Giải trình tự toàn bộ transcriptome và cấu trúc gen sinh khoáng liên quan đến tính chất chất lượng ngọc trai nuôi trồng ở hàu ngọc trai, Pinctada margaritifera

Springer Science and Business Media LLC - Tập 20 - Trang 1-11 - 2019
J. Le Luyer1, P. Auffret1, V. Quillien1, N. Leclerc1, C. Reisser1, J. Vidal-Dupiol1,2, C.-L. Ky1
1Ifremer, UMR 241 Ecosystèmes Insulaires Océaniens (EIO), Labex Corail, Centre Ifremer du Pacifique, Tahiti, French Polynesia
2Ifremer, UMR 5244 Interactions Hôtes-Pathogènes-Environnements, Université de Montpellier, Montpellier, France

Tóm tắt

Ngọc trai nuôi trồng là những viên gem độc đáo được sản xuất bởi các sinh vật sống, chủ yếu là nhuyễn thể thuộc giống Pinctada, thông qua các đặc tính sinh khoáng của mô túi ngọc trai. Cải thiện chất lượng ngọc trai P. margaritifera là một trong những thách thức lớn nhất mà nghiên cứu Polynesia phải đối mặt cho đến nay. Để đạt được mục tiêu này, việc hiểu rõ hơn về các cơ chế phức tạp liên quan đến sự hình thành xà cừ và ngọc trai là điều cần thiết và hiện có thể tiếp cận thông qua việc sử dụng công nghệ giải trình tự song song quy mô lớn. Mục tiêu của nghiên cứu này là sử dụng RNA-seq để so sánh biểu hiện toàn bộ transcriptome của các túi ngọc trai có chất lượng ngọc trai cao và thấp. Để thực hiện điều này, một transcriptome tham chiếu toàn diện của P. margaritifera đã được xây dựng dựa trên việc lấy mẫu từ nhiều mô (màng, cơ sinh dục, toàn bộ động vật), bao gồm các giai đoạn sống khác nhau (vị thành niên, trưởng thành) và kiểu hình (kiểu màu, giới tính). Đáng chú ý, rất ít gen được tìm thấy có sự tăng cường biểu hiện cho ngọc trai chất lượng cao (n = 16) so với các gen tăng cường trong ngọc trai chất lượng thấp (n = 246). Các gen sinh khoáng tăng cường trong ngọc trai chất lượng thấp cụ thể cho các lớp đa diện và lớp prism-xà cừ. Sự cắt nối thay thế cũng đã được xác định trong một số gen sinh khoáng chính dựa trên bộ gen dự thảo gần đây của P. margaritifera. Nghiên cứu này đã làm sáng tỏ sự điều tiết đa tầng của các gen sinh khoáng liên quan đến việc xác định chất lượng ngọc trai.

Từ khóa

#ngọc trai nuôi trồng #Pinctada margaritifera #sinh khoáng #RNA-seq #transcriptome

Tài liệu tham khảo

Taylor JJ, Strack E. Pearl production. In: Southgate PC, Lucas JS, editors. Pearl oyster. Amsterdam: Elsevier. p. 273–302. Gervis MH, Sims NA. The biology and culture of pearl oysters (Bivalvia pteriidae). London: Manila: Overseas Development Administration of the United Kingdom; International Center for Living Aquatic Resources Management; 1992. Kishore P, Southgate PC. A detailed description of pearl-sac development in the black-lip pearl oyster, Pinctada margaritifera (Linnaeus 1758). Aquac Res. 2016;47:2215–26 https://onlinelibrary.wiley.com/doi/epdf/10.1111/are.12674. Accessed 27 Jun 2018. Ky C-L, Blay C, Sham-Koua M, Vanaa V, Lo C, Cabral P. Family effect on cultured pearl quality in black-lipped pearl oyster Pinctada margaritifera and insights for genetic improvement. Aquat Living Resour. 2013;26:133–45. https://doi.org/10.1051/alr/2013055. Ellis S, Haws M. Producing pearls using the black-lip pearl oyster (Pinctada margaritifera). Aquafarmer Inf Sheet. 1999;8. Kvingedal R, Evans BS, Lind CE, Taylor JUU, Dupont-Nivet M, Jerry DR. Population and family growth response to different rearing location, heritability estimates and genotype x environment interaction in the silver-lip pearl oyster (Pinctada maxima). Aquaculture. 2010;304:1–6. Jerry DR, Kvingedal R, Lind CE, Evans BS, Taylor JJU, Safari A. Donor-oyster derived heritability estimates and the effect of genotype x environment interaction on the production of pearl quality traits in the silver-lipped pearl oyster, Pinctada maxima. Aquaculture. 