Abstract

The zebrafish adult pigment pattern has emerged as a useful model for understanding the development and evolution of adult form as well as pattern-forming mechanisms more generally. In this species, a series of horizontal melanophore stripes arises during the larval-to-adult transformation, but the genetic and cellular bases for stripe formation remain largely unknown. Here, we show that the seurat mutant phenotype, consisting of an irregular spotted pattern, arises from lesions in the gene encoding Immunoglobulin superfamily member 11 (Igsf11). We find that Igsf11 is expressed by melanophores and their precursors, and we demonstrate by cell transplantation and genetic rescue that igsf11 functions autonomously to this lineage in promoting adult stripe development. Further analyses of cell behaviors in vitro, in vivo, and in explant cultures ex vivo demonstrate that Igsf11 mediates adhesive interactions and that mutants for igsf11 exhibit defects in both the migration and survival of melanophores and their precursors. These findings identify the first in vivo requirements for igsf11 as well as the first instance of an immunoglobulin superfamily member functioning in pigment cell development and patterning. Our results provide new insights into adult pigment pattern morphogenesis and how cellular interactions mediate pattern formation.

Highlights

  • Pigment patterns are among the most striking of vertebrate traits and nowhere are these patterns more diverse than in teleost fishes [1,2,3,4]

  • We show that one such mutant, seurat, named for the 19th century pointillist, George Seurat, exhibits lesions in the gene encoding a classical cell adhesion molecule (CAM) of the immunoglobulin superfamily, Immunoglobulin superfamily member 11 (Igsf11)

  • We find that Igsf11 mediates cell adhesion and promotes the migration and survival of melanophores and their precursors during adult stripe formation

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Summary

Introduction

Pigment patterns are among the most striking of vertebrate traits and nowhere are these patterns more diverse than in teleost fishes [1,2,3,4]. The zebrafish adult pigment pattern comprises a series of dark horizontal stripes that include black melanophores, alternating with lighter ‘‘interstripes’’ that include yellow–orange xanthophores; a third class of pigment cells, the iridescent iridophore occurs in both stripes and interstripes. Development of this pattern occurs during the larval-to-adult transformation between ,2–4 weeks post-fertilization [9,10,11,12]. Latent precursor cells of presumptive neural crest origin migrate from peripheral nerves and possibly other locations to the hypodermis, between the epidermis and the myotome, where differentiation occurs and the initially intermingled cells organize into stripes [10,13]

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