Spatiotemporal variation in cell proliferation patterns during arthropod axial elongation

Abstract 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. Thi...

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Main Authors: Rodrigo E. Cepeda, John B. Terraza, Renato V. Pardo, Valentina Núñez-Pascual, Marco Mundaca-Escobar, Andres F. Sarrazin
Format: Article
Language:English
Published: Nature Publishing Group 2021-01-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-020-79373-0
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spelling doaj-8363db377acf4a2586d3889be95de2e92021-01-17T12:45:39ZengNature Publishing GroupScientific Reports2045-23222021-01-0111111310.1038/s41598-020-79373-0Spatiotemporal variation in cell proliferation patterns during arthropod axial elongationRodrigo E. Cepeda0John B. Terraza1Renato V. Pardo2Valentina Núñez-Pascual3Marco Mundaca-Escobar4Andres F. Sarrazin5Instituto de Química, Pontificia Universidad Católica de ValparaísoInstituto de Química, Pontificia Universidad Católica de ValparaísoInstituto de Química, Pontificia Universidad Católica de ValparaísoInstituto de Química, Pontificia Universidad Católica de ValparaísoInstituto de Química, Pontificia Universidad Católica de ValparaísoInstituto de Química, Pontificia Universidad Católica de ValparaísoAbstract 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.https://doi.org/10.1038/s41598-020-79373-0
collection DOAJ
language English
format Article
sources DOAJ
author Rodrigo E. Cepeda
John B. Terraza
Renato V. Pardo
Valentina Núñez-Pascual
Marco Mundaca-Escobar
Andres F. Sarrazin
spellingShingle Rodrigo E. Cepeda
John B. Terraza
Renato V. Pardo
Valentina Núñez-Pascual
Marco Mundaca-Escobar
Andres F. Sarrazin
Spatiotemporal variation in cell proliferation patterns during arthropod axial elongation
Scientific Reports
author_facet Rodrigo E. Cepeda
John B. Terraza
Renato V. Pardo
Valentina Núñez-Pascual
Marco Mundaca-Escobar
Andres F. Sarrazin
author_sort Rodrigo E. Cepeda
title Spatiotemporal variation in cell proliferation patterns during arthropod axial elongation
title_short 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_sort spatiotemporal variation in cell proliferation patterns during arthropod axial elongation
publisher Nature Publishing Group
series Scientific Reports
issn 2045-2322
publishDate 2021-01-01
description Abstract 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.
url https://doi.org/10.1038/s41598-020-79373-0
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