Identification of genes associated with shell color in the black-lipped pearl oyster, Pinctada margaritifera

BMC Genomics

Serge Planes¹  Yannick Gueguen²  Denis Saulnier³  Sarah Lemer⁴ 

[1] Laboratoire d’Excellence “CORAIL”, USR 3278 CNRS-CRIOBE- EPHE, Perpignan, France, Papetoai, Moorea, French Polynesia;Present address: Ifremer, UMR 5244 IHPE, UPVD, CNRS, Université de Montpellier, CC 80, Montpellier, F-34095, France;Ifremer, UMR 241 EIO, Laboratoire d’Excellence “CORAIL”, BP 7004, Taravao, 98719, Tahiti, French Polynesia;Present address: Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, 26 Oxford Street, Cambridge 02138, MA, USA

关键词: Albino;    Pigmentation;    Pearl;    Nacre;    Biomineralization;    Differential expression;   

Others  :  1222453
DOI  :  10.1186/s12864-015-1776-x

 received in 2014-12-06, accepted in 2015-07-14,  发布年份 2015

【 授权许可】

   
2015 Lemer et al.

【 参考文献 】

• [1]Liu X, Wu F, Zhao H, Zang G, Guo X. A novel shell color variant of the Pacific abalone Haliotis discus hannai Ino subject to genetic control and dietary influence. J Shellfish Res. 2009; 28:419-424.
• [2]Canales-Gómez E, Correa G, Viana MT. Effect of commercial carotene pigments (astaxanthin, cantaxanthin and β-carotene) in juvenile abalone Haliotis rufescens diets on the color of the shell or nacre. Vet Mexico. 2010; 41:191-200.
• [3]David JI, Leslie EH. Inheritance of a shell-color polymorphism in the mussel. J Hered. 1977; 68:203-204.
• [4]Kraeuter J, Adamkewicz L, Castagna M, Wall R, Karney R. Rib number and shell color in hybridized subspecies of the Atlantic bay scallop, Argopecten irradians. Nautilus. 1984; 98:17-20.
• [5]Adamkewicz L, Castagna M. Genetics of shell color and pattern in the bay scallop Argopecten irradians. J Hered. 1988; 79:14-17.
• [6]Palmer AR. Genetic basis of shell variation in Thais emarginata (Prosobranchia, Muricacea). I. Banding in populations from Vancouver Island. Bio Bull. 1985; 169:638-651.
• [7]Ekendahl A, Johannesson K. Shell colour variation in Littorina saxatilis Olivi (Prosobranchia: Littorinidae): a multi-factor approach. Bio J Linn Soc Lond. 1997; 62:401-419.
• [8]Yusa Y. Inheritance of colour polymorphism and the pattern of sperm competition in the apple snail Pomacea canaliculata (Gastropoda: Ampullariidae). J Molluscan Stud. 2004; 70:43-48.
• [9]Peignon JM, Gerard A, Naciri Y, Ledu C, Phelipot P. Analysis of the shell color determinism in the Manila clam Ruditapes philippinarum. Aquat Living Resour. 1995; 8:181-189.
• [10]Winkler FM, Estevez BF, Jollan LB, Garrido JP. Inheritance of the general shell color in the scallop Argopecten purpuratus (Bivalvia : Pectinidae). J Hered. 2001; 92:521-525.
• [11]Wen H, Gu R, Cao Z, Zhou X, Nie Z, Ge X, Xu P, Hua D. Variation of color and ray pattern in juvenile shells in hatchery-produced freshwater triangle pearl mussels, Hyriopsis cumingii, in China. J World Aquac Soc. 2013; 44:154-160.
• [12]Samata T, Hayashi N, Kono M, Hasegawa K, Horita C, Akera S. A new matrix protein family related to the nacreous layer formation of Pinctada fucata. FEBS Lett. 1999; 462:225-229.
• [13]Weiss IM, Kaufmann S, Mann K, Fritz M. Purification and Characterization of Perlucin and Perlustrin, Two New Proteins from the Shell of the Mollusc Haliotis laevigata. Biochem Biophys Res Commun. 2000; 267:17-21.