2012;338-341:66–71. McGinty E, Zenger KR, Taylor JU, Evans BS, Jerry DR. Diagnostic genetic markers unravel the interplay between host and donor oyster contribution in cultured pearl formation. Aquaculture. 2011;316:20–4. McGinty EL, Evan BS, Taylor JUU, Jerry DR. Xenografts and pearl production in two pearl oyster species, P. Maxima and P. Margaritifera: effect on pearl quality and a key to understanding genetic contribution. Aquaculture. 2010;302:175–81. Blay C, Planes S, Ky C-L. Crossing phenotype heritability and candidate gene expression in grafted black-lipped pearl oyster Pinctada margaritifera, an animal chimera. J Heridity. 2018; in press. Ky C-L, Okura R, Nakasai S, Devaux D. 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. 2016;35:827–35. Latchere O, Le Moullac G, Gaertner-Mazouni N, Fievet J, Magré K, Saulnier D. Influence of preoperative food and temperature conditions on pearl biogenesis in Pinctada margaritifera. Aquaculture. 2017;479 Supplement C:176–87. https://doi.org/10.1016/j.aquaculture.2017.05.046. Li S, Huang J, Liu C, Liu Y, Zheng G, Xie L, et al. Interactive effects of seawater acidification and elevated temperature on the transcriptome and biomineralization in the pearl oyster Pinctada fucata. Environ Sci Technol. 2016;50:1157–65. https://doi.org/10.1021/acs.est.5b05107. Gueguen Y, Czorlich Y, Mastail M, Le Tohic B, Defay D, Lyonnard P, et al. Yes, it turns: experimental evidence of pearl rotation during its formation. R Soc Open Sci. 2015;2:150144. https://doi.org/10.1098/rsos.150144. Tayalé A, Gueguen Y, Treguier C, Grand JL, Cochennec-Laureau N, Montagnani C, et al. Evidence of donor effect on cultured pearl quality from a duplicated grafting experiment on Pinctada margaritifera using wild donors. Aquat Living Resour. 2012;25:269–80. https://doi.org/10.1051/alr/2012034. Ky C-L, Blay C, Sham-Koua M, Lo C, Cabral P. Indirect improvement of pearl grade and shape in farmed Pinctada margaritifera by donor “oyster” selection for green pearls. Aquaculture. 2014;432 Supplement C:154–62. https://doi.org/10.1016/j.aquaculture.2014.05.002. Blay C, Sham-Koua M, Vonau V, Tetumu R, Cabral P, Ky C-L. 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. 2014;22:937–53. https://doi.org/10.1007/s10499-013-9719-5. Ky C-L, Blay C, Aiho V, Cabral P, Le Moullac G, Lo C. Macro-geographical differences influenced by family-based expression on cultured pearl grade, shape and colour in the black-lip ‘pearl oyster’ Pinctada margaritifera: a preliminary bi-local case study in French Polynesia. Aquac Res. 2017;48:270–82. https://doi.org/10.1111/are.12880. Blay C, Planes S, Ky C-L. Optimal age of the donor graft tissue in relation to cultured pearl phenotypes in the mollusc, Pinctada margaritifera. PLOS ONE. 2018;13:e0198505. https://doi.org/10.1371/journal.pone.0198505. Ky C-L, Nakasai S, Parrad S, Broustal F, Devaux D, Louis P. Variation in cultured pearl quality traits in relation to position of saibo cutting on the mantle of black-lipped pearl oyster Pinctada margaritifera. Aquaculture. 2018;493:85–92. https://doi.org/10.1016/j.aquaculture.2018.04.059. Ky C-L, Molinari N, Moe E, Pommier S. Impact of season and grafter skill on nucleus retention and pearl oyster mortality rate in Pinctada margaritifera aquaculture. Aquac Int. 2014;22:1689–701. https://doi.org/10.1007/s10499-014-9774-6. Lemer S, Saulnier D, Gueguen Y, Planes S. Identification of genes associated with shell color in the black-lipped pearl oyster, Pinctada margaritifera. BMC Genomics. 2015;16. Jones DB, Jerry DR, Foret S, Konovalov D, Zenger KR. Genome-wide SNP validation and mantle tissue transcriptome analysis in the silver-lipped pearl oyster, Pinctada maxima. Mar Genomics. 