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Gene Expression Profiling of Atlantic Cod (Gadus morhua) Embryogenesis Using Microarray

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Abstract

Atlantic cod (Gadus morhua) is a fish species of high importance, as a key species in a range of Northern ecosystems, in fisheries, and as an emerging species in aquaculture. So far, little is known about the transcriptional activity during early developmental stages of Atlantic cod. Hence, we decided to use a cDNA microarray covering 7,000 genes to analyze the temporal activity of the transcriptome during cod embryogenesis. Twelve different embryonic time points were selected, covering major developmental stages and processes such as maternally derived mRNA, blastula, gastrula, segmentation, hatching, and first-feeding larval stage. The microarray analysis revealed a highly dynamic transcriptional profile, showing for the first time the differential expression of thousands of known and unknown genes during Atlantic cod embryogenesis. These initial findings will serve as an important baseline for future in-depth studies of candidate genes involved in development, reproductive control, disease resistance, growth, nutrient digestion, and metabolism.

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References

  • Arukwe A, Goksoyr A (2003) Eggshell and egg yolk proteins in fish: hepatic proteins for the next generation: oogenetic, population, and evolutionary implications of endocrine disruption. Comp Hepatol 6:1–24

    Google Scholar 

  • Babb SG, Marrs JA (2004) E-cadherin regulates cell movements and tissue formation in early zebrafish embryos. Dev Dyn 230:263–277

    Article  PubMed  CAS  Google Scholar 

  • Babin PJ, Thisse C, Durliat M, Andre M, Akimenko MA, Thisse B (1997) Both apolipoprotein E and A-I genes are present in a nonmammalian vertebrate and are highly expressed during embryonic development. Proc Natl Acad Sci U S A 94:8622–8627

    Article  PubMed  CAS  Google Scholar 

  • Barrell D, Dimmer E, Huntley RP, Binns D, O'donovan C, Apweiler R (2009) The GOA database in 2009—an integrated gene ontology annotation resource. Nucleic Acids Res 37:D396–D403

    Article  PubMed  CAS  Google Scholar 

  • Bo TH, Dysvik J, Jonassen I (2004) LSimpute: accurate estimation of missing values in microarray data with least squares methods. Nucleic Acids Res 32:e34

    Article  PubMed  Google Scholar 

  • Bond JS, Beynon RJ (1995) The astacin family of metalloendopeptidases. Protein Sci 4:1247–1261

    Article  PubMed  CAS  Google Scholar 

  • Booman M, Borza T, Feng C, Hori T, Higgins B, Culf A, Léger D, Chute I, Belkaid A, Rise M, Gamperl A, Hubert S, Kimball J, Ouellette R, Johnson S, Bowman S, Rise M (2011) Development and experimental validation of a 20 K Atlantic cod (Gadus morhua) oligonucleotide microarray based on a collection of over 150,000 ESTs. Mar Biotechnol. doi:10.1007/s10126-010-9335-6

  • Bozinovic G, Sit TL, Hinton DE, Oleksiak MF (2011) Gene expression throughout a vertebrate's embryogenesis. BMC Genomics 12:10

    Article  Google Scholar 

  • Breitling R, Armengaud P, Amtmann A, Herzyk P (2004) Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Lett 573:83–92

    Article  PubMed  CAS  Google Scholar 

  • Canario AVM, Bargelloni L, Volckaert F, Houston RD, Massault C, Guiguen Y (2008) Genomics toolbox for farmed fish. Rev Fish Sci 16:3–15

    Article  Google Scholar 

  • Chong SW, Korzh V, Jiang YJ (2009) Myogenesis and molecules—insights from zebrafish Danio rerio. J Fish Biol 74:1693–1755

    Article  PubMed  CAS  Google Scholar 

  • Cleveland WS, Devlin SJ (1988) Locally weighted regression—an approach to regression-analysis by local fitting. J Am Stat Assoc 83:596–610

    Article  Google Scholar 

  • Donate C, Balasch JC, Callol A, Bobe J, Tort L, Mackenzie S (2010) The effects of immunostimulation through dietary manipulation in the rainbow trout; evaluation of mucosal immunity. Mar Biotechnol 12:88–99

    Article  PubMed  CAS  Google Scholar 

  • Dysvik B, Jonassen I (2001) J-Express: exploring gene expression data using Java. Bioinformatics 17:369–370

    Article  PubMed  CAS  Google Scholar 

  • Edvardsen RB, Malde K, Mittelholzer C, Taranger GL, Nilsen F (2011) EST resources and establishment and validation of a 16 k cDNA microarray from Atlantic cod (Gadus morhua). Comp Biochem Physiol Part D Genom Proteom 6:23–30

    Google Scholar 

  • Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95:14863–14868

    Article  PubMed  CAS  Google Scholar 

  • Estevao MD, Redruello B, Canario AVM, Power DM (2005) Ontogeny of osteonectin expression in embryos and larvae of sea bream (Sparus auratus). Gen Comp Endocrinol 142:155–162

