Skip to main content
Log in

Transcriptome analysis of the freshwater pearl mussel (Cristaria plicata) mantle unravels genes involved in the formation of shell and pearl

  • Original Article
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Cristaria plicata, a bivalve widespread in Eastern Asia fresh water, is utilized as the freshwater pearl mussel in China. With a high economic value in pearl production, it is also an ideal object used for the studies on biomineralization in freshwater. In the research, we performed a large-scale sequencing of Cristaria plicata mantle transcriptome using Illumina HiSeq™ 2500, obtaining 98,501 unigenes with 67,817,724 bases. 22.28 and 16.64% of the unigenes were annotated in the NR and Swiss-Prot databases, respectively. Most of the annotated unigenes were homologous with proteins of Crassostrea gigas (47.4%) and some were similar to proteins of Aplysia californica (16.7%). Here, we identified 109 homologous unigenes of 15 decided shell matrix proteins, including nacrein, Pif, perlucin, tyrosinase (Tyr), PfN44, PUSP1, chitinase, shell matrix protein, MSI80, fibronectin type III, AmOxCo, perlwapin, BMSP, PfCHS1 and CaLP. Two other mantle transcriptomes of Pinctada margaritifera and Pinctada fucata were also analyzed to perform a biomineralization protein comparison of the three molluscan transcriptomes. All the three compared mollusks shared four proteins, including nacrein, Pif, Tyr and PfCHS1. It was also discovered that Cristaria plicata shared more biomineralization proteins with Pinctada fucata than that with Pinctada margaritifera. Our study explored a whole draft of mantle transcriptome of freshwater mussel and unraveled genes involved in the formation of shell and pearl, making it possible to identify massive novel biomineralization proteins in mollusks.

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

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 

  • Fang Z, Yan Z, Li S, Wang Q, Cao W, Xu G, Xiong X, Xie L, Zhang R (2008) Localization of calmodulin and calmodulin-like protein and their functions in biomineralization in P. fucata. Prog Nat Sci 18:405–412

    Article  CAS  Google Scholar 

  • Funabara D, Ohmori F, Kinoshita S, Koyama H, Mizutani S, Ota A, Osakabe Y, Nagai K, Maeyama K, Okamoto K, Kanoh S, Asakawa S, Watabe 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:e84706

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 

  • Jiao Y, Wang H, Du X, Zhao X, Wang Q, Huang R, Deng Y (2012) Dermatopontin, a shell matrix protein gene from pearl oyster Pinctada martensii, participates in nacre formation. Biochem Biophys Res Commun 425:679–683

    Article  CAS  PubMed  Google Scholar 

  • Joubert C, Piquemal D, Marie B, Manchon L, Pierrat F, Zanella-Cleon I, Cochennec-Laureau N, Gueguen Y, Montagnani C (2010) Transcriptome and proteome analysis of Pinctada margaritifera calcifying mantle and shell: focus on biomineralization. BMC Genom 11:1–13

    Article  Google Scholar 

  • Kennedy WJ, Taylor JD, Hall A (1969) Environmental and biological controls on bivalve shell mineralogy. Biol Rev Camb Philos Soc 44:499–530

    Article  CAS  PubMed  Google Scholar 

  • Klishko OK, Lopes-Lima M, Froufe E, Bogan AE (2014) Are Cristaria herculea (Middendorff, 1847) and Cristaria plicata (Leach, 1815) (Bivalvia, Unionidae) separate species? Zookeys 438:1–15

    Article  Google Scholar 

  • Kong Y, Jing G, Yan Z, Li C, Gong N, Zhu F, Li D, Zhang Y, Zheng G, Wang H, Xie L, Zhang R (2009) Cloning and characterization of Prisilkin-39, a novel matrix protein serving a dual role in the prismatic layer formation from the Oyster Pinctada fucata. J Biol Chem 284:10841–10854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li S, Xie L, Ma Z, Zhang R (2005) cDNA cloning and characterization of a novel calmodulin-like protein from pearl oyster Pinctada fucata. FEBS J 272:4899–4910

    Article  CAS  PubMed  Google Scholar 

  • Lowenstam HA (1989) On Biomineralization. Oxford University, USA

    Google Scholar 

  • Mann K, Jackson DJ (2014) Characterization of the pigmented shell-forming proteome of the common grove snail Cepaea nemoralis. BMC Genom 15:249

