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Cultured Pearl Surface Quality Profiling by the Shell Matrix Protein Gene Expression in the Biomineralised Pearl Sac Tissue of Pinctada margaritifera

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Abstract

Nucleated pearls are produced by molluscs of the Pinctada genus through the biomineralisation activity of the pearl sac tissue within the recipient oyster. The pearl sac originates from graft tissue taken from the donor oyster mantle and its functioning is crucial in determining key factors that impact pearl quality surface characteristics. The specific role of related gene regulation during gem biogenesis was unknown, so we analysed the expression profiles of eight genes encoding nacreous (PIF, MSI60, PERL1) or prismatic (SHEM5, PRISM, ASP, SHEM9) shell matrix proteins or both (CALC1) in the pearl sac (N = 211) of Pinctada margaritifera during pearl biogenesis. The pearls and pearl sacs analysed were from a uniform experimental graft with sequential harvests at 3, 6 and 9 months post-grafting. Quality traits of the corresponding pearls were recorded: surface defects, surface deposits and overall quality grade. Results showed that (1) the first 3 months of culture seem crucial for pearl quality surface determination and (2) all the genes (SHEM5, PRISM, ASP, SHEM9) encoding proteins related to calcite layer formation were over-expressed in the pearl sacs that produced low pearl surface quality. Multivariate regression tree building clearly identified three genes implicated in pearl surface quality, SHEM9, ASP and PIF. SHEM9 and ASP were clearly implicated in low pearl quality, whereas PIF was implicated in high quality. Results could be used as biomarkers for genetic improvement of P. margaritifera pearl quality and constitute a novel perspective to understanding the molecular mechanism of pearl formation.

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References

  • Achari GPK (1982) Project profile of pearl culture. Seaf Export J 14:9–11

    Google Scholar 

  • Addadi L, Weiner S (1985) Interactions between acidic proteins and crystals: stereochemical requirements in biomineralisation. Proc Natl Acad Sci U S A 82:4110–4114

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Arnaud-Haond S, Goyard E, Vonau V, Herbaut C, Prou J, Saulnier D (2007) Pearl formation: persistence of the graft during the entire process of biomineralization. Mar Biotechnol 9(1):113–116

    Article  PubMed  CAS  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 

  • Blay C, Sham-Koua M, Vonau V, Tetumu R, Cabral P, Ky CL (2014) Influence of nacre deposition rate on cultured pearl grade and colour in the black-lipped pearl oyster Pinctada margaritifera using farmed donor families. Aquac Int 22(2):937–953

    Article  CAS  Google Scholar 

  • Blay C, Planes S, Ky CL (2017) Donor and recipient contribution to phenotypic traits and the expression of biomineralisation genes in the pearl oyster model Pinctada margaritifera. Sci Rep 7(1):2696.

  • Cochennec-Laureau N, Montagnani C, Saulnier D, Fougerouse A, Levy P, Lo C (2010) A histological examination of grafting success in pearl oyster Pinctada margaritifera in French Polynesia. Aquat Living Resour 23(1):131–140

    Article  Google Scholar 

  • Cuif JP, Ball AP, Dauphin Y, Farre B, Nouet J, Perez-Huerta A, Salome’ M, Williams CT (2008) Structural, mineralogical and biochemical diversity in the lower part of the pearl layer of cultivated seawater pearls from Polynesia. Microsc Microanal 14:405–417

    Article  PubMed  CAS  Google Scholar 

  • De’Ath G (2002) Multivariate regression trees: a new technique for modeling species-environnement relationships. Ecology 83:1105–1117

    Google Scholar 

  • Ellis S, Haws M (1999) Producing pearls using the black-lip pearl oyster (Pinctada margaritifera). Aquafarmer Information Sheet 141:8

  • Falini G, Albeck S, Weiner S, Addadi L (1996) Control of aragonite or calcite polymorphism by mollusc shell macromolecules. Science 27:167–169

    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  PubMed  PubMed Central  CAS  Google Scholar 

  • Fire A, Xu SQ, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811

    Article  PubMed  CAS  Google Scholar 

  • Funabara D, Ohmori F, Kinoshita S, Koyama H, Mizutani S, Ota A, ..., Kanoh S (2014) Novel genes participating in the formation of prismatic and nacreous layers in the pearl oyster as revealed by their tissue distribution and RNA interference knockdown. PLoS One 9(1):e84706

