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Cited by 5melanin and skin pigmentationDevelopmental Biology and Gene RegulationZebrafish Biomedical Research Applications

kcnj13 regulates pigment cell shapes in zebrafish and has diverged by cis-regulatory evolution between Danio species

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Podobnik, Marco, Singh, Ajeet P., Fu, Zhenqiang, Dooley, Christopher M., Frohnhöfer, Hans Georg, Firlej, Magdalena, Stednitz, Sarah J., Elhabashy, Hadeer +5 more·2023·Development
DOI 10.1242/dev.201627PMC PMC10482006

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Abstract

Teleost fish of the genus Danio are excellent models to study the genetic and cellular bases of pigment pattern variation in vertebrates. The two sister species Danio rerio and Danio aesculapii show divergent patterns of horizontal stripes and vertical bars that are partly caused by the divergence of the potassium channel gene kcnj13. Here, we show that kcnj13 is required only in melanophores for interactions with xanthophores and iridophores, which cause location-specific pigment cell shapes and thereby influence colour pattern and contrast in D. rerio. Cis-regulatory rather than protein coding changes underlie kcnj13 divergence between the two Danio species. Our results suggest that homotypic and heterotypic interactions between the pigment cells and their shapes diverged between species by quantitative changes in kcnj13 expression during pigment pattern diversification.

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  1. Altmannova, V., Blaha, A., Astrinidis, S., Reichle, H. and Weir, J. R. (2021). InteBac: an integrated bacterial and baculovirus expression vector suite. Protein Sci. 30, 108- 114. 10.1002/pro.3957 32955754 PMC7737779 · DOI
  2. Bertoni, M., Kiefer, F., Biasini, M., Bordoli, L. and Schwede, T. (2017). Modeling protein quaternary structure of homo- and hetero-oligomers beyond binary interactions by homology. Sci. Rep. 7, 10480. 10.1038/s41598-017-09654-8 28874689 PMC5585393 · DOI
  3. Bertrand, J. Y., Chi, N. C., Santoso, B., Teng, S., Stainier, D. Y. and Traver, D. (2010). Haematopoietic stem cells derive directly from aortic endothelium during development. Nature 464, 108- 111. 10.1038/nature08738 20154733 PMC2858358 · DOI
  4. Bienert, S., Waterhouse, A., de Beer, T. A., Tauriello, G., Studer, G., Bordoli, L. and Schwede, T. (2017). The SWISS-MODEL Repository-new features and functionality. Nucleic Acids Res. 45, D313- D319. 10.1093/nar/gkw1132 27899672 PMC5210589 · DOI
  5. Bieniossek, C., Imasaki, T., Takagi, Y. and Berger, I. (2012). MultiBac: expanding the research toolbox for multiprotein complexes. Trends Biochem. Sci. 37, 49- 57. 10.1016/j.tibs.2011.10.005 22154230 PMC7127121 · DOI
  6. Brand, M., Granato, M. and Nüsslein-Volhard, C. (2002). Keeping and raising zebrafish. In Zebrafish: A Practical Approach (ed. C. Nüsslein-Volhard and R. Dahm), pp. 7- 37. Oxford University Press.
