Skip to main content
SpringerLink
Log in

Pigmentation formation and expression analysis of tyrosinase in Siniperca chuatsi

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Animal pigmentation primarily depends on the presence and mixing ratio of chromatophores, functioning in animal survival and communication. For the benthic and carnivorous Siniperca chuatsi, pigmentation pattern is key to concealment and predation. In this study, the formation, distribution, and main pattern of chromatophores were observed in the embryos, larvae, skins, and visceral tissues from S. chuatsi. Melanophores were firstly visualized in the yolk sac at segmentation stage, and then they were migrated to the whole body and further clustered into the black stripes, bands, and patches. In adult S. chuatsi, the head, black band, and body side skins mainly contained melanophores, showing as deep or light black. The abdomen skin mainly contained iridophores, showing as silvery. In the eye, the pigment layers were located in the epithelial layers of iris and retina and shown as black. Then, the pigmentation-related gene, tyrosinase gene from S. chuatsi (Sc-tyr) was analyzed by bioinformatics and quantitative methods. The Sc-tyr gene encoded a protein with 540 amino acids (Sc-TYR). The Sc-TYR contained two copper ion binding sites, which were coordinated by six conserved histidines (H182, H205, H214, H366, H370, H393) and necessary for catalytic activity. The Sc-TYR was well conserved compared with TYR of various species with higher degree of sequence similarity with other fishes (77.6–98.3%). The qRT-PCR test showed that the Sc-tyr mRNA reached the peak value at segmentation stage in the embryo development, the black skins displayed a higher expression level than that in silvery skin, and the eye had the highest expression level compared with other tissues. Further research on enzyme activity showed that the expression patterns of tyrosinase activity were similar to that of the Sc-tyr mRNA. Comparing with the results of molecular and phenotype, it was found that the temporal and spatial distributions of tyrosinase corresponded well with changes in pigmentation patterns and the intensity of skin melanization. This study initially explored the pigmentation formation and tyrosinase expression, which served as a foundation for further insight into the genetics mechanism of body color formation in S. chuatsi.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Anistoroaei R, Fredholm M, Christensen K, Leeb T (2008) Albinism in the American mink (Neovison vison) is associated with a tyrosinase nonsense mutation. Anim Genet 39(6):645–648

    CAS  PubMed  Google Scholar 

  • Aspengren S, Sköld HN, Wallin M (2009) Different strategies for color change. Cell Mol Life Sci 66(2):187–191

    CAS  PubMed  Google Scholar 

  • Bendtsen JD, Nielsen H, Gv H, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340(4):783–795

    PubMed  Google Scholar 

  • Bilandžija H, Ma L, Parkhurst A, Jeffery WR (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(11):e80823

    PubMed  PubMed Central  Google Scholar 

  • Braasch I, Schartl M, Volff JN (2007) Evolution of pigment synthesis pathways by gene and genome duplication in fish. BMC Evol Biol 7:74

    PubMed  PubMed Central  Google Scholar 

  • Brenes-Soto A, Dierenfeld ES, Janssens GPJ (2017) Colouration in amphibians as a reflection of nutritional status: the case of tree frogs in Costa Rica. PLoS One 12(8):e0182020

    PubMed  PubMed Central  Google Scholar 

  • Burland TG (2000) DNASTAR’s Lasergene sequence analysis software. Methods Mol Biol 132:71–91

    CAS  PubMed  Google Scholar 

  • Cal L, Suarez-Bregua P, Cerdá-Reverter JM, Braasch I, Rotllant J (2017) Fish pigmentation and the melanocortin system. Comp Biochem Physiol, Part A: Mol Integr Physiol 211:26–33

    CAS  Google Scholar 

  • Camacho-Hübner A, Rossier A, Beermann F (2000) The Fugu rubripes tyrosinase gene promoter targets transgene expression to pigment cells in the mouse. Genesis 28(3–4):99–105

    PubMed  Google Scholar 

  • Camand O, Marchant D, Boutboul S, Péquignot M, Odent S, Dollfus H, Sutherland J, Levin A, Menasche M, Marsac C, Dufier JL, Heon E, Abitbol M (2001) Mutation analysis of the tyrosinase gene in oculocutaneous albinism. Hum Mutat 17(4):352

    CAS  PubMed  Google Scholar 

  • Camp E, Lardelli M (2001) Tyrosinase gene expression in zebrafish embryos. Dev Genes Evol 211(3):150–153

