Suppression of PR1 cleavage-derived peptide-mediated resistance by rhabdovirus glycoprotein facilitates viral transmission by insect vectors in rice.

Abstract

Pathogenesis-related protein 1 (PR1) serves as a canonical plant defense marker; however, its specific role in conferring resistance against insect herbivores has remained elusive. Here, we delineate a complete PR1-mediated defense pathway in rice. We show that the cysteine protease OsXCP2, in a catalytic residue-dependent manner, cleaves PR1a at the conserved CNYS motif to release the OsCAPE1 peptide, which subsequently activates broad-spectrum resistance against phloem-feeding insects. Insect herbivory induces the co-expression of OsXCP2 and OsPR1a specifically in the phloem. And loss-of-function osxcp2 mutants exhibit compromised resistance, underscoring the functional importance of this pathway in rice anti-herbivore defense. Strikingly, the glycoprotein (G) of the leafhopper-transmitted rhabdovirus rice stripe mosaic virus (RSMV) is secreted into the phloem during viruliferous insect feeding. Mechanistically, RSMV G employs a dual strategy to subvert this defense: it competitively binds the C-terminus of PR1a, thereby blocking OsXCP2-mediated cleavage, and simultaneously sequesters the liberated OsCAPE1 peptide. This concerted inhibition suppresses PR1-dependent resistance against insect feeding and consequently promotes viral transmission. In summary, our study identifies a novel PR1-activated anti-herbivore pathway in rice and reveals a sophisticated viral effector mechanism that antagonizes it to facilitate vector-borne viral transmission.