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Feedback circuits are numerous in embryonic gene regulatory networks and offer a stabilizing influence on evolution of those networks

The developmental gene regulatory networks (dGRNs) of two sea urchin species, Lytechinus variegatus (Lv) and Strongylocentrotus purpuratus (Sp), have remained remarkably similar despite about 50 million years since a common ancestor. Hundreds of parallel experimental perturbations of transcription f...

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Autores principales: Massri, Abdull Jesus, McDonald, Brennan, Wray, Gregory A., McClay, David R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10273620/
https://www.ncbi.nlm.nih.gov/pubmed/37322563
http://dx.doi.org/10.1186/s13227-023-00214-y
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author Massri, Abdull Jesus
McDonald, Brennan
Wray, Gregory A.
McClay, David R.
author_facet Massri, Abdull Jesus
McDonald, Brennan
Wray, Gregory A.
McClay, David R.
author_sort Massri, Abdull Jesus
collection PubMed
description The developmental gene regulatory networks (dGRNs) of two sea urchin species, Lytechinus variegatus (Lv) and Strongylocentrotus purpuratus (Sp), have remained remarkably similar despite about 50 million years since a common ancestor. Hundreds of parallel experimental perturbations of transcription factors with similar outcomes support this conclusion. A recent scRNA-seq analysis suggested that the earliest expression of several genes within the dGRNs differs between Lv and Sp. Here, we present a careful reanalysis of the dGRNs in these two species, paying close attention to timing of first expression. We find that initial expression of genes critical for cell fate specification occurs during several compressed time periods in both species. Previously unrecognized feedback circuits are inferred from the temporally corrected dGRNs. Although many of these feedbacks differ in location within the respective GRNs, the overall number is similar between species. We identify several prominent differences in timing of first expression for key developmental regulatory genes; comparison with a third species indicates that these heterochronies likely originated in an unbiased manner with respect to embryonic cell lineage and evolutionary branch. Together, these results suggest that interactions can evolve even within highly conserved dGRNs and that feedback circuits may buffer the effects of heterochronies in the expression of key regulatory genes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13227-023-00214-y.
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spelling pubmed-102736202023-06-17 Feedback circuits are numerous in embryonic gene regulatory networks and offer a stabilizing influence on evolution of those networks Massri, Abdull Jesus McDonald, Brennan Wray, Gregory A. McClay, David R. EvoDevo Research The developmental gene regulatory networks (dGRNs) of two sea urchin species, Lytechinus variegatus (Lv) and Strongylocentrotus purpuratus (Sp), have remained remarkably similar despite about 50 million years since a common ancestor. Hundreds of parallel experimental perturbations of transcription factors with similar outcomes support this conclusion. A recent scRNA-seq analysis suggested that the earliest expression of several genes within the dGRNs differs between Lv and Sp. Here, we present a careful reanalysis of the dGRNs in these two species, paying close attention to timing of first expression. We find that initial expression of genes critical for cell fate specification occurs during several compressed time periods in both species. Previously unrecognized feedback circuits are inferred from the temporally corrected dGRNs. Although many of these feedbacks differ in location within the respective GRNs, the overall number is similar between species. We identify several prominent differences in timing of first expression for key developmental regulatory genes; comparison with a third species indicates that these heterochronies likely originated in an unbiased manner with respect to embryonic cell lineage and evolutionary branch. Together, these results suggest that interactions can evolve even within highly conserved dGRNs and that feedback circuits may buffer the effects of heterochronies in the expression of key regulatory genes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13227-023-00214-y. BioMed Central 2023-06-16 /pmc/articles/PMC10273620/ /pubmed/37322563 http://dx.doi.org/10.1186/s13227-023-00214-y Text en © The Author(s) 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 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
Massri, Abdull Jesus
McDonald, Brennan
Wray, Gregory A.
McClay, David R.
Feedback circuits are numerous in embryonic gene regulatory networks and offer a stabilizing influence on evolution of those networks
title Feedback circuits are numerous in embryonic gene regulatory networks and offer a stabilizing influence on evolution of those networks
title_full Feedback circuits are numerous in embryonic gene regulatory networks and offer a stabilizing influence on evolution of those networks
title_fullStr Feedback circuits are numerous in embryonic gene regulatory networks and offer a stabilizing influence on evolution of those networks
title_full_unstemmed Feedback circuits are numerous in embryonic gene regulatory networks and offer a stabilizing influence on evolution of those networks
title_short Feedback circuits are numerous in embryonic gene regulatory networks and offer a stabilizing influence on evolution of those networks
title_sort feedback circuits are numerous in embryonic gene regulatory networks and offer a stabilizing influence on evolution of those networks
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10273620/
https://www.ncbi.nlm.nih.gov/pubmed/37322563
http://dx.doi.org/10.1186/s13227-023-00214-y
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