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Transcriptome of Atlantic Cod (Gadus morhua L.) Early Embryos from Farmed and Wild Broodstocks

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Abstract

Significant efforts have been made to elucidate factors affecting egg quality in fish. Recently, we have shown that eggs originating from wild broodstock (WB) of Atlantic cod (Gadus morhua L.) are of superior quality to those derived from farmed broodstock (FB), and this is associated with differences in the chemical composition of egg yolk. However, maternal transcripts, accumulated during oogenesis, have not been studied extensively in fish. The aim of the present study was to characterize putative maternal mRNA transcriptome in fertilized eggs of Atlantic cod and to compare transcript pools between WB and FB in order to investigate the relation between egg developmental potential and putative maternal mRNA deposits. We performed high-throughput 454 pyrosequencing. For each WB and FB group, five cDNA libraries were individually tagged and sequenced, resulting in 98,687 (WB) and 119,333 (FB) average reads per library. Sequencing reads were de novo assembled, annotated, and mapped. Out of 13,726 identified isotigs, 238 were differentially expressed between WB and FB, with 155 isotigs significantly upregulated in WB. The sequence reads were mapped to 11,340 different Atlantic cod transcripts and 158 sequences were differentially expressed between the 2 groups. Important transcripts involved in fructose metabolism, fatty acid metabolism, glycerophospholipid metabolism, and oxidative phosphorylation were differentially represented between the two broodstock groups, showing potential as biomarkers of egg quality in teleosts. Our findings contribute to the hypothesis that maternal mRNAs affect egg quality and, consequently, the early development of fish.

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References

  • Aanes H, Winata CL, Lin CH, Chen JQP, Srinivasan KG, Lee SGP, Lim AYM, Hajan HS, Collas P, Bourque G, Gong ZY, Korzh V, Alestrom P, Mathavan S (2011) Zebrafish mRNA sequencing deciphers novelties in transcriptome dynamics during maternal to zygotic transition. Genome Res 21:1328–1338

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Aegerter S, Jalabert B, Bobe J (2005) Large scale real-time PCR analysis of mRNA abundance in rainbow trout eggs in relationship with egg quality and post-ovulatory ageing. Mol Reprod Dev 72:377–385

    Article  CAS  PubMed  Google Scholar 

  • Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2002) Molecular biology of the cell, 4th edn. Garland Science, Taylor & Francis Group, New York

    Google Scholar 

  • Bensaad K, Tsuruta A, Selak MA, Vidal MNC, Nakano K, Bartrons R, Gottlieb E, Vousden KH (2006) TIGAR, a p53-inducible regulator of glycolysis and apoptosis. Cell 126:107–120

    Article  CAS  PubMed  Google Scholar 

  • Bobe J, Labbé C (2010) Egg and sperm quality in fish. Gen Comp Endocrinol 165:535–548

    Article  CAS  PubMed  Google Scholar 

  • Bolaños JP, Almeida A, Moncada S (2010) Glycolysis: a bioenergetic or a survival pathway? Trends Biochem Sci 35:145–149

    Article  PubMed  Google Scholar 

  • Bonnet E, Fostier A, Bobe J (2007) Microarray-based analysis of fish egg quality after natural or controlled ovulation. BMC Genomics 8:55

    Article  PubMed Central  PubMed  Google Scholar 

  • Bowerman B, Kurz T (2006) Degrade to create: developmental requirements for ubiquitin-mediated proteolysis during early C. elegans embryogenesis. Development 133:773–784

    Article  CAS  PubMed  Google Scholar 

  • Brooks S, Tyler CR, Sumpter JP (1997) Egg quality in fish: what makes a good egg? Rev Fish Biol Fish 7:387–416

    Article  Google Scholar 

  • Butts IAE, Trippel EA, Ciereszko A, Soler C, Słowińska M, Alavi SMH, Litvak MK, Babiak I (2011) Seminal plasma biochemistry and spermatozoa characteristics of Atlantic cod (Gadus morhua) of wild and cultivated origin. Comp Biochem Physiol A 159:16–24

