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

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.

SUBMITTER: Williams BP

PROVIDER: S-EPMC4380477 | biostudies-literature | 2015 Mar

REPOSITORIES: biostudies-literature

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

Williams Ben P BP Pignatta Daniela D Henikoff Steven S Gehring Mary M

PLoS genetics 20150331 3

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 majo ...[more]

PMID: 25826366

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Project description:BackgroundUnderstanding the processes governing angiosperm seed growth and development is essential both for fundamental plant biology and for agronomic purposes. Master regulators of angiosperm seed development are expressed in a seed-specific manner. However, it is unclear how this seed specificity of transcription is established. In some vertebrates, DNA methylation valleys (DMVs) are highly conserved and strongly associated with key developmental genes, but comparable studies in plants are limited to Arabidopsis and soybean. Castor bean (Ricinus communis) is a valuable model system for the study of seed biology in dicots and source of economically important castor oil. Unlike other dicots such as Arabidopsis and soybean, castor bean seeds have a relatively large and persistent endosperm throughout seed development, representing substantial structural differences in mature seeds. Here, we performed an integrated analysis of RNA-seq, whole-genome bisulfite sequencing, and ChIP-seq for various histone marks in the castor bean.ResultsWe present a gene expression atlas covering 16 representative tissues and identified 1162 seed-specific genes in castor bean (Ricinus communis), a valuable model for the study of seed biology in dicots. Upon whole-genome DNA methylation analyses, we detected 32,567 DMVs across five tissues, covering ~33% of the castor bean genome. These DMVs are highly hypomethylated during development and conserved across plant species. We found that DMVs have the potential to activate transcription, especially that of tissue-specific genes. Focusing on seed development, we found that many key developmental regulators of seed/endosperm development, including AGL61, AGL62, LEC1, LEC2, ABI3, and WRI1, were located within DMVs. ChIP-seq for five histone modifications in leaves and seeds clearly showed that the vast majority of histone modification peaks were enriched within DMVs, and their remodeling within DMVs has a critical role in the regulation of seed-specific gene expression. Importantly, further experiment analysis revealed that distal DMVs may act as cis-regulatory elements, like enhancers, to activate downstream gene expression.ConclusionsOur results point to the importance of DMVs and special distal DMVs behaving like enhancers, in the regulation of seed-specific genes, via the reprogramming of histone modifications within DMVs. Furthermore, these results provide a comprehensive understanding of the epigenetic regulator roles in seed development in castor bean and other important crops.

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

Publications

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

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