Fish Physiology and Biochemistry

, Volume 43, Issue 2, pp 579–589 | Cite as

Modifications in the proteome of rainbow trout (Oncorhynchus mykiss) embryo and fry as an effect of triploidy induction

  • Samad Bahrami Babaheydari
  • Saeed Keyvanshokooh
  • Salar Dorafshan
  • Seyed Ali Johari
Article

Abstract

Two-dimensional gel electrophoresis (2-DE), matrix-assisted laser desorption/ionization tandem time-of-flight (MALDI-TOF/TOF) mass spectrometry, and database searching were used to analyze the effects of triploidization heat shock treatment on protein expression in rainbow trout eyed embryo and fry. After fertilization, the eggs were incubated at 10 °C for 10 min. Half of the eggs were then subjected to heat shock for 10 min submerged in a 28 °C water bath to induce triploidy. The remainder was incubated normally and used as diploid controls. Specimens of eyed embryos and fry were taken on 18 and 76 days post-fertilization, respectively. In the eyed embryo extracts, seven protein spots were significantly changed in abundance between the control and heat-shocked groups and one of these was decreased while the others were increased in the heat shock-treated group. Of the spots that were shown to change in abundance in the eyed embryos with heat shock treatment, two were identified as vitellogenin, while the others were creatine kinase and angiotensin I. In the 2-DE from the fry muscle extraction, 23 spots were significantly changed in abundance between the diploid and triploid groups. Nineteen of these showed a decreased abundance in diploids, while the remaining four spots had an increased abundance. Triploidization caused differential expression of muscle metabolic proteins including triosephosphate isomerase, glyceraldehyde-3-phosphate dehydrogenase, and beta-enolase. Myosin heavy chain as a structural protein was also found to change in abundance in triploids. The altered expression of both structural and metabolic proteins in triploids was consistent with their increased cell size and lower growth performance.

Keywords

Rainbow trout Proteomics Triploid Embryo Fry Heat shock treatment 

Notes

Acknowledgements

This research was supported by Khorramshahr University of Marine Science and Technology.

Compliance with ethical standards

This study has been performed in accordance with the ethical standards of the American Fisheries Society, the American Society of Ichthyologists and Herpetologists, and the American Institute of Fishery Research Biologists (Nickum et al. 2004).