    Article  Google Scholar 

  • Mann K, Edsinger-Gonzales E, Mann M (2012) In-depth proteomic analysis of a mollusc shell: acid-soluble and acid-insoluble matrix of the limpet Lottia gigantea. Proteome sci 10:28

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marie B, Roy NL, Zanella-Cléon I, Becchi M, Marin F (2011) Molecular evolution of mollusc shell proteins: insights from proteomic analysis of the edible mussel mytilus. J Mol Evol 72:531–546

    Article  CAS  PubMed  Google Scholar 

  • Marin F, Luquet G (2004) Molluscan shell proteins. CR Palevol 3:469–492

    Article  Google Scholar 

  • Marxen JC, Nimtz M, Becker W, Mann K (2003) The major soluble 19.6 kDa protein of the organic shell matrix of the freshwater snail Biomphalaria glabrata is an N-glycosylated dermatopontin. Biochim Biophys Acta Proteins Proteomics 1650:92–98

    Article  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 USA 93:9657–9660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628

    Article  CAS  PubMed  Google Scholar 

  • Nagai K, Yano M, Morimoto K, Miyamoto H (2007) Tyrosinase localization in mollusc shells. Comp Biochem Physiol B Biochem Mol Biol 146:207–214

    Article  PubMed  Google Scholar 

  • Patnaik BB, Wang TH, Kang SW, Hwang HJ, Park SY, Park EB, Chung JM, Song DK, Kim C, Kim S, Lee JS, Han YS, Park HS, Lee YS (2016) Sequencing, De Novo assembly, and annotation of the transcriptome of the endangered freshwater pearl bivalve, Cristaria plicata, provides novel insights into functional genes and marker discovery. PLoS One 11:e0148622

    Article  PubMed  PubMed Central  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 

  • Shi M, Lin Y, Xu G, Xie L, Hu X, Bao Z, Zhang R (2013a) Characterization of the Zhikong Scallop (Chlamys farreri) mantle transcriptome and identification of biomineralization-related genes. Mar Biotechnol 15:706–715

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Simakov O, Marletaz F, Cho S-J, Edsinger-Gonzales E, Havlak P, Hellsten U, Kuo D-H, Larsson T, Lv J, Arendt D, Savage R, Osoegawa K, de Jong P, Grimwood J, Chapman JA, Shapiro H, Aerts A, Otillar RP, Terry AY, Boore JL, Grigoriev IV, Lindberg DR, Seaver EC, Weisblat DA, Putnam NH, Rokhsar DS (2013) Insights into bilaterian evolution from three spiralian genomes. Nature 493:526–531

    Article  CAS  PubMed  Google Scholar 

  • Suzuki M, Sakuda S, Nagasawa H (2007) Identification of chitin in the prismatic layer of the shell and a chitin synthase gene from the Japanese pearl Oyster, Pinctada fucata. Biosci Biotechnol Biochem 71:1735–1744

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Treccani L, Mann K, Heinemann F, Fritz M (2006) Perlwapin, an abalone nacre protein with three four-disulfide core (Whey acidic protein) domains, inhibits the growth of calcium carbonate crystals. Biophys J 91:2601–2608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Yan Z (2007) Biomineralization: functions of calmodulin-like protein in the shell formation of pearl oyster. Biochim Biophys Acta Gen Subjects 1770:1338–1344

    Article  CAS  Google Scholar 

  • 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 PWH, 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 PM, Wang S, Luo L, She Z, Ming Y, Huang W, Zhang S, Huang B, Zhang Y, Qu T, Ni P, Miao G, Wang J, Wang Q, Steinberg CEW, Wang H, Li N, Qian L, Zhang G, Li Y, Yang H, Liu X, Wang J, Yin Y, Wang J (2012) The oyster genome reveals stress adaptation and complexity of shell formation. Nature 490:49–54

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work is supported by the National Natural Science Foundation of China (NSFC) under Grant No. 511022.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhiming Liu.

Ethics declarations

Conflict of interest

Every author declares that he has no conflict of interest.

Ethical approval

All applicable international, national and/or institutional guidelines for the care and use of animals were followed.

Additional information

Communicated by S. Hohmann.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 163 kb)

Supplementary material 2 (XLSX 8973 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, X., Liu, Z. & Wu, W. Transcriptome analysis of the freshwater pearl mussel (Cristaria plicata) mantle unravels genes involved in the formation of shell and pearl. Mol Genet Genomics 292, 343–352 (2017). https://doi.org/10.1007/s00438-016-1278-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-016-1278-9

Keywords

Navigation