Skip to main content
SpringerLink
Log in

Differential Gene Expression in Liver, Gill, and Olfactory Rosettes of Coho Salmon (Oncorhynchus kisutch) After Acclimation to Salinity

Marine Biotechnology Aims and scope Submit manuscript

Cite this article

Abstract

Most Pacific salmonids undergo smoltification and transition from freshwater to saltwater, making various adjustments in metabolism, catabolism, osmotic, and ion regulation. The molecular mechanisms underlying this transition are largely unknown. In the present study, we acclimated coho salmon (Oncorhynchus kisutch) to four different salinities and assessed gene expression through microarray analysis of gills, liver, and olfactory rosettes. Gills are involved in osmotic regulation, liver plays a role in energetics, and olfactory rosettes are involved in behavior. Between all salinity treatments, liver had the highest number of differentially expressed genes at 1616, gills had 1074, and olfactory rosettes had 924, using a 1.5-fold cutoff and a false discovery rate of 0.5. Higher responsiveness of liver to metabolic changes after salinity acclimation to provide energy for other osmoregulatory tissues such as the gills may explain the differences in number of differentially expressed genes. Differentially expressed genes were tissue- and salinity-dependent. There were no known genes differentially expressed that were common to all salinity treatments and all tissues. Gene ontology term analysis revealed biological processes, molecular functions, and cellular components that were significantly affected by salinity, a majority of which were tissue-dependent. For liver, oxygen binding and transport terms were highlighted. For gills, muscle, and cytoskeleton-related terms predominated and for olfactory rosettes, immune response-related genes were accentuated. Interaction networks were examined in combination with GO terms and determined similarities between tissues for potential osmosensors, signal transduction cascades, and transcription factors.

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

  • Assem H, Hanke W (1981) Cortisol and osmotic adjustment of the euryhaline teleost, Sarotherodon-mossambicus. Gen Comp Endocrinol 43:370–380

    Article  CAS  PubMed  Google Scholar 

  • Baird FE, Bett KJ, MacLean C, Tee AR, Hundal HS, Taylor PM (2009) Tertiary active transport of amino acids reconstituted by coexpression of system A and L transporters in Xenopus oocytes. Am J Physiol Endocrinol Metab 297:E822–E829

    Article  CAS  PubMed  Google Scholar 

  • Baker ME, Vidal-Dorsch DE, Ribecco C, Sprague LJ, Angert M, Lekime N, Ludka C, Martella A, Ricciardelli E, Bay SM, Gully JR, Kelley KM, Schlenk D, Carnevali O, Sasik R, Hardiman G (2013) Molecular analysis of endocrine disruption in hornyhead turbot at wasterwater outfalls in southern California using a second generation multi-species mircoarray. PLoS One 8(9):e75553

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Birrer SC, Reusch TBH, Roth O (2012) Salinity change impairs pipefish immune defence. Fish Shellfish Immunol 33:1238–1248

    Article  CAS  PubMed  Google Scholar 

  • Borski RJ, Helms LMH, Richman NH, Grau EG (1991) Cortisol rapidly reduces prolactin-release and cAMP and 45Ca(2+) accumulation in the cichlid fish pituitary in vitro. Proc Natl Acad Sci U S A 88:2758–2762

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bugrim A, Nikolskaya T, Nikolsky Y (2004) Early prediction of drug metabolism and toxicity: systems biology approach and modeling. Drug Discov Today 9:127–135

    Article  CAS  PubMed  Google Scholar 

  • Castilho PC, Buckley BA, Somero G, Block BA (2009) Heterologous hybridization to a complementary DNA microarray reveals the effect of thermal acclimation in the endothermic bluefin tuna (Thunnus orientalis). Mol Ecol 18:2092–2102

    Article  CAS  PubMed  Google Scholar 

  • Chakravarti S, Magnuson T, Lass JH, Jepsen KJ, LaMantia C, Carroll H (1998) Lumican regulates collagen fibril assembly: skin fragility and corneal opacity in the absence of lumican. J Cell Biol 141:1277–1286

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Conway G (1995) A novel gene expressed during zebrafish gastrulation identified by differential RNA display. Mech Dev 52:383–391

    Article  CAS  PubMed  Google Scholar 

  • D’cotta HC, Gallais C, Saulier B, Prunet P (1996) Comparison between parr and smolt Atlantic salmon (Salmo salar) alpha subunit gene expression of Na+/K+ ATPase in gill tissue. Fish Physiol Biochem 15:29–39

    Article  PubMed  Google Scholar 

  • El-Alfy A, Larsen B, Schlenk D (2002) Effect of cortisol and urea on flavin monooxygenase activity and expression in rainbow trout, Oncorhynchus mykiss. Mar Environ Res 54:275–278

