期刊名称：Proceedings of the National Academy of Sciences
印刷版ISSN：0027-8424
电子版ISSN：1091-6490
出版年度：2022
卷号：119
期号：35
DOI：10.1073/pnas.2114064119
语种：English
出版社：The National Academy of Sciences of the United States of America
摘要：Significance
Plant nonhost resistance (NHR) prevents infection by all members of most microbial species, but its molecular mechanisms are not well understood. We found that effector proteins from the potato blight pathogen
Phytophthora infestans, which enhance infection in host plants, fail to enhance susceptibility in nonhost
Arabidopsis. These
P. infestans effectors often failed to interact with
Arabidopsis orthologs of their potato target proteins, whereas many interactions were detected between these
Arabidopsis orthologs and effectors from its adapted pathogen
Hyaloperonospora arabidopsidis. Thus, breakdown in effector–target interactions in distantly related nonhost plants is likely a key component of NHR. Importantly, we demonstrate that exploiting this breakdown and expressing nonhost target orthologs in host plants provide a strategy to prevent crop disease.
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,
Phytophthora infestans and Hyaloperonospora arabidopsidis, enhanced pathogen infection when expressed in host plants (
Nicotiana benthamiana 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
P. 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
P. infestans and
H.
arabidopsidis. Few
P. infestans effector-target protein interactions were conserved from potato to candidate Arabidopsis target orthologues (cAtOrths). However, there was an enrichment of
H.
arabidopsidis RxLR effectors interacting with cAtOrths. We expressed the cAtOrth AtPUB33, which unlike its potato orthologue did not interact with
P.
infestans effector PiSFI3, in potato and Nicotiana benthamiana. Expression of AtPUB33 significantly reduced
P.
infestans 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.
