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Transcriptomic Response to Selective Breeding for Fast Growth in Rainbow Trout (Oncorhynchus mykiss)

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Abstract

Genetic improvement for faster growth is a conventional approach to increase growth rates in aquaculture species; however, the genetic and physiological factors regulating growth performance in fish are not fully characterized. The objective of this study was to identify physiological mechanisms associated with faster growth rates by comparing the liver and muscle transcriptome of a rainbow trout line selectively bred for fast growth (growth line, GL) and a contemporary randomly mated control line (synthetic control, SC) from the same selective breeding program. A third genetic line from a commercial egg supplier (commercial A, CA) was also included to characterize differences in gene expression profiles between populations. Body weight of the GL at harvest was approximately 20% and 8% heavier (p < 0.05) than SC and CA, respectively. There were 145 and 36 differentially expressed genes (DEG) in liver and white muscle, respectively, between the GL and SC that were enriched for the growth hormone/insulin-like growth factor axis (GH/IGF) and PI3K-Akt, JAK-STAT, MAPK, and cAMP signal transduction pathways. A greater concentration of plasma IGF-I was detected in the GL compared with SC (p < 0.05). A unique gene profile was detected in CA, with 11 and 210 DEG in liver and white muscle; these genes associated with innate immunity, complement systems, and metabolic pathways. Collectively, these findings provide a more extensive characterization of the fast-growth phenotype in fish that furthers knowledge of the physiological basis for genetic variation in growth performance in selectively bred rainbow trout.

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References

  • Ali A, Al-Tobasei R, Kenney B, Leeds TD, Salem M (2018) Integrated analysis of IncRNA and mRNA expression in rainbow trout families showing variation in muscle growth and fillet quality traits. Sci Rep 8:12111

    PubMed  PubMed Central  Google Scholar 

  • Alzaid A, Kim JH, Devlin RH, Martin SaM, Macqueen DJ (2018) Growth hormone transgenesis in coho salmon disrupts muscle immune function impacting cross-talk with growth systems. J Exp Biol 221:jeb173146

    PubMed  Google Scholar 

  • Anders S, Pyl PT, Huber W (2015) HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics 31:166–169

    CAS  Google Scholar 

  • Beckman BR (2011) Perspectives on concordant and discordant relations between insulin-like growth factor 1 (IGF1) and growth in fishes. Gen Comp Endocrinol 170:233–252

    CAS  PubMed  Google Scholar 

  • Beckman BR, Fairgrieve W, Cooper KA, Mahnken CVW, Beamish RJ (2004) Evaluation of endocrine indices of growth in individual postsmolt coho salmon. Trans Am Fish Soc 133:1057–1067

    CAS  Google Scholar 

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

  • Bergan HE, Kittilson JD, Sheridan MA (2013) PKC and ERK mediate GH-stimulated lipolysis. J Mol Endocrinol 51:213–224

    CAS  PubMed  Google Scholar 

  • Bergan HE, Kittilson JD, Sheridan MA (2015) Nutritional state modulates growth hormone-stimulated lipolysis. Gen Comp Endocrinol 217-218:1–9

    CAS  PubMed  Google Scholar 

  • Bicskei B, Bron JE, Glover KA, Taggart JB (2014) A comparison of gene transcription profiles of domesticated and wild Atlantic salmon (Salmo salar L.) at early life stages, reared under controlled conditions. BMC Genomics 15:884

    PubMed  PubMed Central  Google Scholar 

  • Bikle DD, Tahimic C, Chang W, Wang Y, Philippou A, Barton ER (2015) Role of IGF-I signaling in muscle bone interactions. Bone 80:79–88

    CAS  PubMed  PubMed Central  Google Scholar 

  • Castillo J, Codina M, Martinez ML, Navarro I, Gutierrez J (2004) Metabolic and mitogenic effects of IGF-I and insulin on muscle cells of rainbow trout. Am J Physiol Regul Integr Comp Physiol 286:R935–R941

    CAS  PubMed  Google Scholar 

  • Castillo J, Ammendrup-Johnsen I, Codina M, Navarro I, Gutierrez J (2006) IGF-I and insulin receptor signal transduction in trout muscle cells. Am J Physiol Regul Integr Comp Physiol 290:R1683–R1690