2013;15:647–58. Jones DB, Jerry DR, Khatkar MS, Raadsma HW, Zenger KR. A high-density SNP genetic linkage map for the silver-lipped pearl oyster, Pinctada maxima: a valuable resource for gene localisation and marker-assisted selection. BMC Genomics. 2013;14:810. https://doi.org/10.1186/1471-2164-14-810. Jones DB, Jerry DR, Khatkar MS, Moser G, Raadsma HW, Taylor JJ, et al. Quantitative trait loci and genetic association analysis reveals insights into complex pearl quality traits in donor silver-lipped pearl oysters. Aquaculture. 2014;434:476–85. https://doi.org/10.1016/j.aquaculture.2014.08.038. Inoue N, Ishibashi R, Ishikawa T, Atsumi T, Aoki H, Komaru A. Comparison of expression patterns of shell matrix protein genes in the mantle tissues between high- and low-quality pearl-producing recipients of the pearl oyster, Pinctada fucata. Zoolog Sci. 2011;28:32–6. https://doi.org/10.2108/zsj.28.32. Inoue N, Ishibashi R, Ishikawa T, Atsumi T, Aoki H, Komaru A. 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 N Y N. 2011;13:48–55. https://doi.org/10.1007/s10126-010-9267-1. Blay C, Planes S, Ky C-L. Cultured pearl surface quality profiling by the shell matrix protein gene expression in the biomineralised pearl sac tissue of Pinctada margaritifera. Mar Biotechnol. 2018;in press. Marie B, Joubert C, Tayalé A, Zanella-Cléon I, Belliard C, Piquemal D, et al. Different secretory repertoires control the biomineralization processes of prism and nacre deposition of the pearl oyster shell. Proc Natl Acad Sci. 2012;109:20986–91. https://doi.org/10.1073/pnas.1210552109. Marie B, Jackson DJ, Ramos-Silva P, Zanella-Cléon I, Guichard N, Marin F. The shell-forming proteome of Lottia gigantea reveals both deep conservations and lineage-specific novelties. FEBS J. 280:214–32. https://doi.org/10.1111/febs.12062. Isowa Y, Sarashina I, Setiamarga DHE, Endo K. A comparative study of the shell matrix protein aspein in pterioid bivalves. J Mol Evol. 2012;75:11–8. https://doi.org/10.1007/s00239-012-9514-3. Takeuchi T, Sarashina I, Iijima M, Endo K. In vitro regulation of CaCO3 crystal polymorphism by the highly acidic molluscan shell protein Aspein. FEBS Lett. 2008;582:591–6. https://doi.org/10.1016/j.febslet.2008.01.026. Tsukamoto D, Sarashina I, Endo K. Structure and expression of an unusually acidic matrix protein of pearl oyster shells. Biochem Biophys Res Commun. 2004;320:1175–80. https://doi.org/10.1016/j.bbrc.2004.06.072. Elhadj S, Yoreo JJD, Hoyer JR, Dove PM. Role of molecular charge and hydrophilicity in regulating the kinetics of crystal growth. Proc Natl Acad Sci. 2006;103:19237–42. https://doi.org/10.1073/pnas.0605748103. Shi Y, He M. Differential gene expression identified by RNA-Seq and qPCR in two sizes of pearl oyster (Pinctada fucata). Gene. 2014;538:313–22. https://doi.org/10.1016/j.gene.2014.01.031. Li S, Liu C, Huang J, Liu Y, Zhang S, Zheng G, et al. Transcriptome and biomineralization responses of the pearl oyster Pinctada fucata to elevated CO2 and temperature. Sci Rep. 2016;6:18943. https://doi.org/10.1038/srep18943. Zhao X, Wang Q, Jiao Y, Huang R, Deng Y, Wang H, et al. Identification of genes potentially related to biomineralization and immunity by transcriptome analysis of pearl sac in pearl oyster Pinctada martensii. Mar Biotechnol. 2012;14:730–9. https://doi.org/10.1007/s10126-012-9438-3. 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;15:175–87. https://doi.org/10.1007/s10126-012-9476-x. Li H, Liu B, Huang G, Fan S, Zhang B, Su J, et al. Characterization of transcriptome and identification of biomineralization genes in winged pearl oyster (Pteria penguin) mantle tissue. Comp Biochem Physiol Part D Genomics Proteomics. 