Global morphogenetic flow is accurately predicted by the spatial distribution of myosin motors

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Cite as: eLife 2018;7:e27454 doi: 10.7554/eLife.27454

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Abstract

During embryogenesis tissue layers undergo morphogenetic flow rearranging and folding into specific shapes. While developmental biology has identified key genes and local cellular processes, global coordination of tissue remodeling at the organ scale remains unclear. Here we combine in toto light-sheet microscopy of the Drosophila embryo with quantitative analysis and physical modeling to relate cellular flow with the patterns of force generation during the gastrulation process. We find that the complex spatio-temporal flow pattern can be predicted from the measured meso-scale myosin density and anisotropy using a simple effective viscous model of the tissue, achieving close to 90% accuracy with one time dependent and two constant parameters. Our analysis uncovers the importance of a) spatial modulation of myosin distribution on the scale of the embryo and b) the non-locality of its effect due to mechanical interaction of cells, demonstrating the need for the global perspective in the study of morphogenetic flow.

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Author details

Sebastian J Streichan

Kavli Institute for Theoretical Physics, University of California, Santa Barbara, Santa Barbara, United States

For correspondence
streicha@kitp.ucsb.edu

Competing interests
The authors declare that no competing interests exist.
Matthew Lefebvre

Department of Molecular Biology, Princeton University, Princeton, United States

Competing interests
The authors declare that no competing interests exist.
Nicholas Noll

Department of Physics, University of California, Santa Barbara, Santa Barbara, United States

Competing interests
The authors declare that no competing interests exist.

0000-0003-1698-7500
Eric F Wieschaus

Department of Molecular Biology, Princeton University, Princeton, United States

Competing interests
The authors declare that no competing interests exist.

0000-0002-0727-3349
Boris I Shraiman

Kavli Institute for Theoretical Physics, University of California, Santa Barbara, Santa Barbara, United States

For correspondence
shraiman@kitp.ucsb.edu

Competing interests
The authors declare that no competing interests exist.

0000-0003-0886-8990

Funding

National Science Foundation (PHY-1220616)

Boris I Shraiman

Howard Hughes Medical Institute

Eric F Wieschaus

National Institutes of Health (NICHD 1K99HD088708)

Sebastian J Streichan

Gordon and Betty Moore Foundation (GBMF #2919)

Boris I Shraiman

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

Frank Jülicher, Max-Planck-Institute for the Physics of Complex Systems, Germany

Publication history

Received: April 5, 2017
Accepted: January 20, 2018
Accepted Manuscript published: February 9, 2018 (version 1)
Version of Record published: March 8, 2018 (version 2)

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.