    CAS  PubMed  Google Scholar 

  • Cao DN, Gong SP, Yang JB, Li WY, Ge Y, Wei YF (2018) Melanin deposition ruled out as cause of color changes in the red-eared sliders (Trachemys scripta elegans). Comp Biochem Physiol, Part B: Biochem Mol Biol 217:79–85

    CAS  Google Scholar 

  • Chen WY, Wang H, Dong B, Dong ZD, Zhou FN, Fu Y, Zeng YQ (2012) Molecular cloning and expression analysis of tyrosinase gene in the skin of Jining gray goat (Capra hircus). Mol Cell Biochem 366:11–20

    CAS  PubMed  Google Scholar 

  • Commo S, Gaillard O, Thibaut S, Bernard BA (2004) Absence of TRP-2 in melanogenic melanocytes of human hair. Pigment Cell Res 17(5):488–497

    CAS  PubMed  Google Scholar 

  • Curran K, Lister JA, Kunkel GR, Prendergast A, Parichy DM, Raible DW (2010) Interplay between Foxd3 and Mitf regulates cell fate plasticity in the zebrafish neural crest. Dev Biol 344:107–118

    CAS  PubMed  PubMed Central  Google Scholar 

  • Darias MJ, Andree KB, Boglino A, Fernández I, Estévez A, Gisbert E (2013) Coordinated regulation of chromatophore differentiation and melanogenesis during the ontogeny of skin pigmentation of Solea senegalensis (Kaup, 1858). PLoS One 8(5):e63005

    CAS  PubMed  PubMed Central  Google Scholar 

  • Đorđić M, Matić IZ, Filipović-Lješković I, Džodić R, Šašić M, Erić-Nikolić A, Vuletić A, Kolundžija B, Damjanović A, Grozdanić N, Nikolić S, Pralica J, Dobrosavljević D, Rašković S, Andrejević S, Juranić Z (2012) Immunity to melanin and to tyrosinase in melanoma patients, and in people with vitiligo. BMC Complementary Altern Med 12:109

    Google Scholar 

  • Eom DS, Bain EJ, Patterson LB, Grout ME, Parichy DM (2015) Long-distance communication by specialized cellular projections during pigment pattern development and evolution. Elife 4:e12401

    PubMed  PubMed Central  Google Scholar 

  • Frohnhöfer HG, Krauss J, Maischein H-M, Nüsslein-Volhard C (2013) Iridophores and their interactions with other chromatophores are required for stripe formation in zebrafish. Development 140(14):2997–3007

    PubMed  PubMed Central  Google Scholar 

  • Frost SK, Robinson SJ (1984) Pigment cell differentiation in the fire-bellied toad, Bombina orientalis. I. Structural, chemical, and physical aspects of the adult pigment pattern. J Morphol 179(3):229–242

    PubMed  Google Scholar 

  • Fukamachi S, Sugimoto M, Mitani H, Shima A (2004) Somatolactin selectively regulates proliferation and morphogenesis of neural-crest derived pigment cells in medaka. Proc Natl Acad Sci U S A 101:10661–10666

    CAS  PubMed  PubMed Central  Google Scholar 

  • Galante Rocha de Vasconcelos FT, Hauzman E, Henriques LD, PRK G, OdF G, Sano RY, GdS S, Alfaro JL, LCDL S, Ventura DF, Bonci DMO (2017) A novel nonsense mutation in the tyrosinase gene is related to the albinism in a capuchin monkey (Sapajus apella). BMC Genet 18:39

    PubMed  PubMed Central  Google Scholar 

  • Galván I, Solano F (2016) Bird integumentary melanins: biosynthesis, forms, function and evolution. Int J Mol Sci 17:520

    PubMed  PubMed Central  Google Scholar 

  • Giebel LB, Strunk KM, Spritz RA (1991) Organization and nucleotide sequences of the human tyrosinase gene and a truncated tyrosinase-related segment. Genomics 9(3):435–445

    CAS  PubMed  Google Scholar 

  • Grønskov K, Jacob E, Brondum-Nielsen K (2007) Oculocutaneous albinism. Orphanet Journal of Rare Diseases 2:43

    PubMed  PubMed Central  Google Scholar 

  • Guo HR, Huang B, Zhang SC, Qi F (2003) Biochemical and histochemical activities of tyrosinase in the skins of normal and albino turbot scophthalmus maximus. Fish Physiol Biochem 29:67–76

    CAS  Google Scholar 

  • Gupta R, Brunak S (2002) Prediction of glycosylation across the human proteome and the correlation to protein function. Pac Symp Biocomput 7(3):310–322