    Article  Google Scholar 

  • Carnevali O, Carletta R, Cambi A, Vita A, Bromage N (1999) Yolk formation and degradation during oocyte maturation in seabream Sparus aurata: involvement of two lysosomal proteinases. Biol Reprod 60:140–146

    Article  CAS  PubMed  Google Scholar 

  • Carnevali O, Mosconi G, Cambi A, Ridolfi S, Zanuy S, Polzonetti-Magni AM (2001) Changes of lysosomal enzyme activities in sea bass (Dicentrarchus labrax) eggs and developing embryos. Aquaculture 202:249–256

    Article  CAS  Google Scholar 

  • Clelland ES, Kelly SP (2010) Tight junction proteins in zebrafish ovarian follicles: stage specific mRNA abundance and response to 17beta-estradiol, human chorionic gonadotropin, and maturation inducing hormone. Gen Comp Endocrinol 168:388–400

    Article  CAS  PubMed  Google Scholar 

  • Garcia de la Serrana D, Estévez A, Andree K, Johnston IA (2012) Fast skeletal muscle transcriptome of the gilthead sea bream (Sparus aurata) determined by next generation sequencing. BMC Genomics 13:181

    Article  PubMed Central  PubMed  Google Scholar 

  • Dekker C, Stirling PC, McCormack EA, Filmore H, Paul A, Brost RL, Costanzo M, Boone C, Leroux MR, Willison KR (2008) The interaction network of the chaperonin CCT. EMBO J 27:1827–1839

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Desrosiers V, Le François NR, Tveiten H, Andreassen I, Blier PU (2008) Ontogenesis of catabolic and energy metabolism capacities during the embryonic development of spotted wolffish (Anarhichas minor). Comp Biochem Physiol B 150:200–206

    Article  PubMed  Google Scholar 

  • Drivenes Ø, Taranger GL, Edvardsen RB (2012) Gene expression profiling of Atlantic cod (Gadus morhua) embryogenesis using microarray. Mar Biotechnol 14:167–176

    Article  CAS  PubMed  Google Scholar 

  • Droege M, Hill B (2008) The Genome Sequencer FLXTM System—longer reads, more applications, straight forward bioinformatics and more complete data sets. J Biotechnol 136:3–10

    Article  CAS  PubMed  Google Scholar 

  • Ekblom R, Slate J, Horsburgh GJ, Birkhead T, Burke T (2012) Comparison between normalised and unnormalised 454-sequencing libraries for small-scale RNA-Seq studies. Comp Funct Genomics 2012:1–8

    Article  Google Scholar 

  • Fabra M, Cerdà J (2004) Ovarian cysteine proteinases in the teleost Fundulus heteroclitus: molecular cloning and gene expression during vitellogenesis and oocyte maturation. Mol Reprod Dev 67:282–294

    Article  CAS  PubMed  Google Scholar 

  • Faulk CK, Holt GJ (2008) Biochemical composition and quality of captive-spawned cobia Rachycentron canadum eggs. Aquaculture 279:70–76

    Article  CAS  Google Scholar 

  • Fernandes JMO, Mommens M, Hagen Ø, Babiak I, Solberg C (2008) Selection of suitable reference genes for real-time PCR studies of Atlantic halibut. Comp Biochem Physiol B 150:23–32

    Article  PubMed  Google Scholar 

  • Finn RN, Fyhn HJ, Evjen MS (1995) Physiological energetics of developing embryos and yolk-sac larvae of Atlantic cod (Gadus morhua). I. Respiration and nitrogen metabolism. Mar Biol 124:355–369

    Article  CAS  Google Scholar 

  • Fraser AJ, Gamble JC, Sargent JR (1988) Changes in lipid content, lipid class composition and fatty acid composition of developing eggs and unfed larvae of cod (Gadus morhua). Mar Biol 99:307–313

