title: 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 adult form.
authors.affiliation: Department of Biology, University of Washington, Seattle, United States.
authors.forename: Dae Seok
authors.initials: DS
authors.lastname: Eom
authors.affiliation: Department of Biology, University of Washington, Seattle, United States.
authors.forename: Emily J
authors.identifier: http://orcid.org/0000-0003-0428-4357
authors.initials: EJ
authors.lastname: Bain
authors.affiliation: Department of Biology, University of Washington, Seattle, United States.
authors.forename: Larissa B
authors.initials: LB
authors.lastname: Patterson
authors.affiliation: Department of Biology, University of Washington, Seattle, United States.
authors.forename: Megan E
authors.initials: ME
authors.lastname: Grout
authors.affiliation: Department of Biology, University of Washington, Seattle, United States.|Institute for Stem Cell and Regenerative Medicine, University of Washington, Seattle, United States.
authors.forename: David M
authors.initials: DM
authors.lastname: Parichy
mesh_terms: D000818:Animals; D002450:Cell Communication; D003530:Cyprinidae / Q000235:genetics / Q000502:physiology*; D005786:Gene Expression Regulation; D008547:Melanophores / Q000502:physiology*; D010860:Pigments, Biological / Q000378:metabolism*; D022142:Secretory Vesicles / Q000378:metabolism*; D015398:Signal Transduction
chemical_list: D010860:Pigments, Biological
keywords: Notch-Delta; cell signaling; developmental biology; evolution; evolutionary biology; genomics; long-distance communication; melanocyte; melanophore; neural crest; pigment pattern; stem cells; xanthophore; zebrafish