Emergence of a geometric pattern of cell fates from tissue-scale mechanics in the Drosophila eye

  1. Kevin D Gallagher
  2. Madhav Mani  Is a corresponding author
  3. Richard W Carthew  Is a corresponding author
  1. Northwestern University, United States

Abstract

Pattern formation of biological structures involves the arrangement of different types of cells in an ordered spatial configuration. In this study, we investigate the mechanism of patterning the Drosophila eye epithelium into a precise triangular grid of photoreceptor clusters called ommatidia. Previous studies had led to a long-standing biochemical model whereby a reaction-diffusion process is templated by recently formed ommatidia to propagate a molecular prepattern across the eye. Here, we find that the templating mechanism is instead, mechanochemical in origin; newly born columns of differentiating ommatidia serve as a template to spatially pattern flows that move epithelial cells into position to form each new column of ommatidia. Cell flow is generated by a source and sink, corresponding to narrow zones of cell dilation and contraction respectively, that straddle the growing wavefront of ommatidia. The newly formed lattice grid of ommatidia cells are immobile, deflecting and focusing the flow of other cells. Thus, the self-organization of a regular pattern of cell fates in an epithelium is mechanically driven.

Data availability

All imaging data has been deposited in Dryad (doi:10.5061/dryad.f4qrfj6wp).

The following data sets were generated

Article and author information

Author details

  1. Kevin D Gallagher

    Department of Molecular Biosciences, Northwestern University, Evanston, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Madhav Mani

    Department of Molecular Biosciences, Northwestern University, Evanston, United States
    For correspondence
    madhav.mani@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
  3. Richard W Carthew

    Department of Molecular Biosciences, Northwestern University, Evanston, United States
    For correspondence
    r-carthew@northwestern.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0343-0156

Funding

National Institutes of Health (R35GM118144)

  • Richard W Carthew

National Science Foundation (1764421)

  • Madhav Mani
  • Richard W Carthew

Simons Foundation (597491)

  • Madhav Mani
  • Richard W Carthew

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

Copyright

© 2022, Gallagher et al.

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.

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  1. Kevin D Gallagher
  2. Madhav Mani
  3. Richard W Carthew
(2022)
Emergence of a geometric pattern of cell fates from tissue-scale mechanics in the Drosophila eye
eLife 11:e72806.
https://doi.org/10.7554/eLife.72806

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https://doi.org/10.7554/eLife.72806