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Histological and Expression Differences Among Different Mantle Regions of the Yesso Scallop (Patinopecten yessoensis) Provide Insights into the Molecular Mechanisms of Biomineralization and Pigmentation

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Abstract

The molecular mechanisms of shell formation and pigmentation are issues of great interest in molluscan studies due to the unique physical and biological properties of shells. The Yesso scallop, Patinopecten yessoensis, is one of the most important maricultural bivalves in Asian countries, and its shell color shows polymorphism. To gain more information about the underlying mechanisms of shell formation and pigmentation, this study presents the first analyses of histological and transcriptional differences between different mantle regions of the Yesso scallop, which are thought to be responsible for the formation of different shell layers. The results showed major microstructural differences between the edge and central mantles, which were closely associated with their functions. Different biomineralization-related GO functions, which might participate in the formation of different shell layers, were significantly enriched in the different mantle regions, indicating the different molecular functions of the two mantle regions in shell formation. The melanogenesis pathway, which controls melanin biosynthesis, was the most significantly enriched pathway in the DEGs between the two mantle regions, indicating its important role in shell pigmentation. Tyr, the key and rate-limiting gene in melanogenesis, was expressed at a remarkably high level in the central mantle, while the upstream regulatory genes included in melanogenesis were mainly upregulated in the edge mantle, suggesting the different molecular functions of the two mantle regions in shell pigmentation.

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References

  1. Addadi L, Joester D, Nudelman F, Weiner S (2006) Mollusk shell formation: a source of new concepts for understanding biomineralization processes. Chem Eur J 12:980–987

  2. Areva S, Peltola T, Säilynoja E, Laajalehto K, Linden M, Rosenholm JB (2002) Effect of albumin and fibrinogen on calcium phosphate formation on sol-gel-derived titania coatings in vitro. Chem Mater 14(4):1614–1621

  3. Audino JA, Marian JEA, Wanninger A, Lopes SG (2015) Mantle margin morphogenesis in Nodipecten nodosus (Mollusca: Bivalvia): new insights into the development and the roles of bivalve pallial folds. BMC Dev Biol 15:22

  4. Bai Z, Zheng H, Lin J, Wang G, Li J (2013) Comparative analysis of the transcriptome in tissues secreting purple and white nacre in the pearl mussel Hyriopsis cumingii. PLoS One 8:e53617

  5. Belcher AM, Wu XH, Christensen RJ, Hansma PK, Stucky GD, Morse DE (1996) Control of crystal phase switching and orientation by soluble mollusc-shell proteins. Nature 381:56–58

  6. Blank S, Arnoldi M, Khoshnavaz S, Treccani L, Kuntz M, Mann K, Grathwohl G, Fritz M (2003) The nacre protein perlucin nucleates growth of calcium carbonate crystals. J Microsc 212(3):280–291

  7. Boettiger A, Ermentrout B, Oster G (2009) The neural origins of shell structure and pattern in aquatic mollusks. Proc Natl Acad Sci 106:6837–6842

  8. Budd A, McDougall C, Green K, Degnan BM (2014) Control of shell pigmentation by secretory tubules in the abalone mantle. Front Zool 11:62

  9. Chang TS (2012) Natural melanogenesis inhibitors acting through the down-regulation of tyrosinase activity. Materials 5:1661–1685

  10. Comfort A (1949a) Acid-soluble pigments of shells. 1. The distribution of porphyrin fluorescence in molluscan shells. Biochem J 44:111–117

  11. Comfort A (1949b) Acid-soluble pigments of molluscan shells. 2. Pigments other than porphyrins. Biochem J 45:199–204

  12. Comfort A (1949c) Acid soluble pigments of molluscan shells. 3. The indigoid character of the blue pigment of Haliotis cracherodii Leach. Biochem J 45:204–208

