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Gene profiling of head mesoderm in early zebrafish development: insights into the evolution of cranial mesoderm

BACKGROUND: The evolution of the head was one of the key events that marked the transition from invertebrates to vertebrates. With the emergence of structures such as eyes and jaws, vertebrates evolved an active and predatory life style and radiated into diversity of large-bodied animals. These orga...

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Autores principales: Wang, Huijia, Holland, Peter W. H., Takahashi, Tokiharu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6612195/
https://www.ncbi.nlm.nih.gov/pubmed/31312422
http://dx.doi.org/10.1186/s13227-019-0128-3
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author Wang, Huijia
Holland, Peter W. H.
Takahashi, Tokiharu
author_facet Wang, Huijia
Holland, Peter W. H.
Takahashi, Tokiharu
author_sort Wang, Huijia
collection PubMed
description BACKGROUND: The evolution of the head was one of the key events that marked the transition from invertebrates to vertebrates. With the emergence of structures such as eyes and jaws, vertebrates evolved an active and predatory life style and radiated into diversity of large-bodied animals. These organs are moved by cranial muscles that derive embryologically from head mesoderm. Compared with other embryonic components of the head, such as placodes and cranial neural crest cells, our understanding of cranial mesoderm is limited and is restricted to few species. RESULTS: Here, we report the expression patterns of key genes in zebrafish head mesoderm at very early developmental stages. Apart from a basic anterior–posterior axis marked by a combination of pitx2 and tbx1 expression, we find that most gene expression patterns are poorly conserved between zebrafish and chick, suggesting fewer developmental constraints imposed than in trunk mesoderm. Interestingly, the gene expression patterns clearly show the early establishment of medial–lateral compartmentalisation in zebrafish head mesoderm, comprising a wide medial zone flanked by two narrower strips. CONCLUSIONS: In zebrafish head mesoderm, there is no clear molecular regionalisation along the anteroposterior axis as previously reported in chick embryos. In contrast, the medial–lateral regionalisation is formed at early developmental stages. These patterns correspond to the distinction between paraxial mesoderm and lateral plate mesoderm in the trunk, suggesting a common groundplan for patterning head and trunk mesoderm. By comparison of these expression patterns to that of amphioxus homologues, we argue for an evolutionary link between zebrafish head mesoderm and amphioxus anteriormost somites. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13227-019-0128-3) contains supplementary material, which is available to authorized users.
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spelling pubmed-66121952019-07-16 Gene profiling of head mesoderm in early zebrafish development: insights into the evolution of cranial mesoderm Wang, Huijia Holland, Peter W. H. Takahashi, Tokiharu EvoDevo Research BACKGROUND: The evolution of the head was one of the key events that marked the transition from invertebrates to vertebrates. With the emergence of structures such as eyes and jaws, vertebrates evolved an active and predatory life style and radiated into diversity of large-bodied animals. These organs are moved by cranial muscles that derive embryologically from head mesoderm. Compared with other embryonic components of the head, such as placodes and cranial neural crest cells, our understanding of cranial mesoderm is limited and is restricted to few species. RESULTS: Here, we report the expression patterns of key genes in zebrafish head mesoderm at very early developmental stages. Apart from a basic anterior–posterior axis marked by a combination of pitx2 and tbx1 expression, we find that most gene expression patterns are poorly conserved between zebrafish and chick, suggesting fewer developmental constraints imposed than in trunk mesoderm. Interestingly, the gene expression patterns clearly show the early establishment of medial–lateral compartmentalisation in zebrafish head mesoderm, comprising a wide medial zone flanked by two narrower strips. CONCLUSIONS: In zebrafish head mesoderm, there is no clear molecular regionalisation along the anteroposterior axis as previously reported in chick embryos. In contrast, the medial–lateral regionalisation is formed at early developmental stages. These patterns correspond to the distinction between paraxial mesoderm and lateral plate mesoderm in the trunk, suggesting a common groundplan for patterning head and trunk mesoderm. By comparison of these expression patterns to that of amphioxus homologues, we argue for an evolutionary link between zebrafish head mesoderm and amphioxus anteriormost somites. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13227-019-0128-3) contains supplementary material, which is available to authorized users. BioMed Central 2019-07-06 /pmc/articles/PMC6612195/ /pubmed/31312422 http://dx.doi.org/10.1186/s13227-019-0128-3 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
Wang, Huijia
Holland, Peter W. H.
Takahashi, Tokiharu
Gene profiling of head mesoderm in early zebrafish development: insights into the evolution of cranial mesoderm
title Gene profiling of head mesoderm in early zebrafish development: insights into the evolution of cranial mesoderm
title_full Gene profiling of head mesoderm in early zebrafish development: insights into the evolution of cranial mesoderm
title_fullStr Gene profiling of head mesoderm in early zebrafish development: insights into the evolution of cranial mesoderm
title_full_unstemmed Gene profiling of head mesoderm in early zebrafish development: insights into the evolution of cranial mesoderm
title_short Gene profiling of head mesoderm in early zebrafish development: insights into the evolution of cranial mesoderm
title_sort gene profiling of head mesoderm in early zebrafish development: insights into the evolution of cranial mesoderm
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6612195/
https://www.ncbi.nlm.nih.gov/pubmed/31312422
http://dx.doi.org/10.1186/s13227-019-0128-3
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