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Spatiotemporal variation in cell proliferation patterns during arthropod axial elongation

An elongated and segmented body plan is a common morphological characteristic of all arthropods and is probably responsible for their high adaptation ability to diverse environments. Most arthropods form their bodies by progressively adding segments, resembling vertebrate somitogenesis. This sequent...

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Autores principales: Cepeda, Rodrigo E., Terraza, John B., Pardo, Renato V., Núñez-Pascual, Valentina, Mundaca-Escobar, Marco, Sarrazin, Andres F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7801698/
https://www.ncbi.nlm.nih.gov/pubmed/33431947
http://dx.doi.org/10.1038/s41598-020-79373-0
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author Cepeda, Rodrigo E.
Terraza, John B.
Pardo, Renato V.
Núñez-Pascual, Valentina
Mundaca-Escobar, Marco
Sarrazin, Andres F.
author_facet Cepeda, Rodrigo E.
Terraza, John B.
Pardo, Renato V.
Núñez-Pascual, Valentina
Mundaca-Escobar, Marco
Sarrazin, Andres F.
author_sort Cepeda, Rodrigo E.
collection PubMed
description An elongated and segmented body plan is a common morphological characteristic of all arthropods and is probably responsible for their high adaptation ability to diverse environments. Most arthropods form their bodies by progressively adding segments, resembling vertebrate somitogenesis. This sequential segmentation relies on a molecular clock that operates in the posterior region of the elongating embryo that combines dynamically with cellular behaviors and tissue rearrangements, allowing the extension of the developing body along its main embryonic axis. Even though the molecular mechanisms involved in elongation and segment formation have been found to be conserved in a considerable degree, cellular processes such as cell division are quite variable between different arthropods. In this study, we show that cell proliferation in the beetle Tribolium castaneum has a nonuniform spatiotemporal patterning during axial elongation. We found that dividing cells are preferentially oriented along the anterior–posterior axis, more abundant and posteriorly localized during thoracic segments formation and that this cell proliferation peak was triggered at the onset of axis elongation. This raise in cell divisions, in turn, was correlated with an increase in the elongation rate, but not with changes in cell density. When DNA synthesis was inhibited over this period, both the area and length of thoracic segments were significantly reduced but not of the first abdominal segment. We discuss the variable participation that different cell division patterns and cell movements may have on arthropod posterior growth and their evolutionary contribution.
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spelling pubmed-78016982021-01-13 Spatiotemporal variation in cell proliferation patterns during arthropod axial elongation Cepeda, Rodrigo E. Terraza, John B. Pardo, Renato V. Núñez-Pascual, Valentina Mundaca-Escobar, Marco Sarrazin, Andres F. Sci Rep Article An elongated and segmented body plan is a common morphological characteristic of all arthropods and is probably responsible for their high adaptation ability to diverse environments. Most arthropods form their bodies by progressively adding segments, resembling vertebrate somitogenesis. This sequential segmentation relies on a molecular clock that operates in the posterior region of the elongating embryo that combines dynamically with cellular behaviors and tissue rearrangements, allowing the extension of the developing body along its main embryonic axis. Even though the molecular mechanisms involved in elongation and segment formation have been found to be conserved in a considerable degree, cellular processes such as cell division are quite variable between different arthropods. In this study, we show that cell proliferation in the beetle Tribolium castaneum has a nonuniform spatiotemporal patterning during axial elongation. We found that dividing cells are preferentially oriented along the anterior–posterior axis, more abundant and posteriorly localized during thoracic segments formation and that this cell proliferation peak was triggered at the onset of axis elongation. This raise in cell divisions, in turn, was correlated with an increase in the elongation rate, but not with changes in cell density. When DNA synthesis was inhibited over this period, both the area and length of thoracic segments were significantly reduced but not of the first abdominal segment. We discuss the variable participation that different cell division patterns and cell movements may have on arthropod posterior growth and their evolutionary contribution. Nature Publishing Group UK 2021-01-11 /pmc/articles/PMC7801698/ /pubmed/33431947 http://dx.doi.org/10.1038/s41598-020-79373-0 Text en © The Author(s) 2021 Open Access This 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/.
spellingShingle Article
Cepeda, Rodrigo E.
Terraza, John B.
Pardo, Renato V.
Núñez-Pascual, Valentina
Mundaca-Escobar, Marco
Sarrazin, Andres F.
Spatiotemporal variation in cell proliferation patterns during arthropod axial elongation
title Spatiotemporal variation in cell proliferation patterns during arthropod axial elongation
title_full Spatiotemporal variation in cell proliferation patterns during arthropod axial elongation
title_fullStr Spatiotemporal variation in cell proliferation patterns during arthropod axial elongation
title_full_unstemmed Spatiotemporal variation in cell proliferation patterns during arthropod axial elongation
title_short Spatiotemporal variation in cell proliferation patterns during arthropod axial elongation
title_sort spatiotemporal variation in cell proliferation patterns during arthropod axial elongation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7801698/
https://www.ncbi.nlm.nih.gov/pubmed/33431947
http://dx.doi.org/10.1038/s41598-020-79373-0
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