Crosstalk between epigenetic silencing and infection by tobacco rattle virus in Arabidopsis

DNA methylation is an important epigenetic mechanism for controlling innate immunity against microbial pathogens in plants. Little is known, however, about the manner in which viral infections interact with DNA methylation pathways. Here we investigate the crosstalk between epigenetic silencing and viral infections in Arabidopsis inflorescences. We found that tobacco rattle virus (TRV) causes changes in the expression of key transcriptional gene silencing factors with RNA‐directed DNA methylation activities that coincide with changes in methylation at the whole genome level. Viral susceptibility/resistance was altered in DNA (de)methylation‐deficient mutants, suggesting that DNA methylation is an important regulatory system controlling TRV proliferation. We further show that several transposable elements (TEs) underwent transcriptional activation during TRV infection, and that TE regulation likely involved both DNA methylation‐dependent and ‐independent mechanisms. We identified a cluster of disease resistance genes regulated by DNA methylation in infected plants that were enriched for TEs in their promoters. Interestingly, TEs and nearby resistance genes were co‐regulated in TRV‐infected DNA (de)methylation mutants. Our study shows that DNA methylation contributes to modulate the outcome of viral infections in Arabidopsis, and opens up new possibilities for exploring the role of TE regulation in antiviral defence.