Natural genetic variation of a single amino acid in beet necrotic yellow vein virus P31 protein modulates evasion of plant ubiquitination-mediated antiviral immunity

Plant virus evolution frequently leads to the emergence of highly virulent strains, posing persistent threats to global crop production. However, the mechanisms by which viral evolution enables evasion of plant defense responses remain poorly understood. Here, we found that Benyvirus necrobetae (beet necrotic yellow vein virus, BNYVV), causing the most destructive rhizomania disease in sugar beet worldwide, exhibits distinct pathogenicity associated with different virus isolates. Two Chinese isolates from Inner Mongolia (NM) and Xin Jiang (XJ) exhibit significantly higher virulence than the Japanese isolate O11 and Germany isolate OW1. Moreover, the high pathogenicity is attributed to the Arg-147 residue in P31NM and P31XJ. The P31 proteins of these isolates exhibit enhanced protein stability, compared with P31O11 and P31OW1 carrying a Lys-147 residue. Furthermore, the E3 ubiquitin ligase Hmg-CoA reductase degradation 1 (HRD1) targets the P31O11 Lys-147 for ubiquitination and subsequent degradation. Whereas, the P31NM Arg-147 evades HRD1-mediated degradation, conferring a virulence advantage. Overexpression of HRD1 obviously inhibits BNYVVO11 infection, rather than BNYVVNM. Moreover, knockout of NbHRD1 in Nicotiana benthamiana enhanced susceptibility to BNYVV infection. Collectively, our findings demonstrate an ongoing evolutionary arms race, in which HRD1 is a critical antiviral component by ubiquitinating viral proteins, while natural mutations in viral genomes enable evasion of host defense.