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Integration of transcriptomics and metabolomics reveals amelanism mechanism of Oscar Astronotus ocellatus (Agassiz, 1831)

  • ADVANCES IN CICHLID RESEARCH V
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Abstract

Oscar Astronotus ocellatus (Agassiz, 1831), an Amazonian cichlid, has normal and amelanism varieties, but studies on its amelanism mechanism are scarce. Here, we investigated the ultrastructure, metabolome, and transcriptome profiles of skin from normal and amelanistic individuals. We found more stellate-shaped melanophores, mature melanosomes and melanin in normal, but less melanin, oval-shaped melanophores and immature melanosomes in amelanistic individuals. A significant separation in metabolome between normal and amelanism was observed. Pathways, e.g., biosynthesis of amino acids and unsaturated fatty acids, of differentially expressed metabolites (DEMs) involved in were significantly enriched. Transcriptome showed 323 differentially expressed genes (DEGs), of which stmn4, tyr, tyrp1, prkca, dusp8, hsp70, and wls were involved in melanin-related pathways especially tyrosine metabolism. Several classical melanin-related genes including slc24a5, acdy2, and acdy6 harbored non-synonymous SNPs in the functional domains. Integration of transcriptome and metabolome showed 18 strong correlations between DEMs and DEGs, e.g., between l-Proline and cds1, styk1, fam83b, and gimap7, between phosphorylcholine/N-alpha-Acetyl-l-lysine and myh, mical2b and mical3a, and between biopterin and dusp8. This study characterized the difference of skin melanophore, melanosome and melanin content between normal and amelanistic Oscar, and identified some candidate amelanism-related genes, metabolites and pathways, helping to understand its amelanism mechanisms.

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References

  • Aardema, M. L., M. L. J. Stiassny & S. Elizabeth Alter, 2021. Genomic analysis of the only blind cichlid reveals extensive inactivation in eye and pigment formation genes. Genome Biology and Evolution 12: 1392–1406.

    Article  Google Scholar 

  • Altschmied, J., J. Delfgaauw, B. Wilde, J. Duschl, L. Bouneau, J. N. Volff & M. Schartl, 2002. Subfunctionalization of duplicate mitf genes associated with differential degeneration of alternative exons in fish. Genetics 161: 259–267.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bahadori, R., O. Rinner, H. B. Schonthaler, O. Biehlmaier, Y. V. Makhankov, P. Rao, P. Jagadeeswaran & S. C. F. Neuhauss, 2006. The zebrafish fade out mutant: a novel genetic model for Hermansky-Pudlak syndrome. Investigative Ophthalmology & Visual Science 47: 4523–4531.

    Article  Google Scholar 

  • Bänziger, C., D. Soldini, C. Schütt, P. Zipperlen, G. Hausmann & K. Basler, 2006. Wntless, a conserved membrane protein dedicated to the secretion of WNT proteins from signaling cells. Cell 125: 509–522.

    Article  PubMed  Google Scholar 

  • Bian, C., R. Li, Z. Wen, W. Ge & Q. Shi, 2021. Phylogenetic analysis of core melanin synthesis genes provides novel insights into the molecular basis of albinism in fish. Frontiers in Genetics 12: 1–9.

    Article  Google Scholar 

  • Bilandžija, H., L. Ma, A. Parkhurst & W. R. Jeffery, 2013. A potential benefit of albinism in astyanax cavefish: downregulation of the oca2 gene increases tyrosine and catecholamine levels as an alternative to melanin synthesis. PLoS ONE 8: e80823.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bonafé, L., B. Thöny, W. Leimbacher, L. Kierat & N. Blau, 2001. Diagnosis of dopa-responsive dystonia and other tetrahydrobiopterin disorders by the study of biopterin metabolism in fibroblasts. Clinical Chemistry 47: 477–485.

    Article  PubMed  Google Scholar 

  • Braasch, I., D. Liedtke, J. N. Volff & M. Schartl, 2009. Pigmentary function and evolution of tyrp1 gene duplicates in fish. Pigment Cell & Melanoma Research 22: 839–850.

    Article  CAS  Google Scholar 

  • Breuer, M., L. Guglielmi, M. Zielonka, V. Hemberger, S. Kölker, J. G. Okun, G. F. Hoffmann, M. Carl, S. W. Sauer & T. Opladen, 2019. QDPR homologues in Danio rerio regulate melanin synthesis, early gliogenesis, and glutamine homeostasis. PLoS ONE 14: 1–19.

    Article  Google Scholar 

  • Bruders, R., H. van Hollebeke, E. J. Osborne, Z. Kronenberg, E. Maclary, M. Yandell & M. D. Shapiro, 2020. A copy number variant is associated with a spectrum of pigmentation patterns in the rock pigeon (Columba livia). PLOS Genetics 16: 1–25.

