Abstract
DNA methylation is an epigenetic mechanism that plays important roles in gene regulation and transposon silencing. Active DNA demethylation has evolved to counterbalance DNA methylation at many endogenous loci. Here, we report that active DNA demethylation also targets viral DNAs, tomato yellow leaf curl China virus (TYLCCNV) and its satellite tomato yellow leaf curl China betasatellite (TYLCCNB), to promote their virulence. We demonstrate that the βC1 protein, encoded by TYLCCNB, interacts with a ROS1-like DNA glycosylase in Nicotiana benthamiana and with the DEMETER (DME) DNA glycosylase in Arabidopsis thaliana. The interaction between βC1 and DME facilitates the DNA glycosylase activity to decrease viral DNA methylation and promote viral virulence. These findings reveal that active DNA demethylation can be regulated by a viral protein to subvert DNA methylation-mediated defense.
Highlights
DNA methylation is an epigenetic mechanism that plays important roles in gene regulation and transposon silencing
We tested their role in the plant-virus interactions by knocking down their expression by using tobacco rattle virus (TRV)-induced gene silencing (VIGS) (Supplementary Figs. 2 and 3a)
Plants infiltrated with pCambia1300 (TRV-free empty vector), with TRV-GUS and with TRV-NbDMLs were mock-inoculated, inoculated with tomato yellow leaf curl China virus (TYLCCNV) alone, or inoculated with TYLCCNV plus tomato yellow leaf curl China betasatellite (TYLCCNB) (TYLCCNV+B). pCambia1300, TRV-GUS- or TRV-NbDMLs-infiltrated plants did not show any symptoms when inoculated with TYLCCNV alone (Fig. 1a and Supplementary Fig. 3b), consistent with the previous finding that TYLCCNV alone does not induce disease symptoms in N. benthamiana[20]
Summary
DNA methylation is an epigenetic mechanism that plays important roles in gene regulation and transposon silencing. The interaction between βC1 and DME facilitates the DNA glycosylase activity to decrease viral DNA methylation and promote viral virulence These findings reveal that active DNA demethylation can be regulated by a viral protein to subvert DNA methylationmediated defense. DME targets thousands of endogenous loci in vegetative cells, the companion cells of sperms[17], and initiates genome-wide active DNA demethylation in central cells, the companion cells of egg cells[18], thereby regulating pollen germination[13] and embryo development[11]. Viral genomic DNA can be methylated[27,28,29], and its replication is suppressed[30,31] To counteract this inhibition, viruses encode suppressor proteins to interfere with DNA methylation[32,33,34,35,36] or the production of SAM22,37–39. Whether active DNA demethylation plays a role in plant-virus interactions and whether the active DNA demethylation machinery is targeted by virus-encoded proteins remain unknown
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