Zebrafish stripes as a model for vertebrate colour pattern formation

Current Biology

Volumn 25, Issue 2, 2015, Pages R81-R92

  Singh, Ajeet Pratap ^a   Nüsslein Volhard, Christiane ^a  

^a MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; DANIO RERIO; VERTEBRATA;

FISH PROTEIN;

ANIMAL; CHROMATOPHORE; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MORPHOGENESIS; PHYSIOLOGY; PIGMENTATION; ZEBRA FISH;

ANIMALS; BODY PATTERNING; CHROMATOPHORES; FISH PROTEINS; MORPHOGENESIS; PIGMENTATION; ZEBRAFISH;

EID: 84921417541     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2014.11.013     Document Type: Review

References (92)

1. T. Caro The colours of extant mammals Semin. Cell Dev. Biol. 24 2013 542 552
2. N.M. Le Douarin, and C. Kalcheim The Neural Crest 1999 Cambridge University Press
3. C. Darwin The Descent of Man, and Selection in Relation to Sex 1871 John Murray London
4. S.L. Johnson, D. Africa, C. Walker, and J.A. Weston Genetic control of adult pigment stripe development in zebrafish Dev. Biol. 167 1995 27 33
5. P. Haffter, J. Odenthal, M.C. Mullins, S. Lin, M.J. Farrell, E. Vogelsang, F. Haas, M. Brand, F.J.M. vanEeden, and M. FurutaniSeiki Mutations affecting pigmentation and shape of the adult zebrafish Dev. Genes Evol. 206 1996 260 276
6. R.N. Kelsh, M. Brand, Y.J. Jiang, C.P. Heisenberg, S. Lin, P. Haffter, J. Odenthal, M.C. Mullins, F.J. van Eeden, and M. Furutani-Seiki Zebrafish pigmentation mutations and the processes of neural crest development Development 123 1996 369 389
7. J. Odenthal, K. Rossnagel, P. Haffter, R.N. Kelsh, E. Vogelsang, M. Brand, F.J. van Eeden, M. Furutani-Seiki, M. Granato, and M. Hammerschmidt Mutations affecting xanthophore pigmentation in the zebrafish, Danio rerio Development 123 1996 391 398
8. A.P. Singh, U. Schach, and C. Nüsslein-Volhard Proliferation, dispersal and patterned aggregation of iridophores in the skin prefigure striped colouration of zebrafish Nat. Cell Biol. 16 2014 604 611
9. M. McClure Development and evolution of melanophore patterns in fishes of the genus Danio (Teleostei: Cyprinidae) J. Morphol. 241 1999 83 105
10. D.M. Parichy, and S.L. Johnson Zebrafish hybrids suggest genetic mechanisms for pigment pattern diversification in Danio Dev. Genes Evol. 211 2001 319 328
11. V. Svetic, G.E. Hollway, S. Elworthy, T.R. Chipperfield, C. Davison, R.J. Adams, J.S. Eisen, P.W. Ingham, P.D. Currie, and R.N. Kelsh Sdf1a patterns zebrafish melanophores and links the somite and melanophore pattern defects in choker mutants Development 134 2007 1011 1022
12. M. Hirata, K. Nakamura, T. Kanemaru, Y. Shibata, and S. Kondo Pigment cell organization in the hypodermis of zebrafish Dev. Dyn. 227 2003 497 503
13. M. Hirata, K. Nakamura, and S. Kondo Pigment cell distributions in different tissues of the zebrafish, with special reference to the striped pigment pattern Dev. Dyn. 234 2005 293 300
14. P. Mahalwar, B. Walderich, A.P. Singh, and C. Nüsslein-Volhard Local reorganization of xanthophores in light and dark stripes fine-tune and color the striped pattern in zebrafish Science 345 2014 1362 1364
15. V.A. Kottler, A. Fadeev, D. Weigel, and C. Dreyer Pigment pattern formation in the guppy, Poecilia reticulata, involves the Kita and Csf1ra receptor tyrosine kinases Genetics 194 2013 631 646
16. I.K. Quigley, J.L. Manuel, R.A. Roberts, R.J. Nuckels, E.R. Herrington, E.L. MacDonald, and D.M. Parichy Evolutionary diversification of pigment pattern in Danio fishes: differential fms dependence and stripe loss in D. albolineatus Development 132 2005 89 104
