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PLoS Genet. 2015 Apr 22;11(4):e1005154. doi: 10.1371/journal.pgen.1005154. eCollection 2015 Apr.

Genome-wide negative feedback drives transgenerational DNA methylation dynamics in Arabidopsis.

Author information

1
Department of Integrated Genetics, National Institute of Genetics, Mishima, Shizuoka, Japan; Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Hongo, Bunkyo-ku, Tokyo, Japan.
2
Department of Integrated Genetics, National Institute of Genetics, Mishima, Shizuoka, Japan; Department of Genetics, School of Life Science, The Graduate University for Advanced Studies (SOKENDAI), Yata, Shizuoka, Japan.
3
Department of Integrated Genetics, National Institute of Genetics, Mishima, Shizuoka, Japan.
4
Ecole Normale Supérieure, Institut de Biologie (IBENS), Centre National de la Recherche Scientifique (CNRS) UMR8197, Institut National de la Santé et de la Recherche Médicale (INSERM) U1024, Paris, France.
5
Okinawa Institute of Science and Technology, Onna-son, Okinawa, Japan.
6
Center for Information Biology, National Institute of Genetics, Yata, Shizuoka, Japan.
7
Department of Genetics, School of Life Science, The Graduate University for Advanced Studies (SOKENDAI), Yata, Shizuoka, Japan; Center for Information Biology, National Institute of Genetics, Yata, Shizuoka, Japan.
8
Department of Integrated Genetics, National Institute of Genetics, Mishima, Shizuoka, Japan; Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Hongo, Bunkyo-ku, Tokyo, Japan; Department of Genetics, School of Life Science, The Graduate University for Advanced Studies (SOKENDAI), Yata, Shizuoka, Japan.

Abstract

Epigenetic variations of phenotypes, especially those associated with DNA methylation, are often inherited over multiple generations in plants. The active and inactive chromatin states are heritable and can be maintained or even be amplified by positive feedback in a transgenerational manner. However, mechanisms controlling the transgenerational DNA methylation dynamics are largely unknown. As an approach to understand the transgenerational dynamics, we examined long-term effect of impaired DNA methylation in Arabidopsis mutants of the chromatin remodeler gene DDM1 (Decrease in DNA Methylation 1) through whole genome DNA methylation sequencing. The ddm1 mutation induces a drastic decrease in DNA methylation of transposable elements (TEs) and repeats in the initial generation, while also inducing ectopic DNA methylation at hundreds of loci. Unexpectedly, this ectopic methylation can only be seen after repeated self-pollination. The ectopic cytosine methylation is found primarily in the non-CG context and starts from 3' regions within transcription units and spreads upstream. Remarkably, when chromosomes with reduced DNA methylation were introduced from a ddm1 mutant into a DDM1 wild-type background, the ddm1-derived chromosomes also induced analogous de novo accumulation of DNA methylation in trans. These results lead us to propose a model to explain the transgenerational DNA methylation redistribution by genome-wide negative feedback. The global negative feedback, together with local positive feedback, would ensure robust and balanced differentiation of chromatin states within the genome.

PMID:
25902052
PMCID:
PMC4406451
DOI:
10.1371/journal.pgen.1005154
[Indexed for MEDLINE]
Free PMC Article

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