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Histone 4 lysine 5/12 acetylation enables developmental plasticity of Pristionchus mouth form

Development can be altered to match phenotypes with the environment, and the genetic mechanisms that direct such alternative phenotypes are beginning to be elucidated. Yet, the rules that govern environmental sensitivity vs. invariant development, and potential epigenetic memory, remain unknown. Her...

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Autores principales: Werner, Michael S., Loschko, Tobias, King, Thomas, Reich, Shelley, Theska, Tobias, Franz-Wachtel, Mirita, Macek, Boris, Sommer, Ralf J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10102330/
https://www.ncbi.nlm.nih.gov/pubmed/37055396
http://dx.doi.org/10.1038/s41467-023-37734-z
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author Werner, Michael S.
Loschko, Tobias
King, Thomas
Reich, Shelley
Theska, Tobias
Franz-Wachtel, Mirita
Macek, Boris
Sommer, Ralf J.
author_facet Werner, Michael S.
Loschko, Tobias
King, Thomas
Reich, Shelley
Theska, Tobias
Franz-Wachtel, Mirita
Macek, Boris
Sommer, Ralf J.
author_sort Werner, Michael S.
collection PubMed
description Development can be altered to match phenotypes with the environment, and the genetic mechanisms that direct such alternative phenotypes are beginning to be elucidated. Yet, the rules that govern environmental sensitivity vs. invariant development, and potential epigenetic memory, remain unknown. Here, we show that plasticity of nematode mouth forms is determined by histone 4 lysine 5 and 12 acetylation (H4K5/12ac). Acetylation in early larval stages provides a permissive chromatin state, which is susceptible to induction during the critical window of environmental sensitivity. As development proceeds deacetylation shuts off switch gene expression to end the critical period. Inhibiting deacetylase enzymes leads to fixation of prior developmental trajectories, demonstrating that histone modifications in juveniles can carry environmental information to adults. Finally, we provide evidence that this regulation was derived from an ancient mechanism of licensing developmental speed. Altogether, our results show that H4K5/12ac enables epigenetic regulation of developmental plasticity that can be stored and erased by acetylation and deacetylation, respectively.
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spelling pubmed-101023302023-04-15 Histone 4 lysine 5/12 acetylation enables developmental plasticity of Pristionchus mouth form Werner, Michael S. Loschko, Tobias King, Thomas Reich, Shelley Theska, Tobias Franz-Wachtel, Mirita Macek, Boris Sommer, Ralf J. Nat Commun Article Development can be altered to match phenotypes with the environment, and the genetic mechanisms that direct such alternative phenotypes are beginning to be elucidated. Yet, the rules that govern environmental sensitivity vs. invariant development, and potential epigenetic memory, remain unknown. Here, we show that plasticity of nematode mouth forms is determined by histone 4 lysine 5 and 12 acetylation (H4K5/12ac). Acetylation in early larval stages provides a permissive chromatin state, which is susceptible to induction during the critical window of environmental sensitivity. As development proceeds deacetylation shuts off switch gene expression to end the critical period. Inhibiting deacetylase enzymes leads to fixation of prior developmental trajectories, demonstrating that histone modifications in juveniles can carry environmental information to adults. Finally, we provide evidence that this regulation was derived from an ancient mechanism of licensing developmental speed. Altogether, our results show that H4K5/12ac enables epigenetic regulation of developmental plasticity that can be stored and erased by acetylation and deacetylation, respectively. Nature Publishing Group UK 2023-04-13 /pmc/articles/PMC10102330/ /pubmed/37055396 http://dx.doi.org/10.1038/s41467-023-37734-z Text en © The Author(s) 2023, corrected publication 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as 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 images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Werner, Michael S.
Loschko, Tobias
King, Thomas
Reich, Shelley
Theska, Tobias
Franz-Wachtel, Mirita
Macek, Boris
Sommer, Ralf J.
Histone 4 lysine 5/12 acetylation enables developmental plasticity of Pristionchus mouth form
title Histone 4 lysine 5/12 acetylation enables developmental plasticity of Pristionchus mouth form
title_full Histone 4 lysine 5/12 acetylation enables developmental plasticity of Pristionchus mouth form
title_fullStr Histone 4 lysine 5/12 acetylation enables developmental plasticity of Pristionchus mouth form
title_full_unstemmed Histone 4 lysine 5/12 acetylation enables developmental plasticity of Pristionchus mouth form
title_short Histone 4 lysine 5/12 acetylation enables developmental plasticity of Pristionchus mouth form
title_sort histone 4 lysine 5/12 acetylation enables developmental plasticity of pristionchus mouth form
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10102330/
https://www.ncbi.nlm.nih.gov/pubmed/37055396
http://dx.doi.org/10.1038/s41467-023-37734-z
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