Rice black-streaked dwarf virus-encoded P6 protein impairs OsPelota-mediated antiviral RNA decay defense via promoting OsSCE1b ubiquitination and degradation in rice

Abstract

Rice black-streaked dwarf virus (RBSDV) is a major viral pathogen threatening rice production worldwide. However, the molecular mechanisms underlying the arms race between RBSDV and its host remain largely elusive. Here, we demonstrate that RBSDV infection, or the expression of viral RNA-silencing suppressor protein P6, promotes the ubiquitination and degradation of rice small ubiquitin-like modifiers (SUMO) conjugating enzyme 1b (OsSCE1b). OsSCE1b catalyzes the SUMOylation of OsPelota, a protein involved in plant antiviral RNA decay. Furthermore, RBSDV P6 enhances the interaction between rice ubiquitin E3 ligases SINAT3/4/5 and OsSCE1b in the cytoplasm, leading to increased ubiquitination and degradation of OsSCE1b. Rice plants overexpressing OsSCE1b exhibited reduced susceptibility to RBSDV infection. Conversely, OsSCE1b knockdown and knockout lines, as well as OsPelota knockout lines, were more susceptible, indicating that both OsSCE1b and OsPelota negatively regulate RBSDV infection. Additionally, our findings show that OsSCE1b-catalyzed SUMOylated OsPelota interacts with the Hsp70 subfamily B suppressor OsHBS1, forming a complex that degrades RBSDV genomic RNAs containing one or more GA₆ motifs. Taken together, our data demonstrate that OsSCE1b negatively regulates RBSDV infection by promoting OsPelota SUMOylation and activating the antiviral RNA decay activity of the OsPelota-OsHBS1 complex. Conversely, RBSDV P6 promotes viral infection by enhancing OsSCE1b ubiquitination and degradation, thereby suppressing OsPelota SUMOylation and the rice antiviral RNA decay defense response.

Keywords: OsPelota; OsSCE1b; P6 protein; RNA decay; SUMOylation; rice; rice black‐streaked dwarf virus; ubiquitination.