17. R.N. Kelsh, M.L. Harris, S. Colanesi, and C.A. Erickson Stripes and belly-spots - a review of pigment cell morphogenesis in vertebrates Semin. Cell Dev. Biol. 20 2009 90 104
18. E.N. Geissler, M.A. Ryan, and D.E. Housman The dominant-white spotting (W) locus of the mouse encodes the c-kit proto-oncogene Cell 55 1988 185 192
19. R. Hauswirth, B. Haase, M. Blatter, S.A. Brooks, D. Burger, C. Drogemuller, V. Gerber, D. Henke, J. Janda, and R. Jude Mutations in MITF and PAX3 cause "splashed white" and other white spotting phenotypes in horses PLoS Genet. 8 2012 e1002653
20. A. Roulin, and A.L. Ducrest Genetics of colouration in birds Semin. Cell Dev. Biol. 24 2013 594 608
21. M. Miwa, M. Inoue-Murayama, H. Aoki, T. Kunisada, T. Hiragaki, M. Mizutani, and S. Ito Endothelin receptor B2 (EDNRB2) is associated with the panda plumage colour mutation in Japanese quail Anim. Genet. 38 2007 103 108
22. G. Streisinger, C. Walker, N. Dower, D. Knauber, and F. Singer Production of clones of homozygous diploid zebra fish (Brachydanio-Rerio) Nature 291 1981 293 296
23. G. Streisinger, F. Singer, C. Walker, D. Knauber, and N. Dower Segregation analyses and gene-centromere distances in zebrafish Genetics 112 1986 311 319
24. C. Walker, and G. Streisinger Induction of mutations by gamma-rays in pregonial germ cells of zebrafish embryos Genetics 103 1983 125 136
25. I. Braasch, F. Brunet, J.N. Volff, and M. Schartl Pigmentation pathway evolution after whole-genome duplication in fish Genome Biol. Evol. 1 2009 479 493
26. P.W. Holland Gene duplication: past, present and future Semin. Cell Dev. Biol. 10 1999 541 547
27. E.M. Mellgren, and S.L. Johnson The evolution of morphological complexity in zebrafish stripes Trends Genet. 18 2002 128 134
28. R.L. Lamason, M.A. Mohideen, J.R. Mest, A.C. Wong, H.L. Norton, M.C. Aros, M.J. Jurynec, X. Mao, V.R. Humphreville, and J.E. Humbert SLC24A5, a putative cation exchanger, affects pigmentation in zebrafish and humans Science 310 2005 1782 1786
29. C.M. Dooley, H. Schwarz, K.P. Mueller, A. Mongera, M. Konantz, S.C. Neuhauss, C. Nüsslein-Volhard, and R. Geisler Slc45a2 and V-ATPase are regulators of melanosomal pH homeostasis in zebrafish, providing a mechanism for human pigment evolution and disease Pigment Cell Melanoma Res. 26 2013 205 217
30. J. Krauss, S. Geiger-Rudolph, I. Koch, C. Nüsslein-Volhard, and U. Irion A dominant mutation in tyrp1A leads to melanophore death in zebrafish Pigment Cell Melanoma Res. 27 2014 827 830
31. F. Liu, B. Wen, and M. Kayser Colorful DNA polymorphisms in humans Semin. Cell Dev. Biol. 24 2013 562 575
32. P.C. Sabeti, P. Varilly, B. Fry, J. Lohmueller, E. Hostetter, C. Cotsapas, X. Xie, E.H. Byrne, S.A. McCarroll, and R. Gaudet Genome-wide detection and characterization of positive selection in human populations Nature 449 2007 913 918
33. K.A. Dutton, A. Pauliny, S.S. Lopes, S. Elworthy, T.J. Carney, J. Rauch, R. Geisler, P. Haffter, and R.N. Kelsh Zebrafish colourless encodes sox10 and specifies non-ectomesenchymal neural crest fates Development 128 2001 4113 4125
34. C.M. Dooley, A. Mongera, B. Walderich, and C. Nüsslein-Volhard On the embryonic origin of adult melanophores: the role of ErbB and Kit signalling in establishing melanophore stem cells in zebrafish Development 140 2013 1003 1013
35. K.A. Hultman, N. Bahary, L.I. Zon, and S.L. Johnson Gene Duplication of the zebrafish kit ligand and partitioning of melanocyte development functions to kit ligand a PLoS Genet. 3 2007 e17
36. D.M. Parichy, J.F. Rawls, S.J. Pratt, T.T. Whitfield, and S.L. Johnson 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 1999 3425 3436