    Article  Google Scholar 

  • Burkhart, C. G. & C. N. Burkhart, 2005. The mole theory: Primary function of melanocytes and melanin may be antimicrobial defense and immunomodulation (not solar protection). International Journal of Dermatology 44: 340–342.

    Article  PubMed  Google Scholar 

  • Cao, J. & X. Cheng, 2020. Molecular evolution and characterization of fish stathmin genes. Animals 10: 1–13.

    Article  CAS  Google Scholar 

  • Chen, R., E. V. Davydov, M. Sirsota & A. J. Butte, 2010. Non-synonymous and synonymous coding SNPS show similar likelihood and effect size of human disease association. PLoS ONE 5: 1–6.

    Article  CAS  Google Scholar 

  • Chen, T., G. Song, H. Yang, L. Mao, Z. Cui & K. Huang, 2018. Development of the swimbladder surfactant system and biogenesis of lysosome-related organelles is regulated by BLOS1 in zebrafish. Genetics 208: 1131–1146.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, Y., Q. Gong, J. Lai, M. Song, Y. Liu, Y. Wu, J. Ai & Z. Long, 2020. Transcriptome analysis identifies candidate genes associated with skin color variation in Triplophysa siluroides. Comparative Biochemistry & Physiology Part D 35: 100682.

    CAS  Google Scholar 

  • Cipriano, R., K. L. S. Miskimen, B. L. Bryson, C. R. Foy, C. A. Bartel & M. W. Jackson, 2013. FAM83B-mediated activation of PI3K/AKT and MAPK signaling cooperates to promote epithelial cell transformation and resistance to targeted therapies. Oncotarget 4: 729–738.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cohen, J. N., N. M. Joseph, J. P. North, C. Onodera, A. Zembowicz, & P. E. LeBoit, 2017. Genomic analysis of pigmented epithelioid melanocytomas reveals recurrent alterations in PRKAR1A, and PRKCA Genes. The American Journal of Surgical Pathology 41: 1333–1346. https://doi.org/10.1097/PAS.0000000000000902.

    Article  PubMed  Google Scholar 

  • D’Alba, L. & M. D. Shawkey, 2019. Melanosomes: biogenesis, properties, and evolution of an ancient organelle. Physiological Reviewsa 99: 1–19.

    Article  Google Scholar 

  • Daly, C. M. S., J. Willer, R. Gregg & J. M. Gross, 2013. Snow white, a model of Hermansky-Pudlak syzndrome type 5. Genetics 195: 481–494.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dastager, S. G., W. J. Li, A. Dayanand, S. K. Tang, X. P. Tian, X. Y. Zhi, L. H. Xu & C. L. Jiang, 2006. Seperation, identification and analysis of pigment (melanin) production in Streptomyces. African Journal of Biotechnology 5: 1131–1134.

    CAS  Google Scholar 

  • Deacon, S. W., A. Nascimento, A. S. Serpinskaya & V. I. Gelfand, 2005. Regulation of bidirectional melanosome transport by organelle bound MAP kinase. Artificial Intelligence in Medicine 15: 459–463.

    CAS  Google Scholar 

  • Dooley, C. M., H. Schwarz, K. P. Mueller, A. Mongera, M. Konantz, S. C. F. Neuhauss, C. Nüsslein-Volhard & R. Geisler, 2013. 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.

    Article  CAS  PubMed  Google Scholar 

  • Edwards, M., A. Bigham, J. Tan, S. Li, A. Gozdzik, K. Ross, L. Jin & E. J. Parra, 2010. Association of the OCA2 polymorphism His615Arg with melanin content in East Asian populations: Further evidence of convergent evolution of skin pigmentation. PLOS Genetics. https://doi.org/10.1371/journal.pgen.1000867.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ehsan, B., Dina, A. E. -M., Hanaa, W., Hoda, M., Omnia, A., Jihan, H., 2015. L-arginine prevents endothelial dysfunction and restores tetrahydrobiopterin level in experimental diabetes. World Journal of Pharmaceutical Sciences.

  • Elliott, D. G., 2011. The skin | The Many Functions of Fish Integument, Elsevier Inc., Amsterdam: Encyclopedia. https://doi.org/10.1016/B978-0-12-374553-8.00285-9.

    Book  Google Scholar 

  • Fang, J., T. Chen, Q. Pan & Q. Wang, 2018. Generation of albino medaka (Oryzias latipes) by CRISPR/Cas9. Journal of Experimental Zoology Part B 330: 242–246.

    Article  CAS  Google Scholar 

  • Faria, C., L. C. Makino, L. A. Vasquez, J. Batista, K. Fernandes, F. N. Valentin, L. Satiko, O. Nakaghi, Do Carmo Faria. Paes & M., Makino, L.C., Vasquez, L.A., Fernandes, J.B.K., Valentin, F.N., Nakaghi, L.S.O., 2015. Induced reproduction and early development histology of Oscar Astronotus ocellatus (Agassiz, 1831). Zygote 23: 237–246.

