Deconstructing evolution of adult phenotypes: Genetic analyses of kit reveal homology and evolutionary novelty during adult pigment pattern development of Danio fishes

Development

Volumn 134, Issue 6, 2007, Pages 1081-1090

  Mills, Margaret G ^a   Nuckels, Richard J ^a   Parichy, David M ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Evolution; Kit; Melanophore; Morphogenesis; Pigment pattern; Zebrafish

Indexed keywords

MUTANT PROTEIN; PROTEIN TYROSINE KINASE; STEM CELL FACTOR;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; EVOLUTIONARY DEVELOPMENTAL BIOLOGY; EVOLUTIONARY HOMOLOGY; FEMALE; GENETIC ANALYSIS; GENETIC CONSERVATION; MALE; MELANOPHORE; METAMORPHOSIS; MOLECULAR DYNAMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PIGMENTATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SPECIES DIFFERENCE; WILD TYPE; ZEBRA FISH;

ANIMALS; BODY PATTERNING; EVOLUTION; MELANOPHORES; METAMORPHOSIS, BIOLOGICAL; MUTATION; PHENOTYPE; PIGMENTATION; PROTO-ONCOGENE PROTEINS C-KIT; REGENERATION; ZEBRAFISH;

DANIO; DANIO ALBOLINEATUS; DANIO RERIO; PISCES;

EID: 34247379144     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02799     Document Type: Article

References (54)

