Expression pattern of genes involved in biomineralization in black and orange mantle tissues of pearl oyster, Pinctada persica

A few species of mollusks display color variation in their soft tissues. In pearl oysters, the color polymorphism in mantle tissue is associated with the color and radiance of shell and pearl. The study of biomineralization related genes in mantle tissue of pearl oysters can be used as a suitable approach to better identify the molecular mechanisms that influence shell and pearl quality and color variations. In this study, we investigated the expression of biomineralization-related genes in black and orange mantle morphotypes of pearl oyster, Pinctada persica in both warm and cool seasons using quantitative real-time PCR. Our results showed that the genes involved in biomineralization of the prismatic and nacre layer, i.e.; ASP, KRMP, MRNP34, SHELL, SHEM1B, LINKINE, PIF, SHEM5, NACREIN, and in pigmentation (TYR2A) were significantly higher expressed in orange phenotype compared to those of black one. The higher expression of ASP, KRMP, SHEM5, LINKINE and NACREIN in orange phenotype was only observed in warm season, but PIF, SHELL, SHEM1B, and TYR2A were upregulated in both warm and cool seasons. These results suggest the existence of different genetic processes between the two color morphs of P. persica and the more active role of genes in orange morphotype, particularly in warmer season. This study provides better understanding of the molecular mechanisms underlying biomineralization in pearl oysters.

[1]  D. Wheatley,et al.  Introduction I , 2021, A History of Irish Women's Poetry.

[2]  Z. Huo,et al.  Identification of shell-color-related microRNAs in the Manila clam Ruditapes philippinarum using high-throughput sequencing of small RNA transcriptomes , 2021, Scientific Reports.

[3]  S. Planes,et al.  Molecular Pathways and Pigments Underlying the Colors of the Pearl Oyster Pinctada margaritifera var. cumingii (Linnaeus 1758) , 2021, Genes.

[4]  A. L. Houde,et al.  Identification of Hypoxia-Specific Biomarkers in Salmonids Using RNA-Sequencing and Validation Using High-Throughput qPCR , 2020, bioRxiv.

[5]  A. Farrell,et al.  Salmonid gene expression biomarkers indicative of physiological responses to changes in salinity and temperature, but not dissolved oxygen , 2019, Journal of Experimental Biology.

[6]  S. Planes,et al.  Relationship of the orange tissue morphotype with shell and pearl colouration in the mollusc Pinctada margaritifera , 2019, Scientific Reports.

[7]  V. Quillien,et al.  Whole transcriptome sequencing and biomineralization gene architecture associated with cultured pearl quality traits in the pearl oyster, Pinctada margaritifera , 2018, bioRxiv.

[8]  S. Planes,et al.  Crossing Phenotype Heritability and Candidate Gene Expression in Grafted Black-Lipped Pearl Oyster Pinctada margaritifera, an Animal Chimera , 2018, The Journal of heredity.

[9]  V. Quillien,et al.  Phenome of pearl quality traits in the mollusc transplant model Pinctada margaritifera , 2018, Scientific Reports.

[10]  F. Parvizi,et al.  Mantle histology and histochemistry of three pearl oysters: Pinctada persica, Pinctada radiata and Pteria penguin , 2018 .

[11]  S. Planes,et al.  Donor and recipient contribution to phenotypic traits and the expression of biomineralisation genes in the pearl oyster model Pinctada margaritifera , 2017, Scientific Reports.

[12]  S. Williams,et al.  Molluscan shell colour , 2017, Biological reviews of the Cambridge Philosophical Society.

[13]  Qi Li,et al.  Identification of conserved proteins from diverse shell matrix proteome in Crassostrea gigas: characterization of genetic bases regulating shell formation , 2017, Scientific Reports.

[14]  Wen-jian Wu,et al.  Transcriptome analysis of the freshwater pearl mussel (Cristaria plicata) mantle unravels genes involved in the formation of shell and pearl , 2016, Molecular Genetics and Genomics.

[15]  P. Southgate,et al.  Swept away: ocean currents and seascape features influence genetic structure across the 18,000 Km Indo-Pacific distribution of a marine invertebrate, the black-lip pearl oyster Pinctada margaritifera , 2017, BMC Genomics.

[16]  C. Ky,et al.  The Mendelian inheritance of rare flesh and shell colour variants in the black-lipped pearl oyster (Pinctada margaritifera). , 2016, Animal genetics.

[17]  L. Xie,et al.  Transcriptome and biomineralization responses of the pearl oyster Pinctada fucata to elevated CO2 and temperature , 2016, Scientific Reports.

[18]  S. Arnaud-Haond,et al.  Rising the Persian Gulf Black-Lip Pearl Oyster to the Species Level: Fragmented Habitat and Chaotic Genetic Patchiness in Pinctada persica , 2015, Evolutionary Biology.

[19]  Y. Guéguen,et al.  Identification of genes associated with shell color in the black-lipped pearl oyster, Pinctada margaritifera , 2015, BMC Genomics.

