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Paternal hypoxia exposure primes offspring for increased hypoxia resistance

BACKGROUND: In a time of rapid environmental change, understanding how the challenges experienced by one generation can influence the fitness of future generations is critically needed. Using tolerance assays and transcriptomic and methylome approaches, we use zebrafish as a model to investigate cro...

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Autores principales: Ragsdale, Alexandria, Ortega-Recalde, Oscar, Dutoit, Ludovic, Besson, Anne A., Chia, Jolyn H. Z., King, Tania, Nakagawa, Shinichi, Hickey, Anthony, Gemmell, Neil J., Hore, Timothy, Johnson, Sheri L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9426223/
https://www.ncbi.nlm.nih.gov/pubmed/36038899
http://dx.doi.org/10.1186/s12915-022-01389-x
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author Ragsdale, Alexandria
Ortega-Recalde, Oscar
Dutoit, Ludovic
Besson, Anne A.
Chia, Jolyn H. Z.
King, Tania
Nakagawa, Shinichi
Hickey, Anthony
Gemmell, Neil J.
Hore, Timothy
Johnson, Sheri L.
author_facet Ragsdale, Alexandria
Ortega-Recalde, Oscar
Dutoit, Ludovic
Besson, Anne A.
Chia, Jolyn H. Z.
King, Tania
Nakagawa, Shinichi
Hickey, Anthony
Gemmell, Neil J.
Hore, Timothy
Johnson, Sheri L.
author_sort Ragsdale, Alexandria
collection PubMed
description BACKGROUND: In a time of rapid environmental change, understanding how the challenges experienced by one generation can influence the fitness of future generations is critically needed. Using tolerance assays and transcriptomic and methylome approaches, we use zebrafish as a model to investigate cross-generational acclimation to hypoxia. RESULTS: We show that short-term paternal exposure to hypoxia endows offspring with greater tolerance to acute hypoxia. We detected two hemoglobin genes that are significantly upregulated by more than 6-fold in the offspring of hypoxia exposed males. Moreover, the offspring which maintained equilibrium the longest showed greatest upregulation in hemoglobin expression. We did not detect differential methylation at any of the differentially expressed genes, suggesting that other epigenetic mechanisms are responsible for alterations in gene expression. CONCLUSIONS: Overall, our findings suggest that an epigenetic memory of past hypoxia exposure is maintained and that this environmentally induced information is transferred to subsequent generations, pre-acclimating progeny to cope with hypoxic conditions. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01389-x.
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spelling pubmed-94262232022-08-31 Paternal hypoxia exposure primes offspring for increased hypoxia resistance Ragsdale, Alexandria Ortega-Recalde, Oscar Dutoit, Ludovic Besson, Anne A. Chia, Jolyn H. Z. King, Tania Nakagawa, Shinichi Hickey, Anthony Gemmell, Neil J. Hore, Timothy Johnson, Sheri L. BMC Biol Research Article BACKGROUND: In a time of rapid environmental change, understanding how the challenges experienced by one generation can influence the fitness of future generations is critically needed. Using tolerance assays and transcriptomic and methylome approaches, we use zebrafish as a model to investigate cross-generational acclimation to hypoxia. RESULTS: We show that short-term paternal exposure to hypoxia endows offspring with greater tolerance to acute hypoxia. We detected two hemoglobin genes that are significantly upregulated by more than 6-fold in the offspring of hypoxia exposed males. Moreover, the offspring which maintained equilibrium the longest showed greatest upregulation in hemoglobin expression. We did not detect differential methylation at any of the differentially expressed genes, suggesting that other epigenetic mechanisms are responsible for alterations in gene expression. CONCLUSIONS: Overall, our findings suggest that an epigenetic memory of past hypoxia exposure is maintained and that this environmentally induced information is transferred to subsequent generations, pre-acclimating progeny to cope with hypoxic conditions. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01389-x. BioMed Central 2022-08-30 /pmc/articles/PMC9426223/ /pubmed/36038899 http://dx.doi.org/10.1186/s12915-022-01389-x Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Ragsdale, Alexandria
Ortega-Recalde, Oscar
Dutoit, Ludovic
Besson, Anne A.
Chia, Jolyn H. Z.
King, Tania
Nakagawa, Shinichi
Hickey, Anthony
Gemmell, Neil J.
Hore, Timothy
Johnson, Sheri L.
Paternal hypoxia exposure primes offspring for increased hypoxia resistance
title Paternal hypoxia exposure primes offspring for increased hypoxia resistance
title_full Paternal hypoxia exposure primes offspring for increased hypoxia resistance
title_fullStr Paternal hypoxia exposure primes offspring for increased hypoxia resistance
title_full_unstemmed Paternal hypoxia exposure primes offspring for increased hypoxia resistance
title_short Paternal hypoxia exposure primes offspring for increased hypoxia resistance
title_sort paternal hypoxia exposure primes offspring for increased hypoxia resistance
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9426223/
https://www.ncbi.nlm.nih.gov/pubmed/36038899
http://dx.doi.org/10.1186/s12915-022-01389-x
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