Skip to main content

Advertisement

SpringerLink
Log in

Transcriptome Profiling of Embryonic Development Rate in Rainbow Trout Advanced Backcross Introgression Lines

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

In rainbow trout (Oncorhynchus mykiss) and other fishes, embryonic development rate is an ecologically and evolutionarily important trait that is closely associated with survival and physiological performance later in life. To identify genes differentially regulated in fast and slow-developing embryos of rainbow trout, we examined gene expression across developmental time points in rainbow trout embryos possessing alleles linked to a major quantitative trait loci (QTL) for fast versus slow embryonic development rate. Whole genome expression microarray analyses were conducted using embryos from a fourth generation backcross family, whereby each backcross generation involved the introgression of the fast-developing alleles for a major development rate QTL into a slow-developing clonal line of rainbow trout. Embryos were collected at 15, 19, and 28 days post-fertilization; sex and QTL genotype were determined using molecular markers, and cDNA from 48 embryos were used for microarray analysis. A total of 183 features were identified with significant differences between embryonic development rate genotypes. Genes associated with cell cycle growth, muscle contraction and protein synthesis were expressed significantly higher in embryos with the fast-developing allele (Clearwater) than those with the slow-developing allele (Oregon State University), which may associate with fast growth and early body mass construction in embryo development. Across time points, individuals with the fast-developing QTL allele appeared to have earlier onset of these developmental processes when compared to individuals with the slow development alleles, even as early as 15 days post-fertilization. Differentially expressed candidate genes chosen for linkage mapping were localized primarily to regions outside of the major embryonic development rate QTL, with the exception of a single gene (very low-density lipoprotein receptor precursor).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Allendorf F, Thorgaard G (1984) Tetraploidy and the evolution of salmonid fishes. In: Turner BJ (ed) Evolutionary genetics of fishes. Plenum Press, New York

    Google Scholar 

  • Allendorf FW, Knudsen KL, Leary RF (1983) Adaptive significance of differences in the tissue-specific expression of a phosphoglucomutase gene in rainbow trout. P Natl Acad Sci USA 80:1397–1400

    Article  CAS  Google Scholar 

  • Baker DA, Russell S (2009) Gene expression during Drosophila melanogaster egg development before and after reproductive diapause. BMC Genomics 10:242

    Article  PubMed  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B Met 57:289–300

    Google Scholar 

  • Breitling R, Li Y, Tesson BM, Fu JY, Wu CL, Wiltshire T, Gerrits A, Bystrykh LV, De Haan G, Su AI, Jansen RC (2008) Genetical genomics: spotlight on QTL hotspots. PLoS Genetics 4:e1000232

    Article  PubMed  Google Scholar 

  • Broadhurst MK, Lee RS, Hawkins S, Wheeler TT (2005) The p100 EBNA-2 coactivator: a highly conserved protein found in a range of exocrine and endocrine cells and tissues in cattle. Biochim Biophys Acta 1681:126–133

    PubMed  CAS  Google Scholar 

  • Brunelli JP, Wertzler KJ, Sundin K, Thorgaard GH (2008) Y-specific sequences and polymorphisms in rainbow trout and Chinook salmon. Genome 51:739–748

    Article  PubMed  CAS  Google Scholar 

  • Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159

    Article  PubMed  CAS  Google Scholar 

  • Collins JH (1991) Myosin light chains and troponin C: structural and evolutionary relationships revealed by amino acid sequence comparisons. J Muscle Res Cell Motil 12:3–25

    Article  PubMed  CAS  Google Scholar 

  • Cox L, Birnbaum S, Vandeberg J (2002) Identification of candidate genes regulating HDL cholesterol using a chromosomal region expression array. Genome Res 12:1693–1702

    Article  PubMed  CAS  Google Scholar 

  • Derome N, Bernatchez L (2006) The transcriptomics of ecological convergence between 2 limnetic coregonine fishes (Salmonidae). Mol Biol and Evol 23:2370–2378

    Article  CAS  Google Scholar 

  • Derome N, Duchesne P, Bernatchez L (2006) Parallelism in gene transcription among sympatric lake whitefish (Coregonus clupeaformis Mitchill) ecotypes. Mol Ecol 15:1239–1249