    CAS  PubMed  Google Scholar 

  • Cleveland BM, Weber GM (2010) Effects of insulin-like growth factor-I, insulin, and leucine on protein turnover and ubiquitin ligase expression in rainbow trout primary myocytes. Am J Physiol Regul Integr Comp Physiol 298:R341–R350

    CAS  PubMed  Google Scholar 

  • Cleveland BM, Leeds TD, Rexroad CE, Summerfelt ST, Good CM, Davidson JW, May T, Crouse C, Wolters WR, Plemmons B, Kenney PB (2017) Genetic line by environment interaction on rainbow trout growth and processing traits. N Am J Aquac 79:140–154

    Google Scholar 

  • Crouse CC, Davidson JW, Good CM, May TC, Summerfelt ST, Kenney PB, Leeds TD, Cleveland BM (2018) Growth and fillet quality attributes of five genetic strains of rainbow trout (Oncorhynchus mykiss) reared in a partial water reuse system and harvested at different sizes. Aquac Res 49:1672–1681

    Google Scholar 

  • Danzmann RG, Kocmarek AL, Norman JD, Rexroad CE 3rd, Palti Y (2016) Transcriptome profiling in fast versus slow-growing rainbow trout across seasonal gradients. BMC Genomics 17:60

    PubMed  PubMed Central  Google Scholar 

  • Daughaday WH, Rotwein P (1989) Insulin-like growth factors I and II. Peptide, messenger ribonucleic acid and gene structures, serum, and tissue concentrations. Endocr Rev 10:68–91

    CAS  PubMed  Google Scholar 

  • Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29:15–21

    CAS  Google Scholar 

  • Fisher MC, Meyer C, Garber G, Dealy CN (2005) Role of IGFBP2, IGF-I and IGF-II in regulating long bone growth. Bone 37:741–750

    CAS  PubMed  Google Scholar 

  • Gabillard JC, Yao K, Vandeputte M, Gutierrez J, Le Bail PY (2006) Differential expression of two GH receptor mRNAs following temperature change in rainbow trout (Oncorhynchus mykiss). J Endocrinol 190:29–37

  • Gjedrem T, Thodesen J (2005) Selection. In: Gjedrem T (ed) Selection and breeding programs in aquaculture, Dordrecht, Netherlands

  • Gonzalez-Pena D, Gao GT, Baranski M, Moen T, Cleveland BM, Kenney PB, Vallejo RL, Palti Y, Leeds TD (2016) Genome-wide association study for identifying loci that affect fillet yield, carcass, and body weight traits in rainbow trout (Oncorhynchus mykiss). Front Genet 7:203

  • Harmon JS, Rieniets LM, Sheridan MA (1993) Glucagon and insulin regulate lipolysis in trout liver by altering phosphorylation of triacylglycerol lipase. Am J Phys 265:R255–R260

    CAS  Google Scholar 

  • Hershberger WK, Myers JM, Iwamoto RN, Mcauley WC, Saxton AM (1990) Genetic changes in the growth of coho salmon (Oncorhynchus-Kisutch) in marine net-pens, produced by 10 years of selection. Aquaculture 85:187–197

    Google Scholar 

  • Jeoung NH, Harris CR, Harris RA (2014) Regulation of pyruvate metabolism in metabolic-related diseases. Rev Endocr Metab Disord 15:99–110

    CAS  PubMed  Google Scholar 

  • Kittilson JD, Jones E, Sheridan MA (2011) ERK, Akt, and STAT5 are differentially activated by the two growth hormone receptor subtypes of a teleost fish (Oncorhynchus Mykiss). Front Endocrinol 2:30

    Google Scholar 

  • Kolditz CI, Paboeuf G, Borthaire M, Esquerre D, Sancristobal M, Lefevre F, Medale F (2008) Changes induced by dietary energy intake and divergent selection for muscle fat content in rainbow trout (Oncorhynchus mykiss), assessed by transcriptome and proteome analysis of the liver. BMC Genomics 9:506