• [14]Suzuki M, Murayamae E, Inoue H, Ozaki N, Tohse H, Kogure T, Nagasawa H. Characterization of Prismalin-14, a novelmatrix protein from the prismatic layer of the Japanese pearl oyster, Pinctada fucata. Biochem J. 2004; 382:205-213.
• [15]Zhang C, Li S, Ma Z, Xie L, Zhang R. A novel matrix protein p10 from the nacre of pearl oyster (Pinctada fucata) and its effects on both CaCO3 crystal formation and mineralogenic cells. Mar Biotechnol (NY). 2006; 8:624-633.
• [16]Marie B, Marie A, Jackson DJ, Dubost L, Degnan BM, Milet C, Marin F. Proteomic analysis of the organic matrix of the abalone Haliotis asinina calcified shell. Proteome Sci. 2010; 8:54. BioMed Central Full Text
• [17]Marie B, Zanella-Cléon I, Roy L, Becchi M, Luquet G, Marin F. Proteomic analysis of the acid-soluble nacre matrix of the bivalve Unio pictorum: Detection of Novel Carbonic Anhydrase and Putative Protease Inhibitor Proteins. ChemBioChem. 2010; 11:2138-2147.
• [18]Marie B, Le Roy N, Zanella-Cléon I, Becchi M, Marin F. Molecular evolution of mollusc shell proteins: insights from proteomic analysis of the edible mussel Mytilus. J Mol Evol. 2011; 72:531-546.
• [19]Marie B, Trinkler N, Zanella-Cléon I, Guichard N, Becchi M, Paillard C, Marin F. Proteomic identification of novel proteins from the calcifying shell matrix of the Manila clam Venerupis philippinarum. Mar Biotechnol (NY). 2011; 13:955-962.
• [20]Marie B, Joubert C, Belliard C, Tayale A, Zanella-Cléon I, Marin F, Gueguen Y, Montagnani C. Characterization of MRNP34, a novel methionine-rich nacre protein from the pearl oysters. Amino Acids. 2012; 42:2009-2017.
• [21]Joubert C, Piquemal D, Marie B, Manchon L, Pierrat F, Zanella-Cleon I, Cochennec-Laureau N, Gueguen Y, Montagnani C. Transcriptome and proteome analysis of Pinctada margaritifera calcifying mantle and shell: focus on biomineralization. BMC Genomics. 2010; 11:613. BioMed Central Full Text
• [22]Miyashita T, Hanashita T, Toriyama M, Takagi R, Akashika T, Higashikubo N. Gene cloning and biochemical characterization of the BMP-2 of Pinctada fucata. Biosci Biotechnol Biochem. 2008; 72:37-47.
• [23]Wang A, Wang Y, Gu Z, Li S, Shi Y, Guo X. Development of expressed sequence tags from the pearl oyster, Pinctada martensii Dunker. Marine Biotechnol. 2011; 13:275-283.
• [24]Berland S, Marie A, Duplat D, Milet C, Sire JY, Bédouet L. Coupling proteomics and transcriptomics for the identification of novel and variant forms of mollusk shell proteins: a study with P. margaritifera. ChemBioChem. 2011; 12:950-961.
• [25]Gardner LD, Milss D, Wiegand A, Leavesley D, Elizur A. Spatial analysis of biomineralization associated gene expression from the mantle organ of the pearl oyster Pinctada maxima. BMC Genomics. 2011; 12:455. BioMed Central Full Text
• [26]Shi Y, Yu C, Gu Z, Zhan X, Wang Y, Wang A. Characterization of the pearl oyster (Pinctada martensii) mantle transcriptome unravels biomineralization genes. Mar Biotechnol. 2013; 15:175-187.
• [27]Liu Y, Shigley JE, Hurwit KN. Iridescence color of a shell of the mollusk Pinctada margaritifera caused by diffraction. Opt Express. 1999; 4:177-182.
