Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defense protease Rcr3

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Abstract
Current models of plant–pathogen interactions stipulate that pathogens secrete effector proteins that disable plant defense components known as virulence targets. Occasionally, the perturbations caused by these effectors trigger innate immunity via plant disease resistance proteins as described by the “guard hypothesis.” This model is nicely illustrated by the interaction between the fungal plant pathogenCladosporium fulvumand tomato.C. fulvumsecretes a protease inhibitor Avr2 that targets the tomato cysteine protease Rcr3pim. In plants that carry the resistance protein Cf2, Rcr3pimis required for resistance toC. fulvumstrains expressing Avr2, thus fulfilling one of the predictions of the guard hypothesis. Another prediction of the guard hypothesis has not yet been tested. Considering that virulence targets are important components of defense, different effectors from unrelated pathogens are expected to evolve to disable the same host target. In this study we confirm this prediction using a different pathogen of tomato, the oomycetePhytophthora infestansthat is distantly related to fungi such asC. fulvum. This pathogen secretes an array of protease inhibitors including EPIC1 and EPIC2B that inhibit tomato cysteine proteases. Here we show that, similar to Avr2, EPIC1 and EPIC2B bind and inhibit Rcr3pim. However, unlike Avr2, EPIC1 and EPIC2B do not trigger hypersensitive cell death or defenses on Cf-2/Rcr3pimtomato. We also found that thercr3–3mutant of tomato that carries a premature stop codon in theRcr3gene exhibits enhanced susceptibility toP. infestans, suggesting a role for Rcr3pimin defense. In conclusion, our findings fulfill a key prediction of the guard hypothesis and suggest that the effectors Avr2, EPIC1, and EPIC2B secreted by two unrelated pathogens of tomato target the same defense protease Rcr3pim. In contrast toC. fulvum,P. infestansappears to have evolved stealthy effectors that carry inhibitory activity without triggering plant innate immunity.