HopM1 and AvrE1 in inducting host abscisic acid signaling. Our results suggest that a change in chloroplastic redox homeostasis induced by biotic stressors acts as an initiator of plant immunity through the production of SA, and that this response is targeted by conserved pathogen effector proteins.