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Ancestral mesodermal reorganization and evolution of the vertebrate head

INTRODUCTION: The vertebrate head is characterized by unsegmented head mesoderm the evolutionary origin of which remains enigmatic. The head mesoderm is derived from the rostral part of the dorsal mesoderm, which is regionalized anteroposteriorly during gastrulation. The basal chordate amphioxus res...

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Autores principales: Onai, Takayuki, Aramaki, Toshihiro, Inomata, Hidehiko, Hirai, Tamami, Kuratani, Shigeru
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4657371/
https://www.ncbi.nlm.nih.gov/pubmed/26605074
http://dx.doi.org/10.1186/s40851-015-0030-3
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author Onai, Takayuki
Aramaki, Toshihiro
Inomata, Hidehiko
Hirai, Tamami
Kuratani, Shigeru
author_facet Onai, Takayuki
Aramaki, Toshihiro
Inomata, Hidehiko
Hirai, Tamami
Kuratani, Shigeru
author_sort Onai, Takayuki
collection PubMed
description INTRODUCTION: The vertebrate head is characterized by unsegmented head mesoderm the evolutionary origin of which remains enigmatic. The head mesoderm is derived from the rostral part of the dorsal mesoderm, which is regionalized anteroposteriorly during gastrulation. The basal chordate amphioxus resembles vertebrates due to the presence of somites, but it lacks unsegmented head mesoderm. Gastrulation in amphioxus occurs by simple invagination with little mesodermal involution, whereas in vertebrates gastrulation is organized by massive cell movements, such as involution, convergence and extension, and cell migration. RESULTS: To identify key developmental events in the evolution of the vertebrate head mesoderm, we compared anterior/posterior (A/P) patterning mechanisms of the dorsal mesoderm in amphioxus and vertebrates. The dorsal mesodermal genes gsc, bra, and delta are expressed in similar patterns in early embryos of both animals, but later in development, these expression domains become anteroposteriorly segregated only in vertebrates. Suppression of mesodermal involution in vertebrate embryos by inhibition of convergence and extension recapitulates amphioxus-like dorsal mesoderm formation. CONCLUSIONS: Reorganization of ancient mesoderm was likely involved in the evolution of the vertebrate head. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s40851-015-0030-3) contains supplementary material, which is available to authorized users.
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spelling pubmed-46573712015-11-24 Ancestral mesodermal reorganization and evolution of the vertebrate head Onai, Takayuki Aramaki, Toshihiro Inomata, Hidehiko Hirai, Tamami Kuratani, Shigeru Zoological Lett Research Article INTRODUCTION: The vertebrate head is characterized by unsegmented head mesoderm the evolutionary origin of which remains enigmatic. The head mesoderm is derived from the rostral part of the dorsal mesoderm, which is regionalized anteroposteriorly during gastrulation. The basal chordate amphioxus resembles vertebrates due to the presence of somites, but it lacks unsegmented head mesoderm. Gastrulation in amphioxus occurs by simple invagination with little mesodermal involution, whereas in vertebrates gastrulation is organized by massive cell movements, such as involution, convergence and extension, and cell migration. RESULTS: To identify key developmental events in the evolution of the vertebrate head mesoderm, we compared anterior/posterior (A/P) patterning mechanisms of the dorsal mesoderm in amphioxus and vertebrates. The dorsal mesodermal genes gsc, bra, and delta are expressed in similar patterns in early embryos of both animals, but later in development, these expression domains become anteroposteriorly segregated only in vertebrates. Suppression of mesodermal involution in vertebrate embryos by inhibition of convergence and extension recapitulates amphioxus-like dorsal mesoderm formation. CONCLUSIONS: Reorganization of ancient mesoderm was likely involved in the evolution of the vertebrate head. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s40851-015-0030-3) contains supplementary material, which is available to authorized users. BioMed Central 2015-11-09 /pmc/articles/PMC4657371/ /pubmed/26605074 http://dx.doi.org/10.1186/s40851-015-0030-3 Text en © Onai et al. 2015 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 Article
Onai, Takayuki
Aramaki, Toshihiro
Inomata, Hidehiko
Hirai, Tamami
Kuratani, Shigeru
Ancestral mesodermal reorganization and evolution of the vertebrate head
title Ancestral mesodermal reorganization and evolution of the vertebrate head
title_full Ancestral mesodermal reorganization and evolution of the vertebrate head
title_fullStr Ancestral mesodermal reorganization and evolution of the vertebrate head
title_full_unstemmed Ancestral mesodermal reorganization and evolution of the vertebrate head
title_short Ancestral mesodermal reorganization and evolution of the vertebrate head
title_sort ancestral mesodermal reorganization and evolution of the vertebrate head
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4657371/
https://www.ncbi.nlm.nih.gov/pubmed/26605074
http://dx.doi.org/10.1186/s40851-015-0030-3
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