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Inter-embryo gene expression variability recapitulates the hourglass pattern of evo-devo

BACKGROUND: The evolution of embryological development has long been characterized by deep conservation. In animal development, the phylotypic stage in mid-embryogenesis is more conserved than either early or late stages among species within the same phylum. Hypotheses to explain this hourglass patt...

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Autores principales: Liu, Jialin, Frochaux, Michael, Gardeux, Vincent, Deplancke, Bart, Robinson-Rechavi, Marc
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7502200/
https://www.ncbi.nlm.nih.gov/pubmed/32950053
http://dx.doi.org/10.1186/s12915-020-00842-z
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author Liu, Jialin
Frochaux, Michael
Gardeux, Vincent
Deplancke, Bart
Robinson-Rechavi, Marc
author_facet Liu, Jialin
Frochaux, Michael
Gardeux, Vincent
Deplancke, Bart
Robinson-Rechavi, Marc
author_sort Liu, Jialin
collection PubMed
description BACKGROUND: The evolution of embryological development has long been characterized by deep conservation. In animal development, the phylotypic stage in mid-embryogenesis is more conserved than either early or late stages among species within the same phylum. Hypotheses to explain this hourglass pattern have focused on purifying the selection of gene regulation. Here, we propose an alternative—genes are regulated in different ways at different stages and have different intrinsic capacities to respond to perturbations on gene expression. RESULTS: To eliminate the influence of natural selection, we quantified the expression variability of isogenetic single embryo transcriptomes throughout fly Drosophila melanogaster embryogenesis. We found that the expression variability is lower at the phylotypic stage, supporting that the underlying regulatory architecture in this stage is more robust to stochastic variation on gene expression. We present evidence that the phylotypic stage is also robust to genetic variations on gene expression. Moreover, chromatin regulation appears to play a key role in the variation and evolution of gene expression. CONCLUSIONS: We suggest that a phylum-level pattern of embryonic conservation can be explained by the intrinsic difference of gene regulatory mechanisms in different stages.
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spelling pubmed-75022002020-09-22 Inter-embryo gene expression variability recapitulates the hourglass pattern of evo-devo Liu, Jialin Frochaux, Michael Gardeux, Vincent Deplancke, Bart Robinson-Rechavi, Marc BMC Biol Research Article BACKGROUND: The evolution of embryological development has long been characterized by deep conservation. In animal development, the phylotypic stage in mid-embryogenesis is more conserved than either early or late stages among species within the same phylum. Hypotheses to explain this hourglass pattern have focused on purifying the selection of gene regulation. Here, we propose an alternative—genes are regulated in different ways at different stages and have different intrinsic capacities to respond to perturbations on gene expression. RESULTS: To eliminate the influence of natural selection, we quantified the expression variability of isogenetic single embryo transcriptomes throughout fly Drosophila melanogaster embryogenesis. We found that the expression variability is lower at the phylotypic stage, supporting that the underlying regulatory architecture in this stage is more robust to stochastic variation on gene expression. We present evidence that the phylotypic stage is also robust to genetic variations on gene expression. Moreover, chromatin regulation appears to play a key role in the variation and evolution of gene expression. CONCLUSIONS: We suggest that a phylum-level pattern of embryonic conservation can be explained by the intrinsic difference of gene regulatory mechanisms in different stages. BioMed Central 2020-09-19 /pmc/articles/PMC7502200/ /pubmed/32950053 http://dx.doi.org/10.1186/s12915-020-00842-z Text en © The Author(s) 2020 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/. 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 in a credit line to the data.
spellingShingle Research Article
Liu, Jialin
Frochaux, Michael
Gardeux, Vincent
Deplancke, Bart
Robinson-Rechavi, Marc
Inter-embryo gene expression variability recapitulates the hourglass pattern of evo-devo
title Inter-embryo gene expression variability recapitulates the hourglass pattern of evo-devo
title_full Inter-embryo gene expression variability recapitulates the hourglass pattern of evo-devo
title_fullStr Inter-embryo gene expression variability recapitulates the hourglass pattern of evo-devo
title_full_unstemmed Inter-embryo gene expression variability recapitulates the hourglass pattern of evo-devo
title_short Inter-embryo gene expression variability recapitulates the hourglass pattern of evo-devo
title_sort inter-embryo gene expression variability recapitulates the hourglass pattern of evo-devo
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7502200/
https://www.ncbi.nlm.nih.gov/pubmed/32950053
http://dx.doi.org/10.1186/s12915-020-00842-z
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