1. Aoki, H., Motohashi, T., Yoshimura, N., Yamazaki, H., Yamane, T.,, Panthier, J. J. and Kunisada, T. (2005). Cooperative and indispensable roles of endothelin 3 and KIT signalings in melanocyte development. Dev. Dyn. 233, 407-417.
2. Asai, R., Taguchi, E., Kume, Y., Saito, M. and Kondo, S. (1999). Zebrafish leopard gene as a component of the putative reaction-diffusion system. Mech. Dev. 89, 87-92.
3. lacZ mouse embryos. Development 122, 3023-3033.
4. Besmer, P., Manova, K., Duttlinger, R., Huang, E. J., Packer, A., Gyssler, C. and Bachvarova, R. F. (1993). The kit-ligand (steel factor) and its receptor c-kit/W: pleiotropic roles in gametogenesis and melanogenesis. Dev Suppl. 1993, 125-137.
5. Braasch, I., Salzburger, W. and Meyer, A. (2006). Asymmetric evolution in two fish-specifically duplicated receptor tyrosine kinase paralogons involved in teleost coloration. Mol. Biol. Evol. 23, 1192-1202.
6. Chapman, S. C., Lawson, A., Macarthur, W. C., Wiese, R. J., Loechel, R. H., Burgos-Trinidad, M., Wakefield, J. K., Ramabhadran, R., Mauch, T. J. and Schoenwolf, G. C. (2005). Ubiquitous GFP expression in transgenic chickens using a lentiviral vector. Development 132, 935-940.
7. Goda, T., Abu-Daya, A., Carruthers, S., Clark, M. D., Stemple, D. L. and Zimmerman, L. B. (2006). Genetic screens for mutations affecting development of Xenopus tropicalis. PLoS Genet. 2, e91.
8. Gompel, N., Prud'homme, B., Wittkopp, P. J., Kassner, V. A. and Carroll, S. B. (2005). Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila. Nature 433, 481-487.
9. Goodrich, H. B. and Nichols, R. (1931). The development and the regeneration of the color pattern in Brachydanio rerio. J. Morphol. 52, 513-523.
10. Grassot, J., Gouy, M., Perriere, G. and Mouchiroud, G. (2006). Origin and molecular evolution of receptor tyrosine kinases with immunoglobulin-like domains. Mol. Biol. Evol. 23, 1232-1241.
11. Hoekstra, H. E., Hirschmann, R. J., Bundey, R. A., Insel, P. A. and Crossland, J. P. (2006). A single amino acid mutation contributes to adaptive beach mouse color pattern. Science 313, 101-104.
12. Hou, L., Pavan, W. J., Shin, M. K. and Arnheiter, H. (2004). Cell-autonomous and cell non-autonomous signaling through endothelin receptor B during melanocyte development. Development 131, 3239-3247.
13. Iwashita, M., Watanabe, M., Ishii, M., Chen, T., Johnson, S. L., Kurachi, Y., Okada, N. and Kondo, S. (2006). Pigment pattern in jaguar/obelix zebrafish is caused by a Kir7.1 mutation: Implications for the regulation of melanosome movement. Plos Genet. 2, 1861-1870.
14. Johnson, S. L., Africa, D., Walker, C. and Weston, J. A. (1995). Genetic control of adult pigment stripe development in zebrafish. Dev Biol. 167, 27-33.
15. Kelsh, R. N. (2004). Genetics and evolution of pigment patterns in fish. Pigment Cell Res. 17,326-336.
16. Kelsh, R. N., Schmid, B. and Eisen, J. S. (2000). Genetic analysis of melanophore development in zebrafish embryos. Dev Biol. 225, 277-293.
17. Kelsh, R. N., Inoue, C., Momoi, A., Kondoh, H., Furutani-Selki, M., Ozato, K. and Wakamatsu, Y. (2004). The Tomita collection of medaka pigmentation mutants as a resource for understanding neural crest cell development. Mech. Dev. 121, 841-859.
18. Langtimm-Sedlak, C. J., Schroeder, B., Saskowski, J. L, Carnahan, J. F. and Sieber-Blum, M. (1996). Multiple actions of stem cell factor in neural crest differentiation in vitro. Dev Biol. 174, 345-359.
19. Mackenzie, M. A., Jordan, S. A., Budd, P. S. and Jackson, I. J. (1997). Activation of the receptor tyrosine kinase Kit is required for the proliferation of melanoblasts in the mouse embryo. Dev Biol. 192, 99-107.
20. Maderspacher, F. and Nusslein-Volhard, C. (2003). Formation of the adult pigment pattern in zebrafish requires leopard and obelix dependent cell interactions. Development 130, 3447-3457.
21. McCauley, D. W., Hixon, E. and Jeffery, W. R. (2004). Evolution of pigment cell regression in the cavefish Astyanax: a late step in melanogenesis. Evol. Dev. 6, 209-218.
22. Mellgren, E. M. and Johnson, S. L. (2004). A requirement for kit in embryonic zebrafish melanocyte differentiation is revealed by melanoblast delay. Dev Genes Evol. 214, 493-502.
23. Mellgren, E. M. and Johnson, S. L. (2005). kitb, a second zebrafish ortholog of mouse Kit. Dev. Genes Evol. 215, 1-8.
24. Nijhout H. F. (1991). The Development and Evolution of Butterfly Wing Patterns. Washington, DC: Smithsonian Institution Press.
25. Nishimura, E. K., Yoshida, H., Kunisada, T. and Nishikawa, S. I. (1999). Regulation of E- and P-cadherin expression correlated with melanocyte migration and diversification. Dev Biol. 215, 155-166.
26. Parichy, D. M. (1996a). Pigment patterns of larval salamanders (Ambystomatidae, Salamandridae): the role of the lateral line sensory system and the evolution of pattern-forming mechanisms. Dev. Biol. 175, 265-282.
27. Parichy, D. M. (1996b). When neural crest and placocles collide: interactions between melanophores and the lateral lines that generate stripes in the salamander Ambystoma tigrinum tigrinum (Ambystomatidae). Dev Biol. 175, 283-300.