    Article  Google Scholar 

  • Ficicioglu, C., 2017. Disorders of amino acid metabolism, metabolic diseases: foundations of clinical management. Genetics, and Pathology. https://doi.org/10.3233/978-1-61499-718-4-47.

    Article  Google Scholar 

  • Figlia, G., P. Willnow & A. A. Teleman, 2020. Metabolites regulate cell signaling and growth via covalent modification of proteins. Developmental Cell 54: 156–170.

    Article  CAS  PubMed  Google Scholar 

  • Fukamachi, S., M. Kinoshita, T. Tsujimura, A. Shimada, S. Oda, A. Shima, A. Meyer, S. Kawamura & H. Mitani, 2008. Rescue from oculocutaneous albinism type 4 using Medaka slc45a2 cDNA driven by its own promoter. Genetics 178: 761–769.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gong, Y., M. Hu, S. Xu, B. Wang, C. Wang, X. Mu, P. Xu & Y. Jiang, 2019. Comparative transcriptome analysis reveals expression signatures of albino Russian sturgeon. Acipenseriformes Gueldenstaedtii. Mar. Genomics 46: 1–7.

    Article  PubMed  Google Scholar 

  • Gordon, P. R. & B. A. Gilchrest, 1989. Human melanogenesis is stimulated by diacylglycerol. Journal of Investigative Dermatology 93: 700–702.

    Article  CAS  PubMed  Google Scholar 

  • Grønskov, K., C. M. Dooley, E. Østergaard, R. N. Kelsh, L. Hansen, M. P. Levesque, K. Vilhelmsen, K. Møllgård, D. L. Stemple & T. Rosenberg, 2013. Mutations in C10orf11, a melanocyte-differentiation gene, cause autosomal-recessive albinism. American Journal of Human Genetics 92: 415–421.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gross, M. C., C. H. Schneider, G. T. Valente, J. I. R. Porto, C. Martins & E. Feldberg, 2010. Comparative cytogenetic analysis of the genus symphysodon (Discus Fishes, Cichlidae): chromosomal characteristics of retrotransposons and minor ribosomal DNA. Cytogenetic and Genome Research 127: 43–53.

    Article  Google Scholar 

  • Guo, H., B. Huang, F. Qi & S. Zhang, 2007. Distribution and ultrastructure of pigment cells in the skins of normal and albino adult turbot Scophthalmus Maximus. Chinese Journal of Oceanology and Limnology 25: 199–208.

    Article  CAS  Google Scholar 

  • Haffter, P., J. Odenthal, M. C. Mullins, S. Lin, M. J. Farrell, E. Vogelsang, F. Haas, M. Brand, F. J. M. Van Eeden, M. Furutani-Seiki, M. Granato, M. Hammerschmidt, C. P. Heisenberg, Y. J. Jiang, D. A. Kane, R. N. Kelsh, N. Hopkins & C. Nüsslein-Volhard, 1996. Mutations affecting pigmentation and shape of the adult zebrafish. Development Genes and Evolution. https://doi.org/10.1007/s004270050051.

    Article  PubMed  Google Scholar 

  • Hara, M., M. Yaar, H. R. Byers, D. Goukassian, R. E. Fine, J. Gonsalves & B. A. Gilchrest, 2000. Kinesin participates in melanosomal movement along melanocyte dendrites. Journal of Investigative Dermatology 114: 438–443.

    Article  CAS  PubMed  Google Scholar 

  • Hart, J. C. & C. T. Miller, 2017. Sequence-based mapping and genome editing reveal mutations in Stickleback Hps5 cause oculocutaneous albinism and the casper phenotype. G3 Genes Genomes, Genetics 7: 3123–3131.

    CAS  PubMed  Google Scholar 

  • Hausmann, G., C. Bänziger & K. Basler, 2007. Helping Wingless take flight: How WNT proteins are secreted. Nature Reviews Molecular Cell Biology 8: 331–336.

    Article  CAS  PubMed  Google Scholar 

  • Huang, Z. R., Y. Z. Liu, J. X. Zhu, H. W. Wu & J. Guo, 2013. Involvement of the dual-specificity phosphatase M3/6 in c-Jun N-terminal kinase inactivation following cerebral ischemia in the rat hippocampus. International Journal of Neuroscience 123: 802–809.

    Article  CAS  PubMed  Google Scholar 

  • Hunt, R., Z. E. Sauna, S. V. Ambudkar, M. M. Gottesman, C. Kimchi-Sarfaty, 2009. Silent (Synonymous) SNPs: Should we care about them?, in: Methods in Molecular Biology (Clifton, N.J.). pp. 23–39. https://doi.org/10.1007/978-1-60327-411-1_2.

  • Jen, F. E. C., C. E. Jones, J. C. Wilson, B. L. Schulz & M. P. Jennings, 2013. Substrate recognition of a structure motif for phosphorylcholine post-translational modification in Neisseria meningitidis. Biochemical and Biophysical Research Communications 431: 808–814.

