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Modular co-option of cardiopharyngeal genes during non-embryonic myogenesis

BACKGROUND: In chordates, cardiac and body muscles arise from different embryonic origins. In addition, myogenesis can be triggered in adult organisms, during asexual development or regeneration. In non-vertebrate chordates like ascidians, muscles originate from embryonic precursors regulated by a c...

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Autores principales: Prünster, Maria Mandela, Ricci, Lorenzo, Brown, Federico D., Tiozzo, Stefano
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6399929/
https://www.ncbi.nlm.nih.gov/pubmed/30867897
http://dx.doi.org/10.1186/s13227-019-0116-7
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author Prünster, Maria Mandela
Ricci, Lorenzo
Brown, Federico D.
Tiozzo, Stefano
author_facet Prünster, Maria Mandela
Ricci, Lorenzo
Brown, Federico D.
Tiozzo, Stefano
author_sort Prünster, Maria Mandela
collection PubMed
description BACKGROUND: In chordates, cardiac and body muscles arise from different embryonic origins. In addition, myogenesis can be triggered in adult organisms, during asexual development or regeneration. In non-vertebrate chordates like ascidians, muscles originate from embryonic precursors regulated by a conserved set of genes that orchestrate cell behavior and dynamics during development. In colonial ascidians, besides embryogenesis and metamorphosis, an adult can propagate asexually via blastogenesis, skipping embryo and larval stages, and form anew the adult body, including the complete body musculature. RESULTS: To investigate the cellular origin and mechanisms that trigger non-embryonic myogenesis, we followed the expression of ascidian myogenic genes during Botryllus schlosseri blastogenesis and reconstructed the dynamics of muscle precursors. Based on the expression dynamics of Tbx1/10, Ebf, Mrf, Myh3 for body wall and of FoxF, Tbx1/10, Nk4, Myh2 for heart development, we show that the embryonic factors regulating myogenesis are only partially co-opted in blastogenesis, and that markers for muscle precursors are expressed in two separate domains: the dorsal tube and the ventral mesenchyma. CONCLUSIONS: Regardless of the developmental pathway, non-embryonic myogenesis shares a similar molecular and anatomical setup as embryonic myogenesis, but implements a co-option and loss of molecular modules. We then propose that the cellular precursors contributing to heart and body muscles may have different origins and may be coordinated by different developmental pathways. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13227-019-0116-7) contains supplementary material, which is available to authorized users.
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spelling pubmed-63999292019-03-13 Modular co-option of cardiopharyngeal genes during non-embryonic myogenesis Prünster, Maria Mandela Ricci, Lorenzo Brown, Federico D. Tiozzo, Stefano EvoDevo Research BACKGROUND: In chordates, cardiac and body muscles arise from different embryonic origins. In addition, myogenesis can be triggered in adult organisms, during asexual development or regeneration. In non-vertebrate chordates like ascidians, muscles originate from embryonic precursors regulated by a conserved set of genes that orchestrate cell behavior and dynamics during development. In colonial ascidians, besides embryogenesis and metamorphosis, an adult can propagate asexually via blastogenesis, skipping embryo and larval stages, and form anew the adult body, including the complete body musculature. RESULTS: To investigate the cellular origin and mechanisms that trigger non-embryonic myogenesis, we followed the expression of ascidian myogenic genes during Botryllus schlosseri blastogenesis and reconstructed the dynamics of muscle precursors. Based on the expression dynamics of Tbx1/10, Ebf, Mrf, Myh3 for body wall and of FoxF, Tbx1/10, Nk4, Myh2 for heart development, we show that the embryonic factors regulating myogenesis are only partially co-opted in blastogenesis, and that markers for muscle precursors are expressed in two separate domains: the dorsal tube and the ventral mesenchyma. CONCLUSIONS: Regardless of the developmental pathway, non-embryonic myogenesis shares a similar molecular and anatomical setup as embryonic myogenesis, but implements a co-option and loss of molecular modules. We then propose that the cellular precursors contributing to heart and body muscles may have different origins and may be coordinated by different developmental pathways. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13227-019-0116-7) contains supplementary material, which is available to authorized users. BioMed Central 2019-03-05 /pmc/articles/PMC6399929/ /pubmed/30867897 http://dx.doi.org/10.1186/s13227-019-0116-7 Text en © The Author(s) 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 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.
spellingShingle Research
Prünster, Maria Mandela
Ricci, Lorenzo
Brown, Federico D.
Tiozzo, Stefano
Modular co-option of cardiopharyngeal genes during non-embryonic myogenesis
title Modular co-option of cardiopharyngeal genes during non-embryonic myogenesis
title_full Modular co-option of cardiopharyngeal genes during non-embryonic myogenesis
title_fullStr Modular co-option of cardiopharyngeal genes during non-embryonic myogenesis
title_full_unstemmed Modular co-option of cardiopharyngeal genes during non-embryonic myogenesis
title_short Modular co-option of cardiopharyngeal genes during non-embryonic myogenesis
title_sort modular co-option of cardiopharyngeal genes during non-embryonic myogenesis
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6399929/
https://www.ncbi.nlm.nih.gov/pubmed/30867897
http://dx.doi.org/10.1186/s13227-019-0116-7
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