[20]  Zhihong Liu,et al.  Characterization of the Mantle Transcriptome of Yesso Scallop (Patinopecten yessoensis): Identification of Genes Potentially Involved in Biomineralization and Pigmentation , 2015, PloS one.

[21]  Baozhong Liu,et al.  Transcriptome Analysis of Shell Color-Related Genes in the Clam Meretrix meretrix , 2015, Marine Biotechnology.

[22]  B. Degnan,et al.  Control of shell pigmentation by secretory tubules in the abalone mantle , 2014, Frontiers in Zoology.

[23]  Y. Guéguen,et al.  Temperature and Food Influence Shell Growth and Mantle Gene Expression of Shell Matrix Proteins in the Pearl Oyster Pinctada margaritifera , 2014, PloS one.

[24]  T. Miyashita,et al.  A cDNA Cloning of a Novel Alpha-Class Tyrosinase of Pinctada fucata: Its Expression Analysis and Characterization of the Expressed Protein , 2014, Enzyme research.

[25]  Maoxian He,et al.  Differential gene expression identified by RNA-Seq and qPCR in two sizes of pearl oyster (Pinctada fucata). , 2014, Gene.

[26]  G. Somero,et al.  The impact of ocean warming on marine organisms , 2014 .

[27]  Yun-Mi Lee,et al.  Characterizations of Shell and Mantle Edge Pigmentation of a Pacific Oyster, Crassostrea gigas, in Korean Peninsula , 2013, Asian-Australasian journal of animal sciences.

[28]  A. Freer,et al.  Biomineral Proteins from Mytilus edulis Mantle Tissue Transcriptome , 2013, Marine Biotechnology.

[29]  Zhifeng Gu,et al.  Characterization of the Pearl Oyster (Pinctada martensii) Mantle Transcriptome Unravels Biomineralization Genes , 2013, Marine Biotechnology.

[30]  Benjamin Marie,et al.  Different secretory repertoires control the biomineralization processes of prism and nacre deposition of the pearl oyster shell , 2012, Proceedings of the National Academy of Sciences.

[31]  D. Hayward,et al.  Whole Transcriptome Analysis of the Coral Acropora millepora Reveals Complex Responses to CO2‐driven Acidification during the Initiation of Calcification , 2012, Molecular ecology.

[32]  Jianshi Lin,et al.  Seawater Acidification and Elevated Temperature Affect Gene Expression Patterns of the Pearl Oyster Pinctada fucata , 2012, PloS one.

[33]  I. Zanella-Cléon,et al.  Characterization of MRNP34, a novel methionine-rich nacre protein from the pearl oysters , 2012, Amino Acids.

[34]  L. Xie,et al.  The role of matrix proteins in the control of nacreous layer deposition during pearl formation , 2012, Proceedings of the Royal Society B: Biological Sciences.

[35]  I. Zanella-Cléon,et al.  Pmarg‐Pearlin is a Matrix Protein Involved in Nacre Framework Formation in the Pearl Oyster Pinctada margaritifera , 2011, Chembiochem : a European journal of chemical biology.

[36]  Aaron Wiegand,et al.  Spatial analysis of biomineralization associated gene expression from the mantle organ of the pearl oyster Pinctada maxima , 2011, BMC Genomics.

[37]  Benjamin Marie,et al.  Transcriptome and proteome analysis of Pinctada margaritifera calcifying mantle and shell: focus on biomineralization , 2010, BMC Genomics.

[38]  Melody S Clark,et al.  Insights into shell deposition in the Antarctic bivalve Laternula elliptica: gene discovery in the mantle transcriptome using 454 pyrosequencing , 2010, BMC Genomics.

[39]  Takashi Kato,et al.  An Acidic Matrix Protein, Pif, Is a Key Macromolecule for Nacre Formation , 2009, Science.

[40]  C. Langdon,et al.  Heritability of shell pigmentation in the Pacific oyster, Crassostrea gigas☆ , 2009 .

[41]  吕一旭 Yixu Lu 引言 (Introduction) , 2009, Provincial China.

[42]  J. Lucas,et al.  Soft tissue anatomy, shell structure and biomineralization , 2008 .

[43]  I. Tëmkin,et al.  Taxonomy and Phylogeny , 2008 .

[44]  T. Kanazawa,et al.  Environmental and physiological controls on shell microgrowth pattern of Ruditapes philippinarum (Bivalvia: Veneridae) from Japan , 2007 .

[45]  L. Xie,et al.  N40, a novel nonacidic matrix protein from pearl oyster nacre, facilitates nucleation of aragonite in vitro. , 2007, Biomacromolecules.

[46]  Hiromichi Nagasawa,et al.  The structure–function relationship analysis of Prismalin‐14 from the prismatic layer of the Japanese pearl oyster, Pinctada fucata , 2007, The FEBS journal.

[47]  L. Xie,et al.  A novel extracellular EF-hand protein involved in the shell formation of pearl oyster. , 2007, Biochimica et biophysica acta.

[48]  Masato Yano,et al.  Tyrosinase localization in mollusc shells. , 2007, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[49]  Cen Zhang,et al.  A novel matrix protein family participating in the prismatic layer framework formation of pearl oyster, Pinctada fucata. , 2006, Biochemical and biophysical research communications.

