Abstract
The mechanism of early fish development as well as the control of egg quality is of great importance for the ability of the oocyte to develop after fertilization. Embryonic development is initially regulated by maternally provided mRNAs and later by the zygotic genome. Maternal mRNAs have an important role in initiating processes crucial to patterning the developing fish embryo. Furthermore, it has been shown that maternal RNA plays an important role in egg quality. The identification and characterization of candidate maternal genes in non-model fish species with important aquaculture interest like the gilthead sea bream Sparus aurata L. is of importance for future studies related to egg quality. The broodstock of the gilthead sea bream produces large quantities of eggs with a high and non-controllable quality variation. In the present study, we have studied the gene expression of 16 genes (gapdh 1 and 2, cathepsin D, L, S and Z, erk1, jnk1, p38 alpha and p38 delta, ppar alpha, beta and gamma, tubulin beta, ferritin M, cyclinA2) of different functional categories in seven developmental stages. The 16 genes were chosen based on their putative involvement in egg quality and regulation of early development. In total, 11 showed a characteristic gene expression pattern pinpointing to the possible function as maternal genes and thus may function as molecular biomarker for egg quality.
Similar content being viewed by others
References
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
Andersen O, Dehli A, Standal H, Giskegjerde TA, Karstensen R, Rorvik KA (1995) Two ferritin subunits of Atlantic salmon (Salmo salar): cloning of the liver cDNAs and antibody preparation. Mol Mar Biol Biotechnol 4:164–170
Andersen O, Pantopoulos K, Kao HT, Muckenthaler M, Youson JH, Pieribone V (1998) Regulation of iron metabolism in the sanguivore lamprey Lampetra fluviatilis—molecular cloning of two ferritin subunits and two iron-regulatory proteins (IRP) reveals evolutionary conservation of the iron-regulatory element (IRE)/IRP regulatory system. Eur J Biochem 254:223–229
Bai J, Solberg C, Fernandes JM, Johnston IA (2007) Profiling of maternal and developmental-stage specific mRNA transcripts in Atlantic halibut Hippoglossus hippoglossus. Gene 386:202–210
Ballif BA, Blenis J (2001) Molecular mechanisms mediating mammalian mitogen-activated protein kinase (MAPK) kinase (MEK)-MAPK cell survival signals. Cell Growth Differ 12:397–408
Bogoyevitch MA, Court NW (2004) Counting on mitogen-activated protein kinases—ERKs 3, 4, 5, 6, 7 and 8. Cell Signal 16:1345–1354
Braissant O, Wahli W (1998) Differential expression of peroxisome proliferator-activated receptor-alpha, -beta, and -gamma during rat embryonic development. Endocrinology 139:2748–2754
Brooks S, Tyler CR, Sumpter JP (1997) Egg quality in fish: what makes a good egg? Rev Fish Biol Fish 7:387–416
Carnevali O, Centonze F, Brooks S, Marota I, Sumpter JP (1999) Molecular cloning and expression of ovarian cathepsin D in seabream, Sparus aurata. Biol Reprod 61:785–791
Carnevali O, Mosconi G, Cambi A, Ridolfi S, Zanuy S, Polzonetti-Magni A (2001) Changes of lysosomal enzyme activities in sea bass Dicentrarchus labrax/eggs and developing embryos. Aquaculture 202:249–256
Carnevali O, Cionna C, Tosti L, Cerda J, Gioacchini G (2008) Changes in cathepsin gene expression and relative enzymatic activity during gilthead sea bream oogenesis. Mol Reprod Dev 75:97–104
Casani D, Randelli E, Costantini S, Facchiano AM, Zou J, Martin S, Secombes CJ, Scapigliati G, Buonocore F (2009) Molecular characterisation and structural analysis of an interferon homologue in sea bass (Dicentrarchus labrax L.). Mol Immunol 46:943–952
Chaves-Pozo E, Mulero V, Meseguer J, Garcia Ayala A (2005) An overview of cell renewal in the testis throughout the reproductive cycle of a seasonal breeding teleost, the gilthead seabream (Sparus aurata L). Biol Reprod 72:593–601
Chaves-Pozo E, Liarte S, Vargas-Chacoff L, Garcia-Lopez A, Mulero V, Meseguer J, Mancera JM, Garcia-Ayala A (2007) 17Beta-estradiol triggers postspawning in spermatogenically active gilthead seabream (Sparus aurata L.) males. Biol Reprod 76:142–148
