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

Autor: Hidetoshi Saze, Yoshiaki Tarutani, Atsushi Toyoda, Vincent Colot, Taiko Kim To, Evelyne Duvernois-Berthet, Tetsuji Kakutani, Mohamed Kassam, Kazuya Takashima, Sandra Cortijo, Tasuku Ito, Asao Fujiyama
Přispěvatelé: Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Department of Integrated Genetics, National Institute of Genetics, Mishima, Department of Genetics, School of Life Science, The Graduate University for Advanced Studies (SOKENDAI), Institut de biologie de l'ENS Paris (IBENS), Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Département de Biologie - ENS Paris, École normale supérieure - Paris (ENS Paris), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-École normale supérieure - Paris (ENS Paris), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Okinawa Institute of Science and Technology Graduate University, Center for Information Biology, National Institute of Genetics, Yata, Institut de biologie de l'ENS Paris (UMR 8197/1024) (IBENS), Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Département de Biologie - ENS Paris, Département de Biologie - ENS Paris, École normale supérieure - Paris (ENS-PSL), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-École normale supérieure - Paris (ENS-PSL), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Duvernois-Berthet, Evelyne
Jazyk: angličtina
Rok vydání: 2015
Předmět:
0106 biological sciences
Cancer Research
lcsh:QH426-470
[SDV]Life Sciences [q-bio]
Arabidopsis
Biology
01 natural sciences
Epigenesis
Genetic
Cytosine
03 medical and health sciences
Epigenetics of physical exercise
Gene Expression Regulation
Plant
Histone methylation
Genetics
Epigenetics
Molecular Biology
RNA-Directed DNA Methylation
Genetics (clinical)
Ecology
Evolution
Behavior and Systematics
ComputingMilieux_MISCELLANEOUS
030304 developmental biology
Epigenomics
Feedback
Physiological
0303 health sciences
Arabidopsis Proteins
Methylation
DNA Methylation
Chromatin Assembly and Disassembly
Chromatin
DNA-Binding Proteins
[SDV] Life Sciences [q-bio]
lcsh:Genetics
Mutation
DNA methylation
DNA Transposable Elements
Genome
Plant
Research Article
Transcription Factors
010606 plant biology & botany
Zdroj: PLoS Genetics, Vol 11, Iss 4, p e1005154 (2015)
PLoS Genetics
PLoS Genetics, Public Library of Science, 2015, 11 (4), pp.e1005154. ⟨10.1371/journal.pgen.1005154⟩
PLoS Genetics, 2015, 11 (4), pp.e1005154. ⟨10.1371/journal.pgen.1005154⟩
ISSN: 1553-7404
1553-7390
Popis: 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.
Author Summary DNA methylation is important for controlling activity of transposable elements and genes. An intriguing feature of DNA methylation in plants is that its pattern can be inherited over multiple generations at high fidelity in a Mendelian manner. However, mechanisms controlling the trans-generational DNA methylation dynamics are largely unknown. Arabidopsis mutants of a chromatin remodeler gene DDM1 (Decrease in DNA Methylation 1) show drastic reduction of DNA methylation in transposons and repeats, and also show progressive changes in developmental phenotypes during propagation through self-pollination. We now show using whole genome DNA methylation sequencing that upon repeated selfing, the ddm1 mutation induces an ectopic accumulation of DNA methylation at hundreds of loci. Remarkably, even in the wild type background, the analogous de novo increase of DNA methylation can be induced in trans by chromosomes with reduced DNA methylation. Collectively, our findings support a model to explain the transgenerational DNA methylation redistribution by genome-wide negative feedback, which should be important for balanced differentiation of DNA methylation states within the genome.
Databáze: OpenAIRE
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