Methylation-sensitive expression of a DNA demethylase gene serves as an epigenetic rheostat.

Genomes must balance active suppression of transposable elements (TEs) with the need to maintain gene expression. In Arabidopsis, euchromatic TEs are targeted by RNA-directed DNA methylation (RdDM). Conversely, active DNA demethylation prevents accumulation of methylation at genes proximal to these TEs. It is unknown how a cellular balance between methylation and demethylation activities is achieved. Here we show that both RdDM and DNA demethylation are highly active at a TE proximal to the major DNA demethylase gene Unexpectedly, and in contrast to most other genomic targets, expression of is promoted by DNA methylation and antagonized by DNA demethylation. We demonstrate that inducing methylation in the duanyu16701 proximal region is sufficient to restore duanyu16701 expression in an RdDM mutant. Additionally, methylation-sensitive expression of duanyu16701 is conserved in other species, suggesting it is adaptive. We propose that the duanyu16701 locus functions as an epigenetic rheostat, tuning the level of demethylase activity in response to methylation alterations, thus ensuring epigenomic stability.

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