  7. Brouard, J. S., Schenkel, F., Marete, A. and Bissonnette, N. (2019). The GATK joint genotyping workflow is appropriate for calling variants in RNA-seq experiments. J. Anim. Sci. Biotechnol. 10, 44. 10.1186/s40104-019-0359-0 31249686 PMC6587293 · DOI
  8. Castel, S. E., Levy-Moonshine, A., Mohammadi, P., Banks, E. and Lappalainen, T. (2015). Tools and best practices for data processing in allelic expression analysis. Genome Biol. 16, 195. 10.1186/s13059-015-0762-6 26381377 PMC4574606 · DOI · Paper page
  9. Chen, S., Zhou, Y., Chen, Y. and Gu, J. (2018). fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884- i890. 10.1093/bioinformatics/bty560 30423086 PMC6129281 · DOI
  10. Danecek, P., Bonfield, J. K., Liddle, J., Marshall, J., Ohan, V., Pollard, M. O., Whitwham, A., Keane, T., McCarthy, S. A., Davies, R. M. et al. (2021). Twelve years of SAMtools and BCFtools. Gigascience 10, giab008. 10.1093/gigascience/giab008 33590861 PMC7931819 · DOI
  11. Distel, M., Wullimann, M. F. and Koster, R. W. (2009). Optimized Gal4 genetics for permanent gene expression mapping in zebrafish. Proc. Natl. Acad. Sci. USA 106, 13365- 13370. 10.1073/pnas.0903060106 19628697 PMC2726396 · DOI
  12. Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M. and Gingeras, T. R. (2013). STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15- 21. 10.1093/bioinformatics/bts635 23104886 PMC3530905 · DOI · Paper page
  13. Dooley, C. M., Mongera, A., Walderich, B. and Nusslein-Volhard, C. (2013a). On the embryonic origin of adult melanophores: the role of ErbB and Kit signalling in establishing melanophore stem cells in zebrafish. Development 140, 1003- 1013. 10.1242/dev.087007 23364329 · DOI
  14. Dooley, C. M., Schwarz, H., Mueller, K. P., Mongera, A., Konantz, M., Neuhauss, S. C., Nusslein-Volhard, C. and Geisler, R. (2013b). 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, 205- 217. 10.1111/pcmr.12053 23205854 · DOI · Paper page
  15. Eom, D. S., Inoue, S., Patterson, L. B., Gordon, T. N., Slingwine, R., Kondo, S., Watanabe, M. and Parichy, D. M. (2012). Melanophore migration and survival during zebrafish adult pigment stripe development require the immunoglobulin superfamily adhesion molecule Igsf11. PLoS Genet. 8, e1002899. 10.1371/journal.pgen.1002899 22916035 PMC3420941 · DOI · Paper page
  16. Eom, D. S., Patterson, L. B., Bostic, R. R. and Parichy, D. M. (2021). Immunoglobulin superfamily receptor Junctional adhesion molecule 3 (Jam3) requirement for melanophore survival and patterning during formation of zebrafish stripes. Dev. Biol. 476, 314- 327. 10.1016/j.ydbio.2021.04.007 33933422 PMC10069301 · DOI · Paper page
  17. Evans, R., O'Neill, M., Pritzel, A., Antropova, N., Senior, A., Green, T., Žídek, A., Bates, R., Blackwell, S., Yim, J. et al. (2022). Protein complex prediction with AlphaFold-Multimer. bioRxiv 2021.2010.2004.463034.
  18. Frohnhöfer, H. G., Krauss, J., Maischein, H. M. and Nusslein-Volhard, C. (2013). Iridophores and their interactions with other chromatophores are required for stripe formation in zebrafish. Development 140, 2997- 3007. 10.1242/dev.096719 23821036 PMC3912879 · DOI · Paper page
  19. Haffter, P., Odenthal, J., Mullins, M. C., Lin, S., Farrell, M. J., Vogelsang, E., Haas, F., Brand, M., van Eeden, F. J., Furutani-Seiki, M. et al. (1996). Mutations affecting pigmentation and shape of the adult zebrafish. Dev. Genes Evol. 206, 260- 276. 10.1007/s004270050051 24173565 · DOI · Paper page
  20. Hamada, H., Watanabe, M., Lau, H. E., Nishida, T., Hasegawa, T., Parichy, D. M. and Kondo, S. (2014). Involvement of Delta/Notch signaling in zebrafish adult pigment stripe patterning. Development 141, 318- 324. 10.1242/dev.099804 24306107 PMC3879813 · DOI
