The molecular battle between virulence weapons of Pseudomonas syringae and integrated defense responses of Arabidopsis thaliana

Plants encounter many different pathogens during their lifetimes, and they defend themselves through a combination of preformed and induced responses. Induced defense responses include basal defense, gene-for-gene resistance, and nonhost resistance activated on perception of non-self or the activities of non-self. To counteract plant defenses, plant pathogens possess weapons to avoid or suppress plant defenses. I investigated the molecular interactions between plant-pathogenic bacteria by using two model organisms, Arabidopsis thaliana and Pseudomonas syringae, and report here three discoveries. First, PAMP (pathogen-associated molecular pattern)-induced basal defense and R-protein mediated gene-for-gene resistance are linked (Chapter 2). I found that two P. syringae type III effectors, AvrRpt2 and AvrRpm1, inhibit PAMP-induced signaling and thus compromise the host's basal defense system. RIN4 is an Arabidopsis protein targeted by AvrRpt2 and AvrRpm1. The R-proteins, RPS2 and RPM1, sense type III effector-induced perturbations of RIN4. Thus, R-proteins guard the plant against type III effectors that inhibit PAMP signaling and provide a mechanistic link between the two plant defense systems. Second, nonhost resistance of Arabidopsis to P. syringae pv. phaseolicola NPS3121 (Pph) is based on multiple, individually effective layers of basal defense (Chapter 3). Arabidopsis is a nonhost for Pph, a bacterial pathogen of bean. I demonstrate that Pph elicits minimally three basal defense-signaling pathways in Arabidopsis. These pathways have unique readouts, including PR-1 expression and morphologically distinct types of callose deposition. Third, RPS2 can be activated by the corresponding effector of RPM1 (Chapter4). Expression of AvrRpm1 in the absence of RPM1 caused chlorosis and necrosis of leaves, and expression of PR-1. I constructed transgenic plants inducibly expressing AvrRpm1 in Arabidopsis containing mutations in rpm1 and additional loci involved in plant defense related signaling. Our results show that additional mutations in defense genes caused a significant reduction in AvrRpm1-induced chlorosis and PR-1 expression. I also demonstrate that AvrRpm1 weakly activate RPS2 in the absence of RPM1. AvrRpm1 induced neither symptoms nor PR-1 expression in the rpm1/rps2 plants. Thus, AvrRpm1 weakly activates RPS2. My results indicate that classical "gene-for-gene" interactions may be blurred by cross-specificity between elicitor/R protein pairs.