Pigment pattern

Overview

Pigmentation is one of the most striking vertebrate traits and is a classic and enduring system for studying cellular mechanisms of pattern formation, differentiation and morphogenesis.  We use the diversity of pigment patterns among zebrafish mutants and closely related species to dissect how these patterns form and how the underlying genes and cell behaviors evolve.

Our studies have identified essential roles for interactions among pigment cell classes and between pigment cells and their environment. Mutational analyses of zebrafish, Danio rerio, have allowed us to identify genes required for these interactions, whereas genetic and other approaches have identified pathways that contribute to interspecific pattern differences.

Current efforts aim to identify new genes and cell behaviors responsible for stripe orientation and boundary formation in zebrafish, and to uncover changes in gene regulatory networks between species. Approaches include genomics, genetics and transgenesis, and time-lapse imaging using zebrafish and other danios.

 

 

 

 

 

Diverse pattern phenotypes of Danio species (A), hybrids (B) and zebrafish mutants (C,D).

Pattern establishment and reiteration

The zebrafish pigment pattern includes dark stripes of melanophores that alternate with light stripes of iridescent iridophores and yellow-orange xanthophores.

We showed that establishment of this pattern depends on iridophores, which specify the locations and orientations of melanophore stripes and promote the differentiation of xanthophores in the interstripe by expressing the xanthogenic growth factor Csf1. The requirements for iridophores are revealed by defects in pattern when we ablate these cells transgenically.

As zebrafish grow, more interstripes and stripes are added dorsally and ventrally. During this process iridophores travel through the stripes to emerge on the other side, where they are required for stripe termination;  without iridophores, stripes are too wide.

  • Patterson et al. 2014.  Nature Communications 5:6299.   PDF   WEB
  • Patterson & Parichy. 2013. PLoS Genetics 9:e100356.    PDF   WEB

irid intact

irid ablated

Stripes and interstripes

stripe

interstripe

stripe

mel

irid

xan

Stripes are defective when iridophores are ablated mosaically

Adult pattern development (7–30 d)

Iridophores (arrows and blue bars) spread  through melanophore stripes

Pattern implementation and maintenance

Once the initial or reiterated pattern is specified by iridophores, interactions between melanophores and xanthophores are essential for pattern implementation: when xanthophores are ablated, normal stripes fail to form, yet they are rescued if the two cell types are juxtaposed in chimeras generated by cell transplantation. These interactions are also required for later maintenance of stripes in the adult, as revealed by experiments using a temperature-sensitive allele of the Csf1 receptor, which is expressed and required by xanthophores.

  Our most recent work has further identified novel mechanisms of long-distance communication between  xanthophore and melanophore lineages that are required for stripe formation, including a role for macrophages in relaying specialized cellular projections and signals.

Late activation of Csr1r allows xanthophore  development and  stripe recovery

  • Eom & Parichy. 2017. Science DOI: 10.1126/science.aal2745.   PDF   VIDEOS (115 Mb zip)   WEB
  • Eom et al. 2015. eLife 10.7554/eLife.12401.  PDF   WEB
  • McMenamin et al. 2014. Science 345:1358–1361.   PDF   WEB
  • Parichy & Turner. 2003. Development 130:817–833.   PDF   WEB

Xanthoblast projections ("airinemes") interact with melanophores

Blocking Csf1r activity causes xanthophore death and stripe degeneration

Xanthoblast airineme  delivers membrane-bound cargo to melanophore

Xanthoblast airineme (green) is picked up by macrophage (blue) and delivered to a melanophore (magenta)

  • Eom et al. 2015. eLife 10.7554/eLife.12401.      PDF   WEB
  • Patterson et al. 2014. Nature Communications 5:6299.  PDF   WEB
  • Mills et al. 2007. Development 134:1081–1090.   PDF   WEB
  • Quigley et al. 2005. Development 132:89–104.   PDF   WEB

zebrafish

++Csf1 late

++Csf1 early

pearl

Species differences in airineme  extension frequency that result from evolutionary changes in xanthophore differentiation timing

Pattern evolution

We are studying the many pigment patterns of Danio species to understand how changes in the nature and context of pigment cells interactions and other factors have contributed to evolutionary diversification. Recent studies have focused on pearl danio, Danio albolineatus, in which pigment cell classes are intermingled and stripes fail to develop. We showed that cis-regulatory changes have resulted in earlier, broader and higher expression of Csf1, which causes the development of excess xanthophores compared to zebrafish. Driving Csf1 similarly in zebrafish recapitulates the pearl danio pattern! So changing the context of pigment cell interactions can generate a very different pattern, even without changing the nature of the interactions themselves.

Current projects include

  • genomic analyses of the pigment cell "interactome" and how it evolves
  • visualization of pigment cell interactions and signaling by super-resolution imaging
  • mechanisms of iridophore morphogenesis and signaling to melanophores
  • genetics and development of species differences across Danio

Pattern formation in Danio dangila proceeds through stripes to a chain-link arrangement

PARICHY LAB

CONTACT

 

 

Department of Biology

University of Virginia

Physical Life Sciences Building

Charlottesville VA 22904

206.221.5007

 

 

 

Copyright © 2016-2017 DM Parichy

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