Mechanism of Pto-Mediated Disease Resistance: Structural Analysis Provides a New Model

Race-specific disease resistance in plants typically requires the action of complementary genes in the pathogen and the host: a functional avirulence (Avr) gene in the pathogen and a corresponding resistance (R) gene in the host. There is solid evidence that Avr and R gene products influence disease resistance pathways in the host and that in the absence of a corresponding R gene, Avr proteins contribute to virulence of the pathogen (Dangl and Jones, 2001). Thus, plants and pathogens are thought to be engaged in an evolutionary arms race wherein pathogens evolve Avr proteins that help them to overcome basal defense responses in specific host plants, and host plants in turn evolve R proteins that interact (directly or indirectly) with the corresponding Avr proteins to activate defense pathways, resulting in the hypersensitive response (HR) that limits the growth of the pathogen and the spread of disease. Avr-activated R proteins often also act to induce systemic acquired resistance (Yang et al., 1997). The largest class of plant R genes that have been identified to date encodes nucleotide binding site leucinerich repeat (NBS-LRR) proteins, and a number of plant species contain hundreds of different R gene–encoded NBS-LRR proteins, supporting the notion that this gene class has undergone adaptive evolution in response to corresponding evolution of pathogen Avr genes (Michelmore and Meyers, 1998; Dangl and Jones, 2001). Tomato Pto, which mediates resistance to bacterial speck disease caused by Pseudomonas syringae pathovar tomato strains carrying the cognate Avr genes AvrPto or AvrPtoB, was the first plant gene cloned that participates in a gene-for-gene interaction with a pathogen (Martin et al., 1993), and it is one of the best-characterized and most intensively studied R genes (Pedley and Martin, 2003). In contrast with the canonical NBS-LRR R genes, Pto encodes a Ser/Thr kinase. AvrPto and AvrPtoB encode proteins that are delivered into host cells via the bacterial type III secretion system and are known as type III effectors. AvrPto was found to have virulence activity and cause increased bacterial growth in host plants lacking a functional Pto pathway (Chang et al., 2000). Both AvrPto and AvrPtoB interact with Pto in the yeast two-hybrid assay (Scofield et al., 1996; Kim et al., 2002), and AvrPto was found to be localized to the plasmamembrane of host cells (Shan et al., 2000). It has been shown thatPto-mediated resistance to bacterial speck disease also requires the NBS-LRR gene Prf (Salmeron et al., 1996). Rathjen et al. (1999) showed that Prf does not act upstream of Pto and thus may act either downstream of or at the same level as Pto. It is possible that Pto participates in a receptor complex with Prf and AvrPto proteins, but the precise in vivo interactions among Pto, Prf, and the Avr proteins remain unknown.