Antioxidant defenses during early developmental stages in tetraploid rainbow trout, Oncorhynchus mykiss

Document Type : Research Paper

Authors

1 Department of Natural Resources, Isfahan University of Technology, Isfahan, 84156-83111, Iran

2 Department of Biotechnology, College of Agriculture, Isfahan University of Technology, Isfahan, 84156-83111, Iran

3 Department of Biology, University of New Brunswick, Fredericton, New Brunswick, E3B 6E1, Canada

10.22124/cjes.2023.7255

Abstract

Antioxidant defense status was examined during early developmental stages of rainbow trout, Oncorhynchus mykiss, as affected by heat shock (HS) treatment to induce tetraploidy. Samples were collected at 3850 degree-min post-fertilization at 10 °C and at eyed, hatch, swim-up, in addition to fry stages to determine the activity of catalase (CAT), superoxide dismutase (SOD), glutathione peroxidase (GPx), and levels of vitamin C, A and E as well as malondialdehyde (MDA). HS treatment caused a significant reduction in survival, but not affected growth compared to the control. CAT and SOD activities peaked at hatch, whereas GPx activity reached a maximum at the swim-up stage, showing similar patterns, however, significantly higher activities in the HS group. Vitamin levels were at their minimum at the hatch in both groups, while significantly lower in the HS groups. Vitamin levels were at their highest at the fry stage, with the exception of low vitamin E in the HS group. The levels of MDA showed a steady increase during development, with consistently higher levels in the HS group. These results suggest that HS treatment and/or tetraploidy status cause high oxidative stress, as evidenced by higher activity of antioxidant enzymes and MDA levels, and lower levels of vitamins.

