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Second-order division in sectors as a prepattern for sensory organs in vertebrate development

Theory in Biosciences volume 141, pages 141–163 (2022)Cite this article

Abstract

We present in vivo observations of chicken embryo development which show that the early chicken embryo presents a principal structure made out of concentric rings and a secondary structure composed of radial sectors. During development, physical forces deform the main rings into axially directed, antero-posterior tubes, while the sectors roll up to form cylinders that are perpendicular to the antero-posterior axis. As a consequence, the basic structure of the chicken embryo is a series of encased antero-posterior tubes (gut, neural tube, body envelope, amnion, chorion) decorated with smaller orifices (ear duct, eye stalk, nasal duct, gills, mouth) forming at right angles to the main body axis. We argue that the second-order divisions reflect the early pattern of cell cleavage, and that the transformation of radial and orthoradial lines into a body with sensory organs is a generic biophysical mechanism more general than the chicken embryo.

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Notes

  1. In rays, growth of a very wide pectoral flap along the Dorso-Ventral edge is a secondary process during embryogenesis.

  2. The AP asymmetry in vertebrates stems from a polar distribution of vitellus in the oocyte, further amplified by the mechanism of sperm entry across the oocyte membrane. Here, we shall not discuss further this asymmetry.

  3. Called blastodisc in the case of chicken.

  4. The term archetype is referred as a different concept in the main text and in the glossary of Darwin’s Origin of species. In the main text, it is referred as the ancestral form, while in the glossary it is referred as: “ideal primitive form upon which all the beings of a group seem to be organised” (Darwin 1872).

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Acknowledgements

We thank Nicolas Chevalier for his interest and support and for a careful reading of the manuscript. We thank an anonymous reviewer for constructive remarks and relevant references.

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Authors and Affiliations

  1. Laboratoire Matière et Systèmes Complexes, UMR 7057, Université de Paris/CNRS, 10 rue Alice Domont et Léonie Duquet, 75013, Paris, France

    Vincent Fleury & Olivia Plateau

  2. UMR 1318, Institut Jean-Pierre Bourgin, INRAE, AgroParisTech, Université Paris-Saclay, 78000, Versailles, France

    Alexis Peaucelle

  3. Laboratoire Mécanismes Adaptatifs et Evolution, UMR 7179 MNHN, CNRS, CP 55, 57 rue Cuvier, 75231, Paris cedex 05, France

    Anick Abourachid & Olivia Plateau

  4. Département de Géosciences, Université de Fribourg, Ch. du Musée 6, 1700, Fribourg, Switzerland

    Olivia Plateau

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Correspondence to Vincent Fleury.

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Fleury, V., Peaucelle, A., Abourachid, A. et al. Second-order division in sectors as a prepattern for sensory organs in vertebrate development. Theory Biosci. 141, 141–163 (2022). https://doi.org/10.1007/s12064-021-00350-w

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  • DOI: https://doi.org/10.1007/s12064-021-00350-w