Darias MJ, Zambonino-Infante JL, Hugot K, Cahu CL, Mazurais D (2008) Gene expression patterns during the larval development of European sea bass (Dicentrarchus labrax) by microarray analysis. Mar Biotechnol (NY) 10:416–428
Davey GC, Calduch-Giner JA, Houeix B, Talbot A, Sitja-Bobadilla A, Prunet P, Perez-Sanchez J, Cairns MT (2011) Molecular profiling of the gilthead sea bream (Sparus aurata L.) response to chronic exposure to the myxosporean parasite Enteromyxum leei. Mol Immunol 48:2102–2112
Ferg M, Sanges R, Gehrig J, Kiss J, Bauer M, Lovas A, Szabo M, Yang L, Straehle U, Pankratz MJ, Olasz F, Stupka E, Muller F (2007) The TATA-binding protein regulates maternal mRNA degradation and differential zygotic transcription in zebrafish. EMBO J 26:3945–3956
Fernandes JM, Mommens M, Hagen O, Babiak I, Solberg C (2008) Selection of suitable reference genes for real-time PCR studies of Atlantic halibut development. Comp Biochem Physiol B Biochem Mol Biol 150: 23–32
Giorgi A, Mignogna G, Bellapadrona G, Gattoni M, Chiaraluce R, Consalvi V, Chiancone E, Stefanini S (2008) The unusual co-assembly of H- and M-chains in the ferritin molecule from the Antarctic teleosts Trematomus bernacchii and Trematomus newnesi. Arch Biochem Biophys 478:69–74
Howe JA, Howell M, Hunt T, Newport JW (1995) Identification of a developmental timer regulating the stability of embryonic cyclin A and a new somatic A-type cyclin at gastrulation. Genes Dev 9:1164–1176
Hu MC, Wang YP, Mikhail A, Qiu WR, Tan TH (1999) Murine p38-delta mitogen-activated protein kinase, a developmentally regulated protein kinase that is activated by stress and proinflammatory cytokines. J Biol Chem 274:7095–7102
Ibabe A, Bilbao E, Cajaraville MP (2005) Expression of peroxisome proliferator-activated receptors in zebrafish (Danio rerio) depending on gender and developmental stage. Histochem Cell Biol 123:75–87
Johnson GL, Dohlman HG, Graves LM (2005) MAPK kinase kinases (MKKKs) as a target class for small-molecule inhibition to modulate signaling networks and gene expression. Curr Opin Chem Biol 9:325–331
Kalendar R, Lee D, Schulman AH (2009) FastPCR software for PCR primer and probe design and repeat search. Genes Genomes Genomics 3(1):1–14
Kane DA, Kimmel CB (1993) The zebrafish midblastula transition. Development 119:447–456
Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253–310
Kjorsvik E, Mangor-Jensen A, Holmefjord I (1990) Egg quality in fishes. Adv Mar Biol 26:71–113
Krens SF, He S, Spaink HP, Snaar-Jagalska BE (2006) Characterization and expression patterns of the MAPK family in zebrafish. Gene Expr Patterns 6:1019–1026
Leaver MJ, Boukouvala E, Antonopoulou E, Diez A, Favre-Krey L, Ezaz MT, Bautista JM, Tocher DR, Krey G (2005) Three peroxisome proliferator-activated receptor isotypes from each of two species of marine fish. Endocrinology 146:3150–3162
Lo J, Lee S, Xu M, Liu F, Ruan H, Eun A, He Y, Ma W, Wang W, Wen Z, Peng J (2003) 15000 unique zebrafish EST clusters and their future use in microarray for profiling gene expression patterns during embryogenesis. Genome Res 13:455–466
Marshall CJ (1995) Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80:179–185
Mathavan S, Lee SG, Mak A, Miller LD, Murthy KR, 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
McCurley AT, Callard GV (2008) Characterization of housekeeping genes in zebrafish: male-female differences and effects of tissue type, developmental stage and chemical treatment. BMC Mol Biol 9:102
Menoyo D, Izquierdo MS, Robaina L, Gines R, Lopez-Bote CJ, Bautista JM (2004) Adaptation of lipid metabolism, tissue composition and flesh quality in gilthead sea bream (Sparus aurata) to the replacement of dietary fish oil by linseed and soyabean oils. Br J Nutr 92:41–52
Mignogna G, Chiaraluce R, Consalvi V, Cavallo S, Stefanini S, Chiancone E (2002) Ferritin from the spleen of the Antarctic teleost Trematomus bernacchii is an M-type homopolymer. Eur J Biochem 269:1600–1606
Mitter K, Kotoulas G, Magoulas A, Mulero V, Sepulcre P, Figueras A, Novoa B, Sarropoulou E (2009) Evaluation of candidate reference genes for QPCR during ontogenesis and of immune-relevant tissues of European seabass (Dicentrarchus labrax). Comp Biochem Physiol B Biochem Mol Biol 153:340–347
