Stable transgenerational epigenetic inheritance requires a DNA methylation-sensing circuit
Epigenetic states are stably propagated in eukaryotes. In plants, DNA methylation patterns are faithfully inherited over many generations but it is unknown how the dynamic activities of cytosine DNA methyltransferases and 5-methylcytosine DNA glycosylases interact to maintain epigenetic homeostasis....
| Main Authors: | , |
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| Format: | Article |
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Nature Publishing Group
2018
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| Online Access: | http://hdl.handle.net/1721.1/113606 https://orcid.org/0000-0003-2280-1522 |
| _version_ | 1826199463808466944 |
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| author | Williams, Ben P. Gehring, Mary |
| author2 | Massachusetts Institute of Technology. Department of Biology |
| author_facet | Massachusetts Institute of Technology. Department of Biology Williams, Ben P. Gehring, Mary |
| author_sort | Williams, Ben P. |
| collection | MIT |
| description | Epigenetic states are stably propagated in eukaryotes. In plants, DNA methylation patterns are faithfully inherited over many generations but it is unknown how the dynamic activities of cytosine DNA methyltransferases and 5-methylcytosine DNA glycosylases interact to maintain epigenetic homeostasis. Here we show that a methylation-sensing gene regulatory circuit centered on a 5-methylcytosine DNA glycosylase gene is required for long-term epigenetic fidelity in Arabidopsis. Disrupting this circuit causes widespread methylation losses and abnormal phenotypes that progressively worsen over generations. In heterochromatin, these losses are counteracted such that methylation returns to a normal level over four generations. However, thousands of loci in euchromatin progressively lose DNA methylation between generations and remain unmethylated. We conclude that an actively maintained equilibrium between methylation and demethylation activities is required to ensure long-term stable inheritance of epigenetic information. |
| first_indexed | 2024-09-23T11:20:18Z |
| format | Article |
| id | mit-1721.1/113606 |
| institution | Massachusetts Institute of Technology |
| last_indexed | 2024-09-23T11:20:18Z |
| publishDate | 2018 |
| publisher | Nature Publishing Group |
| record_format | dspace |
| spelling | mit-1721.1/1136062022-10-01T02:57:39Z Stable transgenerational epigenetic inheritance requires a DNA methylation-sensing circuit Williams, Ben P. Gehring, Mary Massachusetts Institute of Technology. Department of Biology Gehring, Mary Epigenetic states are stably propagated in eukaryotes. In plants, DNA methylation patterns are faithfully inherited over many generations but it is unknown how the dynamic activities of cytosine DNA methyltransferases and 5-methylcytosine DNA glycosylases interact to maintain epigenetic homeostasis. Here we show that a methylation-sensing gene regulatory circuit centered on a 5-methylcytosine DNA glycosylase gene is required for long-term epigenetic fidelity in Arabidopsis. Disrupting this circuit causes widespread methylation losses and abnormal phenotypes that progressively worsen over generations. In heterochromatin, these losses are counteracted such that methylation returns to a normal level over four generations. However, thousands of loci in euchromatin progressively lose DNA methylation between generations and remain unmethylated. We conclude that an actively maintained equilibrium between methylation and demethylation activities is required to ensure long-term stable inheritance of epigenetic information. National Institute of General Medical Sciences (U.S.) (Grant R01GM112851) 2018-02-12T20:58:55Z 2018-02-12T20:58:55Z 2017-12 2017-07 2018-02-09T15:44:55Z Article http://purl.org/eprint/type/JournalArticle 2041-1723 http://hdl.handle.net/1721.1/113606 Williams, Ben P., and Gehring, Mary. “Stable Transgenerational Epigenetic Inheritance Requires a DNA Methylation-Sensing Circuit.” Nature Communications 8, 1 (December 2017) © 2017 The Author(s) https://orcid.org/0000-0003-2280-1522 http://dx.doi.org/10.1038/s41467-017-02219-3 Nature Communications Creative Commons Attribution 4.0 International License https://creativecommons.org/licenses/by/4.0/ application/pdf Nature Publishing Group |
| spellingShingle | Williams, Ben P. Gehring, Mary Stable transgenerational epigenetic inheritance requires a DNA methylation-sensing circuit |
| title | Stable transgenerational epigenetic inheritance requires a DNA methylation-sensing circuit |
| title_full | Stable transgenerational epigenetic inheritance requires a DNA methylation-sensing circuit |
| title_fullStr | Stable transgenerational epigenetic inheritance requires a DNA methylation-sensing circuit |
| title_full_unstemmed | Stable transgenerational epigenetic inheritance requires a DNA methylation-sensing circuit |
| title_short | Stable transgenerational epigenetic inheritance requires a DNA methylation-sensing circuit |
| title_sort | stable transgenerational epigenetic inheritance requires a dna methylation sensing circuit |
| url | http://hdl.handle.net/1721.1/113606 https://orcid.org/0000-0003-2280-1522 |
| work_keys_str_mv | AT williamsbenp stabletransgenerationalepigeneticinheritancerequiresadnamethylationsensingcircuit AT gehringmary stabletransgenerationalepigeneticinheritancerequiresadnamethylationsensingcircuit |