References

  1. Addis MF, Cappuccinelli R, Tedde V, Pagnozzi D, Porcu MC, Bonaglini E, Roggio T, Uzzau S (2010) Proteomic analysis of muscle tissue from gilthead sea bream (Sparus aurata, L.) farmed in offshore floating cages. Aquaculture 309:245–252CrossRefGoogle Scholar
  2. Atkins ME, Benfey TJ (2008) Effect of acclimation temperature on routine metabolic rate in triploid salmonids. Comp Biochem Physiol A Mol Integr Physiol 149:157–161CrossRefPubMedGoogle Scholar
  3. Babaheydari SB, Keyvanshokooh S, Dorafshan S, Johari SA (2016) Proteome changes in rainbow trout (Oncorhynchus mykiss) fertilized eggs as an effect of triploidization heat-shock treatment. Anim Reprod Sci 166:116–121CrossRefGoogle Scholar
  4. Benfey TJ (1999) The physiology and behavior of triploid fishes. Rev Fish Sci 7:39–67CrossRefGoogle Scholar
  5. Benfey TJ, Sutterlin AM, Thompson RJ (1984) Use of erythrocyte measurements to identify triploid salmonids. Can J Fish Aquat Sci 41:980–984CrossRefGoogle Scholar
  6. Bonnet S, Haffray P, Blanc JM, Vallée F, Vauchez C, Fauré A, Fauconneau B (1999) Genetic variation in growth parameters until commercial size in diploid and triploid freshwater rainbow trout (Oncorhynchus mykiss) and seawater brown trout (Salmo trutta). Aquaculture 173:359–375CrossRefGoogle Scholar
  7. Bosworth CA, Chou CW, Cole RB, Rees BB (2005) Protein expression patterns in zebrafish skeletal muscle: initial characterization and the effects of hypoxic exposure. Proteomics 5:1362–1371CrossRefPubMedGoogle Scholar
  8. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefPubMedGoogle Scholar
  9. Candiano G, Bruschi M, Musante L, Santucci L, Ghiggeri GM, Carnemolla B, Orecchia P, Zardi L, Righetti PG (2004) Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 25:1327–1333CrossRefPubMedGoogle Scholar
  10. Ching B, Jamieson S, Heath JW, Heath DD, Hubberstey A (2010) Transcriptional differences between triploid and diploid Chinook salmon (Oncorhynchus tshawytscha) during live Vibrio anguillarum challenge. Heredity 104:224–234CrossRefPubMedGoogle Scholar
  11. Cotter D, O’Donovan V, Drumm A, Roche N, Ling EN, Wilkins NP (2002) Comparison of freshwater and marine performances of all-female diploid and triploid Atlantic salmon (Salmo salar L.). Aquac Res 33:43–53CrossRefGoogle Scholar
  12. Derayat A, Magnússon Á, Steinarsson A, Björnsson B (2013) Growth and gonadal development in diploid and triploid Atlantic cod (Gadus morhua). Fish Physiol Biochem 39:1195–1203CrossRefPubMedGoogle Scholar
  13. Devlin RH, Biagi CA, Yesaki TY (2004) Growth, viability and genetic characteristics of GH transgenic coho salmon strains. Aquaculture 236:607–632CrossRefGoogle Scholar
  14. Doherty MK, McLean L, Hayter JR, Pratt JM, Robertson DH, El-Shafei A, Gaskell SJ, Beynon RJ (2004) The proteome of chicken skeletal muscle: changes in soluble protein expression during growth in a layer strain. Proteomics 4:2082–2093CrossRefPubMedGoogle Scholar
  15. Friars GW, McMillan I, Quinton VM, O’Flynn FM, McGeachy SA, Benfey TJ (2001) Family differences in relative growth of diploid and triploid Atlantic salmon (Salmo salar L.). Aquaculture 192:23–29CrossRefGoogle Scholar
  16. Fougerousse F, Edom-Vovard F, Merkulova T, Ott MO, Durand M, Butler-Browne G, Keller A (2001) The muscle-specific enolase is an early marker of human myogenesis. Journal of Muscle Research & Cell Motility 22:535–544CrossRefGoogle Scholar
  17. Goldspink G, Wilkes D, Ennion S (2001) 3. Myosin expression during ontogeny, post-hatching growth, and adaptation. Fish Physiology 18:43–72CrossRefGoogle Scholar
