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Marine Biotechnology

, Volume 10, Issue 4, pp 416–428 | Cite as

Gene Expression Patterns During the Larval Development of European Sea Bass (Dicentrarchus Labrax) by Microarray Analysis

  • M. J. Darias
  • J. L. Zambonino-Infante
  • K. Hugot
  • C. L. Cahu
  • D. Mazurais
Original Article

Abstract

During the larval period, marine teleosts undergo very fast growth and dramatic changes in morphology, metabolism, and behavior to accomplish their metamorphosis into juvenile fish. Regulation of gene expression is widely thought to be a key mechanism underlying the management of the biological processes required for harmonious development over this phase of life. To provide an overall analysis of gene expression in the whole body during sea bass larval development, we monitored the expression of 6,626 distinct genes at 10 different points in time between 7 and 43 days post-hatching (dph) by using heterologous hybridization of a rainbow trout cDNA microarray. The differentially expressed genes (n = 485) could be grouped into two categories: genes that were generally up-expressed early, between 7 and 23 dph, and genes up-expressed between 25 and 43 dph. Interestingly, among the genes regulated during the larval period, those related to organogenesis, energy pathways, biosynthesis, and digestion were over-represented compared with total set of analyzed genes. We discuss the quantitative regulation of whole-body contents of these specific transcripts with regard to the ontogenesis and maturation of essential functions that take place over larval development. Our study is the first utilization of a transcriptomic approach in sea bass and reveals dynamic changes in gene expression patterns in relation to marine finfish larval development.

Keywords

Fish larvae Development Microarray Gene expression Sea bass 

Notes

Acknowledgments

The authors thank INRA-GADIE resource center for providing microarrays (Jouy en Josas, France) and Genofish program for financial and scientific support. We also thank A. Le Cam and J. Montfort from INRA-SCRIBE genomic platform (Rennes, France) for excellent technical assistance, SIGENAE team (INRA Toulouse, France) for bioinformatic tools development, P. Quazuguel, and Gabriela Hortopan for larval rearing and real-time PCR analysis, respectively, and Helen McCombie for correcting the English. M. J. Darias was supported by a postdoctoral fellowship from the Fundación Ramón Areces (Spain).