    Article  CAS  PubMed  Google Scholar 

  • Evans TG, Somero GN (2008) A microarray-based transcriptomic time-course of hyper- and hypo-osmotic stress signaling events in the euryhaline fish Gillichthys mirabilis: osmosensors to effectors. J Exp Biol 211:3636–3649

    Article  CAS  PubMed  Google Scholar 

  • Evans TG, Hammill E, Kaukinen K et al (2011) Transcriptomics of environmental acclimatization and survival in wild adult Pacific sockeye salmon (Oncorhynchus nerka) during spawning migration. Mol Ecol 20:4472–4489

    Article  CAS  PubMed  Google Scholar 

  • Farghaly AM, Ezzat AA, Shabana MB (1973) Effect of temperature and salinity changes on blood characteristics of tilapia-zilli g in Egyptian littoral lakes. Comp Biochem Physiol 46:183–193

    Article  CAS  Google Scholar 

  • Fiol DF, Chan SY, Kültz D (2006) Identification and pathway analysis of immediate hyperosmotic stress responsive molecular mechanisms in tilapia (Oreochromis mossambicus) gill. Comp Biochem Physiol D Genomics Proteomics 1:344–356

    Article  PubMed  Google Scholar 

  • Fiol DF, Kültz D (2007) Osmotic stress sensing and signaling in fishes. FEBS Journal 274:5790–5798

  • Franchi-Gazzola R, Visigalli R, Bussolati O, Dall’Asta V, Gazzola GC (1999) Adaptive increase of amino acid transport system A requires ERK1/2 activation. J Biol Chem 274:28922–28928

    Article  CAS  PubMed  Google Scholar 

  • Franchi-Gazzola R, Dall’Asta V, Sala R et al (2006) The role of the neutral amino acid transporter SNAT2 in cell volume regulation. Acta Physiol 187:273–283

    Article  CAS  Google Scholar 

  • Gallagher EP, LaVire HM, Bammler TK, Stapleton PL, Beyer RP, Farin FM (2008) Hepatic expression profiling in smolting and adult coho salmon (Onchorhynchus kisutch). Environ Res 106:365–378

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ghai R, Waters P, Roumenina LT et al (2007) C1q and its growing family. Immunobiology 212:253–266

    Article  CAS  PubMed  Google Scholar 

  • Giles MA, Vanstone WE (1976) Ontogenetic variation in multiple hemoglobins of coho salmon (Oncorhynchus-kisutch) AND effect of environmental-factors on their expression. J Fish Res Board Can 33:1144–1149

    Article  CAS  Google Scholar 

  • Glover V, Miles R, Matta S, Modi N, Stevenson J (2005) Glucocorticoid exposure in preterm babies predicts saliva cortisol response to immunization at 4 months. Pediatr Res 58:1233–1237

    Article  CAS  PubMed  Google Scholar 

  • Grillasca JP, Gastaldi M, Khiri H et al (1997) Cloning and initial characterization of human and mouse spot 14 genes. FEBS Lett 401:38–42

    Article  CAS  PubMed  Google Scholar 

  • Hardiman G, Byrnes L, Gannon F (1994) An analysis of hight expressed salmon liver genes during smoltification in the Atlantic salmon (Salmo salar). Mol Mar Biol Biotechnol 3:51–56

    Google Scholar 

  • Hoar WS (1988) The physiology of smolting salmonids. In: Hoar WS, Randall DJ (eds) The physiology of developing fish–Part B. Viviparity and posthatching juveniles. Fish Physiology, vol11. Academic Press, New York, pp 275–343

  • Johnson GL, Lapadat R (2002) Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 298:1911–1912

    Article  CAS  PubMed  Google Scholar 

  • Jones HN, Ashworth CJ, Page KR, McArdle HJ (2006) Cortisol stimulates system A amino acid transport and SNAT2 expression in a human placental cell line (BeWo). Am J Physiol Endocrinol Metab 291:E596–E603

    Article  CAS  PubMed  Google Scholar 

  • Kaplan JH (2002) Biochemistry of Na, K-ATPase. Annu Rev Biochem 71:511–535

    Article  CAS  PubMed  Google Scholar 

  • Katsuhara M (1997) Apoptosis-like cell death in barley roots under salt stress. Plant Cell Physiol 38:1091–1093

    Article  CAS  Google Scholar 

  • Kültz D, Avila K (2001) Mitogen-activated protein kinases are in vivo transducers of osmosensory signals in fish gill cells. Comp Biochem Physiol B Biochem Mol Biol 129:821–829

    Article  PubMed  Google Scholar 

  • Kültz D, Burg MB (1998) Intracellular signaling in response to osmotic stress. Cell Vol Regul 123:94–109

    Article  Google Scholar 

  • Lambris JD (1990) The third component of complement. Chemistry and biology. Curr Topics Microbiol Immunol 153:1–251