    PubMed  PubMed Central  Google Scholar 

  • Kolditz CI, Plagnes-Juan E, Quillet E, Lefevre F, Medale F (2010) Changes in white muscle transcriptome induced by dietary energy levels in two lines of rainbow trout (Oncorhynchus mykiss) selected for muscle fat content. Br J Nutr 103:629–642

  • Lankford SE, Weber GM (2006) Associations between plasma growth hormone, insulin-like growth factor-I, and cortisol with stress responsiveness and growth performance in a selective breeding program for rainbow trout. N Am J Aquac 68:151–159

    Google Scholar 

  • Lao-On U, Attwood PV, Jitrapakdee S (2018) Roles of pyruvate carboxylase in human diseases: from diabetes to cancers and infection. J Mol Med 96:237–247

    CAS  PubMed  Google Scholar 

  • Lawan A, Bennett AM (2017) Mitogen-activated protein kinase regulation in hepatic metabolism. Trends Endocrinol Metab 28:868–878

    CAS  PubMed  PubMed Central  Google Scholar 

  • Leeds TD, Vallejo RL, Weber GM, Gonzalez-Pena D, Silverstein JT (2016) Response to five generations of selection for growth performance traits in rainbow trout (Oncorhynchus mykiss). Aquaculture 465:341–351

  • Liang X, Martyniuk CJ, Cheng G, Zha J, Wang Z (2014) Pyruvate carboxylase as a sensitive protein biomarker for exogenous steroid chemicals. Environ Pollut 189:184–193

    CAS  PubMed  Google Scholar 

  • Lin SM, Shi CM, Mu MM, Chen YJ, Luo L (2018) Effect of high dietary starch levels on growth, hepatic glucose metabolism, oxidative status and immune response of juvenile largemouth bass, Micropterus salmoides. Fish Shellfish Immunol 78:121–126

    CAS  PubMed  Google Scholar 

  • Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-Seq data with DESeq2. BioRxiv 15:550

  • Ma Q, Liu SF, Zhuang ZM, Lin L, Sun ZZ, Liu CL, Su YQ, Tang QS (2011) Genomic structure, polymorphism and expression analysis of growth hormone-releasing hormone and pituitary adenylate cyclase activating polypeptide genes in the half-smooth tongue sole (Cynoglossus semilaevis). Genet Mol Res 10:3828–3846

    CAS  PubMed  Google Scholar 

  • Maehr T, Vecino JL, Wadsworth S, Wang T, Secombes CJ (2014) Four CISH paralogues are present in rainbow trout Oncorhynchus mykiss: differential expression and modulation during immune responses and development. Mol Immunol 62:186–198

    CAS  PubMed  Google Scholar 

  • Magnadottir B (2006) Innate immunity of fish (overview). Fish Shellfish Immunol 20:137–151

    CAS  PubMed  Google Scholar 

  • Marancik D, Gao G, Paneru B, Ma H, Hernandez AG, Salem M, Yao J, Palti Y, Wiens GD (2014) Whole-body transcriptome of selectively bred, resistant-, control-, and susceptible-line rainbow trout following experimental challenge with Flavobacterium psychrophilum. Front Genet 5:453

    PubMed  Google Scholar 

  • Martin M (2019) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnetjournal 17:10–12

    Google Scholar 

  • Mckinley SJ, Hazel JR (2000) Does membrane fluidity contribute to thermal compensation of beta-adrenergic signal transduction in isolated trout hepatocytes? J Exp Biol 203:631–640

    CAS  PubMed  Google Scholar 

  • Mommsen TP, Moon TW (1990) Metabolic response of teleost hepatocytes to glucagon-like peptide and glucagon. J Endocrinol 126:109–118

    CAS  PubMed  Google Scholar 

  • Neto RVR, Yoshida GM, Lhorente JP, Yanez JM (2019) Genome-wide association analysis for body weight identifies candidate genes related to development and metabolism in rainbow trout (Oncorhynchus mykiss). Mol Gen Genomics 294:563–571

    Google Scholar 

  • Peterson BC, Waldbieser GC, Bilodeau L (2004) IGF-I and IGF-II mRNA expression in slow and fast growing families of USDA103 channel catfish (Ictalurus punctatus). Comp Biochem Physiol A Mol Integr Physiol 139:317–323

