Natural variation in the Arabidopsis AGO2 gene is associated with susceptibility to potato virus X

Abstract

RNA silencing functions as an anti-viral defence in plants through the action of DICER-like (DCL) and ARGONAUTE (AGO) proteins. However, there are few known examples of functional variation in RNA silencing components. The AGO2 protein is important for antiviral defense against multiple viruses and has been shown to be a major limiting factor to infection by potato virus X (PVX) of Arabidopsis thaliana but not Nicotiana benthamiana. We show that the AGO2 proteins from these two plants have differential activity against PVX, suggesting that variation in AGO2 is important in plant-virus interactions. Consistent with this, we find that the Arabidopsis thaliana AGO2 gene shows a high incidence of polymorphisms between accessions, with evidence of selective pressure. AGO2 protein variants can be assigned to two groups, in near equal frequency, based on an amino acid change and small deletions in the protein N-terminus. Inoculation of a large number of Arabidopsis accessions shows strong correlation between these alleles and resistance or susceptibility to PVX. These observations were validated using genetic and transgenic complementation analysis, which showed that one type of AGO2 variant is specifically affected in its antiviral activity, without interfering with other AGO2-associated functions such as anti-bacterial resistance or DNA methylation. Our results demonstrate a novel type of genetically-encoded virus resistance and suggest that plant-virus interactions have influenced natural variation in RNA silencing components.