• [28]Tan T, Wong D, Lee P. Iridescence of a shell of mollusk Haliotis glabra. Opt Express. 2004; 12:4847-4854.
• [29]Snow MR, Pring A, Self P, Losic D, Shapter J. The origin of pearls in iridescence from nano-composite structures of the nacre. Am Mineral. 2004; 89:1353-1358.
• [30]Takahashi K, Yamamoto H, Onoda A, Doi M, Inaba T, Chiba M, et al. Highly oriented aragonite nanocrystal-biopolymer composites in an aragonite brick of the nacreous layer of Pinctada fucata. Chem Commun. 2004;996–997.
• [31]Nudelman F, Shimoni E, Klein E, Rousseau M, Bourrat X, Lopez E, Addadi L, Weiner S. Forming nacreous layer of the shells of the bivalves Atrina rigida and Pinctada margaritifera: An environmental- and cryo-scanning electron microscopy study. J Struct Biol. 2008; 162:290-300.
• [32]Farre B, Brunelle A, Laprévote O, Cuif JP, Williams CT, Dauphin Y. Shell layers of the black-lip pearl oyster Pinctada margaritifera: matching microstructures and composition. Comp Biochem Physiol B Biochem Mol Biol. 2011; 159:131-139.
• [33]Raman C. On iridescent shells. Part II. Colours of laminar diffraction. Proc Indian Acad Sci. 1935; A1:574-589.
• [34]Webster R, Anderson BW. Gems, their sources, descriptions and identification. Buterworths, London; 1983.
• [35]Marin F, Luquet G, Marie B, Medakovic D. Molluscan shell proteins: primary structure, origin, and evolution. Curr Top Dev Biol. 2007; 80:209-276.
• [36]Kinoshita S, Wang N, Inoue H, Maeyama K, Okamoto K, Nagai K, Kondo H, Hirono I, Asakawa S, Watabe S. 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. 2011; 6: Article ID e21238
• [37]Marie B, Joubert C, Tayalé A, Zanella-Cléon I, Belliard C, Piquemal D, Cochennec-Laureau N, Marin F, Gueguen Y, Montagnani C. Different secretory repertoires control the biomineralization processes of prism and nacre deposition of the pearl oyster shell. Proc Natl Acad Sci U S A. 2012; 109:20986-20991.
• [38]Belcher AM, Wu X, Christensen R, Hansma P, Stucky G, Morse D. Control of crystal phase switching and orientation by soluble mollusc-shell proteins. Nature. 1996; 381:56-58.
• [39]Falini G, Albeck S, Weiner S, Addadi L. Control of aragonite or calcite polymorphism by mollusk shell macromolecules. Science. 1996; 271:67-69.
• [40]Addadi L, Weiner S. Interactions between acidic proteins and crystals: stereochemical requirements in biomineralization. Proc Natl Acad Sci U S A. 1985; 82:4110-4114.
• [41]Weiner S, Hood L. Soluble protein of the organic matrix of mollusk shells: a potential template for shell formation. Science. 1975; 190:987-989.
• [42]Le Pennec M, Anastas M, Bichet H, Buestel D, Cochard J, Cochennec-Laureau N, Coeroli M, Conte E, Correia A, Fougerousse-Tsing A, Langy S, Le Moullac G, Lo C, Peltzer L, Pham A. Huître Perlière et Perle de Tahiti. Faaa, French Polynesia; 2010.
• [43]Bassi MT, Schiaffino MV, Renieri A, Denigris F, Galli L, Bruttini M, Gebbia M, Bergen AAB, Lewis RA, Ballabio A. Cloning of the gene for ocular albinism type 1 from the distal short arm of the X chromosome. Nat Genet. 1995; 10:13-19.
• [44]King RA, Summers CG. Albinism. Dermatol Clin. 1988; 6:217-228.
• [45]Tomita Y, Takeda A, Okinaga S, Tagami H, Shibahara S. Human oculocutaneous albinism caused by single base insertion in the tyrosinase gene. Biochem Biophys Res Commun. 1989; 164:990-996.
