Abstract
Body composition and fractional rates of protein synthesis (percentage of the protein mass synthesized per day) were determined in female Atlantic salmon returning to the River Tay, Scotland in July and in October after a 95 day period without food, during which time the animals became sexually mature. During the 95 day period of starvation/sexual maturation the ventricle and red muscle remained as a constant proportion of fresh weight whereas the liver, gill and ovary increased and the stomach and white muscle decreased. Fractional rates of protein synthesis increased markedly in the liver, stomach and ovary during the period of starvation/sexual maturation. In the gill, ventricle and white muscle fractional protein synthesis rates increased slightly or remained constant. From the estimated rates of protein loss or gain in the various tissues it is concluded that there is considerable protein turnover and repartitioning of amino acids during the period of starvation and sexual maturation. The absolute rate of protein synthesis rates in the ovary indicates that this tissue made the largest contribution to the energy and amino acid demands of the fish, whilst most of the amino acids required for maturation of the ovary were derived from white muscle, principally as the result of increased muscle protein degradation.
Similar content being viewed by others
References cited
Aksens, A., Gjerde, B. and Roald, S.O. 1986. Biological, chemical and organoleptic changes during maturation of farmed Atlantic salmon (Salmo salar). Aquaculture 53: 7–20.
Ando, S., Yamazaki, F., Hatano, M. and Zama, K. 1986. Deterioration of chum salmon (Oncorhynchus keta) muscle during spawning migration. III. Changes in protein composition and protease activity of juvenile chum salmon muscle upon treatment with sex steroids. Comp. Biochem. Physiol. 83B: 325–330.
Ashford, A.J., Pain, V.M. 1986. Effect of diabetes on the rates of synthesis and degradation of ribosomes in rat muscle and liver in vivo. J. Biol. Chem. 261: 4059–4065.
Aoyagi, Y., Tasaki, I., Okumura, J. and Muramatsu, T. 1988. Energy cost of whole body protein synthesis measured in vivo in chicks. Comp. Biochem. Physiol. 91A: 765–768.
Barbour, A.J.S. 1985. The transition of adult Atlantic salmon (Salmo salar) from saltwater to freshwater. Ph.D. thesis, University of Aberdeen.
Beardall, C.H. and Johnston, I.A. 1983. Muscle atrophy during starvation in a marine teleost. Eur. J. Cell Biol. 29: 209–217.
Crane, L.J. and Miller, D.L. 1977. Plasma protein synthesis by isolated rat hepatocytes. J. Cell Biol. 72: 11–25.
Emmersen, B.K. and Emmersen, J. 1976. Protein, RNA and DNA metabolism in relation to ovarian vitellogenic growth in the flounder (Platichthys flesus). Comp. Biochem. Physiol. 55B: 315–321.
Farrell, A.P., Saunders, R.L., Freeman, H.C. and Mommsen, T.P. 1986. Arteriosclerosis in Atlantic salmon: effects of dietary cholesterol and maturation. Arteriosclerosis 6: 453–461.
Fauconneau, B. 1985. Protein synthesis and protein deposition in fish In Nutrition and Feeding in Fish. pp. 17–46. Edited by C.B. Cowey, A.M. Mackie and J.G. Bell. Academic Press, London.
Frader, P.J. 1987. Atlantic salmon,Salmo salar L., feed in Scottish coastal waters. Aquacult. Fish. Manag. 18: 243–247.
Garlick, P.J., McNurlan, M.A. and Preedy, V.R. 1980. A rapid and convenient technique for measuring the rate of protein synthesis in tissue by injection of [3H]phenylalanine. Biochem. J. 192: 719–723.
Greene, C.W. 1926. The physiology of spawning migration. Physiol. Rev. 6: 201–241.
Houlihan, D.F. 1991. Protein turnover in ectotherms, relation to energetics. In Comparative Environmental Physiology. Vol. 7, pp. 1–43. Edited by R. Gilles. Springer Verlag, Berlin.
Houlihan, D.F., McMillan, D.N. and Laurent, P. 1986. Growth rates, protein synthesis, and protein degradation rates in rainbow trout: effects of body size. Physiol. Zool. 59: 482–493.
Houlihan, D.F., Hall, S.J., Gray, C. and Noble, B.S. 1988. Growth rates and protein turnover in cod,Gadus morhua. Can. J. Fish. Aquat. Sci. 45: 951–964.
Houlihan, D.F., Mathers, E.M. and Foster, A. 1992. Biochemical correlates of growth rate in fish. In Fish Ecophysiology. pp. 45–71. Edited by J.C. Rankin and F.B. Jensen. Chapman and Hall, London.
House, E.W., Dornauer, R.J. and van Lenten, B.J. 1979. Production of coronary arteriosclerosis with sex hormones and human chorionic gonadotrophin (HCG) in juvenile steelhead and rainbow trout,Salmo gairdneri. Atherosclerosis 34: 197–206.
Idler, D.R. and Clemens, W.A. 1959. The energy expenditures of Fraser sockeye salmon during spawning migration to Chilko and Stuart Lakes. Int. Pac. Salmon Fish. Comm. Progr. Rep. 6: 1–80.
Jalabert, B., Breton, B. and Fostier, A. 1978. Precocious induction of oocyte maturation and ovulation in rainbow trout (Salmo gairdneri): problems with using 17 hydoxy-20B-dihydroprogesterone. Ann. Biol. Anim. Biochem. Biophys. 18: 977–984.