    Article  PubMed  CAS  Google Scholar 

  • Ding ST, Lilburn MS (2002) The ontogeny of fatty acid-binding protein in turkey (Meleagridis gallopavo) intestine and yolk sac membrane during embryonic and early posthatch development. Poultry Sci 81:1065–1070

    CAS  Google Scholar 

  • Einum S, Fleming IA (2000) Selection against late emergence and small offspring in Atlantic salmon (Salmo salar). Evolution 54:628–639

    PubMed  CAS  Google Scholar 

  • Evsikov AV, De Evsikova CM (2009) Gene expression during the oocyte-to-embryo transition in mammals. Molecular Reprod Dev 76:805–818

    Article  CAS  Google Scholar 

  • Friedman JE, Watson JA Jr, Lam DW, Rokita SE (2006) Iodotyrosine deiodinase is the first mammalian member of the NADH oxidase/flavin reductase superfamily. J Biol Chem 281:2812–2819

    Article  PubMed  CAS  Google Scholar 

  • Gahr SA, Vallejo RL, Weber GM, Shepherd BS, Silverstein JT, Rexroad CE 3rd (2008) Effects of short-term growth hormone treatment on liver and muscle transcriptomes in rainbow trout (Oncorhynchus mykiss). Physiol Genomics 32:380–392

    PubMed  CAS  Google Scholar 

  • Haidle L, Janssen JE, Gharbi K, Moghadam HK, Ferguson MM, Danzmann RG (2008) Determination of quantitative trait loci (QTL) for early maturation in rainbow trout (Oncorhynchus mykiss). Mar Biotechnol 10:579–592

    Article  PubMed  CAS  Google Scholar 

  • Hatze H (1973) A theory of contraction and a mathematical model of striated muscle. J Theor Biol 40:219–246

    Article  PubMed  CAS  Google Scholar 

  • Jansen RC, Nap JP (2001) Genetical genomics: the added value from segregation. Trends Genet 17:388–391

    Article  PubMed  CAS  Google Scholar 

  • Jarvinen AK, Hautaniemi S, Edgren H, Auvinen P, Saarela J, Kallioniemi OP, Monni O (2004) Are data from different gene expression microarray platforms comparable? Genomics 83:1164–1168

    Article  PubMed  CAS  Google Scholar 

  • Jensen JOT, Jensen ME (1999) IncubWin: a new Windows 95/98, NT computer program for predicting embryonic stages in Pacific salmon and steelhead trout. Bull Aquacult Assoc Canada 99–94:28–30

    Google Scholar 

  • Kawasaki H, Nakayama S, Kretsinger RH (1998) Classification and evolution of EF-hand proteins. Biometals 11:277–295

    Article  PubMed  CAS  Google Scholar 

  • Kroening S, Solomovitch S, Sachs M, Wullich B, Goppelt-Struebe M (2009) Regulation of connective tissue growth factor (CTGF) by hepatocyte growth factor in human tubular epithelial cells. Nephrol Dial Transplant 24:755–762

    Article  PubMed  CAS  Google Scholar 

  • Liu H, Cheng H, Tirunagaru V, Sofer L, Burnside J (2001) A strategy to identify positional candidate genes conferring Marek’s disease resistance by integrating DNA microarrays and genetic mapping. Anim Genet 32:351–359

    Article  PubMed  CAS  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 

  • Mizuno H, Hamada A, Shimada K, Honda H (2007) Tropomyosin as a regulator of the sliding movement of actin filaments. Biosystems 90:449–455

    Article  PubMed  CAS  Google Scholar 

  • Murthi P, Fitzpatrick E, Borg AJ, Donath S, Brennecke SP, Kalionis B (2008) GAPDH, 18 S rRNA and YWHAZ are suitable endogenous reference genes for relative gene expression studies in placental tissues from human idiopathic fetal growth restriction. Placenta 29:798–801

    Article  PubMed  CAS  Google Scholar 

  • Nichols KM, Broman KW, Sundin K, Young JM, Wheeler PA, Thorgaard GH (2007) Quantitative trait loci x maternal cytoplasmic environment interaction for development rate in Oncorhynchus mykiss. Genetics 175:335–347

