Abstract
SummaryDNA 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.
Highlights
RNA-mediated epigenetic silencing includes de novo DNA cytosine methylation, maintenance of methylation and demethylation
tobacco rattle virus (TRV) compromises the expression of DNA methylation genes in Arabidopsis inflorescences As a first approach to infer the potential role of epigenetic silencing during viral infections, we used quantitative real-time RT-PCR to assess changes in the relative transcript accumulation of a subset of genes involved in DNA methylation in plants exposed to TRV infection
Among the methyltransferases involved in DNA methylation, METHYLTRANSFERASE 1 (MET1) exhibited a significant reduction of transcripts in TRV-infected plants compared to mock-inoculated controls at 14 dpi, whereas DOMAIN REARRANGED METHYLTRANSFERASE 2 (DRM2) or CHROMOMETHYLASE 3 (CMT3) were unaffected (Fig. 1b)
Summary
RNA-mediated epigenetic silencing includes de novo DNA cytosine methylation, maintenance of methylation and demethylation. RNA-directed DNA methylation (RdDM) initiates and re-establishes silencing of TEs through de novo methylation of cytosines (Panda et al, 2016; Wendte and Pikaard, 2017; Wendte and Schmitz, 2018). The AGO4 loaded complexes base pair with nascent Pol II transcripts and guide DOMAIN REARRANGED METHYLTRANSFERASE 2 (DRM2) for low levels of DNA methylation of homologous sites (Cao and Jacobsen, 2002; Zhong et al, 2014). This initial methylation marks the target loci
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