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Methylation-Sensitive Expression of a DNA Demethylase Gene Serves As an Epigenetic Rheostat

Author(s)
Williams, Ben P.; Pignatta, Daniela; Henikoff, Steven; Gehring, Mary
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Abstract
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 ROS1. Unexpectedly, and in contrast to most other genomic targets, expression of ROS1 is promoted by DNA methylation and antagonized by DNA demethylation. We demonstrate that inducing methylation in the ROS1 proximal region is sufficient to restore ROS1 expression in an RdDM mutant. Additionally, methylation-sensitive expression of ROS1 is conserved in other species, suggesting it is adaptive. We propose that the ROS1 locus functions as an epigenetic rheostat, tuning the level of demethylase activity in response to methylation alterations, thus ensuring epigenomic stability.
Date issued
2015-03
URI
http://hdl.handle.net/1721.1/97106
Department
Massachusetts Institute of Technology. Department of Biology; Whitehead Institute for Biomedical Research
Journal
PLOS Genetics
Publisher
Public Library of Science
Citation
Williams, Ben P., Daniela Pignatta, Steven Henikoff, and Mary Gehring. “Methylation-Sensitive Expression of a DNA Demethylase Gene Serves As an Epigenetic Rheostat.” Edited by Ortrun Mittelsten Scheid. PLoS Genet 11, no. 3 (March 31, 2015): e1005142.
Version: Final published version
ISSN
1553-7404
1553-7390

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