Abstract
In plants, establishment of de novo DNA methylation is regulated by the RNA-directed DNA methylation (RdDM) pathway. RdDM machinery is known to concentrate in the Cajal body, but the biological significance of this localization has remained elusive. Here, we show that the antiviral methylation of the Tomato yellow leaf curl virus (TYLCV) genome requires the Cajal body in Nicotiana benthamiana cells. Methylation of the viral genome is countered by a virus-encoded protein, V2, which interacts with the central RdDM component AGO4, interfering with its binding to the viral DNA; Cajal body localization of the V2-AGO4 interaction is necessary for the viral protein to exert this function. Taken together, our results draw a long sought-after functional connection between RdDM, the Cajal body, and antiviral DNA methylation, paving the way for a deeper understanding of DNA methylation and antiviral defences in plants.
Highlights
DNA methylation in cytosine residues is a conserved epigenetic mark essential for protecting the eukaryotic genome against invading nucleic acids, namely viruses and transposable elements
We show that V2 from Tomato yellow leaf curl virus (TYLCV) interacts with the central RNA-directed DNA methylation (RdDM) component AGO4; that AGO4 plays a role in the defence against TYLCV; and that V2 interferes with the AGO4 binding to the viral DNA
Since our results indicate that the suppression of the AGO4-mediated methylation of the viral genome occurs in the Cajal body, we decided to test if the Cajal body is required for this anti-viral response
Summary
DNA methylation in cytosine residues is a conserved epigenetic mark essential for protecting the eukaryotic genome against invading nucleic acids, namely viruses and transposable elements. The canonical RdDM pathway requires the activity of two plant-specific RNA polymerase II-related enzymes, Pol IV and Pol V, and leads to cytosine methylation in a sequence-specific manner. Part of the RdDM machinery, including AGO4, was found to concentrate in the Cajal body, a subnuclear compartment that is the site of maturation of ribonucleoprotein complexes (Li et al., 2006). This observation led to the suggestion that Cajal bodies might be a centre for the assembly of an AGO4/NRPE1/siRNA complex, which would facilitate RdDM at target loci (Li et al, 2006)
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