    Google Scholar 

  • Hearing VJ, Tsukamoto K (1991) Enzymatic control of pigmentation in mammals. FASEB J 5(14):2902–2909

    CAS  PubMed  Google Scholar 

  • Hunter JR (1984) Feeding ecology and predation of marine fish larvae. In: Lasker R (ed) Marine fish larvae morphology. Ecology and Relation to Fisheries. Univ Washington Press, Seattle, pp 33–79

    Google Scholar 

  • Imes DL, Geary LA, Grahn RA, Lyons LA (2006) Albinism in the domestic cat (Felis catus) is associated with a tyrosinase (TYR) mutation. Anim Genet 37(2):175–178

    CAS  PubMed  PubMed Central  Google Scholar 

  • Inagaki H, Bessho Y, Koga A, Hori H (1994) Expression of the tyrosinase-encoding gene in a colorless melanophore mutant of the medaka fish, Oryzias latipes. Gene 150(2):319–324

    CAS  PubMed  Google Scholar 

  • Ito S, Wakamatsu K (2008) Chemistry of mixed melanogenesis-pivotal roles of dopaquinone. Photochem Photobiol 84:582–592

    CAS  PubMed  Google Scholar 

  • Iwata M, Corn T, Iwata S, Everett MA, Fuller BB (1990) The relationship between tyrosinase activity and skin color in human foreskins. J Invest Dermatol 95(1):9–15

    CAS  PubMed  Google Scholar 

  • Kelsh RN, Harris ML, Colanesi S, Erickson CA (2009) Stripes and belly-spots-a review of pigment cell morphogenesis in vertebrates. Semin Cell Dev Biol 20(1):90–104

    CAS  PubMed  Google Scholar 

  • Kelsh RN, Sosa KC, Owen JP, Yates CA (2017) Zebrafish adult pigment stem cells are multipotent and form pigment cells by a progressive fate restriction process. BioEssays 39(3):1600234

    Google Scholar 

  • Klaassen H, Wang YF, Adamski K, Rohner N, Kowalko JE (2018) CRISPR mutagenesis confirms the role of oca2 in melanin pigmentation in Astyanax mexicanus. Dev Biol 441(2):313–318

    CAS  PubMed  Google Scholar 

  • Klovins J, Haitina T, Fridmanis D, Kilianova Z, Kapa I (2004) The melanocortin system in Fugu: determination of POMC/AGRP/MCR gene repertoire and synteny, as well as pharmacology and anatomical distribution of the MCRs. Mol Biol Evol 21:563–579

    CAS  PubMed  Google Scholar 

  • Kottler VA, Künstner A, Schartl M (2015) Pheomelanin in fish? Pigment Cell Melanoma Res 28(3):355–356

    CAS  PubMed  Google Scholar 

  • Kubic JD, Young KP, Plummer RS, Ludvik AE, Lang D (2008) Pigmentation PAX-ways, the role of Pax3 in melanogenesis, melanocyte stem cell maintenance, and disease. Pigment Cell Melanoma Res 21:627–645

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lerner AB, Fitzpatrick TB (1950) Biochemistry of melanin formation. Physiol Rev 30(1):91–126

    CAS  PubMed  Google Scholar 

  • Liu QF, Qi YH, Liang QL, Song J, Liu JM, Li WH, Shu YQ, Tao M, Zhang C, Qin QB, Wang J, Liu SJ (2019) Targeted disruption of tyrosinase causes melanin reduction in Carassius auratus cuvieri and its hybrid progeny. Sci China Life Sci 62(9):1194–1202

    CAS  PubMed  Google Scholar 

  • Maan ME, Sefc KM (2013) Colour variation in cichlid fish: developmental mechanisms, selective pressures and evolutionary consequences. Semin Cell Dev Biol 24:516–528

    PubMed  PubMed Central  Google Scholar 

  • Martinez-Levasseur LM, Gendron D, Knell RJ, O’Toole EA, Singh M, Acevedo-Whitehouse K (2011) Acute sun damage and photoprotective responses in whales. Proc Biol Sci 278(1711):1581–1586

    PubMed  Google Scholar 

  • Masuoka Y, Maekawa K (2016) Gene expression changes in the tyrosine metabolic pathway regulate caste-specific cuticular pigmentation of termites. Insect Biochem Mol Biol 74:21–31

    CAS  PubMed  Google Scholar 

  • Matsumoto J, Seikai T (1992) Asymmetric pigmentation and pigment disorders in pleuronectiformes (flounders). Pigment Cell Res Suppl 2:275–282

