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Systematic comparison of sea urchin and sea star developmental gene regulatory networks explains how novelty is incorporated in early development

The extensive array of morphological diversity among animal taxa represents the product of millions of years of evolution. Morphology is the output of development, therefore phenotypic evolution arises from changes to the topology of the gene regulatory networks (GRNs) that control the highly coordi...

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Autores principales: Cary, Gregory A., McCauley, Brenna S., Zueva, Olga, Pattinato, Joseph, Longabaugh, William, Hinman, Veronica F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7719182/
https://www.ncbi.nlm.nih.gov/pubmed/33277483
http://dx.doi.org/10.1038/s41467-020-20023-4
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author Cary, Gregory A.
McCauley, Brenna S.
Zueva, Olga
Pattinato, Joseph
Longabaugh, William
Hinman, Veronica F.
author_facet Cary, Gregory A.
McCauley, Brenna S.
Zueva, Olga
Pattinato, Joseph
Longabaugh, William
Hinman, Veronica F.
author_sort Cary, Gregory A.
collection PubMed
description The extensive array of morphological diversity among animal taxa represents the product of millions of years of evolution. Morphology is the output of development, therefore phenotypic evolution arises from changes to the topology of the gene regulatory networks (GRNs) that control the highly coordinated process of embryogenesis. A particular challenge in understanding the origins of animal diversity lies in determining how GRNs incorporate novelty while preserving the overall stability of the network, and hence, embryonic viability. Here we assemble a comprehensive GRN for endomesoderm specification in the sea star from zygote through gastrulation that corresponds to the GRN for sea urchin development of equivalent territories and stages. Comparison of the GRNs identifies how novelty is incorporated in early development. We show how the GRN is resilient to the introduction of a transcription factor, pmar1, the inclusion of which leads to a switch between two stable modes of Delta-Notch signaling. Signaling pathways can function in multiple modes and we propose that GRN changes that lead to switches between modes may be a common evolutionary mechanism for changes in embryogenesis. Our data additionally proposes a model in which evolutionarily conserved network motifs, or kernels, may function throughout development to stabilize these signaling transitions.
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spelling pubmed-77191822020-12-11 Systematic comparison of sea urchin and sea star developmental gene regulatory networks explains how novelty is incorporated in early development Cary, Gregory A. McCauley, Brenna S. Zueva, Olga Pattinato, Joseph Longabaugh, William Hinman, Veronica F. Nat Commun Article The extensive array of morphological diversity among animal taxa represents the product of millions of years of evolution. Morphology is the output of development, therefore phenotypic evolution arises from changes to the topology of the gene regulatory networks (GRNs) that control the highly coordinated process of embryogenesis. A particular challenge in understanding the origins of animal diversity lies in determining how GRNs incorporate novelty while preserving the overall stability of the network, and hence, embryonic viability. Here we assemble a comprehensive GRN for endomesoderm specification in the sea star from zygote through gastrulation that corresponds to the GRN for sea urchin development of equivalent territories and stages. Comparison of the GRNs identifies how novelty is incorporated in early development. We show how the GRN is resilient to the introduction of a transcription factor, pmar1, the inclusion of which leads to a switch between two stable modes of Delta-Notch signaling. Signaling pathways can function in multiple modes and we propose that GRN changes that lead to switches between modes may be a common evolutionary mechanism for changes in embryogenesis. Our data additionally proposes a model in which evolutionarily conserved network motifs, or kernels, may function throughout development to stabilize these signaling transitions. Nature Publishing Group UK 2020-12-04 /pmc/articles/PMC7719182/ /pubmed/33277483 http://dx.doi.org/10.1038/s41467-020-20023-4 Text en © The Author(s) 2020 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Cary, Gregory A.
McCauley, Brenna S.
Zueva, Olga
Pattinato, Joseph
Longabaugh, William
Hinman, Veronica F.
Systematic comparison of sea urchin and sea star developmental gene regulatory networks explains how novelty is incorporated in early development
title Systematic comparison of sea urchin and sea star developmental gene regulatory networks explains how novelty is incorporated in early development
title_full Systematic comparison of sea urchin and sea star developmental gene regulatory networks explains how novelty is incorporated in early development
title_fullStr Systematic comparison of sea urchin and sea star developmental gene regulatory networks explains how novelty is incorporated in early development
title_full_unstemmed Systematic comparison of sea urchin and sea star developmental gene regulatory networks explains how novelty is incorporated in early development
title_short Systematic comparison of sea urchin and sea star developmental gene regulatory networks explains how novelty is incorporated in early development
title_sort systematic comparison of sea urchin and sea star developmental gene regulatory networks explains how novelty is incorporated in early development
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7719182/
https://www.ncbi.nlm.nih.gov/pubmed/33277483
http://dx.doi.org/10.1038/s41467-020-20023-4
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