The arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin

Assaf Zemach, M. Yvonne Kim, Ping Hung Hsieh, Devin Coleman-Derr, Leor Eshed-Williams, Ka Thao, Stacey L. Harmer, Daniel Zilberman*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

779 Scopus citations

Abstract

Nucleosome remodelers of the DDM1/Lsh family are required for DNA methylation of transposable elements, but the reason for this is unknown. How DDM1 interacts with other methylation pathways, such as small-RNA-directed DNA methylation (RdDM), which is thought to mediate plant asymmetric methylation through DRM enzymes, is also unclear. Here, we show that most asymmetric methylation is facilitated by DDM1 and mediated by the methyltransferase CMT2 separately from RdDM. We find that heterochromatic sequences preferentially require DDM1 for DNA methylation and that this preference depends on linker histone H1. RdDM is instead inhibited by heterochromatin and absolutely requires the nucleosome remodeler DRD1. Together, DDM1 and RdDM mediate nearly all transposon methylation and collaborate to repress transposition and regulate the methylation and expression of genes. Our results indicate that DDM1 provides DNA methyltransferases access to H1-containing heterochromatin to allow stable silencing of transposable elements in cooperation with the RdDM pathway.

Original languageAmerican English
Pages (from-to)193-205
Number of pages13
JournalCell
Volume153
Issue number1
DOIs
StatePublished - 28 Mar 2013

Bibliographical note

Funding Information:
We thank Toshiro Nishimura for computational support, Minyong Chung for Illumina sequencing, and Robert Fischer for critical reading of the manuscript. A.Z. was supported by a fellowship from the Jane Coffin Childs Memorial Fund for Medical Research. P-H.H. is supported by a Taiwan Ministry of Education Scholarship. D.Z. is a Young Investigator of the Arnold and Mabel Beckman Foundation.

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