Cell dynamics underlying oriented growth of the Drosophila wing imaginal disc

Author:

Dye Natalie A.1ORCID,Popović Marko2,Spannl Stephanie1,Etournay Raphaël13ORCID,Kainmüller Dagmar14,Ghosh Suhrid1,Myers Eugene W.15ORCID,Jülicher Frank25,Eaton Suzanne16ORCID

Affiliation:

1. Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, 01309 Dresden, Germany

2. Max Planck Institute for the Physics of Complex Systems, Noethnitzer Strasse 38, 01187 Dresden, Germany

3. Unité de Génétique et Physiologie de l'Audition, Institut Pasteur, 75015 Paris, France

4. Janelia Farm Research Campus, 19700 Helix Dr. Ashburn, VA 20147, USA

5. Center for Systems Biology Dresden, Pfotenhauerstrasse 108, 01309 Dresden, Germany

6. Biotechnologisches Zentrum, Technische Universität Dresden, Tatzberg 47/49, 01309 Dresden, Germany

Abstract

Quantitative analysis of the dynamic cellular mechanisms shaping the Drosophila wing during its larval growth phase has been limited, impeding our ability to understand how morphogen patterns regulate tissue shape. Such analysis requires imaging explants under conditions that maintain both growth and patterning, as well as methods to quantify how much cellular behaviors change tissue shape. Here, we demonstrate a key requirement for the steroid hormone 20-hydroxyecdysone (20E) in the maintenance of numerous patterning systems in vivo and in explant culture. We find that low concentrations of 20E support prolonged proliferation in explanted wing discs in the absence of insulin, incidentally providing novel insight into the hormonal regulation of imaginal growth. We use 20E-containing media to directly observe growth and apply recently developed methods for quantitatively decomposing tissue shape changes into cellular contributions. We discover that while cell divisions drive tissue expansion along one axis, their contribution to expansion along the orthogonal axis is cancelled by cell rearrangements and cell shape changes. This finding raises the possibility that anisotropic mechanical constraints contribute to growth orientation in the wing disc.

Funder

Max-Planck-Gesellschaft

FP7 People: Marie-Curie Actions

European Molecular Biology Organization

Bundesministerium für Bildung und Forschung

Deutsche Forschungsgemeinschaft

Publisher

The Company of Biologists

Subject

Developmental Biology,Molecular Biology

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