Jalabert, B. and Finet, B. 1986. Regulation of oocyte maturation in the rainbow trout (Salmo gairdneri): role of cyclic AMP in the mechanism of action of the maturation-inducing steroid (MIS), 17 hydoxy-20B-dihydroprogesterone. Fish Physiol. Biochem. 2: 65–74.
Khoo, K.H. 1978. The histochemistry and endocrine control of vitellogenesis in goldfish ovaries. Can. J. Zool. 57: 617–626.
Laird, L.M. and Oswald, R.L. 1975. A note on the use of benzocaine (ethyl-P-aminobenzoate) as a fish anaesthetic. J. Ins. Fish. Manag. 6: 92–94.
Loughna, P.T. and Goldspink, G. 1984. The effect of starvation upon protein turnover in red and white myotomal muscle or rainbow trout (Salmo gairdneri Richardson). J. Fish Biol. 25: 223–230.
Love, R.M. 1980. The Chemical Biology of Fishes, Vol. 2. Academic Press, London.
Lowry, O.H., Rosengrough, N.J., Farr, A.L. and Randall, R.J. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193: 265–275.
McKenzie, J.E., House, E.W., McWilliam, J.G. and Johnston, D.W. 1978. Coronary degeneration in sexually mature rainbow trout and steelhead trout,Salmo gairdneri. Arteriosclerosis 29: 431–437.
McMillan, D.N. and Houlihan, D.F. 1988. The effect of refeeding on tissue protein synthesis in rainbow trout. Physiol. Zool. 61: 429–441.
McMillan, D.N. and Houlihan, D.F. 1989. Short term responses of protein synthesis to re-feeding in rainbow trout. Aquaculture 79: 37–46.
McMillan, D.N. and Houlihan, D.F. 1992. Protein synthesis in trout liver is stimulated by both feeding and fasting. Fish Physiol. Biochem. 10: 23–24.
Mejbaum, W. 1939. Uber der bestimmung kleiner pentosemengen, insbesondere in derivaten der adenylsaure. Hoppe-Seyler's Physiol. Chem. 258: 117–120.
Mommsen, T.P., French, C.J. and Hochachka, P.W. 1980. Sites and patterns of protein and amino acid utilization during the spawning migration of salmon. Can. J. Zool. 58: 1785–1799.
Mosse, P.R.A. 1978. The distribution of capillaries in the somatic musculature of two vertebrate types with particular reference to teleost fish. Cell Tiss. Res. 187: 281–303.
Muller, R. 1983. Coronary arteriosclerosis and thyroid hyperplasia in spawning salmon (Oncorhynchus kisutch) from Lake Ontario. Acta Zool. Pathol. Antver. 77: 3–12.
Pannevis, M.C. and Houlihan, D.F. 1992. The energetic cost of protein synthesis in isolated hepatocytes of rainbow trout (Oncorhynchus mykiss). J. Comp. Physiol. 162: 393–400.
Petrino, T.R. and Schuetz, A.W. 1986. Protein synthesis involvement in regulating pituitary-induced progesterone levels in ovarian follicles of Rana pipiens. J. Exp. Zool. 239: 411–421.
Reeds, P.J., Fuller, M.F. and Nicholson, B.A. 1985. Metabolic basis of energy expenditure with particular reference to protein. In Substrate and Energy Metabolism in Man. pp. 46–57. Edited J.S. Garrow and D. Halliday. CRC Press, London.
Schoenheimer, R. 1942. Dynamic State of Body Constituents. Cambridge, Harvard University Press, Boston.
So, Y.P., Idler, D.R. and Hwang, S.J. 1985. Plasma vitellogenin in landlocked Atlantic salmon (Salmo salar): isolation, homologous radioimmunoassay and immunological crossreactivity with vitellogenin from other teleosts. Comp. Biochem. Physiol. 81B: 62–71.
Tyler, C.R., Sumpter, J.P. and Bromage, N.R. 1988. Selectivity of protein sequestration by vitellogenic oocytes of the rainbow trout (Salmongairdneri). J. Exp. Zool. 248: 199–206.
Talbot, C., Preston, T. and East, B.W. 1986. Body composition of Atlantic salmon (Salmon salar L.) studied by neutron activation analysis. Comp. Biochem. Physiol. 85A: 445–450.
van Bohemen, Ch.G. and Lambert, J.G.D. 1981. Estrogen synthesis in relation to estrone, estradiol and vitellogenin plasma levels during the reproductive cycle of female rainbow trout (Salmo gairdneri). Gen. Comp. Endocrinol. 45: 105–114.
Vaillant, C., Le Guellec, C., Pakdel, F. and Valotaire, Y. 1988. Vitellogenin gene expression in primary culture of male rainbow trout hepatocytes. Gen. Comp. Endocrinol. 70: 284–290.
Wallace, R.A. and Selman, K. 1981. Cellular and dynamic aspects of oocyte growth in teleosts. Am. Zool. 21: 325–343.
Weisner, R.J. and Zak, R. 1991. Quantitative approaches for studying gene expression. Am. J. Physiol. 260: L179–L188.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Martin, N.B., Houlihan, D.F., Talbot, C. et al. Protein metabolism during sexual maturation in female Atlantic salmon (Salmo salar L). Fish Physiol Biochem 12, 131–141 (1993). https://doi.org/10.1007/BF00004378
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00004378