    Article  PubMed  Google Scholar 

  • Nichols KM, Felip A, Wheeler PA, Thorgaard GH (2008) The genetic basis of smoltification-related traits in Oncorhynchus mykiss. Genetics 179:1559–1575

    Article  PubMed  Google Scholar 

  • Nichols KM, Young WP, Danzmann RG, Robison BD, Rexroad C, Noakes M, Phillips RB, Bentzen P, Spies I, Knudsen K, Allendorf FW, Cunningham BM, Brunelli J, Zhang H, Ristow S, Drew R, Brown KH, Wheeler PA, Thorgaard GH (2003) A consolidated linkage map for rainbow trout (Oncorhynchus mykiss). Anim Genet 34:102–115

    Article  PubMed  CAS  Google Scholar 

  • Nolte AW, Renaut S, Bernatchez L (2009) Divergence in gene regulation at young life history stages of whitefish (Coregonus sp.) and the emergence of genomic isolation. BMC Evol Biol 9:59

    Article  PubMed  Google Scholar 

  • O’malley KG, Sakamoto T, Danzmann RG, Ferguson MM (2003) Quantitative trait loci for spawning date and body weight in rainbow trout: testing for conserved effects across ancestrally duplicated chromosomes. J Hered 94:273–284

    Article  PubMed  Google Scholar 

  • Olsvik PA, Softeland L, Lie KK (2008) Selection of reference genes for qRT-PCR examination of wild populations of Atlantic cod Gadus morhua. BMC Res Notes 1:47

    Article  PubMed  Google Scholar 

  • Perry SV (1973) The control of muscular contraction. Symp Soc Exp Biol 27:531–550

    PubMed  CAS  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45

    Article  PubMed  CAS  Google Scholar 

  • Phillips RB, Nichols KM, Dekoning JJ, Morasch MR, Keadey KA, Rexroad C, Gahr SA, Danzmann RG, Drew RE, Thorgaard GH (2006) Assignment of rainbow trout linkage groups to specific chromosomes. Genetics 174:1661–1670

    Article  PubMed  CAS  Google Scholar 

  • Purcell MK, Nichols KM, Winton JR, Kurath G, Thorgaard GH, Wheeler P, Hansen JD, Herwig RP, Park LK (2006) Comprehensive gene expression profiling following DNA vaccination of rainbow trout against infectious hematopoietic necrosis virus. Mol Immunol 43:2089–2106

    Article  PubMed  CAS  Google Scholar 

  • Raible F, Brand M (2001) Tight transcriptional control of the ETS domain factors Erm and Pea3 by Fgf signaling during early zebrafish development. Mech Dev 107:105–117

    Article  PubMed  CAS  Google Scholar 

  • Renaut S, Nolte AW, Bernatchez L (2009) Gene expression divergence and hybrid misexpression between lake whitefish species pairs (Coregonus spp. Salmonidae). Mol Biol Evol 26:925–936

    Article  PubMed  CAS  Google Scholar 

  • Robison BD, Wheeler PA, Sundin K, Sikka P, Thorgaard GH (2001) Composite interval mapping reveals a major locus influencing embryonic development rate in rainbow trout (Oncorhynchus mykiss). J Hered 92:16–22

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Zas SL, Schellander K, Lewin HA (2007) Biological interpretations of transcriptomic profiles in mammalian oocytes and embryos. Reprocution 135:129–139

    Google Scholar 

  • Salem M, Kenney PB, Rexroad CE 3rd, Yao J (2006) Microarray gene expression analysis in atrophying rainbow trout muscle: a unique nonmammalian muscle degradation model. Physiol Genomics 28:33–45

    Article  PubMed  CAS  Google Scholar 

  • Salem M, Silverstein J, Rexroad CE 3rd, Yao J (2007) Effect of starvation on global gene expression and proteolysis in rainbow trout (Oncorhynchus mykiss). BMC Genomics 8:328

    Article  PubMed  Google Scholar 

  • Schaub MC, Heizmann CW (2008) Calcium, troponin, calmodulin, S100 proteins: from myocardial basics to new therapeutic strategies. Biochem Biophys Res Commun 369:247–264

