Exploiting breakdown in nonhost effector-target interactions to boost host disease resistance.

Abstract

Plants are resistant to most microbial species due to nonhost resistance (NHR), providing broad-spectrum and durable immunity. However, the molecular components contributing to NHR are poorly characterised. We address the question of whether failure of pathogen effectors to manipulate nonhost plants plays a critical role in NHR. RxLR (Arg-any amino acid-Leu-Arg) effectors from two oomycete pathogens, <i>Phytophthora infestans and Hyaloperonospora arabidopsidis</i>, enhanced pathogen infection when expressed in host plants (<i>Nicotiana benthamiana</i> and Arabidopsis, respectively) but the same effectors performed poorly in distantly related nonhost pathosystems. Putative target proteins in the host plant potato were identified for 64 <i>P</i>. infestans RxLR effectors using yeast 2-hybrid (Y2H) screens. Candidate orthologues of these target proteins in the distantly related non-host plant Arabidopsis were identified and screened using matrix Y2H for interaction with RxLR effectors from both <i>P</i>. infestans and <i>H</i>. <i>arabidopsidis</i>. Few <i>P</i>. infestans effector-target protein interactions were conserved from potato to candidate Arabidopsis target orthologues (cAtOrths). However, there was an enrichment of <i>H</i>. <i>arabidopsidis</i> RxLR effectors interacting with cAtOrths. We expressed the cAtOrth AtPUB33, which unlike its potato orthologue did not interact with <i>P</i>. <i>infestans</i> effector PiSFI3, in potato and Nicotiana benthamiana. Expression of AtPUB33 significantly reduced <i>P</i>. <i>infestans</i> colonization in both host plants. Our results provide evidence that failure of pathogen effectors to interact with and/or correctly manipulate target proteins in distantly related non-host plants contributes to NHR. Moreover, exploiting this breakdown in effector-nonhost target interaction, transferring effector target orthologues from non-host to host plants is a strategy to reduce disease.