    Google Scholar 

  • Murtas D, Pilloni L, Diana A, Casula L, Tomei S, Piras F, Ferreli C, Maxia C, Perra MT (2019) Tyrosinase and nestin immunohistochemical expression in melanocytic nevi as a histopathologic pattern to trace melanocyte differentiation and nevogenesis. Histochem Cell Biol 151(2):175–185

    CAS  PubMed  Google Scholar 

  • Nakamura M, Tadahisa S, Masato A, Reiji M (2010) Dual appearance of xanthophores, and ontogenetic changes in other pigment cells during early development of Japanese flounder Paralichthys olivaceus. Fisher Sci (Tokyo) 76:243–250

    CAS  Google Scholar 

  • Parichy DM, Johnson SL (2001) Zebrafish hybrids suggest genetic mechanisms for pigment pattern diversification in Danio. Dev Genes Evol 211:319–328

    CAS  PubMed  Google Scholar 

  • Parichy DM, Spiewak JE (2015) Origins of adult pigmentation: diversity in pigment stem cell lineages and implications for pattern evolution. Pigm Cell Melanoma Res 28(1):31–50

    CAS  Google Scholar 

  • Patterson LB, Parichy DM, Barsh GS (2013) Interactions with iridophores and the tissue environment required for patterning melanophores and xanthophores during Zebrafish adult pigment stripe formation. PLoS Genet 9(5):e1003561

    CAS  PubMed  PubMed Central  Google Scholar 

  • Polanowski AM, Robinson-Laverick SM, Paton D, Jarman SN (2012) Variation in the tyrosinase gene associated with a white humpback whale (Megaptera novaeangliae). J Hered 103(1):130–133

    CAS  PubMed  Google Scholar 

  • Pomerantz SH, Ances IG (1975) Tyrosinase activity in human skin influence of race and age in newborns. J Clin Invest 55(5):1127–1131

    CAS  PubMed  PubMed Central  Google Scholar 

  • Praetorius C, Grill C, Stacey SN, Metcalf AM, Gorkin DU, Robinson KC, Otterloo EV, Kim RSQ, Bergsteinsdottir K, Ogmundsdottir MH, Magnusdottir E, Mishra PJ, Davis SR, Guo T, Raza Zaidi M, Helgason AS, Sigurdsson MI, Meltzer PS, Merlino G, Petit V, Larue L, Loftus SK, Adams DR, Sobhiafshar U, Tolga Emre NC, Pavan WJ, Cornell R, Smith AG, McCallion AS, Fisher DE, Stefansson K, Sturm RA, Steingrimsson E (2013) A polymorphism in IRF4 affects human pigmentation through a tyrosinase-dependent MITF/TFAP2A pathway. cell 155:1022-1033

  • Rawls JF, Johnson SL (2000) Zebrafish kit mutation reveals primary and secondary regulation of melanocyte development during fin stripe regeneration. Development 127(17):3715–3724

    CAS  PubMed  Google Scholar 

  • Rudh A, Qvarnström A (2013) Adaptive colouration in amphibians. Semin Cell Dev Biol 24:553–561

    PubMed  Google Scholar 

  • Schmutz SM, Berryere TG, Ciobanu DC, Mileham AJ, Schmidtz BH, Fredholm M (2004) A form of albinism in cattle is caused by a tyrosinase frameshift mutation. Mamm Genome 15(1):62–67

    CAS  PubMed  Google Scholar 

  • Schwede T, Kopp J, Guex N, Peitsch MC (2003) SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 31(13):3381–3385

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sefc KM, Brown AC, Clotfelter ED (2014) Carotenoid-based coloration in cichlid fishes. Comp Biochem Physiol, Part A: Mol Integr Physiol 173:42–51

    CAS  Google Scholar 

  • Spritz RA, Ho L, Furumura M, Hearing VJ (1997) Mutational analysis of copper binding by human tyrosinase. J Invest Dermatol 109:207–212

    CAS  PubMed  Google Scholar 

  • Sugimoto M (1993) Morphological color changes in the medaka Oryzias latipes, after prolonged background adaptation-I. Changes in the population and morphology of melanophores. Comp Biochem and Physiol 104(3):513–518

    Google Scholar 

  • Sugumaran M (1998) Unified mechanism for sclerotization of insect cuticle. Adv Insect Physiol 27(8):229–334