[50]  Masato Yano,et al.  Shematrin: a family of glycine-rich structural proteins in the shell of the pearl oyster Pinctada fucata. , 2006, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[51]  Cen Zhang,et al.  A novel putative tyrosinase involved in periostracum formation from the pearl oyster (Pinctada fucata). , 2006, Biochemical and biophysical research communications.

[52]  L. Rasmussen,et al.  Single-step nested multiplex PCR to differentiate between various bivalve larvae , 2005 .

[53]  Peter Self,et al.  The origin of the color of pearls in iridescence from nano-composite structures of the nacre , 2004 .

[54]  H. Nagasawa,et al.  Characterization of Prismalin-14, a novel matrix protein from the prismatic layer of the Japanese pearl oyster (Pinctada fucata). , 2004, The Biochemical journal.

[55]  I. Sarashina,et al.  Structure and expression of an unusually acidic matrix protein of pearl oyster shells. , 2004, Biochemical and biophysical research communications.

[56]  C. Langdon,et al.  Evidence for genetic control of pigmentation of shell and mantle edge in selected families of Pacific oysters, Crassostrea gigas , 2004 .

[57]  A. Palumbo Melanogenesis in the ink gland of Sepia officinalis. , 2003, Pigment cell research.

[58]  A. Moorman,et al.  Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data , 2003, Neuroscience Letters.

[59]  S. Mann Biomineralization: Principles and Concepts in Bioinorganic Materials Chemistry , 2002 .

[60]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[61]  S. Pouvreau Croissance de lËhuître perlière, Pinctada margaritifera, dans neuf sites différents de Polynésie française : bilan de plusieurs plans dËéchantillonnage menés entre 1994 et 1999. , 2001 .

[62]  Park,et al.  Reproductive cycle and biochemical composition of the ark shell Scapharca broughtonii (Schrenck) in a southern coastal bay of Korea , 2001 .

[63]  R. Takagi,et al.  Complementary DNA Cloning and Characterization of Pearlin, a New Class of Matrix Protein in the Nacreous Layer of Oyster Pearls , 2000, Marine Biotechnology.

[64]  T. Samata,et al.  Molecular mechanism of the nacreous layer formation in Pinctada maxima. , 2000, Biochemical and biophysical research communications.

[65]  T. Samata,et al.  A new matrix protein family related to the nacreous layer formation of Pinctada fucata , 1999, FEBS letters.

[66]  Mario Viani,et al.  Molecular mechanistic origin of the toughness of natural adhesives, fibres and composites , 1999, Nature.

[67]  W. Oetting,et al.  Molecular basis of albinism: Mutations and polymorphisms of pigmentation genes associated with albinism , 1999, Human mutation.

[68]  T Morita,et al.  A carbonic anhydrase from the nacreous layer in oyster pearls. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[69]  H. Vogel,et al.  NMR studies of the methionine methyl groups in calmodulin , 1995, FEBS letters.

[70]  白井 祥平 真珠・真珠貝世界図鑑 = Pearls and pearl oysters of the world , 1994 .

[71]  N. Sims,et al.  The biology and culture of pearl oysters (Bivalvia: Pteriidae). , 1992 .

[72]  Barrie Jay Albinism , 1983, Survey of ophthalmology.

[73]  K. Wada White coloration of the prismatic layer in inbred Japanese pearl oyster, Pinctada fucata , 1983 .

[74]  J. Waite,et al.  Quinone-Tanned Scleroproteins , 1983 .

[75]  M. R. Carriker,et al.  Sclerotized protein in the shell matrix of a bivalve mollusc , 1980 .

[76]  養殖研究所 養殖研究所研究報告 = Bulletin of National Research Institute of Aquaculture , 1980 .

[77]  T. Venn,et al.  Seasonal variation in weight and biochemical composition of the tissues of the queen scallop, Chlamys opercularis, from the Clyde Sea area , 1979, Journal of the Marine Biological Association of the United Kingdom.

[78]  J. Waite,et al.  Phenoloxidase in the periostracum of the marine bivalve Modiolus demissus dillwyn , 1976 .

[79]  S. Wise Microstructure and mode of formation of nacre (mother-of-pearl) in pelecypods, gastropods, and cephalopods , 1970 .

[80]  R. H. Parker,et al.  Paleobiochemistry of molluscan shell proteins , 1967 .

[81]  N. Watabe,et al.  STUDIES ON SHELL FORMATION , 1961, The Journal of biophysical and biochemical cytology.

[82]  C. Grégoire TOPOGRAPHY OF THE ORGANIC COMPONENTS IN MOTHER-OF-PEARL , 1957, The Journal of biophysical and biochemical cytology.

[83]  H. L. Jameson On the Identity and Distribution of the Mother‐of‐Pearl Oysters; with a Revision of the Subgenus Margaritifera , 1901 .

[84]  Thomas D. Schmittgen,et al.  Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2 2 DD C T Method , 2022 .