2017;21:67–76. https://doi.org/10.1016/j.cbd.2016.12.002. Joubert C, Piquemal D, Marie B, Manchon L, Pierrat F, Zanella-Cléon I, et al. Transcriptome and proteome analysis of Pinctada margaritifera calcifying mantle and shell: focus on biomineralization. BMC Genomics. 2010;11:613. https://doi.org/10.1186/1471-2164-11-613. Teaniniuraitemoana V, Huvet A, Levy P, Klopp C, Lhuillier E, Gaertner-Mazouni N, et al. Gonad transcriptome analysis of pearl oyster Pinctada margaritifera: identification of potential sex differentiation and sex determining genes. BMC Genomics. 2014;15:491. https://doi.org/10.1186/1471-2164-15-491. Huang X-D, Zhao M, Liu W-G, Guan Y-Y, Shi Y, Wang Q, et al. Gigabase-scale transcriptome analysis on four species of pearl oysters. Mar Biotechnol. 2013;15:253–64. Marin F, Luquet G, Marie B, Medakovic D. Molluscan shell proteins: primary structure, origin, and evolution. Curr Top Dev Biol. 2008;80:209–76. https://doi.org/10.1016/S0070-2153(07)80006-8. Marie B, Arivalagan J, Mathéron L, Bolbach G, Berland S, Marie A, et al. Deep conservation of bivalve nacre proteins highlighted by shell matrix proteomics of the Unionoida Elliptio complanata and Villosa lienosa. J R Soc Interface. 2017;14:20160846. https://doi.org/10.1098/rsif.2016.0846. Kocot KM, Aguilera F, McDougall C, Jackson DJ, Degnan BM. Sea shell diversity and rapidly evolving secretomes: insights into the evolution of biomineralization. Front Zool. 2016;13:23. https://doi.org/10.1186/s12983-016-0155-z Bahn SY, Jo BH, Choi YS, Cha HJ. Control of nacre biomineralization by Pif80 in pearl oyster. Sci Adv. 2017;3. Gu Z, Yin X, Yu C, Zhan X, Shi Y, Wang A. Expression profiles of nine biomineralization genes and their relationship with pearl nacre thickness in the pearl oyster, Pinctada fucata martensii dunker. Aquac Res. 2016;47:1874–84. https://doi.org/10.1111/are.12645. Arivalagan J, Yarra T, Marie B, Sleight VA, Duvernois-Berthet E, Clark MS, et al. Insights from the Shell proteome: biomineralization to adaptation. Mol Biol Evol. 2017;34:66–77. https://doi.org/10.1093/molbev/msw219. Jackson DJ, McDougall C, Woodcroft B, Moase P, Rose RA, Kube M, et al. Parallel evolution of nacre building gene sets in molluscs. Mol Biol Evol. 2010;27:591–608. 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 MGG. 2017;292:343–52. Li S, Liu Y, Huang J, Zhan A, Xie L, Zhang R. The receptor genes PfBMPR1B and PfBAMBI are involved in regulating shell biomineralization in the pearl oyster Pinctada fucata. Sci Rep. 2017;7. Joubert C, Linard C, Moullac GL, Soyez C, Saulnier D, Teaniniuraitemoana V, et al. Temperature and food influence shell growth and mantle gene expression of shell matrix proteins in the pearl oyster Pinctada margaritifera. PLoS One. 2014;9:e103944. https://doi.org/10.1371/journal.pone.0103944. Blay C, Parrad S, Cabral P, Aiho V, Ky C-L. Correlations between cultured pearl size parameters and PIF-177 biomarker expression in Pinctada margaritifera families reared in two contrasting environments. Estuar Coast Shelf Sci. 2016;182 Part B:254–60. https://doi.org/10.1016/j.ecss.2016.05.020. Feng D, Li Q, Yu H, Kong L, Du S. Identification of conserved proteins from diverse shell matrix proteome in Crassostrea gigas: characterization of genetic bases regulating shell formation. Sci Rep. 2017;7:45754. https://doi.org/10.1038/srep45754 Suzuki M, Saruwatari K, Kogure T, Yamamoto Y, Nishimura T, Kato T, et al. An acidic matrix protein, Pif, is a key macromolecule for nacre formation. Science. 