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DNA methylation is maintained with high fidelity in the honey bee germline and exhibits global non-functional fluctuations during somatic development

BACKGROUND: DNA methylation of active genes, also known as gene body methylation, is found in many animal and plant genomes. Despite this, the transcriptional and developmental role of such methylation remains poorly understood. Here, we explore the dynamic range of DNA methylation in honey bee, a m...

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Autores principales: Harris, Keith D., Lloyd, James P. B., Domb, Katherine, Zilberman, Daniel, Zemach, Assaf
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6786280/
https://www.ncbi.nlm.nih.gov/pubmed/31601251
http://dx.doi.org/10.1186/s13072-019-0307-4
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author Harris, Keith D.
Lloyd, James P. B.
Domb, Katherine
Zilberman, Daniel
Zemach, Assaf
author_facet Harris, Keith D.
Lloyd, James P. B.
Domb, Katherine
Zilberman, Daniel
Zemach, Assaf
author_sort Harris, Keith D.
collection PubMed
description BACKGROUND: DNA methylation of active genes, also known as gene body methylation, is found in many animal and plant genomes. Despite this, the transcriptional and developmental role of such methylation remains poorly understood. Here, we explore the dynamic range of DNA methylation in honey bee, a model organism for gene body methylation. RESULTS: Our data show that CG methylation in gene bodies globally fluctuates during honey bee development. However, these changes cause no gene expression alterations. Intriguingly, despite the global alterations, tissue-specific CG methylation patterns of complete genes or exons are rare, implying robust maintenance of genic methylation during development. Additionally, we show that CG methylation maintenance fluctuates in somatic cells, while reaching maximum fidelity in sperm cells. Finally, unlike universally present CG methylation, we discovered non-CG methylation specifically in bee heads that resembles such methylation in mammalian brain tissue. CONCLUSIONS: Based on these results, we propose that gene body CG methylation can oscillate during development if it is kept to a level adequate to preserve function. Additionally, our data suggest that heightened non-CG methylation is a conserved regulator of animal nervous systems.
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spelling pubmed-67862802019-10-17 DNA methylation is maintained with high fidelity in the honey bee germline and exhibits global non-functional fluctuations during somatic development Harris, Keith D. Lloyd, James P. B. Domb, Katherine Zilberman, Daniel Zemach, Assaf Epigenetics Chromatin Research BACKGROUND: DNA methylation of active genes, also known as gene body methylation, is found in many animal and plant genomes. Despite this, the transcriptional and developmental role of such methylation remains poorly understood. Here, we explore the dynamic range of DNA methylation in honey bee, a model organism for gene body methylation. RESULTS: Our data show that CG methylation in gene bodies globally fluctuates during honey bee development. However, these changes cause no gene expression alterations. Intriguingly, despite the global alterations, tissue-specific CG methylation patterns of complete genes or exons are rare, implying robust maintenance of genic methylation during development. Additionally, we show that CG methylation maintenance fluctuates in somatic cells, while reaching maximum fidelity in sperm cells. Finally, unlike universally present CG methylation, we discovered non-CG methylation specifically in bee heads that resembles such methylation in mammalian brain tissue. CONCLUSIONS: Based on these results, we propose that gene body CG methylation can oscillate during development if it is kept to a level adequate to preserve function. Additionally, our data suggest that heightened non-CG methylation is a conserved regulator of animal nervous systems. BioMed Central 2019-10-10 /pmc/articles/PMC6786280/ /pubmed/31601251 http://dx.doi.org/10.1186/s13072-019-0307-4 Text en © The Author(s) 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Harris, Keith D.
Lloyd, James P. B.
Domb, Katherine
Zilberman, Daniel
Zemach, Assaf
DNA methylation is maintained with high fidelity in the honey bee germline and exhibits global non-functional fluctuations during somatic development
title DNA methylation is maintained with high fidelity in the honey bee germline and exhibits global non-functional fluctuations during somatic development
title_full DNA methylation is maintained with high fidelity in the honey bee germline and exhibits global non-functional fluctuations during somatic development
title_fullStr DNA methylation is maintained with high fidelity in the honey bee germline and exhibits global non-functional fluctuations during somatic development
title_full_unstemmed DNA methylation is maintained with high fidelity in the honey bee germline and exhibits global non-functional fluctuations during somatic development
title_short DNA methylation is maintained with high fidelity in the honey bee germline and exhibits global non-functional fluctuations during somatic development
title_sort dna methylation is maintained with high fidelity in the honey bee germline and exhibits global non-functional fluctuations during somatic development
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6786280/
https://www.ncbi.nlm.nih.gov/pubmed/31601251
http://dx.doi.org/10.1186/s13072-019-0307-4
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