The Bacterial Toxin COR, a Hormone Mimic, Modulates Plant Hormone Signaling and Regulates Secondary Metabolism in Arabidopsis

Pseudomona syringae pv. tomato (Pto) is a model pathogen that infects the model plant Arabidopsis thaliana. Pto deploys type III effectors and the phytotoxin COR to cause disease and suppress defense responses. In response to biotrophic pathogens, Arabidopsis activates SA-dependent signaling to activate local defense responses and induce systemic acquired resistance. JA-signaling, which is important in resistance to necrotrophic pathogens and chewing pests, is antagonistic to SA-signaling. Biotrophic bacteria take advantage of the SA/JA antagonism in several ways. First, COR, a hormone JA-Ile mimic, binds to the F-box protein containing co-receptor COI1 to activate JA-signaling and thus suppress SA-signaling. My studies have demonstrated that COR is a multifunctional defense suppressor in the apoplastic space of Arabidopsis. COR suppresses callose deposition in a manner distinct from P. syringae type III effectors HopM1 and AvrE1. In addition to its well documented ability to suppress SA-signaling, COR also suppresses an SA-independent pathway contributing to callose deposition by reducing accumulation of indole glucosinolate metabolism upstream of the activity of the PEN2 myrosinase. Further, we show that, in addition to promoting virulence through targeting of COI1, COR also suppresses callose deposition and promotes bacterial growth in a COI1-independent manner (chapter 2). Second, type III effectors activate COI1-dependent signaling to promote bacterial virulence. We have studied the type III effector AvrRpm1 and AvrRpt2 from P. syringae, which are recognized by plant disease resistance (R) proteins RPM1 and RPS2, respectively, through “gene-for gene” interactions. We have demonstrated that inducible expression of AvrRpm1-HA in rpm1 plants induces PR-1, a classical defense marker of SA-signaling, and symptoms including chlorosis and necrosis. PR-1 expression and symptoms were strongly reduced in rpm1rps2 plants and bacteria expressing AvrRpm1 grew to higher levels on rpm1rps2 than on rpm1 plants. Thus, independent of its classical “gene-for-gene” activation of RPM1, AvrRpm1 also elicits functionally relevant defenses by activating RPS2. Similarly, AvrRpt2 weakly activates RPM1 in addition to its strong activation of RPS2 (chapter 3). The findings of chapter 3 led us to study AvrRpm1 and AvrRpt2 virulence in rpm1rps2 double mutant plants so to avoid the strong and weak effectors-triggered immunity induction by R-proteins. We have examined the ability of these type III effectors to modulate the host hormone signaling. We examine the role of COI1 in the ability of AvrRpm1 and AvrRpt2 to promote virulence of P. syringae. By comparing coi1 and COI1 plants in an rpm1rps2 background, we have tested how AvrRpm1 and AvrRpt2 virulence functions relate to JA-signaling. Our results indicate that inducible expression of AvrRpt2-HA induces COI1 dependent chlorosis and inducible expression of AvrRpm1-HA or AvrRpt2-HA promotes bacterial growth dependent on a COI1-mediated pathway and additively with the action of COR. Further, we found that AvrRpt2-HA induces expression of PDF1.2, a read-out for JA-signaling, to a much higher level in COI1rpm1rps2 than in coi1rpm1rps2 plants (Chapter 4). Thus, my work has demonstrated that P. syringae uses a multifunctional toxin and type III effectors to stimulate JA-signaling and compromise innate immunity in Arabidopsis.