    Article  CAS  Google Scholar 

  • Frydman J (2001) Folding of newly translated proteins in vivo: the role of molecular chaperones. Annu Rev Biochem 70:603–647

    Article  CAS  PubMed  Google Scholar 

  • Furuita H, Ohta H, Unuma T, Tanaka H, Kagawa H, Suzuki N, Yamamoto T (2003) Biochemical composition of eggs in relation to egg quality in Japanese eel, Anguilla japonica. Fish Physiol Biochem 29:37–46

    Article  CAS  Google Scholar 

  • Götz S, García-Gómez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, Robles M, Talón M, Dopazo J, Conesa A (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36:3420–3435

    Article  PubMed Central  PubMed  Google Scholar 

  • Hale MC, McCormick CR, Jackson JR, DeWoody JA (2009) Next-generation pyrosequencing of gonad transcriptomes in the polyploid lake sturgeon (Acipenser fulvescens): the relative merits of normalization and rarefaction in gene discovery. BMC Genomics 10:203

    Article  PubMed Central  PubMed  Google Scholar 

  • Hardison AL, Lichten L, Banerjee-Basu S, Becker TS, Burguess SM (2005) The zebrafish gene claudinj is essential for normal ear function and important for the formation of the otoliths. Mech Dev 122:949–958

    Article  CAS  PubMed  Google Scholar 

  • Harris MA, Clark J, Ireland A, Lomax J, Ashburner M, Foulger R, Eilbeck K, Lewis S, Marshall B, Mungall C, Richter J, Rubin GM, Blake JA, Bult C, Dolan M, Drabkin H, Eppig JT, Hill DP, Ni L, Ringwald M, Balakrishnan R, Cherry JM, Christie KR, Costanzo MC, Dwight SS, Engel S, Fisk DG, Hirschman JE, Hong EL, Nash RS, Sethuraman A, Theesfeld CL, Botstein D, Dolinski K, Feierbach B, Berardini T, Mundodi S, Rhee SY, Apweiler R, Barrell D, Camon E, Dimmer E, Lee V, Chisholm R, Gaudet P, Kibbe W, Kishore R, Schwarz EM, Sternberg P, Gwinn M, Hannick L, Wortman J, Berriman M, Wood V, de la Cruz N, Tonellato P, Jaiswal P, Seigfried T, White R (2004) The gene ontology (GO) database and informatics resource. Nucleic Acids Res 32:D258–D261

    Article  CAS  PubMed  Google Scholar 

  • Hermansson M, Hokynar K, Somerharju P (2011) Mechanisms of glycerophospholipid homeostasis in mammalian cells. Prog Lipid Res 50:240–257

    Article  CAS  PubMed  Google Scholar 

  • Jeong K, Jeong JY, Lee HO, Choi E, Lee H (2010) Inhibition of Plk1 induces mitotic infidelity and embryonic growth defects in developing zebrafish embryos. Dev Biol 345:34–48

    Article  CAS  PubMed  Google Scholar 

  • Kahl CR, Means AR (2003) Regulation of cell cycle progression by calcium/calmodulin-dependent pathways. Endocr Rev 24:719–736

    Article  CAS  PubMed  Google Scholar 

  • Katzmann DJ, Odorizzi G, Emr SD (2002) Receptor downregulation and multivesicular-body sorting. Nat Rev Mol Cell Biol 3:893–905

    Article  CAS  PubMed  Google Scholar 

  • Kim E-J, Ro H, Huh T-L, Lee CJ, Choi J, Rhee M (2008) A novel kinesin-like protein, Surhe is associated with dorsalization in the zebrafish embryos. Animal Cells Syst 12:219–230

    Article  CAS  Google Scholar 

  • Knoll-Gellida A, André M, Gattegno T, Forgue J, Admon A, Babin PJ (2006) Molecular phenotype of zebrafish ovarian follicle by serial analysis of gene expression and proteomic profiling, and comparison with the transcriptomes of other animals. BMC Genomics 7:46

