DDM1 and Lsh remodelers allow methylation of DNA wrapped in nucleosomes

Abstract
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Abstract

Cytosine methylation regulates essential genome functions across eukaryotes, but the fundamental question of whether nucleosomal or naked DNA is the preferred substrate of plant and animal methyltransferases remains unresolved. Here, we show that genetic inactivation of a single DDM1/Lsh family nucleosome remodeler biases methylation toward inter-nucleosomal linker DNA in Arabidopsis thaliana and mouse. We find that DDM1 enables methylation of DNA bound to the nucleosome, suggesting that nucleosome-free DNA is the preferred substrate of eukaryotic methyltransferases in vivo. Furthermore, we show that simultaneous mutation of DDM1 and linker histone H1 in Arabidopsis reproduces the strong linker-specific methylation patterns of species that diverged from flowering plants and animals over a billion years ago. Our results indicate that in the absence of remodeling, nucleosomes are strong barriers to DNA methyltransferases. Linker-specific methylation can evolve simply by breaking the connection between nucleosome remodeling and DNA methylation.

Data availability

The following data sets were generated

1. Lyons DB
2. Zilberman D
(2017) DDM1 and Lsh remodelers allow methylation of DNA wrapped in nucleosomes
GSE96994.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE96994

The following previously published data sets were used

Article and author information

Author details

David B Lyons

Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, United States

Competing interests
No competing interests declared.
Daniel Zilberman

Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, United States

For correspondence
danielz@berkeley.edu

Competing interests
Daniel Zilberman, Reviewing editor, eLife.

"This ORCID iD identifies the author of this article:" 0000-0002-0123-8649

Funding

Howard Hughes Medical Institute

Daniel Zilberman

Horizon 2020 Framework Programme

Daniel Zilberman

National Institutes of Health

David B Lyons

Helen Hay Whitney Foundation

David B Lyons

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.