Advertisement

Journal of Ocean University of China

, Volume 19, Issue 1, pp 183–190 | Cite as

Characteristics of a Novel Tyrosinase Gene Involved in the Formation of Shell Color in Hard Clam Meretrix meretrix

  • Hanhan Yao
  • Baoyue Cui
  • Xiaoying Li
  • Zhihua Lin
  • Yinghui DongEmail author
Article

Abstract

Hard clam (Meretrix meretrix) has a rich shell color variation among individuals from light yellow to bluish gray, brown red, and black, which may associating with melanin. Tyrosinase (Tyr) is a key rate-limiting enzyme for the biosynthesis of melanin, which affects the dark color of animal skin, hair, fur, scales and feathers. Here, we isolated and characterized the full-length cDNA sequence of M. meretrix tyrosinase gene (MmTyr) which encodes a protein with 689 amino acids. Sequence characteristics and phylogenetic analysis showed that there are a variety of Tyr genes in mollusks, which can be divided into different categories. The abundance of MmTyr transcript was detected in six tissues including mantle, adductor muscle, digestive gland, foot, gill and siphon of adult M. meretrix with qRT-PCR. The results showed a higher expression specifically in the mantle, digestive gland and siphon, which was consistent with the phenotypic color difference. In the embryos and larvae at different developmental stages, high expression was found in the trochophore larvae and juvenile clams. Among three M. meretrix strains with different shell colors, the expression level of MmTyr and total melanin content in the mantle edge both showed significant differences, suggesting that MmTyr is involved in the formation of shell color. The results obtained in this study will improve our understanding of molluscan tyrosinase gene function and molecular mechanism of shell color pattern determination.

Key words

Meretrix meretrix shell color tyrosinase melanin 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

This work was supported financially by the National Key Research and Development Program of China (No. 2018YFD0901404), the National Natural Science Foundation of China (No. 31772846), the Zhejiang Provincial Natural Science Foundation (No. LY16C190004), the General project of Zhejiang Provincial Educational Department (No. Y201329410), the Open-End Funds of Jiangsu Key Laboratory of Marine Biotechnology (No. HS16001), and the Modern Agro-Industry Technology Research System (No. CARS-49).