  • Gao J, Chen Y, Yang Y, Liang J, Xie J, Liu J, ..., Zhang R (2016) The transcription factor Pf-POU3F4 regulates expression of the matrix protein genes Aspein and Prismalin-14 in pearl oyster (Pinctada fucata). FEBS J 283(10):1962–1978

  • Gardner LD, Mills D, Wiegand A, Leavesley D, Elizur A (2011) Spatial analysis of biomineralisation associated gene expression from the mantle organ of the pearl oyster Pinctada maxima. BMC Genomics 12(1):455

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Huang XD, Zhao M, Liu WG, Guan YY, Shi Y, Wang Q, ..., He MX (2013) Gigabase-scale transcriptome analysis on four species of pearl oysters. Mar Biotechnol 15(3):253–264

  • Inoue N, Ishibashi R, Ishikawa T, Atsumi T, Aoki H, Komaru A (2010) Gene expression patterns and pearl formation in the Japanese pearl oyster (Pinctada fucata): a comparison of gene expression patterns between the pearl sac and mantle tissues. Aquaculture 308:S68–S74

    Article  CAS  Google Scholar 

  • Inoue N, Ishibashi R, Ishikawa T, Atsumi T, Aoki H, Komaru A (2011a) Can the quality of pearls from the Japanese pearl oyster (Pinctada fucata) be explained by the gene expression patterns of the major shell matrix proteins in the pearl sac? Mar Biotechnol 13(1):48–55

    Article  PubMed  CAS  Google Scholar 

  • Inoue N, Ishibashi R, Ishikawa T, Atsumi T, Aoki H, Komaru A (2011b) Gene expression patterns in the outer mantle epithelial cells associated with pearl sac formation. Mar Biotechnol 13:474–483

    Article  PubMed  CAS  Google Scholar 

  • Joubert C, Piquemal D, Marie B, Manchon L, Pierrat F, Zanella-Cléon I, ..., Montagnani C (2010) Transcriptome and proteome analysis of Pinctada margaritifera calcifying mantle and shell: focus on biomineralisation. BMC Genomics 11:613–626

  • Kishore P, Southgate PC (2014) A detailed description of pearl-sac development in the black-lip pearl oyster, Pinctada margaritifera (Linnaeus 1758). Aquac Res 47(7):2215–2226

  • Ky CL, Blay C, Sham-Koua M, Vanaa V, Lo C, Cabral P (2013) Family effect on cultured pearl quality in black-lipped pearl oyster Pinctada margaritifera and insights for genetic improvement. Aquat Living Resour 26:133–145

    Article  Google Scholar 

  • Ky CL, Molinari N, Moe E, Pommier S (2014) Impact of season and grafter skill on nucleus retention and pearl oyster mortality rate in Pinctada margaritifera aquaculture. Aquac Int 22(5):1689–1701

    Article  Google Scholar 

  • Ky CL, Nakasai S, Molinari N, Devaux D (2015) Influence of grafter skill and season on cultured pearl shape, circles and rejects in Pinctada margaritifera aquaculture in Mangareva lagoon. Aquaculture 435:361–370

    Article  Google Scholar 

  • Ky CL, Okura R, Nakasai S, Devaux D (2016) Quality trait signature at archipelago scale of the cultured pearls produced by the black-lipped pearl oyster (Pinctada margaritifera Var. cumingi) in French Polynesia. J Shellfish Res 35(4):827–835

    Article  Google Scholar 

  • Levi Y, Albeck S, Brack A, Weiner S, Addadi L (1998) Control over aragonite crystal nucleation and growth: an in vitro study of biomineralisation. Chem Eur J 4:389–396

    Article  CAS  Google Scholar 

  • Liu X, Li J, Xiang L, Sun J, Zheng G, Zhang G, Zhang R (2012) The role of matrix proteins in the control of nacreous layer deposition during pearl formation. Proc R Soc Lond B Biol Sci 279(1730):1000–1007

    Article  CAS  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(4):402–408

  • Lowenstam HA, Weiner S (1989) On Biomineralisation. Oxford University Press, Oxford

    Google Scholar 

  • Ma H, Zhang B, Lee IS, Qin Z, Tong Z, Qiu S (2007) Aragonite observed in the prismatic layer of seawater cultured pearls. Front Mater Sci Chin 1:326–329

    Article  Google Scholar 

  • Marie B, Joubert C, Tayalé A, Zanella-Cléon I, Belliard C, Piquemal D, ..., Montagnani C (2012) Different secretory repertoires control the biomineralisation processes of prism and nacre deposition of the pearl oyster shell. Proc Natl Acad Sci 109:20986–20991

