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

Abstract 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 regulate...

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Main Authors: Maria Mandela Prünster, Lorenzo Ricci, Federico D. Brown, Stefano Tiozzo
Format: Article
Language:English
Published: BMC 2019-03-01
Series:EvoDevo
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13227-019-0116-7
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spelling doaj-c66a0496385f427eaf71a2aec610b0882020-11-25T02:25:42ZengBMCEvoDevo2041-91392019-03-0110111510.1186/s13227-019-0116-7Modular co-option of cardiopharyngeal genes during non-embryonic myogenesisMaria Mandela Prünster0Lorenzo Ricci1Federico D. Brown2Stefano Tiozzo3Laboratoire de Biologie du Développement de Villefranche-sur-mer (LBDV), CNRS, Sorbonne UniversitéLaboratoire de Biologie du Développement de Villefranche-sur-mer (LBDV), CNRS, Sorbonne UniversitéDepartamento de Zoologia, Instituto Biociências, Universidade de São PauloLaboratoire de Biologie du Développement de Villefranche-sur-mer (LBDV), CNRS, Sorbonne UniversitéAbstract 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.http://link.springer.com/article/10.1186/s13227-019-0116-7BlastogenesisAscidiansBotryllus schlosseriBuddingMuscleRegeneration
collection DOAJ
language English
format Article
sources DOAJ
author Maria Mandela Prünster
Lorenzo Ricci
Federico D. Brown
Stefano Tiozzo
spellingShingle Maria Mandela Prünster
Lorenzo Ricci
Federico D. Brown
Stefano Tiozzo
Modular co-option of cardiopharyngeal genes during non-embryonic myogenesis
EvoDevo
Blastogenesis
Ascidians
Botryllus schlosseri
Budding
Muscle
Regeneration
author_facet Maria Mandela Prünster
Lorenzo Ricci
Federico D. Brown
Stefano Tiozzo
author_sort Maria Mandela Prünster
title Modular co-option of cardiopharyngeal genes during non-embryonic myogenesis
title_short 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_sort modular co-option of cardiopharyngeal genes during non-embryonic myogenesis
publisher BMC
series EvoDevo
issn 2041-9139
publishDate 2019-03-01
description Abstract 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.
topic Blastogenesis
Ascidians
Botryllus schlosseri
Budding
Muscle
Regeneration
url http://link.springer.com/article/10.1186/s13227-019-0116-7
work_keys_str_mv AT mariamandelaprunster modularcooptionofcardiopharyngealgenesduringnonembryonicmyogenesis
AT lorenzoricci modularcooptionofcardiopharyngealgenesduringnonembryonicmyogenesis
AT federicodbrown modularcooptionofcardiopharyngealgenesduringnonembryonicmyogenesis
AT stefanotiozzo modularcooptionofcardiopharyngealgenesduringnonembryonicmyogenesis
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