References

  1. Baldessari D, Shin Y, Krebs O, Konig R, Koide T, Vinayagam A, Fenger U, Mochii M, Terasaka C, Kitayama A, Peiffer D, Ueno N, Eils R, Cho KW, Niehrs C (2005) Global gene expression profiling and cluster analysis in Xenopus laevis. Mech Dev 122:441–475PubMedCrossRefGoogle Scholar
  2. Baron D, Houlgatte R, Fostier A, Guiguen Y (2005) Large-scale temporal gene expression profiling during gonadal differentiation and early gametogenesis in rainbow trout. Biol Reprod 73:959–966PubMedCrossRefGoogle Scholar
  3. Bobe J, Montfort J, Nguyen T, Fostier A (2006) Identification of new participants in the rainbow trout (Oncorhynchus mykiss) oocyte maturation and ovulation processes using cDNA microarrays. Reprod Biol Endocrinol 4:39–55PubMedCrossRefGoogle Scholar
  4. Bonnet E, Fostier A, Bobe J (2007) Microarray-based analysis of fish egg quality after natural or controlled ovulation. BMC Genomics 8:55–72PubMedCrossRefGoogle Scholar
  5. Buckley BA (2007) Comparative environmental genomics in non-model species: using heterologous hybridization to DNA-based microarrays. J Exp Biol 210:1602–1606PubMedCrossRefGoogle Scholar
  6. Cahu CL, Zambonino Infante JL (1994) Early weaning of sea bass (Dicentrarchus labrax) larvae with a compound diet: effect on digestive enzymes. Comp Biochem Physiol 109A:213–222CrossRefGoogle Scholar
  7. Cathelin R, Lopez F, Klopp C (2007) AGScan: a pluggable microarray image quantification software based on the ImageJ library. Bioinformatics 23:247–248PubMedCrossRefGoogle Scholar
  8. Cohen R, Chalifa-Caspi V, Williams TD, Auslander M, George SG, Chipman JK, Tom M (2007) Estimating the efficiency of fish cross-species cDNA microarray hybridisation. Mar Biotechnol 9:491–499PubMedCrossRefGoogle Scholar
  9. Conceiçao LEC, Verreth JAJ, Verstegen MWA, Huisman EA (1998) A preliminary model for dynamic simulation of growth in fish larvae: application to the African catfish (Clarias gariepinus) and turbot (Scophthalmus maximus). Aquaculture 163:215–235CrossRefGoogle Scholar
  10. Darias MJ, Murray HM, Martinez-Rodriguez G, Cardenas S, Yufera M (2005) Gene expression of pepsinogen during the larval development of red porgy (Pagrus pagrus). Aquaculture 248:245–252CrossRefGoogle Scholar
  11. Darias MJ, Murray HM, Gallant JW, Astola A, Douglas SE, Yufera M, Martinez-Rodriguez G (2006) Characterization of a partial alpha-amylase clone from red porgy (Pagrus pagrus): expression during larval development. Comp Biochem Physiol B Biochem Mol Biol 143:209–218PubMedCrossRefGoogle Scholar
  12. Darias MJ, Murray HM, Gallant JW, Douglas SE, Yufera M, Martinez-Rodriguez G (2007a) The spatiotemporal expression pattern of trypsinogen and bile salt-activated lipase during the larval development of red porgy (Pagrus pagrus, Pisces, Sparidae). Mar Biol 152:109–118CrossRefGoogle Scholar
  13. Darias MJ, Murray HM, Gallant JW, Douglas SE, Yufera M, Martinez-Rodriguez G (2007b) Ontogeny of pepsinogen and gastric proton pump expression in red porgy (Pagrus pagrus): determination of stomach functionality. Aquaculture 270:369–378CrossRefGoogle Scholar
  14. Deane EE, Woo NY (2003) Ontogeny of thyroid hormones, cortisol, hsp70 and hsp90 during silver sea bream larval development. Life Sci 72:805–818PubMedCrossRefGoogle Scholar
  15. de Jesus EG, Hirano T (1992) Changes in whole body concentrations of cortisol, thyroid hormones, and sex steroids during early development of the chum salmon, Oncorhynchus keta. Gen Comp Endocrinol 85:55–61PubMedCrossRefGoogle Scholar
  16. Erwin WM, Ashman K, O'Donnel P, Inman RD (2006) Nucleus pulposus notochord cells secrete connective tissue growth factor and up-regulate proteoglycan expression by intervertebral disc chondrocytes. Arthritis Rheum 54:3859–3867PubMedCrossRefGoogle Scholar
  17. Falk-Petersen IB (2005) Comparative organ differentiation during early life stages of marine fish. Fish Shellfish Immunol 19:397–412PubMedCrossRefGoogle Scholar
  18. Galloway TF, Kjorsvik E, Kryvi H (1999) Muscle growth and development in Atlantic cod larvae (Gadus morhua L.), related to different somatic growth rates. J Exp Biol 202:2111–2120PubMedGoogle Scholar
  19. Gibb AC, Swanson BO, Wesp H, Landels C, Liu C (2006) Development of the escape response in teleost fishes: do ontogenetic changes enable improved performance? Physiol Biochem Zool 79:7–19PubMedCrossRefGoogle Scholar
