Abstract
Biomineralization is a common biological phenomenon resulting in strong tissue, such as bone, tooth, and shell. Pinctada fucata martensii is an ideal animal for the study of biomineralization. Here, microarray technique was used to identify biomineralization gene in mantle edge (ME), mantle center (MC), and both ME and MC (ME-MC) for this pearl oyster. Results revealed that 804, 306, and 1127 contigs expressed at least three times higher in ME, MC, and ME-MC as those in other tissues. Blast against non-redundant database showed that 130 contigs (16.17 %), 53 contigs (17.32 %), and 248 contigs (22.01 %) hit reference genes (E ≤ −10), among which 91 contigs, 48 contigs, and 168 contigs could be assigned to 32, 26, and 63 biomineralization genes in tissue of ME, MC, and ME-MC at a threshold of 3 times upregulated expression level. The ratios of biomineralization contigs to homologous contigs were similar at 3 times, 10 times, and 100 times of upregulated expression level in either ME, MC, or ME-MC. Moreover, the ratio of biomineralization contigs was highest in MC. Although mRNA distribution characters were similar to those in other studies for eight biomineralization genes of PFMG3, Pif, nacrein, MSI7, mantle gene 6, Pfty1, prismin, and the shematrin, most biomineralization genes presented different expression profiles from existing reports. These results provided massive fundamental information for further study of biomineralization gene function, and it may be helpful for revealing gene nets of biomineralization and the molecular mechanisms underlining formation of shell and pearl for the oyster.
Similar content being viewed by others
References
Acosta-Salmón H, Southgate PC (2006) Wound healing after excision of mantle tissue from the Akoya pearl oyster, Pinctada fucata. Comp Biochem Physiol A Mol Integr Physiol 143(2):264–268
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
Chen Q, Gu ZF, Wang AM, Zhan X, Shi YH (2014) Data reassembling reveals more information of transcriptome for Pinctada fucata martensii Dunker. Prog Fish Sci 35(6):97–102. (In Chinese with English abstrct)
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(7):e21860
Gu ZF, Yin XL, Yu CC, Zhan X, Shi YH, Wang AM (2014) Expression profiles of nine biomineralization genes and their relationship with pearl nacre thickness in the pearl oyster, Pinctada fucata martensii Dunker. Aquac Res. doi:10.1111/are.12645
Han Y, Tu WW, Wen YG, Li DP, Qiu GQ, Tang HM, Peng ZH, Zhou CZ (2013) Identification and validation that up-expression of HOXA13 is a novel independent prognostic marker of a worse outcome in gastric cancer based on immunohistochemistry. Med Oncol 30(2):564
Inoue N, Ishibashi R, Ishikawa T, Atsumi T, Aoki H, Komura 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 the mantles tissues. Aquaculture 308:S68–S74
Jiang Y, Li ZS, Jiang FS, Deng X, Yao CS, Nie G (2005) Effects of different ingredients of zedoary on gene expression of HSC-T6 cells. World J Gastroenterol 11(43):6780–6786
Jiang Z, Ge S, Xing L, Han D, Kang Z, Zhang G, Wang X, Wang X, Chen P, Cao A (2013) RLP1.1, a novel wheat receptor-like protein gene, is involved in the defence response against Puccinia striiformis f. sp. tritici. J Exp Bot 64(12):3735–3746
Joubert C, Piquemal D, Marie B, Manchon L, Pierrat F, Zanella-Cléo I, Cochennec-Laureau N, Gueguen Y, Montagnani C (2010) Transcriptome and proteome analysis of Pinctada margaritifera calcifying mantle and shell: focus on biomineralization. BMC Genomics 11:613
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(6):e21238
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 from the oyster Pinctada fucata. J Biol Chem 284:10841–10854
Kono M, Hayashi N, Samata T (2000) Molecular mechanism of the nacreous layer formation in Pinctada maxima. Biochem Biophys Res Commun 269(1):213–218
Li S, Liu Q, Wang Y, Gu Y, Liu D, Wang C, Ding G, Chen J, Liu J, Gu X (2013) Differential gene expression profiling and biological process analysis in proximal nerve segments after sciatic nerve transection. PLoS One 8(2):e57000
Long Y, Li L, Li Q, He X, Cui Z (2012) Transcriptomic characterization of temperature stress responses in larval zebrafish. PLoS One 7(5): e37209
Ma Z, Huang J, Sun J, Wang G, Li C, Xie L, Zhang R (2007) A novel extrapallial fluid protein controls the morphology of nacre lamellae in the pearl oyster, Pinctada fucata. J Biol Chem 282:23253–23263
Mamangkey NG, Southgate PC (2009) Regeneration of excised mantle tissue by the silver-lip pearl oyster, Pinctada maxima (Jameson). Fish Shellfish Immunol 27(2):164–174
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 mollusc Pinctada fucata. Zool Sci 22:311–315
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
Miyashita T, Takagi Y, Miyamoto H, 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
Nagai K, Yano M, Morimoto K, Miyamoto H (2007) Tyrosinase localization in mollusc shells. Comp Biochem Physiol B Biochem Mol Biol 146(2):207–214