37. J.A. Lister, C.P. Robertson, T. Lepage, S.L. Johnson, and D.W. Raible nacre encodes a zebrafish microphthalmia-related protein that regulates neural-crest-derived pigment cell fate Development 126 1999 3757 3767
38. S.L. Johnson, A.N. Nguyen, and J.A. Lister mitfa is required at multiple stages of melanocyte differentiation but not to establish the melanocyte stem cell Dev. Biol. 350 2011 405 413
39. S.S. Lopes, X. Yang, J. Muller, T.J. Carney, A.R. McAdow, G.J. Rauch, A.S. Jacoby, L.D. Hurst, M. Delfino-Machin, and P. Haffter Leukocyte tyrosine kinase functions in pigment cell development PLoS Genet. 4 2008 e1000026
40. D.M. Parichy, E.M. Mellgren, J.F. Rawls, S.S. Lopes, R.N. Kelsh, and S.L. Johnson Mutational analysis of endothelin receptor b1 (rose) during neural crest and pigment pattern development in the zebrafish Danio rerio Dev. Biol. 227 2000 294 306
41. H.G. Frohnhöfer, J. Krauss, H.M. Maischein, and C. Nüsslein-Volhard Iridophores and their interactions with other chromatophores are required for stripe formation in zebrafish Development 140 2013 2997 3007
42. J. Krauss, H.G. Frohnhofer, B. Walderich, C. Weiler, U. Irion, and C. Nüsslein-Volhard Endothelin signalling in iridophore development and stripe pattern formation of zebrafish Biol. Open 3 2014 503 509
43. J. Krauss, P. Astrinides, H.G. Frohnhofer, B. Walderich, and C. Nüsslein-Volhard transparent, a gene affecting stripe formation in Zebrafish, encodes the mitochondrial protein Mpv17 that is required for iridophore survival Biol. Open 2 2013 703 710
44. D.M. Parichy, D.G. Ransom, B. Paw, L.I. Zon, and S.L. Johnson 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 2000 3031 3044
45. D.M. Parichy, and J.M. Turner Temporal and cellular requirements for Fms signaling during zebrafish adult pigment pattern development Development 130 2003 817 833
46. F. Maderspacher, and C. Nüsslein-Volhard Formation of the adult pigment pattern in zebrafish requires leopard and obelix dependent cell interactions Development 130 2003 3447 3457
47. L.B. Patterson, and D.M. Parichy Interactions with iridophores and the tissue environment required for patterning melanophores and xanthophores during zebrafish adult pigment stripe formation PLoS Genet. 9 2013 e1003561
48. A. Nakamasu, G. Takahashi, A. Kanbe, and S. Kondo Interactions between zebrafish pigment cells responsible for the generation of Turing patterns Proc. Natl. Acad. Sci. USA 106 2009 8429 8434
49. M.R. Lang, L.B. Patterson, T.N. Gordon, S.L. Johnson, and D.M. Parichy Basonuclin-2 requirements for zebrafish adult pigment pattern development and female fertility PLoS Genet. 5 2009 e1000744
50. M. Watanabe, M. Iwashita, M. Ishii, Y. Kurachi, A. Kawakami, S. Kondo, and N. Okada Spot pattern of leopard Danio is caused by mutation in the zebrafish connexin41.8 gene EMBO Rep. 7 2006 893 897
51. M. Iwashita, M. Watanabe, M. Ishii, T. Chen, S.L. Johnson, Y. Kurachi, N. Okada, and S. Kondo Pigment pattern in jaguar/obelix zebrafish is caused by a Kir7.1 mutation: implications for the regulation of melanosome movement PLoS Genet. 2 2006 e197
52. R. Asai, E. Taguchi, Y. Kume, M. Saito, and S. Kondo Zebrafish leopard gene as a component of the putative reaction-diffusion system Mech. Dev. 89 1999 87 92
53. M. Yamaguchi, E. Yoshimoto, and S. Kondo Pattern regulation in the stripe of zebrafish suggests an underlying dynamic and autonomous mechanism Proc. Natl. Acad. Sci. USA 104 2007 4790 4793
54. M. Watanabe, and S. Kondo Changing clothes easily: connexin41.8 regulates skin pattern variation Pigment Cell Melanoma Res. 25 2012 326 330