References

  1. Anderson, S. O., 2010. Insect cuticular sclerotization: A review. Insect Biochemistry and Molecular Biology, 40 (3): 166–178.CrossRefGoogle Scholar
  2. Brake, J., Evans, F., and Langdon, C., 2004. Evidence for genetic control of pigmentation of shell and mantle edge in selected families of Pacific oyster, Crassostrea gigas. Aquaculture, 229: 89–98.CrossRefGoogle Scholar
  3. Chen, X. I, Liu, X. J., Bai, Z. Y., Zhao, L. T., and Li, J. L., 2017. HcTyr and HcTyp-1 of Hyriopsis cumingii, novel tyrosinase and tyrosinase-related protein genes involved in nacre color formation. Comparative Biochemistry and Physiology Part B: Biochemistry & Molecular Biology, 204: 1–8.CrossRefGoogle Scholar
  4. Comfort, A., 1951. The pigmentation of molluscan shells. Biological Reviews, 26: 285–301.CrossRefGoogle Scholar
  5. Cong, R., Sun, W., Liu, G., Fan, T., Meng, X., Yang, L., and Zhu, L., 2005. Purification and characterization of phenoloxidase from clam Ruditapes philippinarum. Fish & Shellfish Immunology, 18 (1): 61–70.CrossRefGoogle Scholar
  6. Feng, D. D., Li, Q., Yu, H., Zhao, X. L., and Kong, L. F., 2015. Comparative transcriptome analysis of the Pacific oyster Crassostrea gigas characterized by shell colors: Identification of genetic bases potentially involved in pigmentation. PLoS One, 10 (12): e0145257.CrossRefGoogle Scholar
  7. Giebel, L. B., Strunk, K. M., and Spritz, R. A., 1991. Organization and nucleotide sequences of the human tyrosinase gene and truncated tyrosinase-related segment. Genomics, 9 (3): 435–445.CrossRefGoogle Scholar
  8. Gu, X. F., Lin, Z. H., Dong, Y H., and Yao, H. H., 2014. Analysis and evaluation of general nutritive components of clams (Meretrix meretrix) with three kinds of shell colors and decorative patterns. Chinese Journal of Animal Nutrition, 26 (12): 3850–3857.Google Scholar
  9. Huan, P., Liu, G., Wang, H. X., and Liu, B. Z., 2013. Identification of a tyrosinase gene potentially involved in early larval shell biogenesis of the Pacific oyster Crassostrea gigas. Development Genes and Evolution, 223 (6): 389–394.CrossRefGoogle Scholar
  10. Jolly, C., Berland, S., Milet, C., Borzeix, S., Lopez, E., and Doumenc, D., 2004. Zona localization of shell matrix protein in mantle Haliotis tuberculata (Mollusca, Gastropoda). Marine Biotechnology, 6 (6): 541–551.CrossRefGoogle Scholar
  11. Kanost, M. R., Jiang, H., and Yu, X. Q., 2004. Innate immune responses of a lepidopteran insect, Manduca sexta. Immunological Reviews, 198 (1): 97–105.CrossRefGoogle Scholar
  12. Korner, A., and Pawelek, J., 1982. Mammalian tyrosinase catalyzes three reactions in the biosynthesis of melanin. Science, 217 (4565): 1163–1165.CrossRefGoogle Scholar
  13. Lemer, S., Saulnier, D., Gueguen, Y., and Planes, S., 2015. Identification of genes association with shell color in the black-lipped pearl oyster, Pinctada margaritifera. BMC Genomics, 16 (1): 568.CrossRefGoogle Scholar
  14. Marmaras, V. J., Charalambidis, N. D., and Zervas, C. G., 1996. Immune response in insects: The role of phenoloxidase in defense reactions in relation to melanization and sclerotization. Archives of Insect Biochemistry and Physiology, 31 (2): 119–133.CrossRefGoogle Scholar
  15. Nagai, K., Yano, M., Morimoto, K., and Miyamoto, H., 2007. Tyrosinase localization in mollusc shells. Comparative Biochemistry and Physiology Part B: Biochemistry & Molecular Biology, 146 (2): 207–214.CrossRefGoogle Scholar
  16. Nell, J. A, 2001. The history of oyster farming in Australia. Marine Fisheries Reviews, 63 (3): 14–25.Google Scholar
  17. Soderhall, K., and Cerenius, L., 1998. Role of the prophenoloxidase-activating system in invertebrate immunity. Current Opinion in Immunology, 10 (1): 23–28.CrossRefGoogle Scholar
  18. Sugumaran, M., 2002. Comparative biochemistry of eumelano-genesis and the protective roles of phenoloxidase and melanin in insects. Pigment Cell & Melanoma Research, 15 (1): 2–9.CrossRefGoogle Scholar
