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The complete dorsal structure is formed from only the blastocoel roof of Xenopus blastula: insight into the gastrulation movement evolutionarily conserved among chordates

Gastrulation is a critical event whose molecular mechanisms are thought to be conserved among vertebrates. However, the morphological movement during gastrulation appears to be divergent across species, making it difficult to discuss the evolution of the process. Previously, we proposed a novel amph...

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Autores principales: Sato, Yuki, Narasaki, Izumi, Kunimoto, Takuya, Moriyama, Yuki, Hashimoto, Chikara
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Berlin Heidelberg 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10239386/
https://www.ncbi.nlm.nih.gov/pubmed/36933042
http://dx.doi.org/10.1007/s00427-023-00701-1
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author Sato, Yuki
Narasaki, Izumi
Kunimoto, Takuya
Moriyama, Yuki
Hashimoto, Chikara
author_facet Sato, Yuki
Narasaki, Izumi
Kunimoto, Takuya
Moriyama, Yuki
Hashimoto, Chikara
author_sort Sato, Yuki
collection PubMed
description Gastrulation is a critical event whose molecular mechanisms are thought to be conserved among vertebrates. However, the morphological movement during gastrulation appears to be divergent across species, making it difficult to discuss the evolution of the process. Previously, we proposed a novel amphibian gastrulation model, the “subduction and zippering (S&Z) model”. In this model, the organizer and the prospective neuroectoderm are originally localized in the blastula’s blastocoel roof, and these embryonic regions move downward to make physical contact of their inner surfaces with each other at the dorsal marginal zone. The developmental stage when contact between the head organizer and the anterior-most neuroectoderm is established is called “anterior contact establishment (ACE).” After ACE, the A-P body axis elongates posteriorly. According to this model, the body axis is derived from limited regions of the dorsal marginal zone at ACE. To investigate this possibility, we conducted stepwise tissue deletions using Xenopus laevis embryos and revealed that the dorsal one-third of the marginal zone had the ability to form the complete dorsal structure by itself. Furthermore, a blastocoel roof explant of the blastula, which should contain the organizer and the prospective neuroectoderm in the S&Z model, autonomously underwent gastrulation and formed the complete dorsal structure. Collectively, these results are consistent with the S&Z gastrulation model and identify the embryonic region sufficient for construction of the complete dorsal structure. Finally, by comparing amphibian gastrulation to gastrulation of protochordates and amniotes, we discuss the gastrulation movement evolutionarily conserved among chordates. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00427-023-00701-1.
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spelling pubmed-102393862023-06-05 The complete dorsal structure is formed from only the blastocoel roof of Xenopus blastula: insight into the gastrulation movement evolutionarily conserved among chordates Sato, Yuki Narasaki, Izumi Kunimoto, Takuya Moriyama, Yuki Hashimoto, Chikara Dev Genes Evol Research Gastrulation is a critical event whose molecular mechanisms are thought to be conserved among vertebrates. However, the morphological movement during gastrulation appears to be divergent across species, making it difficult to discuss the evolution of the process. Previously, we proposed a novel amphibian gastrulation model, the “subduction and zippering (S&Z) model”. In this model, the organizer and the prospective neuroectoderm are originally localized in the blastula’s blastocoel roof, and these embryonic regions move downward to make physical contact of their inner surfaces with each other at the dorsal marginal zone. The developmental stage when contact between the head organizer and the anterior-most neuroectoderm is established is called “anterior contact establishment (ACE).” After ACE, the A-P body axis elongates posteriorly. According to this model, the body axis is derived from limited regions of the dorsal marginal zone at ACE. To investigate this possibility, we conducted stepwise tissue deletions using Xenopus laevis embryos and revealed that the dorsal one-third of the marginal zone had the ability to form the complete dorsal structure by itself. Furthermore, a blastocoel roof explant of the blastula, which should contain the organizer and the prospective neuroectoderm in the S&Z model, autonomously underwent gastrulation and formed the complete dorsal structure. Collectively, these results are consistent with the S&Z gastrulation model and identify the embryonic region sufficient for construction of the complete dorsal structure. Finally, by comparing amphibian gastrulation to gastrulation of protochordates and amniotes, we discuss the gastrulation movement evolutionarily conserved among chordates. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00427-023-00701-1. Springer Berlin Heidelberg 2023-03-18 2023 /pmc/articles/PMC10239386/ /pubmed/36933042 http://dx.doi.org/10.1007/s00427-023-00701-1 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research
Sato, Yuki
Narasaki, Izumi
Kunimoto, Takuya
Moriyama, Yuki
Hashimoto, Chikara
The complete dorsal structure is formed from only the blastocoel roof of Xenopus blastula: insight into the gastrulation movement evolutionarily conserved among chordates
title The complete dorsal structure is formed from only the blastocoel roof of Xenopus blastula: insight into the gastrulation movement evolutionarily conserved among chordates
title_full The complete dorsal structure is formed from only the blastocoel roof of Xenopus blastula: insight into the gastrulation movement evolutionarily conserved among chordates
title_fullStr The complete dorsal structure is formed from only the blastocoel roof of Xenopus blastula: insight into the gastrulation movement evolutionarily conserved among chordates
title_full_unstemmed The complete dorsal structure is formed from only the blastocoel roof of Xenopus blastula: insight into the gastrulation movement evolutionarily conserved among chordates
title_short The complete dorsal structure is formed from only the blastocoel roof of Xenopus blastula: insight into the gastrulation movement evolutionarily conserved among chordates
title_sort complete dorsal structure is formed from only the blastocoel roof of xenopus blastula: insight into the gastrulation movement evolutionarily conserved among chordates
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10239386/
https://www.ncbi.nlm.nih.gov/pubmed/36933042
http://dx.doi.org/10.1007/s00427-023-00701-1
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