    Article  CAS  PubMed  Google Scholar 

  • Karunarathne, W. A. H. M., I. M. N. Molagoda, M. S. Kim, Y. H. Choi, M. Oren, E. K. Park & G. Y. Kim, 2019. Flumequine-mediated upregulation of p38 MAPK and JNK results in melanogenesis in B16F10 cells and zebrafish larvae. Biomolecules 9: 1–16.

    Article  Google Scholar 

  • Kato, M., A. Yagami, T. Tsukamoto, Y. Shinkai, T. Kato & H. Kurahashi, 2020. Novel mutation in the KITLG gene in familial progressive hyperpigmentation with or without hypopigmentation. The Journal of Dermatology 47: 669–672.

    Article  CAS  PubMed  Google Scholar 

  • Kelsh, R. N., 2004. Genetics and evolution of pigment patterns in fish. Pigment Cell & Melanoma Research 17: 326–336.

    Article  CAS  Google Scholar 

  • Kemble, H., P. Nghe & O. Tenaillon, 2019. Recent insights into the genotype–phenotype relationship from massively parallel genetic assays. Evolutionary Applications 12: 1721–1742.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kottler, V. A., A. Künstner, I. Koch, M. Flötenmeyer, T. Langenecker, M. Hoffmann, E. Sharma, D. Weigel & C. Dreyer, 2015. Adenylate cyclase 5 is required for melanophore and male pattern development in the guppy (Poecilia reticulata). Pigment Cell & Melanoma Research 28: 545–558.

    Article  CAS  Google Scholar 

  • Kratochwil, C. F., S. Urban & A. Meyer, 2019. Genome of the Malawi golden cichlid fish (Melanochromis auratus) reveals exon loss of oca2 in an amelanistic morph. Pigment Cell & Melanoma Research 32: 719–723.

    CAS  Google Scholar 

  • Lamason, R. L., M. A. P. K. Mohideen, J. R. Mest, A. C. Wong, H. L. Norton, M. C. Aros, M. J. Jurynec, X. Mao, V. R. Humphreville, J. E. Humbert, S. Sinha, J. L. Moore, P. Jagadeeswaran, W. Zhao, G. Ning, I. Makalowska, P. M. McKeigue, D. O’Donnell, R. Kittles, E. J. Parra, N. J. Mangini, D. J. Grunwald, M. D. Shriver, V. A. Canfield & K. C. Cheng, 2005. SLC24A5, a putative cation exchanger, affects pigmentation in zebrafish and humans. Science 80(310): 1782–1786.

    Article  Google Scholar 

  • Lapedriza, A., K. Petratou, R. N. Kelsh, 2014. Neural crest cells and pigmentation, in: Neural Crest Cells: Evolution, Development and Disease. pp. 287–311. https://doi.org/10.1016/B978-0-12-401730-6.00015-6

  • Lee, A.-Y. & M. Noh, 2013. The regulation of epidermal melanogenesis via cAMP and/or PKC signaling pathways: insights for the development of hypopigmenting agents. Archives of Pharmacal Research 36: 792–801.

    Article  CAS  PubMed  Google Scholar 

  • Lee, S. Y. & H. J. Lee, 2020. Comprehensive RNA-seq analysis to evaluate the pigmentation-related genes involved in albinism of cichlid fish, aulonocara baenschi. Frontiers in Marine Science 7: 1–15.

    Article  Google Scholar 

  • Leonoline Ebenezer, J., R. Gunapriya, K. Ranganathan & M. Karthik Ganesh, 2020. Biologically active compounds in Sepia pharaonis fish (Ehrenberg, 1831) ink extract from Chennai seacoast isolated by gas chromatography. Drug Discovery Today 13: 90–93.

    Google Scholar 

  • Levy, C., M. Khaled & D. E. Fisher, 2006. MITF: master regulator of melanocyte development and melanoma oncogene. Trends in Molecular Medicine 12: 406–414.

    Article  CAS  PubMed  Google Scholar 

  • Li, C. Y., J. R. Steighner, G. Sweatt, T. R. Thiele & S. A. Juntti, 2021. Manipulation of the Tyrosinase gene permits improved CRISPR/Cas editing and neural imaging in cichlid fish. Scientific Reports 11: 1–12.

    Google Scholar 

  • Li, J. H., Z. Y. Xu, M. J. Li, W. L. Zheng, X. M. Huang, F. Xiao, Y. H. Cui & H. W. Pan, 2020. LC-MS based metabolomics reveals metabolic pathway disturbance in retinal pigment epithelial cells exposed to hydroxychloroquine. Chemico-Biological Interactions 328: 109212.