    Article  PubMed  CAS  Google Scholar 

  • Schorderet DF, Menasche M, Morand S, Bonnel S, Buchillier V, Marchant D, Auderset K, Bonny C, Abitbol M, Munier FL (2000) Genomic characterization and embryonic expression of the mouse Bigh3 (Tgfbi) gene. Biochem Biophys Res Commun 274:267–274

    Article  PubMed  CAS  Google Scholar 

  • Shockley KR, Churchill GA (2006) Gene expression analysis of mouse chromosome substitution strains. Mamm Genome 17:598–614

    Article  PubMed  CAS  Google Scholar 

  • Singh A, Mcintyre L, Sherman L (2003) Microarray analysis of the genome-wide response to iron deficiency and iron reconstitution in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 132:1825–1839

    Article  PubMed  CAS  Google Scholar 

  • Sladek R, Hudson TJ (2006) Elucidating cis- and trans-regulatory variation using genetical genomics. Trends Genet 22:245–250

    Article  PubMed  CAS  Google Scholar 

  • St-Cyr J, Derome N, Bernatchez L (2008) The transcriptomics of life-history trade-offs in whitefish species pairs (Coregonus sp.). Mol Ecol 17:1850–1870

    Article  PubMed  CAS  Google Scholar 

  • Street NR, Skogstrom O, Sjodin A, Tucker J, Rodriguez-Acosta M, Nilsson P, Jansson S, Taylor G (2006) The genetics and genomics of the drought response in Populus. Plant J 48:321–341

    Article  PubMed  CAS  Google Scholar 

  • Sundin K, Brown KH, Drew RE, Nichols KM, Wheeler PA, Thorgaard GH (2005) Genetic analysis of a development rate QTL in backcrosses of clonal rainbow trout, Oncorhynchus mykiss. Aquaculture 247:75–83

    Article  CAS  Google Scholar 

  • Sundstrom LF, Lohmus M, Devlin RH (2005) Selection on increased intrinsic growth rates in coho salmon, Oncorhynchus kisutch. Evolution 59:1560–1569

    PubMed  Google Scholar 

  • Tabakoff B, Bhave S, Hoffman P (2003) Selective breeding, quantitative trait locus analysis, and gene arrays identify candidate genes for complex drug-related behaviors. J Neurosci 23:4491–4498

    PubMed  CAS  Google Scholar 

  • Tomancak P, Berman BP, Beaton A, Weiszmann R, Kwan E, Hartenstein V, Celniker SE, Rubin GM (2007) Global analysis of patterns of gene expression during Drosophila embryogenesis. Genome Biol 8:R145

    Article  PubMed  Google Scholar 

  • Vallee M, Dufort I, Desrosiers S, Labbe A, Gravel C, Gilbert I, Robert C, Sirard MA (2009) Revealing the bovine embryo transcript profiles during early in vivo embryonic development. Reproduction 138:95–105

    Article  PubMed  CAS  Google Scholar 

  • Verhoeven K, Simonsen K, Mcintyre L (2005) Implementing false discovery rate control: increasing your power. Oikos 108:643–647

    Article  Google Scholar 

  • Vernier J (1969) Table chonologique du developpement embryonaire de la truite are-en-ciel, Salmo gairdneri Rich. 1836. Ann Embryol Morphogen 2:495–520

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Voorips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTL. J Hered 93:77–78

    Article  Google Scholar 

  • Wagner RA, Tabibiazar R, Liao A, Quertermous T (2005) Genome-wide expression dynamics during mouse embryonic development reveal similarities to Drosophila development. Dev Biol 288:595–611

    Article  PubMed  CAS  Google Scholar 

  • Wang YL, Barbacioru C, Hyland F, Xiao WM, Hunkapiller KL, Blake J, Chan F, Gonzalez C, Zhang L, Samaha RR (2006) Large scale real-time PCR validation on gene expression measurements from two commercial long-oligonucleotide microarrays. BMC Genomics 7:59

    Article  PubMed  Google Scholar 

  • Wayne ML, Mcintyre LM (2002) Combining mapping and arraying: an approach to candidate gene identification. P Natl Aca Sci 99:14903–14906