  21. Harris, M. P. (2021). Bioelectric signaling as a unique regulator of development and regeneration. Development 148, dev180794. 10.1242/dev.180794 33999994 PMC8180260 · DOI
  22. Hart, J. C., Ellis, N. A., Eisen, M. B. and Miller, C. T. (2018). Convergent evolution of gene expression in two high-toothed stickleback populations. PLoS Genet. 14, e1007443. 10.1371/journal.pgen.1007443 29897962 PMC6016950 · DOI
  23. Hejtmancik, J. F., Jiao, X., Li, A., Sergeev, Y. V., Ding, X., Sharma, A. K., Chan, C. C., Medina, I. and Edwards, A. O. (2008). Mutations in KCNJ13 cause autosomal-dominant snowflake vitreoretinal degeneration. Am. J. Hum. Genet. 82, 174- 180. 10.1016/j.ajhg.2007.08.002 18179896 PMC2253967 · DOI
  24. Henke, K., Daane, J. M., Hawkins, M. B., Dooley, C. M., Busch-Nentwich, E. M., Stemple, D. L. and Harris, M. P. (2017). Genetic screen for postembryonic development in the Zebrafish (Danio rerio): dominant mutations affecting adult form. Genetics 207, 609- 623. 10.1534/genetics.117.300187 28835471 PMC5629327 · DOI
  25. Inaba, M., Yamanaka, H. and Kondo, S. (2012). Pigment pattern formation by contact-dependent depolarization. Science 335, 677. 10.1126/science.1212821 22323812 · DOI · Paper page
  26. Irion, U. and Nusslein-Volhard, C. (2019). The identification of genes involved in the evolution of color patterns in fish. Curr. Opin. Genet. Dev. 57, 31- 38. 10.1016/j.gde.2019.07.002 31421397 PMC6838669 · DOI
  27. Irion, U., Frohnhofer, H. G., Krauss, J., Colak Champollion, T., Maischein, H. M., Geiger-Rudolph, S., Weiler, C. and Nusslein-Volhard, C. (2014a). Gap junctions composed of connexins 41.8 and 39.4 are essential for colour pattern formation in zebrafish. eLife 3, e05125. 10.7554/eLife.05125 25535837 PMC4296512 · DOI · Paper page
  28. Irion, U., Krauss, J. and Nusslein-Volhard, C. (2014b). Precise and efficient genome editing in zebrafish using the CRISPR/Cas9 system. Development 141, 4827- 4830. 10.1242/dev.115584 25411213 PMC4299274 · DOI
  29. 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, e197. 10.1371/journal.pgen.0020197 17121467 PMC1657052 · DOI · Paper page
  30. Jones, F. C., Grabherr, M. G., Chan, Y. F., Russell, P., Mauceli, E., Johnson, J., Swofford, R., Pirun, M., Zody, M. C., White, S. et al. (2012). The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484, 55- 61. 10.1038/nature10944 22481358 PMC3322419 · DOI
  31. Kane, D. A. and Kishimoto, Y. (2002). Cell labelling and transplantation techniques. In Zebrafish: A Practical Approach (ed. C. Nüsslein-Volhard and R. Dahm), pp. 95- 119. Oxford University Press.
  32. Kawakami, K. and Shima, A. (1999). Identification of the Tol2 transposase of the medaka fish Oryzias latipes that catalyzes excision of a nonautonomous Tol2 element in zebrafish Danio rerio. Gene 240, 239- 244. 10.1016/S0378-1119(99)00444-8 10564832 · DOI
  33. Kelsh, R. N., Brand, M., Jiang, Y. J., Heisenberg, C. P., Lin, S., Haffter, P., Odenthal, J., Mullins, M. C., van Eeden, F. J., Furutani-Seiki, M. et al. (1996). Zebrafish pigmentation mutations and the processes of neural crest development. Development 123, 369- 389. 10.1242/dev.123.1.369 9007256 · DOI · Paper page
  34. Kratochwil, C. F., Liang, Y., Gerwin, J., Woltering, J. M., Urban, S., Henning, F., Machado-Schiaffino, G., Hulsey, C. D. and Meyer, A. (2018). Agouti-related peptide 2 facilitates convergent evolution of stripe patterns across cichlid fish radiations. Science 362, 457- 460. 10.1126/science.aao6809 30361373 · DOI · Paper page
  35. Kwan, K. M., Fujimoto, E., Grabher, C., Mangum, B. D., Hardy, M. E., Campbell, D. S., Parant, J. M., Yost, H. J., Kanki, J. P. and Chien, C. B. (2007). The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev. Dyn. 236, 3088- 3099. 10.1002/dvdy.21343 17937395 · DOI