    Article  CAS  PubMed  Google Scholar 

  • Li, Y., X. Geng, L. Bao, A. Elaswad, K. W. Huggins, R. Dunham & Z. Liu, 2017. A deletion in the Hermansky-Pudlak syndrome 4 (Hps4) gene appears to be responsible for albinism in channel catfish. Molecular Genetics & Genomic 292: 663–670.

    Article  CAS  Google Scholar 

  • Liu, L., X. Z. Yu, T. S. Li, L. X. Song, P. . La. Chen, T. L. Suo, Y. H. Li, S. D. Wang, Y. Chen, Y. M. Ren, S. P. Zhang, Z. J. Chang & X. Y. Fu, 2004. A novel protein tyrosine kinase NOK that shares homology with platelet-derived growth factor/fibroblast growth factor receptors induces tumorigenesis and metastasis in nude mice. Cancer Research 64: 3491–3499.

    Article  CAS  PubMed  Google Scholar 

  • Liu, R. & J. D. Molkentin, 2016. Regulation of cardiac hypertrophy and remodeling through the dual-specificity MAPK phosphatases (DUSPs). Journal of Molecular and Cellular Cardiology 101: 44–49.

    Article  PubMed  PubMed Central  Google Scholar 

  • Livak, K. J. & T. D. Schmittgen, 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25: 402–408.

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Maestre, H., L. Brinza, C. Marchet, J. Kielbassa, S. Bastien, M. Boutigny, D. Monnin, A. . El. Filali, C. M. Carareto, C. Vieira, F. Picard, N. Kremer, F. Vavre, M. F. Sagot & V. Lacroix, 2016. SNP calling from RNA-seq data without a reference genome: Identification, quantification, differential analysis and impact on the protein sequence. Nucleic Acids Research 44: 1–13.

    Google Scholar 

  • Lundquist, M. R., A. J. Storaska, T. C. Liu, S. D. Larsen, T. Evans, R. R. Neubig & S. R. Jaffrey, 2014. Redox modification of nuclear actin by MICAL-2 regulates SRF signaling. Cell 156: 563–576.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mazzuchelli, J. & C. Martins, 2009. Genomic organization of repetitive DNAs in the cichlid fish Astronotus ocellatus. Genetica 136: 461–469.

    Article  CAS  PubMed  Google Scholar 

  • Mégarbané, A., D. Piquemal, A. S. Rebillat, S. Stora, F. Pierrat, R. Bruno, F. Noguier, C. Mircher, A. Ravel, M. Vilaire-Meunier, S. Durand & G. Lefranc, 2020. Transcriptomic study in women with trisomy 21 identifies a possible role of the GTPases of the immunity-associated proteins (GIMAP) in the protection of breast cancer. Scientific Reports 10: 1–9.

    Article  Google Scholar 

  • Mello, S. A. N. D., G. J. Finlay, B. C. Baguley, M. E. Askarian-Amiri & D’mello, S.A.N., Finlay, G.J., Baguley, B.C., Askarian-Amiri, M.E., 2016. Signaling pathways in melanogenesis. Molecular Sciences 17: 1144.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mizusawa, K., Y. Yamamura, S. Kasagi & J. M. Cerdá-reverter, 2018. Expression of genes for melanotropic peptides and their receptors for morphological color change in goldfish Carassius auratus. General and Comparative Endocrinology 264: 138–150.

    Article  CAS  PubMed  Google Scholar 

  • Motiani, R. K., J. Tanwar, D. A. Raja, A. Vashisht, S. Khanna, S. Sharma, S. Srivastava, S. Sivasubbu, V. T. Natarajan & R. S. Gokhale, 2018. STIM 1 activation of adenylyl cyclase 6 connects Ca 2+ and cAMP signaling during melanogenesis. The EMBO Journal 37: 1–18.

    Article  Google Scholar 

  • Nakashima, S., 2013. Protein Kinase Cα (PKCα), in: Encyclopedia of Metalloproteins. New York: Springer, pp. 1822–1822. https://doi.org/10.1007/978-1-4614-1533-6_101019Navarro

  • Navarro, R.E., Ramos-Balderas, J.L., Guerrero, I., Pelcastre, V., Maldonado, E., 2008. Pigment dilution mutants from fish models with connection to lysosome-related organelles and vesicular traffic genes. Zebrafish 5, 309–318.

    Article  CAS  PubMed  Google Scholar 

  • Nouar, R., G. Breuzard, S. Bastonero, S. Gorokhova, P. Barbier, F. Devred, H. Kovacic & V. Peyrot, 2016. Direct evidence for the interaction of stathmin along the length and the plus end of microtubules in cells. The FASEB Journal 30: 3202–3215.

    Article  CAS  PubMed  Google Scholar 

  • Oetting, W. S. & R. A. King, 1999. Molecular basis of albinism: Mutations and polymorphisms of pigmentation genes associated with albinism. Human Mutation 13: 99–115.