    Article  PubMed  CAS  Google Scholar 

  • Falk-Petersen IB (2005) Comparative organ differentiation during early life stages of marine fish. Fish Shellfish Immunol 19:397–412

    Article  PubMed  CAS  Google Scholar 

  • Fjelldal PG, Van Der Meeren T, Jorstad KE, Hansen TJ (2009) A radiological study on vertebral deformities in cultured and wild Atlantic cod (Gadus morhua, L.). Aquaculture 289:6–12

    Article  Google Scholar 

  • Fjose A, Drivenes Ø (2006) RNAi and microRNAs: from animal models to disease therapy. Birth Defects Res Part C Embryo Today: Rev 78:150–171

    Article  CAS  Google Scholar 

  • Giraldez AJ, Mishima Y, Rihel J, Grocock RJ, Van Dongen S, Inoue K, Enright AJ, Schier AF (2006) Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 312:75–79

    Article  PubMed  CAS  Google Scholar 

  • Hall TE, Smith P, Johnston IA (2004) Stages of embryonic development in the Atlantic cod Gadus morhua. J Morphol 259:255–270

    Article  PubMed  Google Scholar 

  • Helvik J, Oppen-Berntsen D, Walther B (1991) The hatching mechanism in Atlantic halibut (Hippoglossus hippoglossus). Int J Dev Biol 35:9–16

    PubMed  CAS  Google Scholar 

  • Huang XQ, Madan A (1999) CAP3: a DNA sequence assembly program. Genome Res 9:868–877

    Article  PubMed  CAS  Google Scholar 

  • Johansen SD, Coucheron DH, Andreassen M, Karlsen BO, Furmanek T, Jorgensen TE, Emblem A, Breines R, Nordeide JT, Moum T, Nederbragt AJ, Stenseth NC, Jakobsen KS (2009) Large-scale sequence analyses of Atlantic cod. New Biotechnol 25:263–271

    Article  CAS  Google Scholar 

  • Kamisaka Y, Totland GK, Tagawa M, Kurokawa T, Suzuki T, Tanaka M, Ronnestad I (2001) Ontogeny of cholecystokinin-immunoreactive cells in the digestive tract of Atlantic halibut, Hippoglossus hippoglossus, larvae. Gen Comp Endocrinol 123:31–37

    Article  PubMed  CAS  Google Scholar 

  • Kawaguchi M, Yasumasu S, Shimizu A, Sano K, Iuchi I, Nishida M (2010) Conservation of the egg envelope digestion mechanism of hatching enzyme in Euteleostean fishes. FEBS J 277:4973–4987

    Article  PubMed  CAS  Google Scholar 

  • Kjorsvik E, Vandermeeren T, Kryvi H, Arnfinnson J, Kvenseth PG (1991) Early development of the digestive-tract of cod larvae, Gadus morhua L., during start-feeding and starvation. J Fish Biol 38:1–15

    Article  Google Scholar 

  • Lee Y, Tsai J, Sunkara S, Karamycheva S, Pertea G, Sultana R, Antonescu V, Chan A, Cheung F, Quackenbush J (2005) The TIGR gene indices: clustering and assembling EST and known genes and integration with eukaryotic genomes. Nucleic Acids Res 33:D71–D74

    Article  PubMed  CAS  Google Scholar 

  • Lepage T, Gache C (1990) Early expression of a collagenase-like hatching enzyme gene in the sea-urchin embryo. EMBO J 9:3003–3012

    PubMed  CAS  Google Scholar 

  • Liu Z (2011) Development of genomic resources in support of sequencing, assembly, and annotation of the catfish genome. Comp Biochem Physiol Part D Genom Proteom 6:11–17

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Millan A, Gomez-Tato A, Fernandez C, Pardo BG, Alvarez-Dios JA, Calaza M, Bouza C, Vazquez M, Cabaleiro S, Martinez P (2010) Design and performance of a Turbot (Scophthalmus maximus) oligo-microarray based on ESTs from immune tissues. Mar Biotechnol 12:452–465

    Article  PubMed  CAS  Google Scholar 

  • Muller K, Thisse C, Thisse B, Raz E (2002) Expression of a linker histone-like gene in the primordial germ cells in zebrafish. Mech Dev 117:253–257

    Article  PubMed  CAS  Google Scholar 

  • Paschke KA, Lottspeich F, Stuermer CAO (1992) Neurolin, a cell-surface glycoprotein on growing retinal axons in the goldfish visual-system, is reexpressed during retinal axonal regeneration. J Cell Biol 117:863–875

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Pelster B, Burggren WW (1996) Disruption of hemoglobin oxygen transport does not impact oxygen-dependent physiological processes in developing embryos of zebra fish (Danio rerio). Circ Res 79:358–362

    PubMed  CAS  Google Scholar 

  • Pertea G, Huang XQ, 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  PubMed  CAS  Google Scholar 

  • Qiu GF, Ramachandra RK, Rexroad CE, Yao JB (2008) Molecular characterization and expression profiles of cyclin B1, B2 and Cdc2 kinase during oogenesis and spermatogenesis in rainbow trout (Oncorhynchus mykiss). Anim Reprod Sci 105:209–225