55. H. Yamanaka, and S. Kondo In vitro analysis suggests that difference in cell movement during direct interaction can generate various pigment patterns in vivo Proc. Natl. Acad. Sci. USA 111 2014 1867 1872
56. U. Irion, H.G. Frohnhöfer, J. Krauss, T. Çolak Champollion, H. Maischein, S. Geiger-Rudolph, C. Weiler, and C. Nüsslein-Volhard Gap junctions composed of connexins 41.8 and 39.4 are essential for colour pattern formation in zebrafish eLife 2014 10.7554/eLife.05125
57. D.S. Eom, S. Inoue, L.B. Patterson, T.N. Gordon, R. Slingwine, S. Kondo, M. Watanabe, and D.M. Parichy Melanophore migration and survival during zebrafish adult pigment stripe development require the immunoglobulin superfamily adhesion molecule Igsf11 PLoS Genet. 8 2012 e1002899
58. M. Inaba, H. Yamanaka, and S. Kondo Pigment pattern formation by contact-dependent depolarization Science 335 2012 677
59. S. Inoue, S. Kondo, D.M. Parichy, and M. Watanabe Tetraspanin 3c requirement for pigment cell interactions and boundary formation in zebrafish adult pigment stripes Pigment Cell Melanoma Res. 27 2014 190 200
60. H. Hamada, M. Watanabe, H.E. Lau, T. Nishida, T. Hasegawa, D.M. Parichy, and S. Kondo Involvement of Delta/Notch signaling in zebrafish adult pigment stripe patterning Development 141 2014 1418
61. E.H. Budi, L.B. Patterson, and D.M. Parichy Post-embryonic nerve-associated precursors to adult pigment cells: genetic requirements and dynamics of morphogenesis and differentiation PLoS Genet. 7 2011 e1002044
62. E.H. Budi, L.B. Patterson, and D.M. Parichy Embryonic requirements for ErbB signaling in neural crest development and adult pigment pattern formation Development 135 2008 2603 2614
63. K.A. Hultman, E.H. Budi, D.C. Teasley, A.Y. Gottlieb, D.M. Parichy, and S.L. Johnson Defects in ErbB-dependent establishment of adult melanocyte stem cells reveal independent origins for embryonic and regeneration melanocytes PLoS Genet. 5 2009 e1000544
64. S.K. McMenamin, E.J. Bain, A.E. McCann, L.B. Patterson, D.S. Eom, Z.P. Waller, J.C. Hamill, J.A. Kuhlman, J.S. Eisen, and D.M. Parichy Thyroid hormone-dependent adult pigment cell lineage and pattern in zebrafish Science 345 2014 1358 1361
65. S. Tu, and S.L. Johnson Clonal analyses reveal roles of organ founding stem cells, melanocyte stem cells and melanoblasts in establishment, growth and regeneration of the adult zebrafish fin Development 137 2010 3931 3939
66. G. Takahashi, and S. Kondo Melanophores in the stripes of adult zebrafish do not have the nature to gather, but disperse when they have the space to move Pigment Cell Melanoma Res. 21 2008 677 686
67. E.M. Mellgren, and S.L. Johnson pyewacket, a new zebrafish fin pigment pattern mutant Pigment Cell Res. 19 2006 232 238
68. S. Kondo, and T. Miura Reaction-diffusion model as a framework for understanding biological pattern formation Science 329 2010 1616 1620
69. K.J. Painter, P.K. Maini, and H.G. Othmer Stripe formation in juvenile Pomacanthus explained by a generalized turing mechanism with chemotaxis Proc. Natl. Acad. Sci. USA 96 1999 5549 5554
70. L.B. Patterson, E.J. Bain, and D.M. Parichy Pigment cell interactions and differential xanthophore recruitment underlying zebrafish stripe reiteration and Danio pattern evolution Nat. Commun. 5 2014 5299
71. M.G. Mills, R.J. Nuckels, and D.M. Parichy Deconstructing evolution of adult phenotypes: genetic analyses of kit reveal homology and evolutionary novelty during adult pigment pattern development of Danio fishes Development 134 2007 1081 1090