28. Parichy, D. M. (2005). Variation and developmental biology: prospects for the future. In Variation: A Hierarchical Examination of a Central Concept in Biology (ed. B. Halgrimsson and B. K. Hall), pp. 475-498. New York: Academic Press.
29. Parichy, D. M. (2006). Evolution of danio pigment pattern development. Heredity 97, 200-210.
30. Parichy, D. M. and Johnson, S. L. (2001). Zebrafish hybrids suggest genetic mechanisms for pigment pattern diversification in Danio. Dev Genes Evol. 211, 319-328.
31. Parichy, D. M. and Turner, J. M. (2003a). Temporal and cellular requirements for Fms signaling during zebrafish adult pigment pattern development. Development 130, 817-833.
32. Parichy, D. M. and Turner, J. M. (2003b). Zebrafish puma mutant decouples pigment pattern and somatic metamorphosis. Dev Biol. 256, 242-257.
33. Parichy, D. M., Rawls, J. F., Pratt, S. J., Whitfield, T. T. and Johnson, S. L. (1999). Zebrafish sparse corresponds to an orthologue of c-kit and is required for the morphogenesis of a subpopulation of melanocytes, but is not essential for hematopoiesis or primordial germ cell development. Development 126, 3425-3436.
34. Parichy, D. M., Mellgren, E. M., Rawls, J. F., Lopes, S. S., Kelsh, R. N. and Johnson, S. L. (2000a). Mutational analysis of endothelin receptor b1 (rose) during neural crest and pigment pattern development in the zebrafish Danio rerio. Dev. Biol. 227, 294-306.
35. Parichy, D. M., Ransom, D. G., Paw, B., Zon, L. I. and Johnson, S. L. (2000b). An orthologue of the kit-related gene fms is required for development of neural crest-derived xanthophores and a subpopulation of adult melanocytes in the zebrafish, Danio rerio. Development 127, 3031-3044.
36. Parichy, D. M., Reedy, M. V. and Erickson, C. A. (2006). Regulation of melanoblast migration and differentiation. In The Pigmentary System: Physiology and Pathophysiology. 2nd edn (ed. J. J. Nordland, R. E. Boissy, V. J. Hearing, R. A. King, W. S. Oetting and J. P. Ortonne). New York: Oxford University Press.
37. Quigley, I. K., Turner, J. M., Nuckels, R. J., Manuel, J. L., Budi, E. H., Macdonald, E. L. and Parichy, D. M. (2004). Pigment pattern evolution by differential deployment of neural crest and post-embryonic melanophore lineages in Danio fishes. Development 131, 6053-6069.
38. Quigley, I. K., Manuel, J. L., Roberts, R. A., Nuckels, R. J., Herrington, E. R., Macdonald, E. L. and Parichy, D. M. (2005). Evolutionary diversification of pigment pattern in Danio fishes: differential fms dependence and stripe loss in D. albolineatus. Development 132, 89-104.
39. Rawls, J. F. and Johnson, S. L. (2000). Zebrafish kit mutation reveals primary and secondary regulation of melanocyte development during fin stripe regeneration. Development 127, 3715-3724.
40. Rawls, J. F. and Johnson, S. L. (2003). Temporal and molecular separation of the kit receptor tyrosine kinase's roles in zebrafish melanocyte migration and survival. Dev Biol. 262, 152-161.
41. Rawls, J. F., Mellgren, E. M. and Johnson, S. L. (2001). How the zebrafish gets its stripes. Dev. Biol. 240, 301-314.
42. + progenitors. Dev Biol. 169, 568-579.
43. v substitution on hair pigmentation and erythrocytes. Genetics 34, 708-723.
44. Santiago, A. and Erickson, C. A. (2002). Ephrin-B ligands play a dual role in the control of neural crest cell migration. Development 129, 3621-3632.
45. Shapiro, M. D., Marks, M. E., Peichel, C. L., Blackman, B. K., Nereng, K. S., Jonsson, B., Schluter, D. and Kingsley, D. M. (2004). Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 428, 717-723.
46. Sobkow, L., Epperlein, H. H., Herklotz, S., Straube, W. L. and Tanaka, E. M. (2006). A germline GFP transgenic axolotl and its use to track cell fate: dual origin of the fin mesenchyme during development and the fate of blood cells during regeneration. Dev Biol. 290, 386-397.
47. Solnica-Krezel, L., Schier, A. F. and Driever, W. (1994). Efficient recovery of ENU-induced mutations from the zebrafish germline. Genetics 136, 1401-1420.
48. Watanabe, M., Iwashita, M., Ishii, M., Kurachi, Y., Kawakami, A., Kondo, S. and Okada, N. (2006). Spot pattern of leopard Danio is caused by mutation in the zebrafish connexin4l.8 gene. EMBO Rep. 7, 893-897.
49. Wehrle-Haller, B. (2003). The role of Kit-ligand in melanocyte development and epidermal homeostasis. Pigment Cell Res. 16, 287-296.
50. Wehrle-Haller, B. and Weston, J. A. (1995). Soluble and cell-bound forms of steel factor activity play distinct roles in melanocyte precursor dispersal and survival on the lateral neural crest migration pathway Development 121, 731-742.
51. Yamamoto, Y., Stock, D. W. and Jeffery, W. R. (2004). Hedgehog signalling controls eye degeneration in blind cavefish. Nature 431, 844-847.
52. Yang, C. T. and Johnson, S. L. (2006). Small molecule-induced ablation and subsequent regeneration of larval zebrafish melanocytes. Development 133, 3563-3573.
53. Yang, C. T, Sengelmann, R. D. and Johnson, S. L. (2004). Larval melanocyte regeneration following laser ablation in zebrafish. J. Invest Dermatol. 123, 924-929.
54. Yoshida, H., Kunisada, T., Kusakabe, M., Nishikawa, S. and Nishikawa, S. I. (1996). Distinct stages of melanocyte differentiation revealed by analysis of nonuniform pigmentation patterns. Development 122, 1207-1214.