  18. Goo IB, Im JH, Gil HW, Lim SG, Park IS (2015) Comparison of cell and nuclear size difference between diploid and induced Triploid in marine medaka, Oryzias dancena. Development & Reproduction 19:127–134CrossRefGoogle Scholar
  19. Greenlee AR, Dodson MV, Yablonka-Reuveni Z, Kersten CA, Cloud JG (1995) In vitro differentiation of myoblasts from skeletal muscle of rainbow trout. J Fish Biol 46:731–747Google Scholar
  20. Gündel U, Benndorf D, von Bergen M, Altenburger R, Küster E (2007) Vitellogenin cleavage products as indicators for toxic stress in zebra fish embryos: a proteomic approach. Proteomics 7:4541–4554CrossRefPubMedGoogle Scholar
  21. Hamelin M, Sayd T, Chambon C, Bouix J, Bibé B, Milenkovic D, Levéziel H, Georges M, Clop A, Marinova P, Laville E (2006) Proteomic analysis of ovine muscle hypertrophy. J Anim Sci 84:3266–3276CrossRefPubMedGoogle Scholar
  22. Hiramatsu N, Todo T, Sullivan CV, Schilling J, Reading BJ, Matsubara T, Ryu YW, Mizuta H, Luo W, Nishimiya O, Wu M (2015) Ovarian yolk formation in fishes: molecular mechanisms underlying formation of lipid droplets and vitellogenin-derived yolk proteins. Gen Comp Endocrinol 221:9–15CrossRefPubMedGoogle Scholar
  23. Ihssen PE, McKay LR, McMillan I, Phillips RB (1990) Ploidy manipulation and gynogenesis in fishes: cytogenetic and fisheries applications. Trans Am Fish Soc 119:698–717CrossRefGoogle Scholar
  24. Johnson RM, Shrimpton JM, Cho GK, Heath DD (2007) Dosage effects on heritability and maternal effects in diploid and triploid Chinook salmon (Oncorhynchus tshawytscha). Heredity 98:303–310CrossRefPubMedGoogle Scholar
  25. Johnson RM, Shrimpton JM, Heath JW, Heath DD (2004) Family, induction methodology and interaction effects on the performance of diploid and triploid Chinook salmon (Oncorhynchus tshawytscha). Aquaculture 234:123–142CrossRefGoogle Scholar
  26. Kanaya S, Ujiie Y, Hasegawa K, Sato T, Imada H, Kinouchi M, Kudo Y, Ogata T, Ohya H, Kamada H, Itamoto K (2000) Proteome analysis of Oncorhynchus species during embryogenesis. Electrophoresis 21:1907–1913CrossRefPubMedGoogle Scholar
  27. Keyvanshokooh S, Tahmasebi-Kohyani A (2012) Proteome modifications of fingerling rainbow trout (Oncorhynchus mykiss) muscle as an effect of dietary nucleotides. Aquaculture 324:79–84CrossRefGoogle Scholar
  28. Larsen PF, Nielsen EE, Williams TD, Loeschcke V (2008) Intraspecific variation in expression of candidate genes for osmoregulation, heme biosynthesis and stress resistance suggests local adaptation in European flounder (Platichthys flesus). Heredity 101:247–259CrossRefPubMedGoogle Scholar
  29. Mendelsohn BA, Malone JP, Townsend RR, Gitlin JD (2009) Proteomic analysis of anoxia tolerance in the developing zebrafish embryo. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics 4:21–31Google Scholar
  30. Muirhead H, Watson H (1992) Glycolytic enzymes: from hexose to pyruvate. Curr Opin Struct Biol 2:870–876CrossRefGoogle Scholar
  31. Nickum JG, Bart Jr HL, Bowser PR, Greer IE, Hubbs C, Jenkins JA, MacMillan JR, Rachlin FW, Rose RD, Sorensen PW and Tomasso JR (2004) Guidelines for the use of fishes in research. American Fisheries Society, American Society of Ichthyologists and Herpetologists, and the American Institute of Fishery Research BiologistsGoogle Scholar
  32. Nishimura H (2004) Phylogeny and ontogeny of the renin-angiotensin system. In Angiotensin Vol. I (pp. 31–70). Springer Berlin HeidelbergGoogle Scholar
  33. Opstad I, Fjelldal PG, Karlsen Ø, Thorsen A, Hansen TJ, Taranger GL (2013) The effect of triploidization of Atlantic cod (Gadus morhua L.) on survival, growth and deformities during early life stages. Aquaculture 388:54–59CrossRefGoogle Scholar