    Article  CAS  Google Scholar 

  • Whitehead A, Crawford DL (2006a) Neutral and adaptive variation in gene expression. P Natl Aca Sci USA 103:5425–5430

    Article  CAS  Google Scholar 

  • Whitehead A, Crawford DL (2006b) Variation within and among species in gene expression: raw material for evolution. Mol Ecol 15:1197–1211

    Article  PubMed  CAS  Google Scholar 

  • Yang J, Aittomaki S, Pesu M, Carter K, Saarinen J, Kalkkinen N, Kieff E, Silvennoinen O (2002) Identification of p100 as a coactivator for STAT6 that bridges STAT6 with RNA polymerase II. Embo J 21:4950–4958

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Tricia Lundrigan, University of Victoria, for her helpful suggestion on microarray hybridization. We acknowledge consortium for Genomic Research on All Salmonids Project (cGRASP) for the microarray resource generated for the salmonid community. The authors also thank Dorothea Thompson, Purdue University for providing real-time PCR equipment. Finally, we thank anonymous reviewers for their comments. This research was funded by USDA NRI (2006-04796) to KMN.

Author information

Author notes

  1. Peng Xu

    Present address: Applied Aquatic Genomics Center, Chinese Academy of Fishery Sciences, Beijing, 100039, China

Authors and Affiliations

  1. Department of Biological Sciences, Purdue University, West Lafayette, IN, 47907, USA

    Peng Xu, Julie Scardina & Krista M. Nichols

  2. Department of Molecular Genetics and Microbiology, University of Florida, Gainesville, FL, 32601, USA

    Lauren M. McIntyre

  3. School of Biological Sciences and Center for Reproductive Biology, Washington State University, Pullman, WA, 99164, USA

    Paul A. Wheeler & Gary H. Thorgaard

  4. Department of Forestry and National Resources, Purdue University, West Lafayette, IN, 47907, USA

    Krista M. Nichols

Authors
  1. Peng Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lauren M. McIntyre
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Julie Scardina
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Paul A. Wheeler
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gary H. Thorgaard
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Krista M. Nichols
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Krista M. Nichols.

Electronics Supplementary Materials

Below is the link to the electronic supplementary material.

Supplemental Table 1

Primer sequences used for marker-assisted selection and qRT-PCR (DOC 54 kb)

Supplemental Table 2

Primer sequences and details for genes successfully amplified for linkage mapping (DOC 56 kb)

Supplemental Figure 1

Comparison of gene expression results from qRT-PCR analysis and microarray analysis. On the y-axis, the positive values indicate the genes have higher expression in CW embryos, and the negative values indicate the genes have higher expression in OSU embryos. Ten genes examined in the qRT-PCR analysis are presented as subunit of the THO complex (THO differentially expressed at 28 dpf), transforming growth factor-beta-induced protein ig-h3 precursor (TGFBI differentially expressed at 19 dpf), high choriolytic enzyme 1 precursor (HCE1 differentially expressed at 28 dpf ), myosin light chain 1, skeletal muscle isoform (MYL1differentially expressed at 19 dpf), myosin regulatory light chain 2 (MYL2 differentially expressed at 19 dpf), myosin light chain 3, skeletal muscle isoform (MYL3 differentially expressed at 19 dpf), thiosulfate sulfurtransferase KAT (KAT, differentially expressed at 15 dpf), ceruloplasmin precursor (CP differentially expressed at 19 dpf), parvalbumin beta 1 (pvalb1 differentially expressed at 15 dpf and 19 dpf), parvalbumin beta 2 (pvalb2 differentially expressed at 19 dpf). The asterisk is used to indicate the statistical significance in the qRT-PCR at the p < 0.05 level (DOC 44 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Xu, P., McIntyre, L.M., Scardina, J. et al. Transcriptome Profiling of Embryonic Development Rate in Rainbow Trout Advanced Backcross Introgression Lines. Mar Biotechnol 13, 215–231 (2011). https://doi.org/10.1007/s10126-010-9283-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-010-9283-1

Keywords

Search

Navigation