  13. Comfort A (1951) The pigmentation of molluscan shells. Biol Rev 26:285–301

  14. Ding J, Zhao L, Chang Y, Zhao W, Du Z, Hao Z (2015) Transcriptome sequencing and characterization of Japanese scallop Patinopecten yessoensis from different shell color lines. PLoS One 10:e0116406

  15. Dou J, Li X, Fu Q, Jiao W, Li Y, Li T, Wang Y, Hu X, Wang S, Bao Z (2016) Evaluation of the 2b-RAD method for genomic selection in scallop breeding. Sci Rep 6:19244

  16. Fang D, Xu G, Hu Y, Pan C, Xie L, Zhang R (2011) Identification of genes directly involved in shell formation and their functions in pearl oyster, Pinctada fucata. PLoS One 6:e21860

  17. Feng D, Li Q, Yu H, Zhao X, Kong L (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:e0145257

  18. Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545

  19. Fu G, Valiyaveettil S, Wopenka B, Morse DE (2005) CaCO3 biomineralization: acidic 8-kDa proteins isolated from aragonitic abalone shell nacre can specifically modify calcite crystal morphology. Biomacromolecules 6:1289–1298

  20. Hedegaard C, Bardeau J-F, Chateigner D (2006) Molluscan shell pigments: an in situ resonance Raman study. J Molluscan Stud 72:157–162

  21. Hou R, Bao Z, Wang S, Su H, Li Y, Du H, Hu J, Wang S, Hu X (2011) Transcriptome sequencing and de novo analysis for Yesso scallop (Patinopecten yessoensis) using 454 GS FLX. PLoS One 6:e21560

  22. Huang J, Zhang C, Ma Z, Xie L, Zhang R (2007) A novel extracellular EF-hand protein involved in the shell formation of pearl oyster. Biochim Biophys Acta Gen Subj 1770:1037–1044

  23. Joubert C, Piquemal D, Marie B, Manchon L, Pierrat F, Zanella-Cléon I, Cochennec-Laureau N, Montagnani C (2010) Transcriptome and proteome analysis of Pinctada margaritifera calcifying mantle and shell: focus on biomineralization. BMC Genomics 11:613

  24. Kinoshita S, Wang N, Inoue H, Maeyama K, Okamoto K, Nagai K, Kondo H, Hirono I, Asakawa S, Watabe S (2011) Deep sequencing of ESTs from nacreous and prismatic layer producing tissues and a screen for novel shell formation-related genes in the pearl oyster. PLoS One 6:e21238

  25. Kröger N (2009) The molecular basis of nacre formation. Science 325:1351–1352

  26. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359

  27. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

  28. Lemer S, Saulnier D, Gueguen Y, Planes S (2015) Identification of genes associated with shell color in the black-lipped pearl oyster, Pinctada margaritifera. BMC Genomics 16:568

  29. Li Y, Zhang L, Li Y, Li W, Guo Z, Li R, Hu X, Bao Z, Wang S (2019) Dynamics of DNA methylation and DNMT expression during gametogenesis and early development of scallop Patinopecten yessoensis. Mar Biotechnol 21:196–205

  30. Liu H, Liu S, Ge Y, Liu J, Wang X, Xie L, Zhang R, Wang Z (2007) Identification and characterization of a biomineralization related gene PFMG1 highly expressed in the mantle of Pinctada fucata. Biochemistry 46:844–851

  31. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25:402–408

  32. Luo YJ, Takeuchi T, Koyanagi R, Yamada L, Kanda M, Khalturina M, Fujie M, S-i Y, Endo K, Satoh N (2015) The Lingula genome provides insights into brachiopod evolution and the origin of phosphate biomineralization. Nat Commun 6:8301

  33. Lydie MAO, Golubic S, Le Campion-Alsumard T, Payri C (2001) Developmental aspects of biomineralisation in the Polynesian pearl oyster Pinctada margaritifera var. cumingii. Oceanol Acta 24:37–49

