1. Developmental Biology
  2. Evolutionary Biology
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Evolutionary expansion of apical extracellular matrix is required for the elongation of cells in a novel structure

  1. Sarah Jacquelyn Smith
  2. Lance A Davidson
  3. Mark Rebeiz  Is a corresponding author
  1. University of Pittsburgh, United States
Research Article
  • Cited 4
  • Views 1,589
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Cite this article as: eLife 2020;9:e55965 doi: 10.7554/eLife.55965

Abstract

One of the fundamental gaps in our knowledge of how novel anatomical structures evolve is understanding the origins of the morphogenetic processes that form these features. Here, we traced the cellular development of a recently evolved morphological novelty, the posterior lobe of D. melanogaster. We found that this genital outgrowth forms through extreme increases in epithelial cell height. By examining the apical extracellular matrix (aECM), we also uncovered a vast matrix associated with the developing genitalia of lobed and non-lobed species. The aECM protein Dumpy is spatially expanded in lobe-forming species, connecting the posterior lobe to the ancestrally derived aECM network. Further analysis demonstrated that Dumpy attachments are necessary for cell height increases during posterior lobe development. We propose that the aECM presents a rich reservoir for generating morphological novelty and highlights a yet unseen role for aECM in regulating extreme cell height.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 2, 6, 7

Article and author information

Author details

  1. Sarah Jacquelyn Smith

    Department of Biological Sciences, University of Pittsburgh, Pittsburgh, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1469-1821
  2. Lance A Davidson

    Department of Bioengineering, University of Pittsburgh, Pittsburgh, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2956-0437
  3. Mark Rebeiz

    Department of Biological Sciences, University of Pittsburgh, Pittsburgh, United States
    For correspondence
    rebeiz@pitt.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5731-5570

Funding

National Institutes of Health (GM107387)

  • Mark Rebeiz

National Institutes of Health (HD044750)

  • Lance A Davidson

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

Reviewing Editor

  1. Antonis Rokas, Vanderbilt University, United States

Publication history

  1. Received: February 12, 2020
  2. Accepted: April 6, 2020
  3. Accepted Manuscript published: April 27, 2020 (version 1)
  4. Version of Record published: June 2, 2020 (version 2)

Copyright

© 2020, Smith 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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