72. M.E. Santos, I. Braasch, N. Boileau, B.S. Meyer, L. Sauteur, A. Bohne, H.G. Belting, M. Affolter, and W. Salzburger The evolution of cichlid fish egg-spots is linked with a cis-regulatory change Nat. Commun. 5 2014 5149
73. I. Adameyko, F. Lallemend, J.B. Aquino, J.A. Pereira, P. Topilko, T. Muller, N. Fritz, A. Beljajeva, M. Mochii, and I. Liste Schwann cell precursors from nerve innervation are a cellular origin of melanocytes in skin Cell 139 2009 366 379
74. X. Xu, G.X. Dong, X.S. Hu, L. Miao, X.L. Zhang, D.L. Zhang, H.D. Yang, T.Y. Zhang, Z.T. Zou, and T.T. Zhang The genetic basis of white tigers Curr. Biol. 23 2013 1031 1035
75. W.Y. Hwang, Y. Fu, D. Reyon, M.L. Maeder, S.Q. Tsai, J.D. Sander, R.T. Peterson, J.R. Yeh, and J.K. Joung Efficient genome editing in zebrafish using a CRISPR-Cas system Nat. Biotechnol. 31 2013 227 229
76. U. Irion, J. Krauss, and C. Nüsslein-Volhard Precise and efficient genome editing in zebrafish using the CRISPR/Cas9 system Development 141 2014 4827 4830
77. J.T. Bagnara, and J.D. Taylor Differences in pigment-containing organelles between color forms of the red-backed salamander, Plethodon cinereus Z. Zellforsch. Mikrosk. Anat. 106 1970 412 417
78. N. Oshima, and K. Akiko Iridophores Involved in Generation of Skin Color in the Zebrafish, Brachydanio rerio Forma 17 2002 91 101
79. M.F. Land The physics and biology of animal reflectors Prog. Biophys. Mol. Biol. 24 1972 75 106
80. J.T. Bagnara, P.J. Fernandez, and R. Fujii On the blue coloration of vertebrates Pigment Cell Res. 20 2007 14 26
81. N.K. Michiels, N. Anthes, N.S. Hart, J. Herler, A.J. Meixner, F. Schleifenbaum, G. Schulte, U.E. Siebeck, D. Sprenger, and M.F. Wucherer Red fluorescence in reef fish: a novel signalling mechanism? BMC Ecol. 8 2008 16
82. J.S. Sparks, R.C. Schelly, W.L. Smith, M.P. Davis, D. Tchernov, V.A. Pieribone, and D.F. Gruber The covert world of fish biofluorescence: a phylogenetically widespread and phenotypically variable phenomenon PLoS ONE 9 2014 e83259
83. M. Olsson, D. Stuart-Fox, and C. Ballen Genetics and evolution of colour patterns in reptiles Semin. Cell Dev. Biol. 24 2013 529 541
84. G.F. Grether, G.R. Kolluru, and K. Nersissian Individual colour patches as multicomponent signals Biol. Rev. Camb. Philos. Soc. 79 2004 583 610
85. R. Fujii The regulation of motile activity in fish chromatophores Pigment Cell Res. 13 2000 300 319
86. M. Goda, M. Ohata, H. Ikoma, Y. Fujiyoshi, M. Sugimoto, and R. Fujii Integumental reddish-violet coloration owing to novel dichromatic chromatophores in the teleost fish, Pseudochromis diadema Pigment Cell Melanoma Res. 24 2011 614 617
87. J.T. Bagnara, J.D. Taylor, and M.E. Hadley The dermal chromatophore unit J. Cell Biol. 38 1968 67 79
88. H. Nilsson Sköld, S. Aspengren, and M. Wallin Rapid color change in fish and amphibians - function, regulation, and emerging applications Pigment Cell Melanoma Res. 26 2013 29 38
89. D.W. Logan, S.F. Burn, and I.J. Jackson Regulation of pigmentation in zebrafish melanophores Pigment Cell Res. 19 2006 206 213
90. N. Oshima, E. Nakata, M. Ohta, and S. Kamagata Light-induced pigment aggregation in xanthophores of the medaka, Oryzias latipes Pigment Cell Res. 11 1998 362 367
91. N. Oshima, and A. Yokozeki Direct control of pigment aggregation and dispersion in tilapia erythrophores by light Zoolog. Sci. 16 1999 51 54
92. S.M. Doucet, M.D. Shawkey, G.E. Hill, and R. Montgomerie Iridescent plumage in satin bowerbirds: structure, mechanisms and nanostructural predictors of individual variation in colour J. Exp. Biol. 209 2006 380 390