  34. Mao J, Zhang W, Zhang X, Tian Y, Wang X, Hao Z, Chang Y (2018) Transcriptional changes in the Japanese scallop (Mizuhopecten yessoensis) shellinfested by Polydora provide insights into the molecular mechanism of shell formation and immunomodulation. Sci Rep 8:17664

  35. Mao J, Zhang X, Zhang W, Tian Y, Wang X, Hao Z, Chang Y (2019) Genome-wide identification, characterization and expression analysis of the MITF gene in Yesso scallops (Patinopecten yessoensis) with different shell colors. Gene 688:155–162

  36. Miyamoto H, Hamaguchi M, Okoshi K (2002) Analysis of genes expressed in the mantle of oyster Crassostrea gigas. Fish Sci 68:651–658

  37. Naka K, Chujo Y (2001) Control of crystal nucleation and growth of calcium carbonate by synthetic substrates. Chem Mater 13:3245–3259

  38. Pang Y, Ding J, Tian Y, Hao Z, Chang Y (2015) Analysis of shell microstructure and five surface elements of Patinopecten yessoensis at different ages. Mar Sci 39:28–34

  39. Reindl S, Haszprunar G (1996) Fine structure of caeca and mantle of arcoid and limopsoid bivalves (Mollusca: Pteriomorpha). Veliger 39:101–116

  40. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425

  41. Samata T, Hayashi N, Kono M, Hasegawa K, Horita C, Akera S (1999) A new matrix protein family related to the nacreous layer formation of Pinctada fucata. FEBS Lett 462:225–229

  42. Sudo S, Fujikawa T, Nagakura T, Ohkubo T, Sakaguchi K, Tanaka M, Nakashima K, Takahashi T (1997) Structures of mollusc shell framework proteins. Nature 387:563–564

  43. Sun X, Yang A, Wu B, Zhou L, 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

  44. Sun X, Liu Z, Zhou L, Wu B, Dong Y, Yang A (2016) Integration of next generation sequencing and EPR analysis to uncover molecular mechanism underlying shell color variation in scallops. PLoS One 11:e0161876

  45. Sun X, Wu B, Zhou L, Liu Z, Dong Y, Yang A (2017) Isolation and characterization of melanin pigment from Yesso scallop Patinopecten yessoensis. J Ocean Univ China 16:279–284

  46. Suzuki M, Murayama E, Inoue H, Ozaki N, Tohse H, Kogure T, Nagasawa H (2004) Characterization of Prismalin-14, a novel matrix protein from the prismatic layer of the Japanese pearl oyster (Pinctada fucata). Biochem J 382:205–213

  47. Suzuki M, Iwashima A, Kimura M, Kogure T, Nagasawa H (2013) The molecular evolution of the Pif family proteins in various species of mollusks. Mar Biotechnol 15:145–158

  48. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

  49. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, Van Baren MJ, Salzberg S, Wold B, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515

  50. Tsukamoto D, Sarashina I, Endo K (2004) Structure and expression of an unusually acidic matrix protein of pearl oyster shells. Biochem Biophys Res Commun 320:1175–1180

  51. Vance KW, Goding CR (2004) The transcription network regulating melanocyte development and melanoma. Pigment Cell Res 17:318–325

  52. Wang S, Hou R, Bao Z, Du H, He Y, Su H, Zhang Y, Fu X, Jiao W, Li Y, Zhang L, Wang S, Zhang L (2013) Transcriptome sequencing of Zhikong scallop (Chlamys farreri) and comparative transcriptomic analysis with Yesso scallop (Patinopecten yessoensis). PLoS One 8:e63927

  53. Wang S, Lv J, Zhang L, Dou J, Sun Y, Li X, Fu X, Dou H, Mao J, Hu X, Bao Z (2015) MethylRAD: a simple and scalable method for genome-wide DNA methylation profiling using methylation-dependent restriction enzymes. Open Biol 5:150130