2009;325:1388–90. https://doi.org/10.1126/science.1173793. Livingston BT, Killian CE, Wilt F, Cameron A, Landrum MJ, Ermolaeva O, et al. A genome-wide analysis of biomineralization-related proteins in the sea urchin Strongylocentrotus purpuratus. Dev Biol. 2006;300:335–48. https://doi.org/10.1016/j.ydbio.2006.07.047. Chuong EB, Elde NC, Feschotte C. Regulatory activities of transposable elements: from conflicts to benefits. Nat Rev Genet. 2017;18:71–86. https://doi.org/10.1038/nrg.2016.139. Hirsch CD, Springer NM. Transposable element influences on gene expression in plants. Biochim Biophys Acta BBA - Gene Regul Mech. 1860;2017:157–65. https://doi.org/10.1016/j.bbagrm.2016.05.010. Trizzino M, Park Y, Holsbach-Beltrame M, Aracena K, Mika K, Caliskan M, et al. Transposable elements are the primary source of novelty in primate gene regulation. Genome Res. 2017:gr.218149.116. https://doi.org/10.1101/gr.218149.116. Ahmed M, Liang P. Transposable elements are a significant contributor to tandem repeats in the Human genome. Comparative and Functional Genomics; 2012. Sharma A, Wolfgruber TK, Presting GG. Tandem repeats derived from centromeric retrotransposons. BMC Genomics. 2013;14:142. https://doi.org/10.1186/1471-2164-14-142. Liu J, Yang D, Liu S, Li S, Xu G, Zheng G, et al. Microarray: a global analysis of biomineralization-related gene expression profiles during larval development in the pearl oyster, Pinctada fucata. BMC Genomics. 2015;16. https://doi.org/10.1186/s12864-015-1524-2. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;15:2114-20. https://doi.org/10.1093/bioinformatics/btu170. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, et al. De novo transcript sequence reconstruction from RNA-seq using the trinity platform for reference generation and analysis. Nat Protoc. 2013;8:1494–512. Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015;31:3210–2. Smith-Unna R, Boursnell C, Patro R, Hibberd JM, Kelly S. TransRate: reference-free quality assessment of de novo transcriptome assemblies. Genome Res. 2016;26:1134–44. Wu TD, Reeder J, Lawrence M, Becker G, Brauer MJ. GMAP and GSNAP for genomic sequence alignment: enhancements to speed, accuracy, and functionality. Statistical Genomics: Methods and Protocols. 2016:283–334. Bairoch A, Apweiler R. The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000. Nucleic Acids Res. 2000;28:45–8 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC102476/. Accessed 20 Dec 2016. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389–402. Ky C-L, Lau C, Koua MS, Lo C. Growth performance comparison of Pinctada margaritifera juveniles produced by thermal dhock or gonad scarification spawning procedures. J Shellfish Res. 2015;34:811–7. McGinty EL, Zenger KR, Jones DB, Jerry DR. Transcriptome analysis of biomineralisation-related genes within the pearl sac: host and donor oyster contribution. Mar Genomics. 2012;5:27–33. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25:2078–9. Anders S, Pyl PT, Huber W. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics. 2015;31:166–9. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550. Klopfenstein DV, Zhang L, Pedersen BS, Ramírez F, Warwick Vesztrocy A, Naldi A, et al. GOATOOLS: a Python library for gene ontology analyses. Sci Rep. 2018;8:10872. https://doi.org/10.1038/s41598-018-28948-z. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods San Diego Calif. 2001;25:402–8. https://doi.org/10.1006/meth.2001.1262. Andersen CL, Jensen JL, Ørntoft TF. Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 2004;64:5245–50. Hartley SW, Mullikin JC. QoRTs: a comprehensive toolset for quality control and data processing of RNA-Seq experiments. BMC Bioinformatics. 2015;16. Hartley SW, Mullikin JC. Detection and visualization of differential splicing in RNA-Seq data with JunctionSeq. Nucleic Acids Res. 2016;44:15. https://doi.org/10.1093/nar/gkw501