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Species-specific contribution of volumetric growth and tissue convergence to posterior body elongation in vertebrates.

Accepted version
Peer-reviewed

Repository DOI


Type

Article

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Authors

Steventon, Benjamin  ORCID logo  https://orcid.org/0000-0001-7838-839X
Duarte, Fernando 
Lagadec, Ronan 
Mazan, Sylvie 
Nicolas, Jean-François 

Abstract

Posterior body elongation is a widespread mechanism propelling the generation of the metazoan body plan. The posterior growth model predicts that a posterior growth zone generates sufficient tissue volume to elongate the posterior body. However, there are energy supply-related differences between vertebrates in the degree to which growth occurs concomitantly with embryogenesis. By applying a multi-scalar morphometric analysis in zebrafish embryos, we show that posterior body elongation is generated by an influx of cells from lateral regions, by convergence-extension of cells as they exit the tailbud, and finally by a late volumetric growth in the spinal cord and notochord. Importantly, the unsegmented region does not generate additional tissue volume. Fibroblast growth factor inhibition blocks tissue convergence rather than volumetric growth, showing that a conserved molecular mechanism can control convergent morphogenesis through different cell behaviours. Finally, via a comparative morphometric analysis in lamprey, dogfish, zebrafish and mouse, we propose that elongation via posterior volumetric growth is linked to increased energy supply and is associated with an overall increase in volumetric growth and elongation.

Description

Keywords

Dogfish, Energy supply, Lamprey, Mouse, Multi-scalar morphometric analysis, Zebrafish, Animals, Body Patterning, Cell Movement, Cell Proliferation, Dogfish, Fibroblast Growth Factors, Lampreys, Mice, Notochord, Organogenesis, Signal Transduction, Species Specificity, Spinal Cord, Tail, Vertebrates, Zebrafish

Journal Title

Development

Conference Name

Journal ISSN

0950-1991
1477-9129

Volume Title

Publisher

The Company of Biologists
Sponsorship
Wellcome Trust (109408/Z/15/Z)
Jean-François Nicolas, Estelle Hirsinger: Core funding from the Institut Pasteur and Agence Nationale de la Recherche (ANR-10-BLAN-121801 DEVPROCESS). Estelle Hirsinger and Sylvie Mazan are from the Centre National de la Recherche Scientifique (CNRS). Benjamin Steventon was funded by the Agence Nationale de la Recherche (ANR- 10-BLAN-121801 DEVPROCESS), then a Roux fellowship (Institut Pasteur) then an AFM-Téléthon fellowship (number 16829).