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Rhythmicity is linked to expression cost at the protein level but to expression precision at the mRNA level

Many genes have nycthemeral rhythms of expression, i.e. a 24-hours periodic variation, at either mRNA or protein level or both, and most rhythmic genes are tissue-specific. Here, we investigate and discuss the evolutionary origins of rhythms in gene expression. Our results suggest that rhythmicity o...

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Autores principales: Laloum, David, Robinson-Rechavi, Marc
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9518874/
https://www.ncbi.nlm.nih.gov/pubmed/36095022
http://dx.doi.org/10.1371/journal.pcbi.1010399
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author Laloum, David
Robinson-Rechavi, Marc
author_facet Laloum, David
Robinson-Rechavi, Marc
author_sort Laloum, David
collection PubMed
description Many genes have nycthemeral rhythms of expression, i.e. a 24-hours periodic variation, at either mRNA or protein level or both, and most rhythmic genes are tissue-specific. Here, we investigate and discuss the evolutionary origins of rhythms in gene expression. Our results suggest that rhythmicity of protein expression could have been favored by selection to minimize costs. Trends are consistent in bacteria, plants and animals, and are also supported by tissue-specific patterns in mouse. Unlike for protein level, cost cannot explain rhythm at the RNA level. We suggest that instead it allows to periodically reduce expression noise. Noise control had the strongest support in mouse, with limited evidence in other species. We have also found that genes under stronger purifying selection are rhythmically expressed at the mRNA level, and we propose that this is because they are noise sensitive genes. Finally, the adaptive role of rhythmic expression is supported by rhythmic genes being highly expressed yet tissue-specific. This provides a good evolutionary explanation for the observation that nycthemeral rhythms are often tissue-specific.
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spelling pubmed-95188742022-09-29 Rhythmicity is linked to expression cost at the protein level but to expression precision at the mRNA level Laloum, David Robinson-Rechavi, Marc PLoS Comput Biol Research Article Many genes have nycthemeral rhythms of expression, i.e. a 24-hours periodic variation, at either mRNA or protein level or both, and most rhythmic genes are tissue-specific. Here, we investigate and discuss the evolutionary origins of rhythms in gene expression. Our results suggest that rhythmicity of protein expression could have been favored by selection to minimize costs. Trends are consistent in bacteria, plants and animals, and are also supported by tissue-specific patterns in mouse. Unlike for protein level, cost cannot explain rhythm at the RNA level. We suggest that instead it allows to periodically reduce expression noise. Noise control had the strongest support in mouse, with limited evidence in other species. We have also found that genes under stronger purifying selection are rhythmically expressed at the mRNA level, and we propose that this is because they are noise sensitive genes. Finally, the adaptive role of rhythmic expression is supported by rhythmic genes being highly expressed yet tissue-specific. This provides a good evolutionary explanation for the observation that nycthemeral rhythms are often tissue-specific. Public Library of Science 2022-09-12 /pmc/articles/PMC9518874/ /pubmed/36095022 http://dx.doi.org/10.1371/journal.pcbi.1010399 Text en © 2022 Laloum, Robinson-Rechavi https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Laloum, David
Robinson-Rechavi, Marc
Rhythmicity is linked to expression cost at the protein level but to expression precision at the mRNA level
title Rhythmicity is linked to expression cost at the protein level but to expression precision at the mRNA level
title_full Rhythmicity is linked to expression cost at the protein level but to expression precision at the mRNA level
title_fullStr Rhythmicity is linked to expression cost at the protein level but to expression precision at the mRNA level
title_full_unstemmed Rhythmicity is linked to expression cost at the protein level but to expression precision at the mRNA level
title_short Rhythmicity is linked to expression cost at the protein level but to expression precision at the mRNA level
title_sort rhythmicity is linked to expression cost at the protein level but to expression precision at the mrna level
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9518874/
https://www.ncbi.nlm.nih.gov/pubmed/36095022
http://dx.doi.org/10.1371/journal.pcbi.1010399
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