Narsai R, Wang C, Chen J, Wu J, Shou H, Whelan J (2013) Antagonistic, overlapping and distinct responses to biotic stress in rice (Oryza sativa) and interactions with abiotic stress. BMC Genomics 14:93
Rose-Martel M, Smiley S, Hincke MT (2015) Novel identification of matrix proteins involved in calcitic biomineralization. J Proteomics. doi:10.1016/j.jprot.2015.01.002
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
Sato Y, Inoue N, Ishikawa T, Ishibashi R, Obata M, Aoki H, Atsumi T, Komaru A (2013) Pearl microstructure and expression of shell matrix protein genes MSI31 and MSI60 in the pearl sac epithelium of Pinctada fucata by in situ hybridization. PLoS One 8(1):e52372
Shi YH, Yu CC, Gu ZF, Zhan X, Wang Y, Wang AM (2013) Characterization of the pearl oyster (Pinctada martensii) mantle transcriptome unravels biomineralization genes. Mar Biotechnol 15:175–187
Sudo S, Fujikawa T, Nagakura T, Tanaka M, Nakashima K, Takahashi T (1997) Structure of mollusk shell framework proteins. Nature 387:563–564
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
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
Takagi R, Miyashita T (2010) Prismin: a new matrix protein family in the Japanese pearl oyster (Pinctada fucata) involved in prismatic layer formation. Zool Sci 27:416–426
Takahashi J, Takagi M, Okihana Y, Takeo K, Ueda T, Touhata K, Maegawa S, Toyohara H (2012) A novel silk-like shell matrix gene is expressed in the mantle edge of the Pacific oyster prior to shell regeneration. Gene 499(1):130–134
Takeuchi T, Endo K (2006) Biphasic and dually coordinated expression of the genes encoding major shell matrix proteins in the pearl oyster Pinctada fucata. Mar Biotechnol 8:52–61
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
Wada KT, Komaru A (1996) Color and weight of pearls produced by grafting the mantle tissue from a selected population for white shell color of the Japanese pearl oyster Pinctada fucata martensii (Dunker). Aquaculture 142:25–32
Wang N, Kinoshita S, Nomura N, Riho C, Maeyama K, Nagai K, Watabe S (2012) The mining of pearl formation genes in pearl oyster Pinctada fucata by cDNA suppression subtractive hybridization. Mar Biotechnol 14(2):177–188
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
Wang X, Liu S, Xie L, Zhang R, Wang Z (2011) Pinctada fucata mantle gene 3 (PFMG3) promotes differentiation in mouse osteoblasts (MC3T3-E1). Comp Biochem Physiol B Biochem Mol Biol 158(2):173–180
Xiang L, Su J, Zheng G, Liang J, Zhang G, Wang H, Xie L, Zhang R (2013) Patterns of expression in the matrix proteins responsible for nucleation and growth of aragonite crystals in flat pearls of Pinctada fucata. PLoS One 8(6):e66564
Yan J, Du T, Zhao W, Hartmann T, Lu H, Lü Y, Ouyang H, Jiang X, Sun L, Jin C (2013) Transcriptome and biochemical analysis reveals that suppression of GPI-anchor synthesis leads to autophagy and possible necroptosis in Aspergillus fumigatus. PLoS One 8(3):e59013
Yano M, Nagai K, Morimoto K, Miyamoto H (2007) A novel nacre protein N19 in the pearl oyster Pinctada fucata. Biochem Biophys Res Commun 362:158–163
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 144:254–262
Zhan X, Gu ZF, Yu CC, Wen HY, Shi YH, Wang AM (2015) Expressed sequence tags 454 sequencing and biomineralization gene expression for pearl sac of the pearl oyster, Pinctada fucata martensii. Aquac Res 46(3):745–758
Zhang Y, Xie L, Meng Q, Jiang T, Pu R, Chen L, Zhang R (2003) A novel matrix protein participating in the nacre framework formation of pearl oyster, Pinctada fucata. Comp Biochem Physiol B Biochem Mol Biol 135:565–573
Zhang C, Xie L, Huang J, Liu X, Zhang R (2006) A novel matrix protein family participating in the prismatic layer framework formation of pearl oyster, Pinctada fucata. Biochem Biophys Res Commun 344(3):735–740
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
Acknowledgments
This study was funded by the National Science Foundation of China (41366003 and 41076112).
Author information
Authors and Affiliations
Corresponding authors
Additional information
Yaohua Shi and Xing Zheng are co-first authors
Electronic Supplementary Material
Below is the link to the electronic supplementary material.
Online Resource 1
Housekeeping genes. (XLS 1132 kb)
Online Resource 2
Probe sequences. (TXT 2195 kb)
Online Resource 3
Sequences of contig with at least 3 times up-regulated expression level in mantle tissues of P. fucata martensii. (XLS 154 kb)
Online Resource 4
Consensus and special contigs with at least 3 times up-regulated expression level compared between mantle tissues of ME and ME-MC, or MC and ME-MC of P. fucata martensii. (XLS 274 kb)
Online Resource 5
Expression level and blast results for the contigs with at least 3 times up-regulated expression level in mantle tissues of P. fucata martensii. (FA 553 kb)
Rights and permissions
About this article
Cite this article
Shi, Y., Zheng, X., Zhan, X. et al. cDNA Microarray Analysis Revealing Candidate Biomineralization Genes of the Pearl Oyster, Pinctada fucata martensii . Mar Biotechnol 18, 336–348 (2016). https://doi.org/10.1007/s10126-016-9699-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10126-016-9699-3