• [46]Nakamura K, Ozaki A, Akutsu T, Iwai K, Sakamoto T, Yoshizaki G, Okamoto N. Genetic mapping of the dominant albino locus in rainbow trout (Oncorhynchus mykiss). Mol Genet Genomics. 2001; 265:687-693.
• [47]King RA, Willaert RK, Schmidt RM, Pietsch J, Savage S, Brott MJ, Fryer JP, Summers CG, Oetting WS. MC1R mutations modify the classic phenotype of oculocutaneous albinism type 2 (OCA2). Am J Hum Genet. 2003; 73:638-645.
• [48]Boissy RE, Zhao HQ, Oetting WS, Austin LM, Wildenberg SC, Boissy YL, Zhao Y, Sturm RA, Hearing VJ, King RA, Nordlund JJ. Mutation in and lack of expression of tyrosinase-related protein-1 (TRP-1) in melanocytes from an individual with brown oculocutaneous albinism: A new subtype of albinism classified as ”OCA3”. Am J Hum Genet. 1996; 58:1145-1156.
• [49]Newton JM, Cohen-Barak O, Hagiwara N, Gardner JM, Davisson MT, King RA, Brilliant MH. Mutations in the human orthologue of the mouse underwhite gene (uw) underlie a new form of oculocutaneous albinism, OCA4. Am J Hum Genet. 2001; 69:981-988.
• [50]Fox DL, Hochachka PW. Biochromy of the Mollusca. In: The Mollusca. Volume 2. Saleudin ASM, Wilbur KM, editors. Academic, New York; 1983: p.281-303.
• [51]Jabbour-Zahab R, Chagot D, Blanc F, Grizel H. Mantle histology, histochemistry and ultrastructure of the pearl oyster pinctada margaritifera (L.). Aquat Living Res. 1992; 5:287-298.
• [52]Zhang C, Xie LP, Huang J, Chen L, Zhang RQ. A novel putative tyrosinase involved in periostracum formation from the pearl oyster (Pinctada fucata). Biochem Biophys Res Commun. 2006; 342:632-639.
• [53]Nagai K, Yano M, Morimoto K, Miyamoto H. Tyrosinase localization in mollusc shells. Comp Comp Biochem Physiol B Biochem Mol Biol. 2007; 146:207-214.
• [54]Diatchenko L, Lukyanov S, Lau YFC, Siebert PD. Suppression subtractive hybridization: A versatile method for identifying differentially expressed genes. Methods Enzymol. 1999; 303:349-380.
• [55]Rebrikov DV, Britanova OV, Gurskaya NG, Lukyanov KA, Tarabykin VS, Lukyanov SA. Mirror orientation selection (MOS): a method for eliminating false positive clones from libraries generated by suppression subtractive hybridization. Nucleic Acids Res. 2000; 28:e90.
• [56]Supek F, Bošnjak M, Škunca N, Šmuc T. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One. 2011; 6: Article ID e21800
• [57]Joubert C, Linard C, Le Moullac G, Soyez C, Saulnier D, Teaniniuraitemoana V, Ky CL, Gueguen Y. Temperature and food influence shell growth and mantle gene expression of shell matrix proteins in the pearl oyster Pinctada margaritifera. PLoS One. 2014; 9: Article ID e103944
• [58]Larsen JB, Frischer ME, Rasmussen LJ, Hansen BW. Single-step nested multiplex PCR to differentiate between various bivalve larvae. Mar Biol. 2005; 146:1119-1129.
• [59]Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2 ΔΔCT method. Methods. 2001; 25:402-408.
• [60]Wang W, Yang L, Suwa T, Casson PR, Hornsby PJ. Differentially expressed genes in zona reticularis cells of the human adrenal cortex. Mol Cell Endocrinol. 2001; 173:127-134.
• [61]Larkin P. Expression profiling of estrogenic compounds using a sheepshead minnow cDNA macroarray. Environ Health Perspect. 2003; 111:83962.