    Article  PubMed Central  PubMed  Google Scholar 

  • Kramer ER, Gieffers C, Hölzl G, Hengstschläger M, Peters JM (1998) Activation of the human anaphase-promoting complex by proteins of the CDC20/Fizzy family. Curr Biol 8:1207–1210

    Article  CAS  PubMed  Google Scholar 

  • Kwon JY, Prat F, Randall C, Tyler CR (2001) Molecular characterization of putative yolk processing enzymes and their expression during oogenesis and embryogenesis in rainbow trout (Oncorhynchus mykiss). Biol Reprod 65:1701–1709

    Article  CAS  PubMed  Google Scholar 

  • Lahnsteiner F (2005) Carbohydrate metabolism of eggs of the whitefish, Coregonus spp. during embryogenesis and its relationship with egg quality. Comp Biochem Physiol B 142:46–55

    Article  PubMed  Google Scholar 

  • Lahnsteiner F, Patarnello P (2003) Investigations on the metabolism of viable and nonviable gilthead sea bream (Sparus aurata) eggs. Aquaculture 223:159–174

    Article  CAS  Google Scholar 

  • Lahnsteiner F, Weismann T, Patzner RA (1999) Physiological and biochemical parameters for egg quality determination in lake trout, Salmo trutta lacustris. Fish Physiol Biochem 20:375–388

    Article  CAS  Google Scholar 

  • Lahnsteiner F, Urbanyi B, Horvath A, Weismann T (2001) Bio-markers for egg quality determination in cyprinid fish. Aquaculture 195:331–352

    Article  CAS  Google Scholar 

  • Lanes CFC, Bizuayehu TT, Bolla S, Martins C, Fernandes JMO, Bianchini A, Kiron V, Babiak I (2012a) Biochemical composition and performance of Atlantic cod (Gadus morhua L.) eggs and larvae obtained from farmed and wild broodstocks. Aquaculture 324–325:267–275

    Article  Google Scholar 

  • Lanes CFC, Fernandes JMO, Kiron V, Babiak I (2012b) Profiling of key apoptotic, stress, and immune-related transcripts during embryonic and postembryonic development of Atlantic cod (Gadus morhua L.). Theriogenology 78:1583–1596

    Article  CAS  PubMed  Google Scholar 

  • Lubzens E, Young G, Bobe J, Cerdà J (2010) Oogenesis in teleosts: how fish eggs are formed? Gen Comp Endocrinol 165:367–389

    Article  CAS  PubMed  Google Scholar 

  • Mathavan S, Lee SGP, Mak A, Miller LD, Murthy KRK, Govindarajan KR, Tong Y, Wu YL, Lam SH, Yang H, Ruan Y, Korzh V, Gong Z, Liu ET, Lufkin T (2005) Transcriptome analysis of zebrafish embryogenesis using microarrays. PLoS Genet 1:260–276

    Article  CAS  PubMed  Google Scholar 

  • Meehan RR (2003) DNA methylation in animal development. Semin Cell Dev Biol 14:53–65

    Article  CAS  PubMed  Google Scholar 

  • Micallef G, Bickerdike R, Reiff C, Fernandes JMO, Bowman AS, Martin SAM (2012) Exploring the transcriptome of Atlantic salmon (Salmo salar) skin, a major defense organ. Mar Biotechnol 14:559–569

    Article  CAS  PubMed  Google Scholar 

  • Mommens M, Fernandes JMO, Bizuayehu TT, Bolla SL, Johnston IA, Babiak I (2010) Maternal gene expression in Atlantic halibut (Hippoglossus hippoglossus L.) and its relation to egg quality. BMC Res Notes 3:138

    Article  PubMed Central  PubMed  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 

  • Pelegri F (2003) Maternal factors in zebrafish development. Dev Dyn 228:535–554

