Plant viruses convergently target NPR1 with various strategies to suppress salicylic acid-mediated antiviral immunity

Abstract

NONEXPRESSER OF PATHOGENESIS-RELATED GENES 1 (NPR1), the receptor for salicylic acid (SA), plays a central role in the SA-mediated basal antiviral responses. Recent studies have shown that two different plant RNA viruses encode proteins that suppress such antiviral responses by inhibiting its SUMOylation and inducing its degradation, respectively. However, it is unclear whether targeting NPR1 is a general phenomenon in viruses and whether viruses have novel strategies to inhibit NPR1. In the present study, we report that two different positive-sense single-stranded RNA (+ssRNA) viruses, namely, alfalfa mosaic virus (AMV) and potato virus X (PVX); one negative-sense single-stranded RNA (−ssRNA) virus (calla lily chlorotic spot virus, CCSV); and one single-stranded DNA virus (beet severe curly-top virus, BSCTV) that also encode one or more proteins that interact with NPR1. In addition, we found that the AMV-encoded coat protein (CP) can induce NPR1 degradation by recruiting S-phase kinase-associated protein 1 (Skp1), a key component of the Skp1/cullin1/F-box (SCF) E3 ligase. In contrast, the BSCTV-encoded V2 protein inhibits NPR1 function, probably by affecting its nucleocytoplasmic distribution via the nuclear export factor ALY. Taken together, these data suggest that NPR1 is one of the central hubs in the molecular arms race between plants and viruses and that different viruses have independently evolved different strategies to target NPR1 and disrupt its function.