DNA Geminivirus Infection Induces an Imprinted E3 Ligase Gene to Epigenetically Activate Viral Gene Transcription.

Flowering plants and mammals encode imprinted genes that are primarily expressed in the endosperm and placenta in a parent-of-origin manner. In this study, we show that early activation of the geminiviral C2 and C3 genes in Arabidopsis plants, which encode a viral suppressor of RNA interference (RNAi) and a replication enhancer protein, respectively, correlates with transiently vegetative expression of Variant In Methylation 5 (VIM5), an endosperm imprinted gene conserved in diverse plant species. We demonstrate that VIM5 is a ubiquitin E3 ligase and directly targets DNA methyltransferases MET1 and CMT3 for degradation by the ubiquitin 26S proteasome proteolytic pathway. Infection with Beet severe curly top virus induces expression of VIM5 in rosette leaf tissues, possibly by the expression of the viral Rep protein, leading to the early activation of C2 and C3 coupled with reduced symmetric methylation in C2-3 promoter and the onset of disease symptoms. These findings show that this small DNA virus recruits a host imprinted gene for epigenetic activation of viral transcription. Our work reveals a distinct strategy of plant pathogens to exploit the host machinery to inhibit methylation-mediated defense response in establishing infection.