Long-distance communication by specialized cellular projections during pigment pattern development and evolution

Abstract

Changes in gene activity are essential for evolutionary diversification. Yet, elucidating the cellular behaviors that underlie modifications to adult form remains a profound challenge. We use neural crest-derived adult pigmentation of zebrafish and pearl danio to uncover cellular bases for alternative pattern states. We show that stripes in zebrafish require a novel class of thin, fast cellular projection to promote Delta-Notch signaling over long distances from cells of the xanthophore lineage to melanophores. Projections depended on microfilaments and microtubules, exhibited meandering trajectories, and stabilized on target cells to which they delivered membraneous vesicles. By contrast, the uniformly patterned pearl danio lacked such projections, concomitant with Colony stimulating factor 1-dependent changes in xanthophore differentiation that likely curtail signaling available to melanophores. Our study reveals a novel mechanism of cellular communication, roles for differentiation state heterogeneity in pigment cell interactions, and an unanticipated morphogenetic behavior contributing to a striking difference in form.

Article and author information

Author details

  1. Dae Seok Eom

    Department of Biology, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Emily J Bain

    Department of Biology, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Larissa B Patterson

    Department of Biology, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Megan E Grout

    Department of Biology, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. David M Parichy

    Department of Biology, University of Washington, Seattle, United States
    For correspondence
    dparichy@u.washington.edu
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Robb Krumlauf, Stowers Institute for Medical Research, United States

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All animals were handled according to approved institutional animal care and use committee (IACUC) protocol (#4094) of the University of Washington.

Version history

  1. Received: October 18, 2015
  2. Accepted: December 23, 2015
  3. Accepted Manuscript published: December 23, 2015 (version 1)
  4. Version of Record published: February 15, 2016 (version 2)

Copyright

© 2015, Eom 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. Dae Seok Eom
  2. Emily J Bain
  3. Larissa B Patterson
  4. Megan E Grout
  5. David M Parichy
(2015)
Long-distance communication by specialized cellular projections during pigment pattern development and evolution
eLife 4:e12401.
https://doi.org/10.7554/eLife.12401

Share this article

https://doi.org/10.7554/eLife.12401

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