Dual functional plant gene inhibits viral infection and development of systemic necrosis symptom by distinct mechanisms in Arabidopsis

Specific targeting of host genes by plant viruses leads to the induction of distinct disease symptoms with devastating consequences for agriculture. However, it i unknown whether plants have evolved genes to specifically inhibit development of viral disease symptoms. Here we identified the causal gene of two Arabidopsis thaliana mutants that develop prominent systemic necrosis after infection with both wild-type cucumber mosaic virus (CMV) and its mutant (CMV-Δ2b) defective in the suppression of antiviral RNA interference (RNAi). We found that Antiviral RNAi 5 (AVI5) is in a large chromosomal deletion of both Arabidopsis mutants. We demonstrate that AVI5 acts to inhibit CMV-Δ2b viral accumulation in the antiviral RNAi pathway by promoting the biogenesis of the virus-derived small interfering RNAs (vsiRNAs) before host amplification of vsiRNAs. We further show that systemic necrosis symptom associated with cell death and a reactive oxygen species burst is induced by CMV infection and potently inhibited by AVI5. Unlike its suppression of virus accumulation, however, AVI5 inhibits development of systemic necrosis symptom without reducing viral titers or inducing antiviral RNAi. Together, our study demonstrates that Arabidopsis plants have evolved a dual functional gene for antiviral protection to inhibit viral infection and symptom development by distinct mechanisms.