  54. Wang S, Zhang J, Jiao W, Li J, Xun X, Sun Y, Guo X, Huan P, Dong B, Zhang L, Hu X, Sun X, Wang J, Zhao C, Wang Y, Wang D, Huang X, Wang R, Lv J, Li Y, Zhang Z, Liu B, Lu W, Hui Y, Liang J, Zhou Z, Hou R, Li X, Liu Y, Li H, Ning X, Lin Y, Zhao L, Xing Q, Dou J, Li Y, Mao J, Guo H, Dou H, Li T, Mu C, Jiang W, Fu Q, Fu X, Miao Y, Liu J, Yu Q, Li R, Liao H, Li X, Kong Y, Jiang Z, Chourrout D, Li R, Bao Z (2017) Scallop genome provides insights into evolution of bilaterian karyotype and development. Nat Ecol Evol 1:0120

  55. Weiss IM, Kaufmann S, Mann K, Fritz M (2000) Purification and characterization of perlucin and perlustrin, two new proteins from the shell of the mollusc Haliotis laevigata. Biochem Biophys Res Commun 267:17–21

  56. Wheeler AP, Sikes CS (1984) Regulation of carbonate calcification by organic matrix. Am Zool 24:933–944

  57. Wilbur KM, Saleuddin ASM (1983) Shell formation. In: Saleuddin ASM, Wilbur KM (eds) The mollusca, vol 4. Academic Press, New York, pp 235–287

  58. Williams ST (2016) Molluscan shell colour. Biol Rev 92(2):1039–1058

  59. Yue X, Nie Q, Xiao G, Liu B (2015) Transcriptome analysis of shell color-related genes in the clam Meretrix meretrix. Mar Biotechnol 17:364–374

  60. Zhang C, Zhang R (2006) Matrix proteins in the outer shells of molluscs. Mar Biotechnol 8:572–586

  61. Zhang M, Wang Y, Li Y, Li W, Li R, Xie X, Wang S, Hu X, Zhang L, Bao Z (2018) Identification and characterization of neuropeptides by transcriptome and proteome analyses in a bivalve mollusc Patinopecten yessoensis. Front Genet 9:197

  62. Zhao X, Wang Q, Jiao Y, Huang R, Deng Y, Wang H, Du X (2012) Identification of genes potentially related to biomineralization and immunity by transcriptome analysis of pearl sac in pearl oyster Pinctada martensii. Mar Biotechnol 14:730–739

  63. Zhao L, Li Y, Li Y, Yu J, Liao H, Wang S, Lv J, Liang J, Huang X, Bao Z (2017) A genome-wide association study identifies the genomic region associated with shell color in yesso scallop, Patinopecten yessoensis. Mar Biotechnol 19:301–309

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Acknowledgments

We thank Dalian Zhangzidao Fishery Group Co., Ltd. (Dalian, China) for providing the scallop materials.

Funding Information

This project was supported by the National Natural Science Foundation of China (31702342), the Major Science and Technology Research Project of Liaoning Province (2017203003), and the Doctoral Startup Foundation of Liaoning Province (20170520095).

Author information

Conceived and designed the experiments: JM and YC. Prepared the samples: XW, JS, and DY. Performed the experiments: JM, WZ, and YT. Analyzed the data: JM, WZ, ZH, and BH. Wrote the paper: JM and YC.

Correspondence to Yaqing Chang.

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Mao, J., Zhang, W., Wang, X. et al. Histological and Expression Differences Among Different Mantle Regions of the Yesso Scallop (Patinopecten yessoensis) Provide Insights into the Molecular Mechanisms of Biomineralization and Pigmentation. Mar Biotechnol 21, 683–696 (2019). https://doi.org/10.1007/s10126-019-09913-x

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Keywords

  • Yesso scallop
  • Mantle tissue
  • Shell formation
  • Pigmentation
  • Melanogenesis