  • Marin F, Luquet G, Marie B, Medakovic D (2007) Molluscan shell proteins: primary structure, origin, and evolution. Curr Top Dev Biol 80:209–276

    Article  CAS  Google Scholar 

  • McGinty EL, Zenger KR, Jones DB, Jerry DR (2012) Transcriptome analysis of biomineralisation-related genes within the pearl sac: host and donor oyster contribution. Mar Genomics 5:27–33

    Article  PubMed  CAS  Google Scholar 

  • Miyamoto H, Miyashita T, Okushima M, Nakano S, Morita T, Matsushiro A (1996) A carbonic anhydrase from the nacreous layer in oyster pearls. Proc Natl Acad Sci U S A 93:9657–9660

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Miyamoto H, Miyoshi F, Kohno J (2005) The carbonic anhydrase domain protein nacrein is expressed in the epithelial cells of the mantle and acts as a negative regulator in calcification in the mollusk Pinctada fucata. Zool Sci 22:311–315

    Article  PubMed  CAS  Google Scholar 

  • Miyamoto H, Endo H, Hashimoto N, Isowa Y, Kinoshita S, Kotaki T, ..., Notazawa A (2013) The diversity of shell matrix proteins: genome-wide investigation of the pearl oyster, Pinctada fucata. Zool Sci 30:801–816

  • Miyashita T, Takagi R, Okushima M, Nakano S, Miyamoto H, Nishikawa E, Matsushiro A (2000) Complementary DNA cloning and characterization of pearlin, a new class of matrix protein in the nacreous layer of oyster pearls. Mar Biotechnol 2:409–418

    PubMed  CAS  Google Scholar 

  • Montagnani C, Marie B, Marin F, Belliard C, Riquet F, Tayalé A, ..., Cochennec-Laureau N (2011) Pmarg-Pearlin is a matrix protein involved in nacre framework formation in the pearl oyster Pinctada margaritifera. Chembiochem 12:2033–2043

  • Owens L, Malham S (2015) Review of the RNA interference pathway in molluscs including some possibilities for use in bivalves in aquaculture. J Mar Sci Eng 3(1):87–99

    Article  Google Scholar 

  • Scoones SJR (1996) The development of the pearl sac in Pinctada maxima (Jameson, 1901) (Lamellibranchia:Pteriidae) and the implications for the quality of cultured pearls. Master of Science. The University of Western Australia, Perth, p 36e79

    Google Scholar 

  • Shi Y, Yu C, Gu Z, Zhan X, Wang Y, Wang A (2013) Characterization of the pearl oyster (Pinctada martensii) mantle transcriptome unravels biomineralisation genes. Mar Biotechnol 15(2):175–187

    Article  PubMed  CAS  Google Scholar 

  • Southgate PC (2008) Pearl oyster culture. In: Southgate PC, Lucas JS (eds) The pearl oyster. Elsevier, Oxford, pp 231–272

  • Southgate PC (2011) The pearl oyster culture. In: Southgate P, Lucas J (Eds.) The pearl Oyster. Elsevier Science Publishers BV, Amsterdam, p 257

  • 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  PubMed  CAS  Google Scholar 

  • Suzuki M, Nagasawa H (2007) The structure–function relationship analysis of prismalin-14 from the prismatic layer of the Japanese pearl oyster, Pinctada fucata. FEBS J 274:5158–5166

    Article  PubMed  CAS  Google Scholar 

  • Suzuki M, Nagasawa H (2013) Mollusk shell structures and their formation mechanism. Can J Zool 91:349–366

    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  PubMed  PubMed Central  CAS  Google Scholar 

  • Suzuki M, Saruwatari K, Kogure T, Yamamoto Y, Nishimura T, Kato T, Nagasawa H (2009) An acidic matrix protein, Pif, is a key macromolecule for nacre formation. Science 325:1388–1390

    Article  PubMed  CAS  Google Scholar 

  • Takeuchi T, Sarashina I, Iijima M, Endo K (2008) In vitro regulation of CaCO3 crystal polymorphism by the highly acidic molluscan shell protein Aspein. FEBS Lett 582:591–596

    Article  PubMed  CAS  Google Scholar 

  • Tayalé A, Gueguen Y, Treguier C, Le Grand J, Cochennec-Laureau N, Montagnani C, Ky CL (2012) Evidence of donor effect on cultured pearl quality from a duplicated grafting experiment on Pinctada margaritifera using wild donors. Aquat Living Resour 25:269–280

