Temporal and cellular requirements for Fms signaling during zebrafish adult pigment pattern development.
Ectothermic vertebrates exhibit a diverse array of adult pigment patterns. A common element of these patterns is alternating dark and light stripes each comprising different classes of neural crest-derived pigment cells. In the zebrafish, Danio rerio, alternating horizontal stripes of black melanophores and yellow xanthophores are a prominent feature of the adult pigment pattern. In fms mutant zebrafish, however, xanthophores fail to develop and melanophore stripes are severely disrupted. fms encodes a type III receptor tyrosine kinase expressed by xanthophores and their precursors and is the closest known homologue of kit, which has long been studied for roles in pigment pattern development in amniotes. In this study we assess the cellular and temporal requirements for Fms activity in promoting adult pigment pattern development. By transplanting cells between fms mutants and either wild-type or nacre mutant zebrafish, we show that fms acts autonomously to the xanthophore lineage in promoting the striped arrangement of adult melanophores. To identify critical periods for fms activity, we isolated temperature sensitive alleles of fms and performed reciprocal temperature shift experiments at a range of stages from embryo to adult. These analyses demonstrate that Fms is essential for maintaining cells of the xanthophore lineage as well as maintaining the organization of melanophore stripes throughout development. Finally, we show that restoring Fms activity even at late larval stages allows essentially complete recovery of xanthophores and the development of a normal melanophore stripe pattern. Our findings suggest that fms is not required for establishing a population of precursor cells during embryogenesis but is required for recruiting pigment cell precursors to xanthophore fates, with concomitant effects on melanophore organization.
Parichy
David M
DM
Section of Integrative Biology, Section of Molecular, Cell and Developmental Biology, Institute for Cellular and Molecular Biology, University of Texas at Austin, 1 University Station C0930, Austin, TX 78712, USA. dparichy@mail.utexas.edu
Turner
Jessica M
JM
D000483:Alleles; D000818:Animals; D019521:Body Patterning; D016923:Cell Death / Q000502:physiology; D017690:Cell Transplantation; D002678:Chimera / Q000502:physiology; D002856:Chromatophores / Q000378:metabolism*; D004268:DNA-Binding Proteins / Q000235:genetics / Q000378:metabolism; D004625:Embryo, Nonmammalian / Q000033:anatomy & histology / Q000502:physiology; D018507:Gene Expression Regulation, Developmental; D005838:Genotype; D020287:In Situ Nick-End Labeling; D051739:Microphthalmia-Associated Transcription Factor; D009024:Morphogenesis; D009154:Mutation; D010641:Phenotype; D010858:Pigmentation / Q000235:genetics / Q000502:physiology*; D016186:Receptor, Macrophage Colony-Stimulating Factor / Q000235:genetics / Q000378:metabolism*; D015398:Signal Transduction / Q000502:physiology*; D013696:Temperature; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism; D015027:Zebrafish / Q000033:anatomy & histology / Q000235:genetics / Q000254:growth & development* / Q000502:physiology; D029961:Zebrafish Proteins
D004268:DNA-Binding Proteins; D051739:Microphthalmia-Associated Transcription Factor; D014157:Transcription Factors; D029961:Zebrafish Proteins; C497237:mitfa protein, zebrafish; D016186:Receptor, Macrophage Colony-Stimulating Factor