Dual functional plant gene inhibits viral infection and development of systemic necrosis symptoms 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 is unknown whether plants have evolved genes to specifically inhibit the development of viral disease symptoms. Here we identified the causal gene in 2 Arabidopsis thaliana mutants that develop prominent systemic necrosis after infection with both wild-type cucumber mosaic virus (CMV) and its mutant (CMV-Δ2b), which is defective in the suppression of antiviral RNA interference. We found that antiviral RNAi 5 (AVI5) is located in a large chromosomal deletion in both Arabidopsis mutants. We demonstrate that AVI5 acts to inhibit CMV-Δ2b viral accumulation by promoting the biogenesis of virus-derived small interfering RNAs in the antiviral RNA interference pathway before the host amplifies these small interfering RNAs. We further show that cucumber mosaic virus infection induces systemic necrosis symptoms associated with cell death and a reactive oxygen species burst and that AVI5 potently inhibits them. Unlike its suppression of virus accumulation, however, AVI5 inhibits the development of systemic necrosis symptoms without reducing viral titers or inducing antiviral RNA interference. 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.