Viral RNA polymerase as a SUMOylation decoy inhibits RNA quality control to promote potyvirus infection in plants

Abstract Potyvirids (viruses in the Potyviridae family) are the largest group of plant RNA viruses. Our recent study has shown that Pelota, a core component of RNA quality controls (RQC), promotes the degradation of potyvirids’ genomic RNA by recognizing a specific G1-2A6-7 motif within the P3 cistron. Here, using turnip mosaic virus (TuMV) as a potyvirid model, we demonstrated that potyvirids have evolved a counteracting mechanism to inhibit Pelota-mediated RQC antiviral activities and promote virus infection. In this mechanism, the viral RNA-dependent RNA polymerase (also known as NIb) acts as a SUMOylation decoy to effectively reduce Pelota SUMOylation by competing with SCE1, the only SUMO E2 conjugating enzyme to inhibit Pelota-mediated RQC. TuMV NIb is comprised of two functional SUMO interacting motif (SIM) sites: SIM2 and SIM3. The former is identified as the key site for NIb’s SUMOylation, whereas the latter is responsible for the interaction with SCE1. These two SIMs are conserved among the majority of potyvirids-encoded NIbs. The other potyvirid NIb orthologs and their SIMs have similar functions in interacting with SCE1 and perturbing the Pelota-mediated RQC. Thus, virus protein-mediated SUMOylation decoy strategy to suppress host defense may be a common feature in plant virus pathosystems. Taken together, these findings highlight a dynamic interplay between plant defense mechanism and viral counter-strategy by orchestrating the post-translational modifications of virus and host defense components.