    CAS  Google Scholar 

  • Tripathy PS, Devi NC, Parhi J, Priyadarshi H, Patel AB, Pandey PK, Mandal SC (2019) Molecular mechanisms of natural carotenoid-based pigmentation of queen loach, Botia dario (Hamilton, 1822) under captive condition. Sci Rep 9(12585):1–12

    CAS  Google Scholar 

  • Wang SH, Wang YL, Zhang ZP, Xie FJ, Lin P, Tai ZG (2009) Tyrosinase, a new innate humoral immune parameter in large yellow croaker (Pseudosciaena crocea R). Chin J Oceanol Limnol 27(3):527–535

    CAS  Google Scholar 

  • Wu XF, Hammer JA (2014) Melanosome transfer: it is best to give and receive. Curr Opin in Cell Biol 29:1–7

    Google Scholar 

  • Wu XS, Masedunskas A, Weigert R, Copeland NG, Jenkins NA, Hammer JA (2012) Melanoregulin regulates a shedding mechanism that drives melanosome transfer from melanocytes to keratinocytes. Proc Natl Acad Sci U S A 109(31):2101–2109

    Google Scholar 

  • Yamada T, Okauchi M, Araki K (2010) Origin of adult-type pigment cells forming the asymmetric pigment pattern, in Japanese flounder (Paralichthys olivaceus). Dev Dyn 239:3147–3162

    PubMed  Google Scholar 

  • Yang BY, Pu F, Li LL, You WW, Ke CH, Feng DQ (2017) Functional analysis of a tyrosinase gene involved in early larval shell biogenesis in Crassostrea angulata and its response to ocean acidification. Comp Biochem Physiol 206:8–15

    CAS  Google Scholar 

  • Yang J, Liu XL, Zhang JQ, Qing BP, Lu BZ (2012) Molecular cloning and biochemical analysis of tyrosinase from the crested ibis in China. Biochem Genet 50:936–945

    CAS  PubMed  Google Scholar 

  • Yu FF, Pan ZN, Qu BL, Yu XY, Xu KH, Deng YW, Liang FL (2018) Identification of a tyrosinase gene and its functional analysis in melanin synthesis of Pteria penguin. Gene 656:1–8

    CAS  PubMed  Google Scholar 

  • Yu X, Yu H, Kong LF, Guo F, Zhu G, Li Q (2014) Molecular cloning and differential expression in tissues of a tyrosinase gene in the Pacific oyster Crassostrea gigas. Mol Biol Rep 41(8):5403–5411

    CAS  PubMed  Google Scholar 

  • Zanna PT, Maida I, Arciuli M, Jimenez-Cervantes C, Garcia-Borron JC, Cicero R, Guida G (2009) Molecular cloning and biochemical characterization of the skin tyrosinase from Rana esculenta L. Comp Biochem Physiol, Part B: Biochem Mol Biol 152(3):234–242

    Google Scholar 

Download references

Funding

This work was financially supported by the Anhui Provincial Natural Science Foundation (1808085QC81) and the China Agriculture Research System (CARS-46, 45).

Author information

Author notes

  1. Minglin Wu and Xiaowu Chen contributed equally to this work.

Authors and Affiliations

  1. Fisheries Research Institute, Anhui Academy of Agricultural Sciences, NO.40 South Nongke Road, Luyang District, Hefei, 230031, Anhui, China

    Minglin Wu, Kai Cui, Haiyang Li & Yangyang Jiang

  2. Anhui Province Key Laboratory of Aquaculture & Stock Enhancement, NO.40 South Nongke Road, Luyang District, Hefei, 230031, Anhui, China

    Minglin Wu, Kai Cui, Haiyang Li & Yangyang Jiang

  3. National Demonstration Center for Experimental Fisheries Science Education (Shanghai Ocean University), Shanghai, 201306, China

    Xiaowu Chen

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

    Xiaowu Chen

  5. Shanghai Collaborative Innovation for Aquatic Animal Genetics and Breeding, Shanghai, 201306, China

    Xiaowu Chen

Authors
  1. Minglin Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaowu Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kai Cui
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Haiyang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yangyang Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kai Cui.

Ethics declarations

All experiments were performed according to the Experimental Animal Management Law of China and approved by the Animal Ethics Committee of Anhui Academy of Agricultural Sciences.

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wu, M., Chen, X., Cui, K. et al. Pigmentation formation and expression analysis of tyrosinase in Siniperca chuatsi. Fish Physiol Biochem 46, 1279–1293 (2020). https://doi.org/10.1007/s10695-020-00788-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-020-00788-7

Keywords

Search

Navigation