  19. Sun, X., Yang, A., Wu, B., Zhou, L., and Liu, Z., 2015. Characterization of the mantle transcriptome of Yesso scallop (Patinopecten yessoensis): Identification of genes potentially involved in biomineralization and pigmentation. PLoS One, 10: e0122967.CrossRefGoogle Scholar
  20. Sun, X., Wu, B., Zhou, L., Liu, Z., Dong, Y., and Yang, A., 2017. Isolation and characterization of melanin pigment from Yesso scallop Patinopecten yessoensis. Journal of Ocean University of China, 16 (2): 279–284.CrossRefGoogle Scholar
  21. Takgi, R., and Miyashita, T., 2014. A cDNA cloning of a novel alpha-class tyrosinase of Pinctada fucata: Its expression analysis and characterization of the expressed protein. Enzyme Research, 2014: 1–9.CrossRefGoogle Scholar
  22. Wakamatsu, K., and Ito, S., 2002. Advanced chemical methods in melanin determination. Pigment Cell & Melanoma Research, 15 (3): 174–183.CrossRefGoogle Scholar
  23. Wakamatsu, K., Fujikawa, K., Zucca, F. A., Zecca, L., and Ito, S., 2003. The structure of neuromelanin as studied by chemical degradative methods. Journal of Neurochemistry, 86 (4): 1015–1023.CrossRefGoogle Scholar
  24. Wang, R. C., Wang, Z. P., and Zhang, J. Z., 1993. Marine Shellfish Aquaculture. Qingdao Ocean University Press, Qingdao, 322–324.Google Scholar
  25. Williams, S. T., 2017. Molluscan shell colour. Biological Reviews, 92 (2): 1039–1058.CrossRefGoogle Scholar
  26. Yu, X., Yu, H., Kong, L. F., Guo, F. G., Zhu, G., and Li, Q., 2014. Molecular cloning and differential expression in tissues of a tyrosinase gene in the Pacific oyster Crassostrea gigas. Molecular Biology Reports, 41 (8): 5403–5411.CrossRefGoogle Scholar
  27. Yue, X., Nie, Q., Xiao, G. Q., and Liu, B. Z., 2015. Transcriptome analysis of shell color-related genes in the clam Meretrix meretrix. Marine Biotechnology, 17 (3): 364–374.CrossRefGoogle Scholar
  28. Zhang, C., Xie, L. P., Huang, J., Chen, L., and Zhang, R. Q., 2006. A novel putative tyrosinase involved in periostracum formation from the peal oyster (Pinctada fucata). Biochemical and Biophysical Research Communications, 342 (2): 632–639.CrossRefGoogle Scholar
  29. Zhang, G., Fang, X., Guo, X., Li, L., Luo, R., Xu, F., Yang, P., Zhang, L., Wang, X., Qi, H., Xiong, Z., Que, H., Xie, Y., Holland, P. W., Paps, J., Zhu, Y., Wu, F., Chen, Y., Wang, J., Peng, C., Meng, J., Yang, L., Liu, J., Wen, B., Zhang, N., Huang, Z., Zhu, Q., Feng, Y., Mount, A., Hedgecock, D., Xu, Z., Liu, Y., Domazet- Loso, T., Du, Y., Sun, X., Zhang, S., Liu, B., Cheng, P., Jiang, X., Li, J., Fan, D., Wang, W., Fu, W., Wang, T., Wang, B., Zhang, J., Peng, Z., Li, Y., Li, N., Wang, J., Chen, M., He, Y., Tan, F., Song, X., Zheng, Q., Huang, R., Yang, H., Du, X., Chen, L., Yang, M., Gaffney, P. M., Wang, S., Luo, L., She, Z., Ming, Y., Huang, W., Zhang, S., Huang, B., Zhang, Y., Qu, T., Ni, P., Mao, G., Wang, J., Wang, Q., Steinberg, C. E., Wang, H., Li, N., Qian, L., Zhang, G., Li, Y., Yang, H., Liu, X., Wang, J., Yin, Y., and Wang, J., 2012. The oyster genome reveals stress adaptation and complexity of shell formation. Nature, 490 (7418): 49–54.CrossRefGoogle Scholar
  30. Zhou, Z., Ni, D. J., Wang, M. Q., Wang, L. L., Shi, X. W., Yue, F., Liu, R., and Song, L. S., 2012. The phenoloxidase activity and antibacterial function of a tyrosinase from scallop Chlamysfarreri. Fish & Shellfish Immunology, 33 (2): 375–381.CrossRefGoogle Scholar
  31. Zhu, D. L., Lin, Z. H., Dong, Y. H., and Yao, H. H., 2011. Genetic variation analysis of four strains of Meretrix meretrix that have different shell colors and decorative patterns. Oceanlogia et Limnologia Sinica, 42 (3): 374–379.Google Scholar

Copyright information

© Ocean University of China, Science Press and Springer-Verlag GmbH Germany 2020

Authors and Affiliations

  • Hanhan Yao
    • 1
  • Baoyue Cui
    • 1
  • Xiaoying Li
    • 2
  • Zhihua Lin
    • 1
  • Yinghui Dong
    • 1
    Email author
  1. 1.Zhejiang Key Laboratory of Aquatic Germplasm Resources, College of Biological & Environmental SciencesZhejiang Wanli UniversityNingboChina
  2. 2.Jiangsu Key Laboratory of Marine BiotechnologyJiangsu Ocean UniversityLianyungangChina

Personalised recommendations