Genome-wide negative feedback drives transgenerational DNA methylation dynamics in Arabidopsis.
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. Howeve...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2015-04-01
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| Series: | PLoS Genetics |
| Online Access: | http://europepmc.org/articles/PMC4406451?pdf=render |
| _version_ | 1819171702428401664 |
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| author | Tasuku Ito Yoshiaki Tarutani Taiko Kim To Mohamed Kassam Evelyne Duvernois-Berthet Sandra Cortijo Kazuya Takashima Hidetoshi Saze Atsushi Toyoda Asao Fujiyama Vincent Colot Tetsuji Kakutani |
| author_facet | Tasuku Ito Yoshiaki Tarutani Taiko Kim To Mohamed Kassam Evelyne Duvernois-Berthet Sandra Cortijo Kazuya Takashima Hidetoshi Saze Atsushi Toyoda Asao Fujiyama Vincent Colot Tetsuji Kakutani |
| author_sort | Tasuku Ito |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-22T19:55:29Z |
| format | Article |
| id | doaj.art-9c5e91134b8d40ada56f02fb2c25ba05 |
| institution | Directory Open Access Journal |
| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2024-12-22T19:55:29Z |
| publishDate | 2015-04-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj.art-9c5e91134b8d40ada56f02fb2c25ba052022-12-21T18:14:26ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042015-04-01114e100515410.1371/journal.pgen.1005154Genome-wide negative feedback drives transgenerational DNA methylation dynamics in Arabidopsis.Tasuku ItoYoshiaki TarutaniTaiko Kim ToMohamed KassamEvelyne Duvernois-BerthetSandra CortijoKazuya TakashimaHidetoshi SazeAtsushi ToyodaAsao FujiyamaVincent ColotTetsuji KakutaniEpigenetic 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.http://europepmc.org/articles/PMC4406451?pdf=render |
| spellingShingle | Tasuku Ito Yoshiaki Tarutani Taiko Kim To Mohamed Kassam Evelyne Duvernois-Berthet Sandra Cortijo Kazuya Takashima Hidetoshi Saze Atsushi Toyoda Asao Fujiyama Vincent Colot Tetsuji Kakutani Genome-wide negative feedback drives transgenerational DNA methylation dynamics in Arabidopsis. PLoS Genetics |
| title | Genome-wide negative feedback drives transgenerational DNA methylation dynamics in Arabidopsis. |
| title_full | Genome-wide negative feedback drives transgenerational DNA methylation dynamics in Arabidopsis. |
| title_fullStr | Genome-wide negative feedback drives transgenerational DNA methylation dynamics in Arabidopsis. |
| title_full_unstemmed | Genome-wide negative feedback drives transgenerational DNA methylation dynamics in Arabidopsis. |
| title_short | Genome-wide negative feedback drives transgenerational DNA methylation dynamics in Arabidopsis. |
| title_sort | genome wide negative feedback drives transgenerational dna methylation dynamics in arabidopsis |
| url | http://europepmc.org/articles/PMC4406451?pdf=render |
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