• [62]Suzuki M, Saruwatari K, Kogure T, Yamamoto Y, Nishimura T, Kato T, Nagasawa H. An acidic matrix protein, Pif, is a key macromolecule for nacre formation. Science. 2009; 325:1388-1390.
• [63]Ehrlich H. Chitin and collagen as universal and alternative templates in biomineralization. Int Geol Rev. 2010; 52:661-699.
• [64]Suzuki M, Nagasawa H. The structure-function relationship analysis of Prismalin-14 from the prismatic layer of the Japanese pearl oyster, Pinctada fucata. FEBS J. 2007; 274:5158-5166.
• [65]Miyashita T, Takagi R, Okushima M, Nakano S, Miyamoto H, Nishikawa E, Matsushiro A. Complementary DNA cloning and characterization of pearlin, a new class of matrix protein in the nacreous layer of oyster pearls. Mar Biotechnol. 2000; 2:409-418.
• [66]Yan ZG, Jing G, Gong NP, Li CZ, Zhou YJ, Xie LP, Zhang RQ. N40, a novel nonacidic matrix protein from pearl oyster nacre, facilitates nucleation of aragonite in vitro. Biomacromolecules. 2007; 8:3597-3601.
• [67]Kono M, Hayashi N, Samata T. Molecular mechanism of the nacreous layer formation in Pinctada maxima. Biochem Biophys Res Commun. 2000; 269:213-218.
• [68]Montagnani C, Marie B, Marin F, Beliard C, Riquet F, Tayalé A, Zanella-Cléon I, Fleury E, Gueguen Y, Piquemal D. Pmarg-Pearlin is a matrix protein involved in nacre framework formation in the pearl oyster Pinctada margaritifera. Chembiochem. 2011; 12:2033-2043.
• [69]Yano M, Nagai K, Morimoto K, Miyamoto H. Shematrin: A family of glycine-rich structural proteins in the shell of the pearl oyster Pinctada fucata. Comp Biochem Physiol B Biochem Mol Biol. 2006; 144:254-262.
• [70]Takeuchi T, Endo K. Biphasic and dually coordinated expression of the genes encoding major shell matrix proteins in the pearl oyster Pinctada fucata. Mar Biotechnol. 2005; 8:52-61.
• [71]Tsukamoto D, Sarashina I, Endo K. Structure and expression of an unusually acidic matrix protein of pearl oyster shells. Biochem Biophys Res Commun. 2004; 320:1175-1180.
• [72]Zhang C, Xie L, Huang J, Liu X, Zhang R. A novel matrix protein family participating in the prismatic layer framework formation of pearl oyster, Pinctada fucata. Biochem Biophys Res Commun. 2006; 344:735-740.
• [73]Theos AC, Truschel ST, Raposo G, Marks MS. The Silver locus product Pmel17/gp100/Silv/ME20: controversial in name and in function. Pigment Cell Res. 2005; 18:322-336.
• [74]Asokan R, Arumugam M, Mullainadhan P. Activation of prophenoloxidase in the plasma and haemocytes of the marine mussel Perna viridis Linnaeus. Dev Comp Immunol. 1997; 21:1-12.
• [75]Cong R, Sun W, Liu G, Fan T, Meng X, Yang L, Zhu L. Purification and characterization of phenoloxidase from clam Ruditapes philippinarum. Fish Shellfish Immunol. 2005; 18:61-70.
• [76]Waite JH. Quinone-tanned scleroproteins. In: The Mollusca. Volume 4. Saleudin ASM, Wilbur KM, editors. Academic, New York; 1983: p.467-504.
• [77]Hunt S. Comparison of three extracellular structural proteins in the gastropod mollusc Buccinum undatum L., the periostracum, egg capsule and operculum. Comp Biochem Physiol B: Comp Biochem. 1971; 40:37-40.
• [78]Bai G, Brown JF, Watson C, Yoshino TP. Isolation and Characterization of Phenoloxidase from Egg Masses of the Gastropod Mollusc, Biomphalaria glabrata. Comp Biochem Physiol B: Comp Biochem. 1997; 118:463-469.