    Google Scholar 

  • Lee SJ, Wang-Buhler JL, Cok I et al (1998) Cloning, sequencing, and tissue expression of CYP3A27, a new member of the CYP3A subfamily from embryonic and adult rainbow trout livers. Arch Biochem Biophys 360:53–61

    Article  CAS  PubMed  Google Scholar 

  • Lekstrom-Himes J, Xanthopoulos KG (1998) Biological role of the CCAAT enhancer-binding protein family of transcription factors. J Biol Chem 273:28545–28548

    Article  CAS  PubMed  Google Scholar 

  • Lionetto MG, Pedersen SF, Hoffmann EK, Giordano ME, Schettino T (2002) Roles of the cytoskeleton and of protein phosphorylation events in the osmotic stress response in EEL intestinal epithelium. Cell Physiol Biochem 12:163

    Article  CAS  PubMed  Google Scholar 

  • Mancera JM, McCormick SD (1998) Osmoregulatory actions of the GH/IGF axis in non-salmonid teleosts. Comp Biochem Physiol B Biochem Mol Biol 121:43–48

    Article  Google Scholar 

  • Marshall WS, Ossum CG, Hoffmann EK (2005) Hypotonic shock mediation by p38 MAPK, JNK, PKC, FAK, OSR1 and SPAK in osmosensing chloride secreting cells of killifish opercular epithelium. J Exp Biol 208:1063–1077

    Article  CAS  PubMed  Google Scholar 

  • McCormick SD (2001) Endocrine control of osmoregulation in teleost fish. Am Zool 41:781–794

    CAS  Google Scholar 

  • McCormick SD, Saunders RL, Macintyre AD (1989) Mitochondrial enzyme and NA+, K + −ATpase activity, and ion regulation during parr-smolt transformation of Atlantic salmon (salmo-salar). Fish Physiol Biochem 6:231–241

    Article  CAS  PubMed  Google Scholar 

  • McLean E, Devlin RH, Byatt JC, Clarke WC, Donaldson EM (1997) Impact of a controlled release formulation of recombinant bovine growth hormone upon growth and seawater adaptation in coho (Oncorhynchus kisutch) and chinook (Oncorhynchus tshawytscha) salmon. Aquaculture 156:113–128

    Article  CAS  Google Scholar 

  • Moser B, Loetscher P (2001) Lymphocyte traffic control by chemokines. Nat Immunol 2:123–128

    Article  CAS  PubMed  Google Scholar 

  • Ollivier H, Pichavant-Rafini K, Puill-Stephan E, Calves P, Nonnotte L, Nonnotte G (2006) Effects of hyposmotic stress on exocytosis in isolated turbot, Scophthalmus maximus, hepatocytes. J Comp Physiol B 176:643–652

    Article  CAS  PubMed  Google Scholar 

  • Quinn TP (2005) The behavior and ecology of Pacific salmon and trout. American Fisheries Society, Bethesda, pp 1–320

  • Riar N, Crago J, Jiang WY, Maryoung LA, Gan J, Schlenk D (2013) Effects of salinity acclimation on the endocrine disruption and acute toxicity of bifenthrin in freshwater and euryhaline strains of Oncorhynchus mykiss. Environ Toxicol Chem 32:2779–2785

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Richards JG, Semple JW, Bystriansky JS, Schulte PM (2003) Na+/K + −ATPase (alpha-isoform switching in gills of rainbow trout (Oncorhynchus mykiss) during salinity transfer. J Exp Biol 206:4475–4486

    Article  CAS  PubMed  Google Scholar 

  • Rozen S, Skaletsky H (1999) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386

    Google Scholar 

  • Sangiao-Alvarellos S, Laiz-Carrion R, Guzman JM et al (2003) Acclimation of S-aurata to various salinities alters energy metabolism of osmoregulatory and nonosmoregulatory organs. Am J Physiol Regul Integr Comp Physiol 285:R897–R907

    Article  CAS  PubMed  Google Scholar 

  • Sasik R, Woelk CH, Corbeil J (2004) Microarray truths and consequences. J Mol Endocrinol 33:1–9

    Article  CAS  PubMed  Google Scholar 

  • Schwartz LM, Osborne BA (1993) Programmed cell-death, apoptosis and killer genes. Immunol Today 14:582–590

    Article  CAS  PubMed  Google Scholar 

  • Schweiger S, Foerster J, Lehman T et al (1999) The Opitz syndrome gene product, MID1, associates with microtubules. Proc Natl Acad Sci U S A 96:2794–2799

    Article  PubMed Central  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Soengas JL, Aldegunde M, Andres MD (1995) Gradual transfer to sea-water of rainbow-trout - effects on liver carbohydrate-metabolism. J Fish Biol 47:466–478

    Article  CAS  Google Scholar 

  • Subramanian A, Tamayo P, Mootha VK et al (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 102:15545–15550