    Article  PubMed  CAS  Google Scholar 

  • Quinn NL, Levenkova N, Chow W, Bouffard P, Boroevich KA, Knight JR, Jarvie TP, Lubieniecki KP, Desany BA, Koop BF, Harkins TT, Davidson WS (2008) Assessing the feasibility of GS FLX pyrosequencing for sequencing the Atlantic salmon genome. BMC Genomics 9:404

    Article  PubMed  Google Scholar 

  • Rankin T, Familari M, Lee E, Ginsberg A, Dwyer N, Blanchettemackie J, Drago J, Westphal H, Dean J (1996) Mice homozygous for an insertional mutation in the Zp3 gene lack a zona pellucida and are infertile. Development 122:2903–2910

    PubMed  CAS  Google Scholar 

  • Renninger SL, Gesemann M, Neuhauss SCF (2011) Cone arrestin confers cone vision of high temporal resolution in zebrafish larvae. Eur J Neurosci 33:658–667

    Article  PubMed  Google Scholar 

  • Ronnestad I, Kamisaka Y, Conceicao LEC, Morais S, Tonheim SK (2007) Digestive physiology of marine fish larvae: hormonal control and processing capacity for proteins, peptides and amino acids. Aquaculture 268:82–97

    Article  CAS  Google Scholar 

  • Sarropoulou E, Kotoulas G, Power DM, Geisler R (2005) Gene expression profiling of gilthead sea bream during early development and detection of stress-related genes by the application of cDNA microarray technology. Physiol Genomics 23:182–191

    Article  PubMed  CAS  Google Scholar 

  • Seear PJ, Carmichael SN, Talbot R, Taggart JB, Bron JE, Sweeney GE (2010) Differential gene expression during smoltification of Atlantic salmon (Salmo salar L.): a first large-scale microarray study. Mar Biotechnol 12:126–140

    Article  PubMed  CAS  Google Scholar 

  • Shimizu T, Yabe T, Muraoka O, Yonemura S, Aramaki S, Hatta K, Bae YK, Nojima H, Hibi M (2005) E-cadherin is required for gastrulation cell movements in zebrafish. Mech Dev 122:747–763

    Article  PubMed  CAS  Google Scholar 

  • Skoglund P, Rolo A, Chen XJ, Gumbiner BM, Keller R (2008) Convergence and extension at gastrulation require a myosin IIB-dependent cortical actin network. Development 135:2435–2444

    Article  PubMed  CAS  Google Scholar 

  • Solnica-Krezel L (2005) Conserved patterns of cell movements during vertebrate gastrulation. Curr Biol 15:R213–R228

    Article  PubMed  CAS  Google Scholar 

  • Swain P, Nayak SK (2009) Role of maternally derived immunity in fish. Fish Shellfish Immunol 27:89–99

    Article  PubMed  CAS  Google Scholar 

  • Taranger GL, Carrillo M, Schulz RW, Fontaine P, Zanuy S, Felip A, Weltzien FA, Dufour S, Karlsen O, Norberg B, Andersson E, Hausen T (2010) Control of puberty in farmed fish. Gen Comp Endocrinol 165:483–515

    Article  PubMed  CAS  Google Scholar 

  • Weinmann L, Hock J, Ivacevic T, Ohrt T, Mutze J, Schwille P, Kremmer E, Benes V, Urlaub H, Meister G (2009) Importin 8 is a gene silencing factor that targets Argonaute proteins to distinct mRNAs. Cell 136:496–507

    Article  PubMed  CAS  Google Scholar 

  • Wu Q (2005) Comparative genomics and diversifying selection of the clustered vertebrate protocadherin genes. Genetics 169:2179–2188

    Article  PubMed  CAS  Google Scholar 

  • Wu XM, Viveiros MM, Eppig JJ, Bai YC, Fitzpatrick SL, Matzuk MM (2003) Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition. Nat Genet 33:187–191

    Article  PubMed  CAS  Google Scholar 

  • Yasumasu S, Yamada K, Akasaka K, Mitsunaga K, Iuchi I, Shimada H, Yamagami K (1992) Isolation of cDNAs for lce and hce, 2 constituent proteases of the hatching enzyme of oryzias-latipes, and concurrent expression of their messenger-rnas during development. Dev Biol 153:250–258

    Article  PubMed  CAS  Google Scholar 

  • Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We would like to thank Stig Mæhle and Elin Sørhus for technical assistance with the microarray hybridizations and real-time PCR experiments, respectively, and Ketil Malde for bioinformatics assistance in the annotation of the microarray probes.

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Correspondence to Rolf B. Edvardsen.

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Drivenes, Ø., Taranger, G.L. & Edvardsen, R.B. Gene Expression Profiling of Atlantic Cod (Gadus morhua) Embryogenesis Using Microarray. Mar Biotechnol 14, 167–176 (2012). https://doi.org/10.1007/s10126-011-9399-y

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