• [79]Brown C. Some structural proteins of Mytilus edulis. Q J Microsc Sci. 1952; 3:487-502.
• [80]Waite J, Tanzer M. The bioadhesive of Mytilus byssus: a protein containing L-dopa. Biochem Biophys Res Commun. 1980; 96:1554-1561.
• [81]Degens ET, Spencer DW, Parker RH. Paleobiochemistry of molluscan shell proteins. Comp Biochem Physiol. 1967; 20:553-579.
• [82]Gordon J, Carriker M. Sclerotized protein in the shell matrix of a bivalve mollusc. Mar Biol. 1980; 57:251-260.
• [83]Waite JH, Wilbur KM. Phenoloxidase in the periostracum of the marine bivalve Modiolus demissus Dillwyn. J Exp Zool. 1976; 195:359-367.
• [84]Checa AG, Salas C, Harper EM, Bueno-Pérez JD. Early stage biomineralization in the periostracum of the ‘living fossil’ bivalve Neotrigonia. PLoS One. 2014; 9:e90033.
• [85]Saleuddin ASM, Petit HP, Wilbur KM. The mode of formation and the structure of the periostracum. In: The Mollusca. Volume 4. Saleudin ASM, Wilbur KM, editors. Academic, New York; 1983: p.199-234.
• [86]Wilbur K, Saleuddin A. Shell formation. In: The Mollusca. Volume 4. Saleudin ASM, Wilbur KM, editors. Academic, New York; 1983: p.235-287.
• [87]Wada K. Electron microscopic observations of the formation of the periostracum of Pinctada fucata. Bull Nat Pearl Res Lab. 1968; 13:1540-1560.
• [88]Petit H, Davis WL, Jones RG, Hagler H. Morphological studies on the calcification process in the fresh-water mussel Amblema. Tissue Cell. 1980; 12:13-28.
• [89]Checa A. A new model for periostracum and shell formation in Unionidae (Bivalvia, Mollusca). Tissue Cell. 2000; 32:405-416.
• [90]Oetting WS, King RA. Molecular basis of albinism: Mutations and polymorphisms of pigmentation genes associated with albinism. Hum Mut. 1999; 13:99-115.
• [91]Flint SD, Jordan PW, Caldwell MM. Plant protective response to enhanced UV-B radiation under field conditions: leaf optical properties and photosynthesis. Photochem Photobiol. 1985; 41:95-99.
• [92]Harborne JB, Williams CA. Advances in flavonoid research since 1992. Phytochem. 2000; 55:481-504.
• [93]Middleton EM, Teramura AH. Understanding photosynthesis, pigment and growth responses induced by UV-B and UV-A irradiances. Photochemi Photobiol. 1994; 60:38-45.
• [94]Iwanaga S, Lee BL. Recent advances in the innate immunity of invertebrate animals. BMB Rep. 2005; 38:128-150.
• [95]Quattrocchio F, Wing J, van der Woude K, Souer E, de Vetten N, Mol J, Koes R. Molecular analysis of the anthocyanin2 gene of Petunia and its role in the evolution of flower color. Plant Cell. 1999; 11:1433-1444.
• [96]Nikapitiya C, De Zoysa M, Oh C, Lee Y, Ekanayake PM, Whang I, Choi CY, Lee J-S, Lee J. Disk abalone (Haliotis discus discus) expresses a novel antistasin-like serine protease inhibitor: Molecular cloning and immune response against bacterial infection. Fish Shellfish Immunol. 2010; 28:661-671.
• [97]Ponting CP. Evidence for PDZ domains in bacteria, yeast, and plants. Prot Sci. 1997; 6:464-468.
• [98]Ponting CP, Phillips C, Davies KE, Blake DJ. PDZ Domains: Targeting signalling molecules to sub-membranous sites. BioEssays. 1997; 19:469-479.
• [99]Ralf LC. The control of color in Birds. Am Zool. 1969; 9:521-530.