Skip to main content
Log in

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

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

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.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

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

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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

Download references

Acknowledgments

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

Funding

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

Authors and Affiliations

Authors

Contributions

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.

Corresponding author

Correspondence to Yaqing Chang.

Ethics declarations

Competing Interests

The authors declare that they have no competing interests.

Additional information

Publisher’s Note

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

Electronic Supplementary Material

ESM 1

(DOCX 80 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-019-09913-x

Keywords

Navigation