    Article  Google Scholar 

  • Team RC (2015) R: A language and environment for statistical computing [Internet]. R Foundation for Statistical Computing; 2014, Vienna

  • Therneau TM, Atkinson B, Ripley B, Oksanen J, De’ath G (2013) mvpart: Multivariate partitioning R package version 16–1. http://CRAN.R-project.org/package=mvpart

  • 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  PubMed  CAS  Google Scholar 

  • Wada K (1968) Machanism of growth of nacre in bivalvia. Bull Natl Pearl Resour Lab 13:1490–1539

    Google Scholar 

  • Wang N, Kinoshita S, Riho C, Maeyama K, Nagai K, Watabe S (2009) Quantitative expression analysis of nacreous shell matrix protein genes in the process of pearl biogenesis. Comp Biochem Physiol B Biochem Mol Biol 154(3):346–350

    Article  PubMed  CAS  Google Scholar 

  • Weiner S, Hood L (1975) Soluble protein of the organic matrix of mollusk shells: a potential template for shell formation. Science 190:987–989

    Article  PubMed  CAS  Google Scholar 

  • Yan F, Jiao Y, Deng Y, Du X, Huang R, Wang Q, Chen W (2014) Tissue inhibitor of metalloproteinase gene from pearl oyster Pinctada martensii participates in nacre formation. Biochem Biophys Res Commun 450(1):300–305

    Article  PubMed  CAS  Google Scholar 

  • Yano M, Nagai K, Morimoto K, Miyamoto H (2006) Shematrin: a family of glycine-rich structural proteins in the shell of the pearl oyster Pinctada fucata. Comp Biochem Physiol B Biochem Mol Biol 144(2):254–262

    Article  PubMed  CAS  Google Scholar 

  • Zhan X, Gu Z, Yu C, Wen H, Shi Y, Wang A (2015) Expressed sequence tags 454 sequencing and biomineralisation gene expression for pearl sac of the pearl oyster, Pinctada fucata martensii. Aquac Res 46(3):745–758

    Article  CAS  Google Scholar 

  • Zhang G, Fang X, Guo X, Li L, Luo R, Xu F, Wang J (2012) The oyster genome reveals stress adaptation and complexity of shell formation. Nature 490:49–54

    Article  PubMed  CAS  Google Scholar 

  • Zhao M, He M, Huang X, Wang Q (2014) A homeodomain transcription factor gene, PfMSX, activates expression of Pif gene in the pearl oyster Pinctada fucata. PLoS One 9(8):e103830

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhu W, Fan S, Huang G, Zhang D, Liu B, Bi X, Yu D (2015) Highly expressed EGFR in pearl sac may facilitate the pearl formation in the pearl oyster, Pinctada fucata. Gene 566(2):201–211

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

The authors would especially like to thank the host sites: SCA Regahiga Pearls (Mangareva island, Gambier archipelago, French Polynesia) and Gauguin’s pearl farm (Rangiroa atoll, Tuamotu archipelago, French Polynesia) for their generous support. The authors are indebted to S. Parrad and S. Nakasai for their helpful assistance. C. Blay was jointed funded by an Ifremer PhD grant, with a support from the “Direction des ressources marines” and CRIOBE EPHE.

Funding

This study was supported by grants from the “Direction des ressources marines et Minières”, through the TripaGEN project (2015–2017).

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Authors and Affiliations

  1. Ifremer, UMR EIO241, Labex Corail, Centre du Pacifique, BP 49, 98719, Taravao, Tahiti, French Polynesia

    Carole Blay & Chin-Long Ky

  2. PSL Research University: EPHE-UPVD-CNRS, USR 3278 CRIOBE, Université de Perpignan, 52 Avenue Paul Alduy, 66860, Perpignan Cedex, France

    Carole Blay & Serge Planes

  3. Laboratoire d’Excellence “CORAIL”, Tahiti, French Polynesia

    Carole Blay, Serge Planes & Chin-Long Ky

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  1. Carole Blay
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  2. Serge Planes
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Correspondence to Chin-Long Ky.

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Blay, C., Planes, S. & Ky, CL. Cultured Pearl Surface Quality Profiling by the Shell Matrix Protein Gene Expression in the Biomineralised Pearl Sac Tissue of Pinctada margaritifera. Mar Biotechnol 20, 490–501 (2018). https://doi.org/10.1007/s10126-018-9811-y

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