  36. Li, H. (2013). Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv: Genomics.
  37. Lister, J. A., Robertson, C. P., Lepage, T., Johnson, S. L. and Raible, D. W. (1999). nacre encodes a zebrafish microphthalmia-related protein that regulates neural-crest-derived pigment cell fate. Development 126, 3757- 3767. 10.1242/dev.126.17.3757 10433906 · DOI · Paper page
  38. Love, M. I., Huber, W. and Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550. 10.1186/s13059-014-0550-8 25516281 PMC4302049 · DOI · Paper page
  39. 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. 10.1242/dev.00519 12810592 · DOI · Paper page
  40. Mahalwar, P., Walderich, B., Singh, A. P. and Nusslein-Volhard, C. (2014). Local reorganization of xanthophores fine-tunes and colors the striped pattern of zebrafish. Science 345, 1362- 1364. 10.1126/science.1254837 25214630 · DOI
  41. McCluskey, B. M. and Postlethwait, J. H. (2015). Phylogeny of zebrafish, a “model species,” within Danio, a “model genus”. Mol. Biol. Evol. 32, 635- 652. 10.1093/molbev/msu325 25415969 PMC4327152 · DOI · Paper page
  42. McCluskey, B. M., Liang, Y., Lewis, V. M., Patterson, L. B. and Parichy, D. M. (2021a). Pigment pattern morphospace of Danio fishes: evolutionary diversification and mutational effects. Biol. Open 10, bio058814. 10.1242/bio.058814 34463758 PMC8487636 · DOI · Paper page
  43. McCluskey, B. M., Uji, S., Mancusi, J. L., Postlethwait, J. H. and Parichy, D. M. (2021b). A complex genetic architecture in zebrafish relatives Danio quagga and D. kyathit underlies development of stripes and spots. PLoS Genet. 17, e1009364. 10.1371/journal.pgen.1009364 33901178 PMC8102007 · DOI · Paper page
  44. McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M. et al. (2010). The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297- 1303. 10.1101/gr.107524.110 20644199 PMC2928508 · DOI · Paper page
  45. Meeker, N. D., Hutchinson, S. A., Ho, L. and Trede, N. S. (2007). Method for isolation of PCR-ready genomic DNA from zebrafish tissues. BioTechniques 43, 610, 612, 614. 10.2144/000112619 18072590 · DOI
  46. Mongera, A., Singh, A. P., Levesque, M. P., Chen, Y. Y., Konstantinidis, P. and Nusslein-Volhard, C. (2013). Genetic lineage labeling in zebrafish uncovers novel neural crest contributions to the head, including gill pillar cells. Development 140, 916- 925. 10.1242/dev.091066 23362350 · DOI
  47. Odenthal, J., Rossnagel, K., Haffter, P., Kelsh, R. N., Vogelsang, E., Brand, M., van Eeden, F. J., Furutani-Seiki, M., Granato, M., Hammerschmidt, M. et al. (1996). Mutations affecting xanthophore pigmentation in the zebrafish, Danio rerio. Development 123, 391- 398. 10.1242/dev.123.1.391 9007257 · DOI · Paper page
  48. Orteu, A. and Jiggins, C. D. (2020). The genomics of coloration provides insights into adaptive evolution. Nat. Rev. Genet. 21, 461- 475. 10.1038/s41576-020-0234-z 32382123 · DOI
  49. Parichy, D. M. (2015). Advancing biology through a deeper understanding of zebrafish ecology and evolution. eLife 4, e05635. 10.7554/eLife.05635 25807087 PMC4373672 · DOI · Paper page
  50. Parichy, D. M. (2021). Evolution of pigment cells and patterns: recent insights from teleost fishes. Curr. Opin. Genet. Dev. 69, 88- 96. 10.1016/j.gde.2021.02.006 33743392 PMC8364858 · DOI · Paper page
  51. 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. 10.1007/s004270100155 11466528 · DOI · Paper page
  52. Parichy, D. M., Elizondo, M. R., Mills, M. G., Gordon, T. N. and Engeszer, R. E. (2009). Normal table of postembryonic zebrafish development: staging by externally visible anatomy of the living fish. Dev. Dyn. 238, 2975- 3015. 10.1002/dvdy.22113 19891001 PMC3030279 · DOI · Paper page
  53. 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. 10.1006/dbio.2000.9899 11071756 · DOI · Paper page
  54. 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. 10.1242/dev.127.14.3031 10862741 · DOI · Paper page
  55. Patterson, L. B. and Parichy, D. M. (2013). Interactions with iridophores and the tissue environment required for patterning melanophores and xanthophores during zebrafish adult pigment stripe formation. PLoS Genet. 9, e1003561. 10.1371/journal.pgen.1003561 23737760 PMC3667786 · DOI · Paper page