    Article  CAS  PubMed  Google Scholar 

  • Otsuki, Y., Y. Okuda, K. Naruse & H. Saya, 2020. Identification of kit-ligand a as the gene responsible for the medaka pigment cell mutant few melanophore. G3: Genes, Genomes, Genetics 10: 311–319.

    Article  CAS  PubMed  Google Scholar 

  • Park, H. Y., M. Kosmadaki, M. Yaar & B. A. Gilchrest, 2009. Cellular mechanisms regulating human melanogenesis. Cellular and Molecular Life Sciences 66: 1493–1506.

    Article  CAS  PubMed  Google Scholar 

  • Park, J. S., J. H. Ryu, T. I. Choi, Y. K. Bae, S. Lee, H. J. Kang & C. H. Kim, 2016. Innate color preference of zebrafish and its use in behavioral analyses. Molecules and Cells 39: 750–755.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng, J., M. Wagle, T. Mueller, P. Mathur, B. L. Lockwood, S. Bretaud & S. Guo, 2009. Ethanol-modulated camouflage response screen in zebrafish uncovers a novel role for cAMP and extracellular signal-regulated kinase signaling in behavioral sensitivity to ethanol. Journal of Neuroscience 29: 8408–8418.

    Article  CAS  PubMed  Google Scholar 

  • Pennamen, P., A. Tingaud-Sequeira, I. Gazova, M. Keighren, L. McKie, S. Marlin, S. Gherbi Halem, J. Kaplan, C. Delevoye, D. Lacombe, C. Plaisant, V. Michaud, E. Lasseaux, S. Javerzat, I. Jackson & B. Arveiler, 2021. Dopachrome tautomerase variants in patients with oculocutaneous albinism. Genetics in Medicine 23: 479–487.

    Article  CAS  PubMed  Google Scholar 

  • Pinto, P. I. S., C. C. Guerreiro, R. A. Costa, J. F. Martinez-Blanch, C. Carballo, F. M. Codoñer, M. Manchado & D. M. Power, 2019. Understanding pseudo-albinism in sole (Solea senegalensis): a transcriptomics and metagenomics approach. Scientific Reports 9: 1–16.

    Article  Google Scholar 

  • Preller, M. & D. J. Manstein, 2012. Myosin motors: Structural aspects and functionality. Comprehensive Biophysics. https://doi.org/10.1016/B978-0-12-374920-8.00410-0.

    Article  Google Scholar 

  • Raposo, G. & M. S. Marks, 2002. The dark side of lysosome-related organelles: Specialization of the endocytic pathway for melanosome biogenesis. Traffic 3: 237–248.

    Article  PubMed  Google Scholar 

  • Rogers, S. L., I. S. Tint, P. C. Fanapour & V. I. Gelfand, 1997. Regulated bidirectional motility of melanophore pigment granules along micro tubules in vitro. Proceedings of the National Academy of Sciences of the United States of America 94: 3720–3725.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sacomoto, G. A. T., J. Kielbassa, R. Chikhi, R. Uricaru, P. Antoniou, M. F. Sagot, P. Peterlongo & V. Lacroix, 2012. Kissplice: De-novo calling alternative splicing events from RNA-seq data. BMC Bioinformatics. https://doi.org/10.1186/1471-2105-13-S6-S5.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sasaki, M., T. Horikoshi, H. Uchiwa & Y. Miyachi, 2000. Up-regulation of tyrosinase gene by nitric oxide in human melanocytes. Pigment Cell & Melanoma Research 13: 248–252.

    Article  CAS  Google Scholar 

  • Schallreuter, K. U. & J. M. Wood, 1999. The importance of L-phenylalanine transport and its autocrine turnover to L-tyrosine for melanogenesis in human epidermal melanocytes. Biochemical and Biophysical Research Communications 262: 423–428.

    Article  CAS  PubMed  Google Scholar 

  • Sköld, H. N., E. Norström & M. Wallin, 2002. Regulatory control of both microtubule- and actin-dependent fish melanosome movement. Pigment Cell & Melanoma Research 15: 357–366.

    Article  Google Scholar 

  • Slominski, A., D. J. Tobin, S. Shibahara & J. Wortsman, 2004. Melanin pigmentation in mammalian skin and its hormonal regulation. Physiological Reviews 84: 1155–1228.

    Article  CAS  PubMed  Google Scholar 

  • Song, K. H., M. Kim, J. S. Yu & A. K. Kim, 2009. The effect of L-arginine on antioxidant activity and melanogenesis in murine melanoma cells. Asian Pacific Journal of Cancer Prevention 14: 242–247.

    Google Scholar 

  • Stahl, B. A., C. R. Sears, L. Ma, M. Perkins & J. B. Gross, 2018. Pmela and Tyrp1b contribute to melanophore variation in mexican cavefis. Origin and Evolution of Biodiversity. https://doi.org/10.1007/978-3-319-95954-2.