Mommens M, Fernandes JM, 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
Pavlidis M, Mylonas C (2011) Sparidae. Biology and aquaculture of gilthead seabream and other species. Wiley-Blackwell, Oxford
Pelegri F (2003) Maternal factors in zebrafish development. Dev Dyn 228:535–554
Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36
Picone G, Engelsen SB, Savorani F, Testi S, Badiani A, Capozzi F (2012) Metabolomics as a powerful tool for molecular quality assessment of the fish Sparus aurata. Nutrients 3:212–227
Roux PP, Blenis J (2004) ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol Mol Biol Rev 68:320–344
Sarropoulou E, Kotoulas G, Power DM, Geisler R (2005a) 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
Sarropoulou E, Power DM, Magoulas A, Geisler R, Kotoulas G (2005b) Comparative analysis and characterization of expressed sequence tags in gilthead sea bream (Sparus aurata) liver and embryos. Aquaculture 243:69–81
Sarropoulou E, Sepulcre P, Poisa-Beiro L, Mulero V, Meseguer J, Figueras A, Novoa B, Terzoglou V, Reinhardt R, Magoulas A, Kotoulas G (2009) Profiling of infection specific mRNA transcripts of the European seabass Dicentrarchus labrax. BMC Genomics 10:157
Sarropoulou E, Fernandes JM, Mitter K, Magoulas A, Mulero V, Sepulcre MP, Figueras A, Novoa B, Kotoulas G (2010) Evolution of a multifunctional gene: The warm temperature acclimation protein Wap65 in the European seabass Dicentrarchus labrax. Mol Phylogenet Evol 55:640–649
Sarropoulou E, Nousdili D, Kotoulas G, Magoulas A (2011) Functional divergences of GAPDH isoforms during early development in two perciform fish species. Mar Biotechnol (NY) 13:1115–1124
Sun YN, Xu TJ, Wang JX, Cheng YZ, Wang RX (2011) Sequence and expression analysis of cathepsin S gene in the miiuy croaker Miichthys miiuy. Fish Physiol Biochem 37:761–765
Tata JR (1986) Coordinated assembly of the developing egg. Bioessays 4:197–201
Traverso JM, Fostier A, Bobe J (2012) Egg transcriptome, the maternal legacy to the embryo. In: Garth MRA, Fletcher (eds) Aquaculture biotechnology. Blackwell, Chichester
Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:RESEARCH0034
Wang W, Zhang M, Sun L (2011) Ferritin M of Cynoglossus semilaevis: an iron-binding protein and a broad-spectrum antimicrobial that depends on the integrity of the ferroxidase center and nucleation center for biological activity. Fish Shellfish Immunol 31:269–274
Wen C, Zhang Z, Ma W, Xu M, Wen Z, Peng J (2005) Genome-wide identification of female-enriched genes in zebrafish. Dev Dyn 232:171–179
Yufera M, Halm S, Beltran S, Fuste B, Planas JV, Martinez-Rodriguez G (2012) Transcriptomic characterization of the larval stage in gilthead seabream (Sparus aurata) by 454 pyrosequencing. Mar Biotechnol (NY)
Zhao S, Fernald RD (2005) Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol 12:1047–1064
Acknowledgments
Authors would like to thank the Department of Aquaculture and specifically Dr. Constantinos Mylonas and Dr. Pascal Divanach for providing embryonic and larvae stages. We also would like to thank FPU (MICINN, Spanish Ministry of Science and Innovation, AP2007–03178).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplement data 1
Developmental stages used in the present study. (S1) 2,4 cell stage, (S2) 16 cell stage, (S3) towards morula, (S4) morula, (S5) high blastula (S6) start of gastrula and (S7) ½ epibolie. (JPEG 60 kb)
Supplement data 2
Primer list including primer sequences, annealing temperature, PCR product size and references. (CSV 1 kb)
Supplement data 3
DNA sequence of nine newly characterized genes of the gilthead sea bream Sparus aurata (FAS 11 kb)
Supplement data 4
RT PCR of ppar alpha, beta and gamma using genomic DNA, cDNA of pooled developmental stages, liver and Control. (JPEG 79 kb)
Rights and permissions
About this article
Cite this article
Fernández, C.G., Roufidou, C., Antonopoulou, E. et al. Expression of Developmental-Stage-Specific Genes in the Gilthead Sea Bream Sparus aurata L.. Mar Biotechnol 15, 313–320 (2013). https://doi.org/10.1007/s10126-012-9486-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10126-012-9486-8