    PubMed  Google Scholar 

  • Reindl KM, Sheridan MA (2012) Peripheral regulation of the growth hormone-insulin-like growth factor system in fish and other vertebrates. Comp Biochem Physiol A Mol Integr Physiol 163:231–245

    CAS  PubMed  Google Scholar 

  • Reindl KM, Kittilson JD, Sheridan MA (2009) Differential ligand binding and agonist-induced regulation characteristics of the two rainbow trout GH receptors, Ghr1 and Ghr2, in transfected cells. J Endocrinol 202:463–471

    CAS  PubMed  Google Scholar 

  • Reindl KM, Kittilson JD, Bergan HE, Sheridan MA (2011) Growth hormone-stimulated insulin-like growth factor-1 expression in rainbow trout (Oncorhynchus mykiss) hepatocytes is mediated by ERK, PI3K-AKT, and JAK-STAT. Am J Physiol Regul Integr Comp Physiol 301:R236–R243

    CAS  PubMed  Google Scholar 

  • Small BC, Peterson BC (2005) Establishment of a time-resolved fluoroimmunoassay for measuring plasma insulin-like growth factor I (IGF-I) in fish: effect of fasting on plasma concentrations and tissue mRNA expression of IGF-I and growth hormone (GH) in channel catfish (Ictalurus punctatus). Domest Anim Endocrinol 28:202–215

    CAS  PubMed  Google Scholar 

  • Sutherland BJ, Hanson KC, Jantzen JR, Koop BF, Smith CT (2014) Divergent immunity and energetic programs in the gills of migratory and resident Oncorhynchus mykiss. Mol Ecol 23:1952–1964

    CAS  PubMed  Google Scholar 

  • Taylor JF, Porter MJR, Bromage NR, Migaud H (2008) Relationships between environmental changes, maturity, growth rate and plasma insulin-like growth factor-I (IGF-I) in female rainbow trout. Gen Comp Endocrinol 155:257–270

    CAS  PubMed  Google Scholar 

  • Tsai HY, Hamilton A, Guy DR, Tinch AE, Bishop SC, Houston RD (2015) The genetic architecture of growth and fillet traits in farmed Atlantic salmon (Salmo salar). BMC Genet 16:51

  • Very NM, Kittilson JD, Norbeck LA, Sheridan MA (2005) Isolation, characterization, and distribution of two cDNAs encoding for growth hormone receptor in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol B Biochem Mol Biol 140:615–628

  • Walock CN, Kittilson JD, Sheridan MA (2014) Characterization of a novel growth hormone receptor-encoding cDNA in rainbow trout and regulation of its expression by nutritional state. Gene 533:286–294

    CAS  PubMed  Google Scholar 

  • Wang T, Secombes CJ (2008) Rainbow trout suppressor of cytokine signalling (SOCS)-1, 2 and 3: molecular identification, expression and modulation. Mol Immunol 45:1449–1457

    CAS  PubMed  Google Scholar 

  • Wood AW, Duan C, Bern HA (2005) Insulin-like growth factor signaling in fish. Int Rev Cytol 243:215–285

    CAS  PubMed  Google Scholar 

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Acknowledgments

The authors acknowledge the technical and animal caretaking contributions from Lisa Radler, Josh Kretzer, Kyle Jenkins, James Everson, and Jenea McGowan. Mention of trade names is solely for accuracy and does not represent endorsement or support by the USDA. The USDA is an equal opportunity employer and provider.

Funding

Funding support comes from USDA/ARS project number 8082-31000-012-00D.

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Correspondence to Beth M. Cleveland.

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All experimental procedures and protocols received approval from the NCCCWA Institutional Animal Care and Use Committee (IACUC) and adhered to IACUC guidelines (protocol #093).

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Cleveland, B.M., Gao, G. & Leeds, T.D. Transcriptomic Response to Selective Breeding for Fast Growth in Rainbow Trout (Oncorhynchus mykiss). Mar Biotechnol 22, 539–550 (2020). https://doi.org/10.1007/s10126-020-09974-3

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