    Article  Google Scholar 

  • Sultana, H., D. Seo, N. R. Choi, M. S. A. Bhuiyan, S. H. Lee, K. N. Heo & J. H. Lee, 2018. Identification of polymorphisms in MITF and DCT genes and their associations with plumage colors in Asian duck breeds. Asian-Australasian Journal of Animal Sciences 31: 180–188.

    Article  CAS  PubMed  Google Scholar 

  • Sun, Q., P. Rabbani, M. Takeo, S. H. Lee, C. H. Lim, E. N. S. Noel, M. M. Taketo, P. Myung, S. Millar & M. Ito, 2018. Dissecting WNT Signaling for Melanocyte Regulation during Wound Healing. Journal of Investigative Dermatology 138: 1591–1600.

    Article  CAS  PubMed  Google Scholar 

  • Turner, W. A., J. D. Taylor & T. T. Tchen, 1975. Melanosome formation in the goldfish: the role of multivesicular bodies. Journal of Ultrastructure Research 51: 16–31.

    Article  CAS  PubMed  Google Scholar 

  • Vinayavekhin, N. & A. Saghatelian, 2010. Untargeted metabolomics. Current Protocols in Molecular Biology. https://doi.org/10.1002/0471142727.mb3001s90.

    Article  PubMed  Google Scholar 

  • Wadhwa, R., L. Li, R. Singh, J. Wang, R. Gao, N. Nigam, S. Forestier, N. Ando & S. C. Kaul, 2019. Modulation of diacylglycerol-induced melanogenesis in human melanoma and primary melanocytes: role of stress chaperone mortalin. Evidence-Based Complementary and Alternative Medicine. https://doi.org/10.1155/2019/9848969.

    Article  PubMed  PubMed Central  Google Scholar 

  • Walsh, I. M., M. A. Bowman, I. F. Soto Santarriaga, A. Rodriguez & P. L. Clark, 2020. Synonymous codon substitutions perturb cotranslational protein folding in vivo and impair cell fitness. Proceedings of the National Academy of Sciences of the United States of America 117: 3528–3534.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, C., B. Lu, T. Li, G. Liang, M. Xu, X. Liu, W. Tao, L. Zhou, T. D. Kocher & D. Wang, 2021. Nile tilapia: a model for studying teleost color patterns. Journal of Heredity 112: 469–484.

    Article  CAS  PubMed  Google Scholar 

  • Wang, J., L. Hou, R. Zhang, X. Zhao, L. Jiang, W. Sun, J. An & X. Li, 2007. The tyrosinase gene family and albinism in fish. Journal of Oceanology and Limnology 25: 191–198.

    Article  CAS  Google Scholar 

  • Wang, J., P. D. Westenskow, M. Fang, M. Friedlander & G. Siuzdak, 2016. Quantitative metabolomics of photoreceptor degeneration and the effects of stem cell-derived retinal pigment epithelium transplantation. Philosophical Transactions of the Royal Society A. https://doi.org/10.1098/rsta.2015.0376.

    Article  Google Scholar 

  • Wang, Y., S. M. Li, J. Huang, S. Y. Chen & Y. P. Liu, 2014. Mutations of TYR and MITF genes are associated with plumage colour phenotypes in geese. Asian-Australasian Journal of Animal Sciences 27: 778–783.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei, L., Y. Lyu, H. Zou, Y. Wen, B. Gan, G. Zhang, S. Zhang, X. Yan & X. Ye, 2020. Skin melanin synthesis of Jinbian carp and expression analysis of transport related genes. South African Journal of Chemical Engineering 51: 453–460.

    CAS  Google Scholar 

  • Wen, B., J. Q. Zhou, J. Z. Gao, H. R. Chen, Y. Q. Shen & Z. Z. Chen, 2020. Sex-dependent changes in the skin mucus metabolome of discus fish (Symphysodon haraldi) during biparental care. Journal of Proteomics 221: 103784.

    Article  CAS  PubMed  Google Scholar 

  • Xing, L., L. Sun, S. Liu, X. Li, T. Miao, L. Zhang & H. Yang, 2017. Comparison of pigment composition and melanin content among white, light-green, dark-green, and purple morphs of sea cucumber Apostichopus Japonicus. Acta Oceanologica Sinica. 36: 45–51.

    Article  CAS  Google Scholar 

  • Xing, L., L. Sun, S. Liu, L. Zhang, J. Sun & H. Yang, 2021. Metabolomic analysis of white, green and purple morphs of sea cucumber Apostichopus japonicus during body color pigmentation process. Comparative Biochemistry and Physiology-Part D 39: 100827.

    CAS  Google Scholar 

  • Yang, B. T., B. Wen, Y. Ji, Q. Wang, H. R. Zhang, Y. Zhang, J. Z. Gao & Z. Z. Chen, 2021. Comparative metabolomics analysis of pigmentary and structural coloration in discus fish (Symphysodon haraldi). Journal of Proteomics. https://doi.org/10.1016/j.jprot.2020.104085.