  20. Govoni JJ, Boehlert GW, Watanabe Y (1986) The physiology of digestion in fish larvae. Env Biol Fish 16:59–77CrossRefGoogle Scholar
  21. Govoroun M, Le Gac F, Guiguen Y (2006) Generation of a large scale repertoire of Expressed Sequence Tags (ESTs) from normalised rainbow trout cDNA libraries. BMC Genomics 7:196–203PubMedCrossRefGoogle Scholar
  22. Horiuchi K, Amizuka N, Takeshita S, Takamatsu H, Katsuura M, Ozawa H, Toyama Y, Bonewald LF, Kudo A (1999) Identification and characterization of a novel protein, periostin, with restricted expression to periosteum and periodontal ligament and increased expression by transforming growth factor beta. J Bone Miner Res 14:1239–1249PubMedCrossRefGoogle Scholar
  23. Hosack DA, Dennis G Jr, Sherman BT, Lane HC, Lempicki RA (2003) Identifying biological themes within lists of genes with EASE. Genome Biol 4:R70PubMedCrossRefGoogle Scholar
  24. Jamers A, Van der Ven K, Moens L, Robbens J, Potters G, Guisez Y, Blust R, De Coen W (2006) Effect of copper exposure on gene expression profiles in Chlamydomonas reinhardtii based on microarray analysis. Aquat Toxicol 80:249–260PubMedCrossRefGoogle Scholar
  25. Jenny MJ, Chapman RW, Mancia A, Chen YA, McKillen DJ, Trent H, Lang P, Escoubas JM, Bachere E, Boulo V, Liu ZJ, Gross PS, Cunningham C, Cupit PM, Tanguy A, Guo X, Moraga D, Boutet I, Huvet A, De Guise S, Almeida JS, Warr GW (2007) A cDNA microarray for Crassostrea virginica and C. gigas. Mar Biotechnol 9:577–591PubMedCrossRefGoogle Scholar
  26. Kassahn KS, Caley MJ, Ward AC, Connolly AR, Stone G, Crozier RH (2007) Heterologous microarray experiments used to identify the early gene response to heat stress in a coral reef fish. Mol Ecol 16:1749–1763PubMedCrossRefGoogle Scholar
  27. Mascarello F, Rowlerson A, Radaelli G, Scapolo PA, Veggetti A (1995) Differentiation and growth of muscle in the fish Sparus aurata (L): I. Myosin expression and organization of fibre types in lateral muscle from hatching to adult. J Muscle Res Cell Motil 16:213–222PubMedCrossRefGoogle Scholar
  28. Mazurais D, Montfort J, Delalande C, Gac FL (2005) Transcriptional analysis of testis maturation using trout cDNA macroarrays. Gen Comp Endocrinol 142:143–154PubMedCrossRefGoogle Scholar
  29. Meyer RA, Sweeney HL, Kushmerick MJ (1984) A simple analysis of the “phosphocreatine shuttle”. Am J Physiol 246:365–377Google Scholar
  30. Mori T, Hiraka I, Kurata Y, Kawachi H, Mano N, Devlin RH, Nagoya H, Araki K (2007) Changes in hepatic gene expression related to innate immunity, growth and iron metabolism in GH-transgenic amago salmon (Oncorhynchus masou) by cDNA subtraction and microarray analysis, and serum lysozyme activity. Gen Comp Endocrinol 151:42–54PubMedCrossRefGoogle Scholar
  31. Moriya S, Urawa S, Suzuki O, Urano A, Abe S (2004) DNA microarray for rapid detection of mitochondrial DNA haplotypes of chum salmon. Mar Biotechnol 6:430–434PubMedCrossRefGoogle Scholar
  32. Moriya S, Sato S, Azumaya T, Suzuki O, Urawa S, Urano A, Abe S (2007) Genetic stock identification of chum salmon in the Bering Sea and North Pacific Ocean using mitochondrial DNA microarray. Mar Biotechnol 9:179–191Google Scholar
  33. Murray HM, Perez-Casanova JC, Gallant JW, Johnson SC, Douglas SE (2004) Trypsinogen expression during the development of the exocrine pancreas in winter flounder (Pleuronectes americanus). Comp Biochem Physiol A Mol Integr Physiol 138:53–59PubMedCrossRefGoogle Scholar
  34. Nguyen C, Rocha D, Granjeaud S, Baldit M, Bernard K, Naquet P, Jordan BR (1995) Differential gene expression in the murine thymus assayed by quantitative hybridization of arrayed cDNA clones. Genomics 29:207–216PubMedCrossRefGoogle Scholar
  35. Parra G, Yufera M (2001) Comparative energetics during early development of two marine fish species, Solea senegalensis (Kaup) and Sparus aurata (L.). J Exp Biol 204:2175–2183PubMedGoogle Scholar
  36. Person-LeRuyet J, Fischer C, Mugnier C (1991) Potentiel de croissance du bar (Dicentrarchus labrax) pendant la phase ecloserie: relation tailles/poids. CIEM F 38:16–31Google Scholar
  37. Renn SC, Aubin-Horth N, Hofmann HA (2004) Biologically meaningful expression profiling across species using heterologous hybridization to a cDNA microarray. BMC Genomics 5:42–55PubMedCrossRefGoogle Scholar