  56. Patterson, L. B. and Parichy, D. M. (2019). Zebrafish Pigment Pattern Formation: Insights into the Development and Evolution of Adult Form. Annu. Rev. Genet. 53, 505- 530. 10.1146/annurev-genet-112618-043741 31509458 · DOI · Paper page
  57. Patterson, L. B., Bain, E. J. and Parichy, D. M. (2014). Pigment cell interactions and differential xanthophore recruitment underlying zebrafish stripe reiteration and Danio pattern evolution. Nat. Commun. 5, 5299. 10.1038/ncomms6299 25374113 PMC4224114 · DOI · Paper page
  58. Podobnik, M., Frohnhofer, H. G., Dooley, C. M., Eskova, A., Nusslein-Volhard, C. and Irion, U. (2020). Evolution of the potassium channel gene Kcnj13 underlies colour pattern diversification in Danio fish. Nat. Commun. 11, 6230. 10.1038/s41467-020-20021-6 33277491 PMC7718271 · DOI · Paper page
  59. Preibisch, S., Saalfeld, S. and Tomancak, P. (2009). Globally optimal stitching of tiled 3D microscopic image acquisitions. Bioinformatics 25, 1463- 1465. 10.1093/bioinformatics/btp184 19346324 PMC2682522 · DOI · Paper page
  60. Quinlan, A. R. and Hall, I. M. (2010). BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841- 842. 10.1093/bioinformatics/btq033 20110278 PMC2832824 · DOI · Paper page
  61. Sergouniotis, P. I., Davidson, A. E., Mackay, D. S., Li, Z., Yang, X., Plagnol, V., Moore, A. T. and Webster, A. R. (2011). Recessive mutations in KCNJ13, encoding an inwardly rectifying potassium channel subunit, cause leber congenital amaurosis. Am. J. Hum. Genet. 89, 183- 190. 10.1016/j.ajhg.2011.06.002 21763485 PMC3135807 · DOI
  62. Silic, M. R., Wu, Q., Kim, B. H., Golling, G., Chen, K. H., Freitas, R., Chubykin, A. A., Mittal, S. K. and Zhang, G. (2020). Potassium channel-associated bioelectricity of the dermomyotome determines fin patterning in Zebrafish. Genetics 215, 1067- 1084. 10.1534/genetics.120.303390 32546498 PMC7404225 · DOI
  63. Singh, A. P. and Nusslein-Volhard, C. (2015). Zebrafish stripes as a model for vertebrate colour pattern formation. Curr. Biol. 25, R81- R92. 10.1016/j.cub.2014.11.013 25602311 · DOI · Paper page
  64. Singh, A. P., Schach, U. and Nusslein-Volhard, C. (2014). Proliferation, dispersal and patterned aggregation of iridophores in the skin prefigure striped colouration of zebrafish. Nat. Cell Biol. 16, 607- 614. 10.1038/ncb2955 24776884 · DOI · Paper page
  65. Singh, A. P., Dinwiddie, A., Mahalwar, P., Schach, U., Linker, C., Irion, U. and Nusslein-Volhard, C. (2016). Pigment cell progenitors in Zebrafish remain multipotent through metamorphosis. Dev. Cell 38, 316- 330. 10.1016/j.devcel.2016.06.020 27453500 · DOI · Paper page
  66. Spiewak, J. E., Bain, E. J., Liu, J., Kou, K., Sturiale, S. L., Patterson, L. B., Diba, P., Eisen, J. S., Braasch, I., Ganz, J. et al. (2018). Evolution of Endothelin signaling and diversification of adult pigment pattern in Danio fishes. PLoS Genet. 14, e1007538. 10.1371/journal.pgen.1007538 30226839 PMC6161917 · DOI · Paper page
  67. Stern, D. L. (2014). Identification of loci that cause phenotypic variation in diverse species with the reciprocal hemizygosity test. Trends Genet. 30, 547- 554. 10.1016/j.tig.2014.09.006 25278102 · DOI
  68. Studer, G., Rempfer, C., Waterhouse, A. M., Gumienny, R., Haas, J. and Schwede, T. (2020). QMEANDisCo-distance constraints applied on model quality estimation. Bioinformatics 36, 1765- 1771. 10.1093/bioinformatics/btz828 31697312 PMC7075525 · DOI
  69. Studer, G., Tauriello, G., Bienert, S., Biasini, M., Johner, N. and Schwede, T. (2021). ProMod3-A versatile homology modelling toolbox. PLoS Comput. Biol. 17, e1008667. 10.1371/journal.pcbi.1008667 33507980 PMC7872268 · DOI
  70. Toms, M., Burgoyne, T., Tracey-White, D., Richardson, R., Dubis, A. M., Webster, A. R., Futter, C. and Moosajee, M. (2019a). Phagosomal and mitochondrial alterations in RPE may contribute to KCNJ13 retinopathy. Sci. Rep. 9, 3793. 10.1038/s41598-019-40507-8 30846767 PMC6405871 · DOI