  34. Pandian TJ, Koteeswaran R (1998) Ploidy induction and sex control in fish. Hydrobiologia 384:167–243CrossRefGoogle Scholar
  35. Peng XX (2013) Proteomics and its applications to aquaculture in China: infection, immunity, and interaction of aquaculture hosts with pathogens. Developmental & Comparative Immunology 39:63–71CrossRefGoogle Scholar
  36. Peruzzi S, Varsamos S, Chatain B, Fauvel C, Menu B, Falguière JC, Sévère A, Flik G (2005) Haematological and physiological characteristics of diploid and triploid sea bass, Dicentrarchus labrax L. Aquaculture 244:359–367CrossRefGoogle Scholar
  37. Piferrer F, Beaumont A, Falguière JC, Flajšhans M, Haffray P, Colombo L (2009) Polyploid fish and shellfish: production, biology and applications to aquaculture for performance improvement and genetic containment. Aquaculture 293:125–156CrossRefGoogle Scholar
  38. Rodrigues PM, Silva TS, Dias J, Jessen F (2012) Proteomics in aquaculture: applications and trends. J Proteome 75:4325–4345CrossRefGoogle Scholar
  39. Salem M, Kenney PB, Rexroad CE, Yao J (2010) Proteomic signature of muscle atrophy in rainbow trout. J Proteome 73:778–789CrossRefGoogle Scholar
  40. Shrimpton JM, Heath JW, Devlin RH, Heath DD (2012) Effect of triploidy on growth and ionoregulatory performance in ocean-type Chinook salmon: a quantitative genetics approach. Aquaculture 362:248–254CrossRefGoogle Scholar
  41. Shrimpton JM, Sentlinger AM, Heath JW, Devlin RH, Heath DD (2007) Biochemical and molecular differences in diploid and triploid ocean-type chinook salmon (Oncorhynchus tshawytscha) smolts. Fish Physiol Biochem 33:259–268CrossRefGoogle Scholar
  42. Tay TL, Lin Q, Seow TK, Tan KH, Hew CL, Gong Z (2006) Proteomic analysis of protein profiles during early development of the zebrafish, Danio rerio. Proteomics 6:3176–3188CrossRefPubMedGoogle Scholar
  43. Tiwary BK, Kirubagaran R, Ray AK (2004) The biology of triploid fish. Rev Fish Biol Fish 14:391–402CrossRefGoogle Scholar
  44. Tombes RM, Shapiro BM (1989) Energy transport and cell polarity: relationship of phosphagen kinase activity to sperm function. J Exp Zool 251:82–90CrossRefPubMedGoogle Scholar
  45. Veiseth-Kent E, Grove H, Færgestad EM, Fjæra SO (2010) Changes in muscle and blood plasma proteomes of Atlantic salmon (Salmo salar) induced by crowding. Aquaculture 309:272–279CrossRefGoogle Scholar
  46. Wallimann T and Hemmer W (1994) Creatine kinase in non-muscle tissues and cells. In Cellular bioenergetics: role of coupled creatine kinases (pp. 193–220). Springer USGoogle Scholar
  47. Wallimann T, Moser H, Zurbriggen B, Wegmann G, Eppenberger HM (1986) Creatine kinase isoenzymes in spermatozoa. Journal of Muscle Research & Cell Motility 7:25–34CrossRefGoogle Scholar
  48. Wallimann T, Wyss M, Brdiczka D, Nicolay K, Eppenberger HM (1992) Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the ‘phosphocreatine circuit’ for cellular energy homeostasis. Biochem J 281(Pt 1):21CrossRefPubMedPubMedCentralGoogle Scholar
  49. Withler RE, Clarke WC, Blackburn J, Baker I (1998) Effect of triploidy on growth and survival of pre-smolt and post-smolt coho salmon (Oncorhynchus kisutch). Aquaculture 168:413–422CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Samad Bahrami Babaheydari
    • 1
  • Saeed Keyvanshokooh
    • 1
  • Salar Dorafshan
    • 2
  • Seyed Ali Johari
    • 3
  1. 1.Department of Fisheries, Faculty of Marine Natural ResourcesKhorramshahr University of Marine Science and TechnologyKhorramshahrIran
  2. 2.Department of Natural ResourcesIsfahan University of TechnologyIsfahanIran
  3. 3.Department of Fisheries, Faculty of Natural ResourcesUniversity of KurdistanSanandajIran

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