    Article  CAS  PubMed  Google Scholar 

  • Penney RW, Lush PL, Wade J, Brown JA, Parrish CC, Burton MPM (2006) Comparative utility of egg blastomere morphology and lipid biochemistry for prediction of hatching success in Atlantic cod, Gadus morhua L. Aquacult Res 37:272–283

    Article  CAS  Google Scholar 

  • Pertea G, Huang X, Liang F, Antonescu V, Sultana R, Karamycheva S, Lee Y, White J, Cheung F, Parvizi B, Tsai J, Quackenbush J (2003) TIGR gene indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics 19:651–652

    Article  CAS  PubMed  Google Scholar 

  • Rai K, Nadauld LD, Chidester S, Manos EJ, James SR, Karpf AR, Cairns BR, Jones DA (2006) Zebra fish Dnmt1 and Suv39h1 regulate organ-specific terminal differentiation during development. Mol Cell Biol 26:7077–7085

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Reading BJ, Chapman RW, Schaff JE, Scholl EH, Opperman CH, Sullivan CV (2012) An ovary transcriptome for all maturational stages of the striped bass (Morone saxatilis), a highly advanced perciform fish. BMC Res Notes 5:111

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Roshak AK, Capper EA, Imburgia C, Fornwald J, Scott G, Marshall LA (2000) The human polo-like kinase, PLK, regulates cdc2/cyclin B through phosphorylation and activation of the cdc25C phosphate. Cell Signal 12:405–411

    Article  CAS  PubMed  Google Scholar 

  • Salze G, Tocher DR, Roy WJ, Robertson DA (2005) Egg quality determinants in cod (Gadus morhua L.): egg performance and lipids in eggs from farmed and wild broodstock. Aquac Res 36:1488–1499

    Article  CAS  Google Scholar 

  • Sánchez CC, Weber GM, Gao G, Cleveland BM, Yao J, Rexroad CE (2011) Generation of a reference transcriptome for evaluating rainbow trout responses to various stressors. BMC Genomics 12:626

    Article  PubMed Central  PubMed  Google Scholar 

  • Sargent JR, Tocher DR, Bell JG (2002) The lipids. In: Halver JE, Hardy RW (eds) Fish nutrition. Academic, San Diego

  • Sawanboonchun J, Roy WJ, Robertson DA, Bell JG (2008) The impact of dietary supplementation with astaxanthin on egg quality in Atlantic cod broodstock. Aquaculture 283:97–101

    Article  CAS  Google Scholar 

  • Schafer KA (1998) The cell cycle: a review. Vet Pathol 35:461–478

    Article  CAS  PubMed  Google Scholar 

  • Shen-Orr SS, Pilpel Y, Hunter CP (2010) Composition and regulation of maternal and zygotic transcriptomes reflects species-specific reproductive mode. Genome Biol 11:R58

    Article  PubMed Central  PubMed  Google Scholar 

  • Siddiqui M, Sheikh H, Tran C, Bruce AEE (2010) The tight junction component claudin E is required for zebrafish epiboly. Dev Dyn 239:715–722

    Article  CAS  PubMed  Google Scholar 

  • Slanchev K, Carney TJ, Stemmler MP, Koschorz B, Amsterdam A, Schwarz H, Hammerschmidt M (2009) The epithelial cell adhesion molecule EpCAM is required for epithelial morphogenesis and integrity during zebrafish epiboly and skin development. PLoS Genet 5:e1000563

    Article  PubMed Central  PubMed  Google Scholar 

  • Standart N, Hunt T, Ruderman JV (1986) Differential accumulation of ribonucleotide reductase subunits in clam oocytes: the large subunit is stored as a polypeptide, the small subunit as unstranslated mRNA. J Cell Biol 103:2129–2136

    Article  CAS  PubMed  Google Scholar 

  • Trzpis M, Bremer E, McLaughlin PM, de Leij LF, Harmsen MC (2008) EpCAM in morphogenesis. Front Biosci 13:5050–5055