  71. Toms, M., Dubis, A. M., Lim, W. S., Webster, A. R., Gorin, M. B. and Moosajee, M. (2019b). Missense variants in the conserved transmembrane M2 protein domain of KCNJ13 associated with retinovascular changes in humans and zebrafish. Exp. Eye Res. 189, 107852. 10.1016/j.exer.2019.107852 31647904 PMC6899441 · DOI
  72. Verta, J. P. and Jones, F. C. (2019). Predominance of cis-regulatory changes in parallel expression divergence of sticklebacks. eLife 8, e43785. 10.7554/eLife.43785 31090544 PMC6550882 · DOI
  73. 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 connexin41.8 gene. EMBO Rep. 7, 893- 897. 10.1038/sj.embor.7400757 16845369 PMC1559663 · DOI · Paper page
  74. Watanabe, M., Sawada, R., Aramaki, T., Skerrett, I. M. and Kondo, S. (2016). The physiological characterization of Connexin41.8 and Connexin39.4, which are involved in the striped pattern formation of Zebrafish. J. Biol. Chem. 291, 1053- 1063. 10.1074/jbc.M115.673129 26598520 PMC4714190 · DOI · Paper page
  75. Waterhouse, A., Bertoni, M., Bienert, S., Studer, G., Tauriello, G., Gumienny, R., Heer, F. T., de Beer, T. A. P., Rempfer, C., Bordoli, L. et al. (2018). SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res. 46, W296- W303. 10.1093/nar/gky427 29788355 PMC6030848 · DOI
  76. Wickham, H.. (2016). ggplot2: Elegant Graphics for Data Analysis, 2nd edn. Cham: Springer International Publishingr.
  77. Yelon, D., Horne, S. A. and Stainier, D. Y. (1999). Restricted expression of cardiac myosin genes reveals regulated aspects of heart tube assembly in zebrafish. Dev. Biol. 214, 23- 37. 10.1006/dbio.1999.9406 10491254 · DOI
  78. Yin, W., Kim, H. T., Wang, S., Gunawan, F., Wang, L., Kishimoto, K., Zhong, H., Roman, D., Preussner, J., Guenther, S. et al. (2018). The potassium channel KCNJ13 is essential for smooth muscle cytoskeletal organization during mouse tracheal tubulogenesis. Nat. Commun. 9, 2815. 10.1038/s41467-018-05043-5 30022023 PMC6052067 · DOI
  79. Young, G., Hundt, N., Cole, D., Fineberg, A., Andrecka, J., Tyler, A., Olerinyova, A., Ansari, A., Marklund, E. G., Collier, M. P. et al. (2018). Quantitative mass imaging of single biological macromolecules. Science 360, 423- 427. 10.1126/science.aar5839 29700264 PMC6103225 · DOI

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Authors
Podobnik, M., Singh, A. P., Fu, Z., Dooley, C. M., Frohnhöfer, H. G., Firlej, M., Stednitz, S. J., Elhabashy, H., Weyand, S., Weir, J. R., Lu, J., Nüsslein-Volhard, C., & Irion, U.
Affiliations
  • Max Planck Institute for Biology (DE)
  • Novartis Institutes for BioMedical Research 2 Chemical Biology and Therapeutics , , Cambridge, MA 02139 , USA
  • Sun Yat-sen University (CN)
  • Max Planck Institute for Heart and Lung Research (DE)
  • Max Planck Society (DE)
  • The University of Melbourne (AU)
  • University of Cambridge (GB)
  • School of Marine Sciences, Sun Yat-sen University 3 , Zhuhai 519082 , China
  • Max Planck Institute for Biology 1 , 72076 Tübingen , Germany
Corresponding author
Irion, Uwe
ORCID
Venue
Development
Publisher
The Company of Biologists
Published
2023-08-15
Volume
150
Issue
16
ISSN
  • 0950-1991 (ISSN-L)
  • 1477-9129
DOI
10.1242/dev.201627
PMC
PMC10482006
OpenAlex
W4385477211
Cited by
5
References
3
Citations by year
2026: 1 · 2025: 1 · 2024: 2 · 2023: 1
FWCI
0.72
Type
journal article
Language
en
Open access
Licence
Locations
  • Development (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Apollo (University of Cambridge) (submittedVersion, cc-by)
Funders
  • European Research Council (694289)
  • Max-Planck-Gesellschaft
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › melanin and skin pigmentation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
Keywords
KCNJ13, potassium channels, melanophores, xanthophores, iridophores, cis-regulatory evolution, zebrafish, horizontal stripes, vertical bars, color pattern, gene expression divergence
MeSH terms
Animals, Melanophores, Pigmentation, Skin, Zebrafish, Potassium Channels, Inwardly Rectifying, Cell Shape

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