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Prenatal acoustic programming of mitochondrial function for high temperatures in an arid-adapted bird

Sound is an essential source of information in many taxa and can notably be used by embryos to programme their phenotypes for postnatal environments. While underlying mechanisms are mostly unknown, there is growing evidence for the involvement of mitochondria—main source of cellular energy (i.e. ATP...

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Autores principales: Udino, Eve, George, Julia M., McKenzie, Matthew, Pessato, Anaïs, Crino, Ondi L., Buchanan, Katherine L., Mariette, Mylene M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8651415/
https://www.ncbi.nlm.nih.gov/pubmed/34875198
http://dx.doi.org/10.1098/rspb.2021.1893
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author Udino, Eve
George, Julia M.
McKenzie, Matthew
Pessato, Anaïs
Crino, Ondi L.
Buchanan, Katherine L.
Mariette, Mylene M.
author_facet Udino, Eve
George, Julia M.
McKenzie, Matthew
Pessato, Anaïs
Crino, Ondi L.
Buchanan, Katherine L.
Mariette, Mylene M.
author_sort Udino, Eve
collection PubMed
description Sound is an essential source of information in many taxa and can notably be used by embryos to programme their phenotypes for postnatal environments. While underlying mechanisms are mostly unknown, there is growing evidence for the involvement of mitochondria—main source of cellular energy (i.e. ATP)—in developmental programming processes. Here, we tested whether prenatal sound programmes mitochondrial metabolism. In the arid-adapted zebra finch, prenatal exposure to ‘heat-calls’—produced by parents incubating at high temperatures—adaptively alters nestling growth in the heat. We measured red blood cell mitochondrial function, in nestlings exposed prenatally to heat- or control-calls, and reared in contrasting thermal environments. Exposure to high temperatures always reduced mitochondrial ATP production efficiency. However, as expected to reduce heat production, prenatal exposure to heat-calls improved mitochondrial efficiency under mild heat conditions. In addition, when exposed to an acute heat-challenge, LEAK respiration was higher in heat-call nestlings, and mitochondrial efficiency low across temperatures. Consistent with its role in reducing oxidative damage, LEAK under extreme heat was also higher in fast growing nestlings. Our study therefore provides the first demonstration of mitochondrial acoustic sensitivity, and brings us closer to understanding the underpinning of acoustic developmental programming and avian strategies for heat adaptation.
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spelling pubmed-86514152021-12-23 Prenatal acoustic programming of mitochondrial function for high temperatures in an arid-adapted bird Udino, Eve George, Julia M. McKenzie, Matthew Pessato, Anaïs Crino, Ondi L. Buchanan, Katherine L. Mariette, Mylene M. Proc Biol Sci Development and Physiology Sound is an essential source of information in many taxa and can notably be used by embryos to programme their phenotypes for postnatal environments. While underlying mechanisms are mostly unknown, there is growing evidence for the involvement of mitochondria—main source of cellular energy (i.e. ATP)—in developmental programming processes. Here, we tested whether prenatal sound programmes mitochondrial metabolism. In the arid-adapted zebra finch, prenatal exposure to ‘heat-calls’—produced by parents incubating at high temperatures—adaptively alters nestling growth in the heat. We measured red blood cell mitochondrial function, in nestlings exposed prenatally to heat- or control-calls, and reared in contrasting thermal environments. Exposure to high temperatures always reduced mitochondrial ATP production efficiency. However, as expected to reduce heat production, prenatal exposure to heat-calls improved mitochondrial efficiency under mild heat conditions. In addition, when exposed to an acute heat-challenge, LEAK respiration was higher in heat-call nestlings, and mitochondrial efficiency low across temperatures. Consistent with its role in reducing oxidative damage, LEAK under extreme heat was also higher in fast growing nestlings. Our study therefore provides the first demonstration of mitochondrial acoustic sensitivity, and brings us closer to understanding the underpinning of acoustic developmental programming and avian strategies for heat adaptation. The Royal Society 2021-12-08 2021-12-08 /pmc/articles/PMC8651415/ /pubmed/34875198 http://dx.doi.org/10.1098/rspb.2021.1893 Text en © 2021 The Authors. https://creativecommons.org/licenses/by/4.0/Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, provided the original author and source are credited.
spellingShingle Development and Physiology
Udino, Eve
George, Julia M.
McKenzie, Matthew
Pessato, Anaïs
Crino, Ondi L.
Buchanan, Katherine L.
Mariette, Mylene M.
Prenatal acoustic programming of mitochondrial function for high temperatures in an arid-adapted bird
title Prenatal acoustic programming of mitochondrial function for high temperatures in an arid-adapted bird
title_full Prenatal acoustic programming of mitochondrial function for high temperatures in an arid-adapted bird
title_fullStr Prenatal acoustic programming of mitochondrial function for high temperatures in an arid-adapted bird
title_full_unstemmed Prenatal acoustic programming of mitochondrial function for high temperatures in an arid-adapted bird
title_short Prenatal acoustic programming of mitochondrial function for high temperatures in an arid-adapted bird
title_sort prenatal acoustic programming of mitochondrial function for high temperatures in an arid-adapted bird
topic Development and Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8651415/
https://www.ncbi.nlm.nih.gov/pubmed/34875198
http://dx.doi.org/10.1098/rspb.2021.1893
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