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sullivan CV, Dickhoff WW, Mahnken CVW, Hershberger WK (1985) Changes in the hemoglobin system of the coho salmon oncorhynchus-kisutch during smoltification and triiodothyronine and propylthiouracil treatment. Comp Biochem Physiol A Physiol 81:807–813

    Article  CAS  Google Scholar 

  • Treisman R (1996) Regulation of transcription by MAP kinase cascades. Curr Opin Cell Biol 8:205–215

    Article  CAS  PubMed  Google Scholar 

  • Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98:5116–5121

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vanstone WE, Tsuyuki H, Roberts E (1964) Changes in multiple hemoglobin patterns of some pacific salmon genus Oncorhynchus during parr-smolt transformation. Can J Physiol Pharmacol 42:697

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Yada T, Nakanishi T (2002) Interaction between endocrine and immune systems in fish. Int Rev Cytol 220:35–92

    Article  CAS  PubMed  Google Scholar 

  • Yada T, Azuma T, Hyodo S, Hirano T, Grau EG, Schreck CB (2007) Differential expression of corticosteroid receptor genes in rainbow trout (Oncorhynchus mykiss) immune system in response to acute stress. Can J Fish Aquat Sci 64:1382–1389

    Article  CAS  Google Scholar 

  • Yada T, Hyodo S, Schreck CB (2008) Effects of seawater acclimation on mRNA levels of corticosteroid receptor genes in osmoregulatory and immune systems in trout. Gen Comp Endocrinol 156:622–627

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the University of Washington Superfund Research Program (NIEHS P42ES04696) and the University of California, Riverside Agricultural Experiment Station (RSAP). L.A.M. was supported by a National Research Service Award Institutional Training Grant (T32 ES018827). GH gratefully acknowledges support from National Institutes of Health grants DK063491, CA023100, and DK080506 and UC Senate grant RK126H-HARDIMAN. We would also like to thank Dr. Roman Sasik from The University of California, San Diego, for his help with this project.

Author information

Authors and Affiliations

  1. Department of Environmental Sciences, University of California, 2258 Geology Building, 900 University Ave, Riverside, CA, 92521, USA

    Lindley A. Maryoung, Ramon Lavado & Daniel Schlenk

  2. Department of Environmental and Occupational Health Sciences, University of Washington, Seattle, WA, 98195, USA

    Theo K. Bammler, Evan P. Gallagher, Patricia L. Stapleton, Richard P. Beyer & Federico M. Farin

  3. Department of Medicine and Public Health and Center for Genomics Medicine, Medical University of South Carolina, 135 Cannon Street, Suite 303 MSC 835, Charleston, SC, 29425, USA

    Gary Hardiman

Authors
  1. Lindley A. Maryoung
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ramon Lavado
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Theo K. Bammler
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Evan P. Gallagher
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Patricia L. Stapleton
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Richard P. Beyer
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Federico M. Farin
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Gary Hardiman
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Daniel Schlenk
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lindley A. Maryoung.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 13 kb)

Supplemental Figure 1

Interaction network pathway using MetaCore™ knowledge base (Bugrim et al. 2004) for liver comparing freshwater acclimated fish to fish acclimated to high (32 ppth) salinity using a 1.75 fold cutoff. Blue signifies down regulation and red signifies upregulation. A link show an interaction, a bullet is binding of protein products, an arrow mean regulation of transcription or activation, and a hammer means inhibition or deactivation. (JPEG 1112 kb)

Supplemental Figure 2

Interaction network pathway using MetaCore™ knowledge base (Bugrim et al. 2004) for gills comparing freshwater acclimated fish to fish acclimated to high (32 ppth) salinity using a 1.50 fold cutoff. Blue signifies down regulation and red signifies upregulation. A link show an interaction, a bullet is binding of protein products, an arrow mean regulation of transcription or activation, and a hammer means inhibition or deactivation. (EPS 21881 kb)

High resolution image (GIF 166 kb)

Supplemental Figure 3

Interaction network pathway using MetaCore™ knowledge base (Bugrim et al. 2004) for olfactory rosettes comparing freshwater acclimated fish to fish acclimated to high (32 ppth) salinity using a 1.25 fold cutoff. Blue signifies down regulation and red signifies upregulation. A link show an interaction, a bullet is binding of protein products, an arrow mean regulation of transcription or activation, and a hammer means inhibition or deactivation. (GIF 714 kb)

High resolution image (EPS 5455 kb)

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maryoung, L.A., Lavado, R., Bammler, T.K. et al. Differential Gene Expression in Liver, Gill, and Olfactory Rosettes of Coho Salmon (Oncorhynchus kisutch) After Acclimation to Salinity. Mar Biotechnol 17, 703–717 (2015). https://doi.org/10.1007/s10126-015-9649-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-015-9649-5

Keywords

search

Navigation