    Article  PubMed  Google Scholar 

  • Yang, Z., B. Zeng, Y. Pan, P. Huang & C. Wang, 2018. Autophagy participates in isoliquiritigenin–induced melanin degradation in human epidermal keratinocytes through PI3K/AKT/mTOR signaling. Biomedicine & Pharmacotherapy 97: 248–254. https://doi.org/10.1016/j.biopha.2017.10.070.

    Article  CAS  Google Scholar 

  • Yilmaz, A., O. Üniversitesi, F. Deniz & B. Fakültesi, 2013. Oscar ( Astronotus ocellatus Agassiz, 1831) Rearing. Turkish Journal of Science 6: 51–55.

    Google Scholar 

  • Zhang, H., C. Jiang, J. Ren, J. Dong, X. Shi, X. Zhao, X. Wang, J. Wang, C. Zhong, S. Zhao, X. Liu, S. Gao & H. Yu, 2020. An advanced lipid metabolism system revealed by transcriptomic and lipidomic analyses plays a central role in peanut cold tolerance. Frontiers in Plant Science. https://doi.org/10.3389/fpls.2020.01110.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang, S., X. Li, J. Pan, M. Wang, L. Zhong, J. Wang, Q. Qin, H. Liu, J. Shao, X. Chen & W. Bian, 2019. Use of comparative transcriptome analysis to identify candidate genes related to albinism in channel catfish (Ictalurus punctatus). Aquaculture 500: 75–81.

    Article  CAS  Google Scholar 

  • Zhang, Yan, J. Xiong, J. Wang, X. Shi, G. Bao, Yang Zhang & Z. Zhu, 2008. Regulation of melanocyte apoptosis by Stathmin 1 expression. Journal of Biochemistry and Molecular Biology 41: 765–770.

    CAS  Google Scholar 

  • Zhong, Z., Z. Wu, J. Zhang & J. Chen, 2021. A novel BLOC1S5-related HPS-11 patient and zebrafish with bloc1s5 disruption. Pigment Cell & Melanoma Research 34: 1112–1119.

    Article  CAS  Google Scholar 

  • Zhu, X., R. Hao, C. Tian, J. Zhang, C. Zhu & G. Li, 2021. Integrative transcriptomics and metabolomics analysis of body color formation in the leopard coral grouper (Plectropomus leopardus). Frontiers in Marine Science 8: 1–13.

    Article  CAS  Google Scholar 

  • Zou, M., X. Zhang, Z. Shi, L. Lin, G. Ouyang, G. Zhang, H. Zheng, K. Wei & W. Ji, 2015. A comparative transcriptome analysis between wild and albino yellow catfish (Pelteobagrus fulvidraco). PLoS ONE 10: 1–16.

    Article  CAS  Google Scholar 

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Acknowledgements

This research work was supported by Natural Science Foundation of Shanghai (20ZR1423600) and Shanghai Sailing Program, China (19YF1419400).

Funding

This work was funded by the Shanghai Sailing Program, China (19YF1419400) and the Natural Science Foundation of Shanghai (20ZR1423600).

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Authors and Affiliations

  1. Key Laboratory of Freshwater Aquatic Genetic Resources, Ministry of Agriculture and Rural Affairs, Shanghai Ocean University, Shanghai, 201306, China

    Qin Wang, Bin Wen, Adekunle David Micah, Jian-Zhong Gao & Zai-Zhong Chen

  2. Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai, 201306, China

    Qin Wang, Bin Wen, Adekunle David Micah, Jian-Zhong Gao & Zai-Zhong Chen

  3. Shanghai Collaborative Innovation for Aquatic Animal Genetics and Breeding, Shanghai Ocean University, Shanghai, 201306, China

    Qin Wang, Bin Wen, Adekunle David Micah, Jian-Zhong Gao & Zai-Zhong Chen

  4. Shanghai Engineering Research Center of Aquaculture, Shanghai Ocean University, Shanghai, 201306, China

    Qin Wang, Bin Wen, Adekunle David Micah, Jian-Zhong Gao & Zai-Zhong Chen

  5. College of Fisheries and Life Science, National Demonstration Center for Experimental Fisheries Science Education, Shanghai Ocean University, Shanghai, 201306, China

    Bin Wen, Jian-Zhong Gao & Zai-Zhong Chen

Authors
  1. Qin Wang
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  2. Bin Wen
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  3. Adekunle David Micah
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  4. Jian-Zhong Gao
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  5. Zai-Zhong Chen
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Wang, Q., Wen, B., Micah, A.D. et al. Integration of transcriptomics and metabolomics reveals amelanism mechanism of Oscar Astronotus ocellatus (Agassiz, 1831). Hydrobiologia 850, 2275–2298 (2023). https://doi.org/10.1007/s10750-022-04921-w

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