    Article  CAS  PubMed  Google Scholar 

  • Tsukita S, Furuse M (2002) Claudin-based barrier in simple and stratified cellular sheets. Curr Opin Cell Biol 14:531–536

    Article  CAS  PubMed  Google Scholar 

  • Tsunematsu T, Yamauchi E, Shibata H, Maki M, Ohta T, Konishi H (2010) Distinct functions of human MVB12A and MVB12B in the ESCRIT-I dependent on their posttranslational modifications. Biochem Biophys Res Commun 399:232–237

    Article  CAS  PubMed  Google Scholar 

  • Vesterlund L, Jiao H, Unneberg P, Hovatta O, Kere J (2011) The zebrafish transcriptome during early development. BMC Dev Biol 11:30

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Villablanca EJ, Renucci A, Sapède D, Lec V, Soubiran F, Sandoval PC, Dambly-Chaudière C, Ghysen A, Allende ML (2006) Control of cell migration in the zebrafish lateral line: implication of the gene “tumour-associated calcium signal transducer,” tacstd. Dev Dyn 235:1578–1588

    Article  CAS  PubMed  Google Scholar 

  • Wall PK, Leebens-Mack J, Chanderbali AS, Barakat A, Wolcott E, Liang H, Landherr L, Tomsho LP, Hu Y, Carlson JE, Ma H, Schuster SC, Soltis DE, Soltis PS, Altman N, dePamphilis CW (2009) Comparison of next generation sequencing technologies for transcriptome characterization. BMC Genomics 10:347

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang L, Tripurani S, Wanna W, Rexroad CE, Yao J (2010) Fbos, a novel oocyte-specific protein, interacts with proteins important for oocyte development in rainbow trout (Oncorhynchus mykiss). Biol Reprod 83:410

    Google Scholar 

  • Xiang L, He D, Dong W, Zhang Y, Shao J (2010) Deep sequencing-based transcriptome profiling analysis of bacteria-challenged Lateolabrax japonicus reveals insight into the immune-relevant genes in marine fish. BMC Genomics 11:472

    Article  PubMed Central  PubMed  Google Scholar 

  • Yang P, Li X, Shipp MJ, Shockey JM, Cahoon EB (2010) Mining the bitter melon (Momordica charantia L.) seed transcriptome by 454 analysis of non-normalized and normalized cDNA populations for conjugated fatty acid metabolism-related genes. BMC Plant Biol 10:250

    Article  PubMed Central  PubMed  Google Scholar 

  • Yuan J, Eckerdt F, Bereiter-Hahn J, Kurunci-Csacsko E, Kaufmann M, Strebhardt K (2002) Cooperative phosphorylation including the activity of polo-like kinase 1 regulates the subcellular localization of cyclin B1. Oncogene 21:8282–8292

    Article  CAS  PubMed  Google Scholar 

  • Yúfera M, Halm S, Beltran S, Fusté B, Planas JV, Martínez-Rodríguez G (2012) Transcriptomic characterization of the larval stage in gilthead seabream (Sparus aurata) by 454 pyrosequencing. Mar Biotechnol 14:423–435

    Article  PubMed  Google Scholar 

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Acknowledgments

The study was funded by the Research Council of Norway, project 182653/V10. The authors gratefully thank Bjørnar Eggen for the technical assistance during egg collection and incubation. The authors are also thankful to Morten Krogstad and Marianne Fossum for their help in procuring wild fish for the study. We also thank Macrogen Incorporated (Seoul, South Korea) for providing the 454 pyrosequencing service. C.F.C. Lanes’ Ph.D. scholarship is partially supported by the Research Council of Norway and the University of Nordland.

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Lanes, C.F.C., Bizuayehu, T.T., de Oliveira Fernandes, J.M. et al. Transcriptome of Atlantic Cod (Gadus morhua L.) Early Embryos from Farmed and Wild Broodstocks. Mar Biotechnol 15, 677–694 (2013). https://doi.org/10.1007/s10126-013-9527-y

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