  38. Riva A, Carpentier AS, Torrésani B, Hénaut A (2005) Comments on selected fundamental aspects of microarray analysis. Comput Biol Chem 29:319–336PubMedCrossRefGoogle Scholar
  39. Ronnestad I, Thorsen A, Finn RN (1999) Fish larval nutrition: a review of recent advances in the roles of amino acids. Aquaculture 177:201–216CrossRefGoogle Scholar
  40. Sapede D, Gompel N, Dambly-Chaudiere C, Ghysen A (2002) Cell migration in the postembryonic development of the fish lateral line. Development 129:605–615PubMedGoogle Scholar
  41. 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 23:182–191PubMedCrossRefGoogle Scholar
  42. Segner H, Storch V, Reinecke M, Kloas W, Hanke W (1994) The development of functional digestive and metabolic organs in turbot, Scophthalmus maximus. Mar Biol 119:471–486CrossRefGoogle Scholar
  43. Srivastava AS, Kurokawa T, Suzuki T (2002) mRNA expression of pancreatic enzyme precursors and estimation of protein digestibility in first feeding larvae of the Japanese flounder, Paralichthys olivaceus. Comp Biochem Physiol A Mol Integr Physiol 132:629–635PubMedCrossRefGoogle Scholar
  44. Szisch V, Papandroulakis N, Fanouraki E, Pavlidis M (2005) Ontogeny of the thyroid hormones and cortisol in the gilthead sea bream, Sparus aurata. Gen Comp Endocrinol 142:186–192PubMedCrossRefGoogle Scholar
  45. Tanaka M, Kawai S, Seikai T, Burke JS (1996) Development of the digestive organ system in Japanese flounder in relation to metamorphosis and settlement. Mar Fresh Behav Physiol 28:19–31CrossRefGoogle Scholar
  46. Tanaka TS, Jaradat SA, Lim MK, Kargul GJ, Wang X, Grahovac MJ, Pantano S, Sano Y, Piao Y, Nagaraja R, Doi H, Wood WH 3rd, Becker KG, Ko MS (2000) Genome-wide expression profiling of mid-gestation placenta and embryo using a 15,000 mouse developmental cDNA microarray. Proc Natl Acad Sci U S A 97:9127–9132PubMedCrossRefGoogle Scholar
  47. Ton C, Stamatiou D, Dzau VJ, Liew CC (2002) Construction of a zebrafish cDNA microarray: gene expression profiling of the zebrafish during development. Biochem Biophys Res Commun 296:1134–1142PubMedCrossRefGoogle Scholar
  48. Villeneuve LA, Gisbert E, Moriceau J, Cahu CL, Zambonino-Infante JL (2006) Intake of high levels of vitamin A and polyunsaturated fatty acids during different developmental periods modifies the expression of morphogenesis genes in European sea bass (Dicentrarchus labrax). Br J Nutr 95:677–687PubMedCrossRefGoogle Scholar
  49. Von Schalburg KR, Rise ML, Cooper GA, Brown GD, Gibbs AR, Nelson CC, Davidson WS, Koop BF (2005) Fish and chips: various methodologies demonstrate utility of a 16,006-gene salmonid microarray. BMC Genomics 6:126–133CrossRefGoogle Scholar
  50. Wang B, Li F, Dong B, Zhang X, Zhang C, Xiang J (2006) Discovery of the genes in response to white spot syndrome virus (WSSV) infection in Fenneropenaeus chinensis through cDNA microarray. Mar Biotechnol 8:491–500PubMedCrossRefGoogle Scholar
  51. Weiner S, Traub W (1986) Organization of hydroxyapatite crystals within collagen fibrils. FEBS Lett 206:262–266PubMedCrossRefGoogle Scholar
  52. White KP, Rifkin SA, Hurban P, Hogness DS (1999) Microarray analysis of Drosophila development during metamorphosis. Science 286:2179–2184PubMedCrossRefGoogle Scholar
  53. Wieser W (1995) Energetics of fish larvae, the smallest vertebrates. Acta Physiol Scand 154:279–290PubMedGoogle Scholar
  54. Wullimann MF, Puelles L, Wicht H (1999) Early postembryonic neural development in the zebrafish: a 3-D reconstruction of forebrain proliferation zones shows their relation to prosomeres. Eur J Morphol 37:117–121PubMedCrossRefGoogle Scholar
  55. Zambonino Infante JL, Cahu CL (2001) Ontogeny of the gastrointestinal tract of marine fish larvae. Comp Biochem Physiol C Toxicol Pharmacol 130:477–487PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • M. J. Darias
    • 1
  • J. L. Zambonino-Infante
    • 1
  • K. Hugot
    • 2
  • C. L. Cahu
    • 1
  • D. Mazurais
    • 1
  1. 1.Ifremer, Nutrition Aquaculture and Genomics Research Unit, UMR 1067Ifremer, Technopole Brest-IroisePlouzanéFrance
  2. 2.INRA, DGA, UMR314, Laboratoire de Radiobiologie et d’Etude du GénomeJouy en JosasFrance

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