Keywords

References

Aceto, A, Amicarelli, F, Sacchetta, P, Dragani, B, Bucciarelli, T, Masciocco, L, Miranda, M & Ilio, CD 1994, Developmental aspects of detoxifying enzymes in fish (Salmo irideus). Free Radical Research, 21: 285-294.
Aegerter, S & Jalabert, B 2004, Effects of post-ovulatory oocyte ageing and temperature on egg quality and on the occurrence of triploid fry in rainbow trout, Oncorhynchus mykiss. Aquaculture, 231: 59-71.
Ahmad S 1995, Antioxidant mechanisms of enzymes and proteins. Oxidative stress and antioxidant defenses in biology, pp. 238-272. https://link.springer.com/chapter/10.1007/978-1-4615-9689-9_7.
Ahmed, RS, Suke, SG, Seth, V, Jain, A, Bhattacharya, SN & Banerjee, BD 2006, Impact of oral vitamin E supplementation on oxidative stress & lipid peroxidation in patients with polymorphous light eruption. Indian Journal of Medical Research, 123: 781-787.
Arai, K & Fujimoto T 2018, Chromosome manipulation techniques and applications to aquaculture. Sex control in Aquaculture, 26: 137-162.
Arslan, T, Erdogan, F & Erdogan, M 2012, The production of functional sex-reversed male rainbow trout (Oncorhynchus mykiss). Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 18(2).
Atkins, ME & Benfey, TJ 2008, Effect of acclimation temperature on routine metabolic rate in triploid salmonids. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 149: 157-161.
Babaheydari, SB, Keyvanshokooh, S, Dorafshan, S & Johari, SA 2016, Effects of tetraploidy induction on rainbow trout (Oncorhynchus mykiss, Walbaum, 1792) proteome at early stages of development. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics, 20: 57-64
Barim, O & Karatepe, M 2010, The effects of pollution on the vitamins A, E, C, β-carotene contents and oxidative stress of the freshwater crayfish, Astacus leptodactylus. Ecotoxicology and Environmental Safety, 73: 138-142.
Barim-Oz O & Yilmaz, S 2017, Effects of dietary antioxidants on oxidative stress, antioxidant defence and growth of freshwater crayfish Astacus leptodactylus (Eschscholtz, 1823) during the reproductive period in females. Aquaculture Research, 48: 2516-2527.
Beers, RF & Sizer, IW 1952, A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. Journal Biological Chemistry, 195: 133-140.
Bell, JG, Cowey, CB, Adron, JW & Shanks, AM 1985, Some effects of vitamin E and selenium deprivation on tissue enzyme levels and indices of tissue peroxidation in rainbow trout (Salmo gairdneri). British Journal of Nutrition, 53: 149-157.
Benfey TJ 1999, The physiology and behavior of triploid fishes. Reviews in Fisheries Science, 7(1):39-67.
Blanc, JM, Poisson, H, Escaffre, AM, Aguirre, P & Vallée, F 1993, Inheritance of fertilizing ability in male tetraploid rainbow trout (Oncorhynchus mykiss). Aquaculture, 110 (1):61-70.
Buege, JA & Aust, SD 1978, Microsomal lipid peroxidation. Methods in Enzymology, Academic Press, 52: 302-310, DOI: 10.1016/s0076-6879(78)52032-6.
Chourrout, D, Chevassus, B, Krieg, F, Happe, A, Burger, G & Renard P 1986, Production of second generation triploid and tetraploid rainbow trout by mating tetraploid males and diploid females-potential of tetraploid fish. Theoretical and Applied Genetics, 72: 193-206.
Cousin-Gerber, M, Burger, G, Boisseau, C & Chevassus, B 1989, Effect of methyltestosterone on sex differentiation and gonad morphogenesis in rainbow trout Oncorhynchus mykiss. Aquatic Living Resources, 2: 225-230. 
Cowey, CB, Bell, JG, Knox, D, Fraser, A & Youngson, A 1985, Lipids and lipid antioxidant systems in developing eggs of salmon (Salmo salar). Lipids, 20: 567-572.
Dandapat, J, Chainy, GB & Rao, KJ 2003, Lipid peroxidation and antioxidant defence status during larval development and metamorphosis of giant prawn, Macrobrachium rosenbergii. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 135: 221-233
de Alvarenga, ÉR, Fernandes, AF, Lopes, LR, Soares, TE, de Oliveira Alves, GF, da Costa, FF, de Sales, SC, Lima, GK & Turra, EM 2020, Attempt to produce a Nile tilapia tetraploid line by heat shock induction. Aquaculture, 529: 735647.
Davies, KJ, Rice-Evans, C, Halliwell, B & Lunt, GG 1995, Oxidative stress: the paradox of aerobic life. In Biochemical Society Symposia, 61: 1-31. Portland Press.
Díaz, ME, Furné, M, Trenzado, CE, García-Gallego, M, Domezain, A & Sanz, A 2010, Antioxidant defenses in the first life phases of the sturgeon Acipenser naccarii. Aquaculture, 307 (1-2):123-129.
do Nascimento, NF, Pereira-Santos, M, Levy-Pereira, N, Monzani, PS, Niedzielski, D, Fujimoto, T, Senhorini, JA, Nakaghi, LSO & Yasui, GS 2020, High percentages of larval tetraploids in the yellowtail tetra Astyanax altiparanae induced by heat-shock: The first case in Neotropical characins. Aquaculture, 520: 734938.
Farahmand, H, Abdul Razak, SH, Hwang, GL, Maclean, N & Rahman, MA 2007, Induction of tetraploidy in transgenic tilapia (Oreochromis niloticus) using physical shocks. Iranian Journal of Fisheries Sciences, 7: 27-46.
Fontagné, S, Lataillade, E, Breque, J & Kaushik, S 2008, Lipid peroxidative stress and antioxidant defence status during ontogeny of rainbow trout (Oncorhynchus mykiss). British Journal of Nutrition, 100: 102-111.
Fraser, TW, Fjelldal, PG, Hansen, T & Mayer, I 2012, Welfare considerations of triploid fish. Reviews in Fisheries Science, 20: 192-211.
Fridovich I 1998, Oxygen toxicity: A radical explanation. The Journal of Experimental Biology, 201: 1203-1209.
El Gamal, AR, Davis, KB, Jenkins, JA & Torrans, EL 1999, Induction of triploidy and tetraploidy in Nile tilapia, Oreochromis niloticus (L.). Journal of the World Aquaculture Society, 30: 269-275.
Farabi, SMV, Golaghaei, M, Sharifian, M, Daryanabard, G, Karimian, E 2022, Effects of rainbow trout farming on water quality around the sea farms in the south of the Caspian Sea. Caspian Journal of Environmental Sciences, 20: 729-737.
Gao, Z, Wang, W, Abbas, K, Zhou, X, Yang, Y, Diana, JS, Wang, H, Wang, H, Li, Y & Sun, Y 2007, Haematological characterization of loach Misgurnus anguillicaudatus: comparison among diploid, triploid and tetraploid specimens. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 147: 1001-1008.
Halliwell, B & Gutteridge, JM 2015, Free radicals in biology and medicine. Oxford University Press, USA.
Harsij, M, Kanani, HG & Adineh, H 2020, Effects of antioxidant supplementation (nano‑selenium, vitamin C and E) on growth performance, blood biochemistry, immune status and body composition of rainbow trout (Oncorhynchus mykiss) under sub-lethal ammonia exposure. Aquaculture, 521: 734942.
Heming, TA & Buddington, RK 1988, Yolk absorption in embryonic and larval fishes. In Fish Physiology, 11:407-446.
Hershberger WK, & Hostuttler MA 2005, Variation in time to first cleavage in rainbow trout Oncorhynchus mykiss embryos: a major factor in induction of tetraploids. Journal of the World Aquaculture Society, 36: 96-102.
Hershberger, WK & Hostuttler MA 2007, Protocols for more effective induction of tetraploid rainbow trout. North American Journal of Aquaculture, 69: 367-372.
Hörstgen-Schwark G 1993, Initiation of tetraploid breeding line development in rainbow trout, Oncorhynchus mykiss (Walbaum). Aquaculture Research, 24: 641-652.
Hussein, HA, Khudair, SA, Alwan, M, Aljawahiry, TT, Qasim, MV & Pavlova, I 2022, Impact of pollution caused by salmon breeding centres on river water quality. Caspian Journal of Environmental Sciences, 20: 1039-1045.
Imanpour Namin, J, Safarbibi, K, Allaf Noveirian, H & Amini, K 2022, Effects of cage culture of rainbow trout, Oncorhynchus mykiss on phytoplankton and zooplankton communities (Case study: Golestan Reservoir 1, Gorgan, Iran). Caspian Journal of Environmental Sciences, 20: 1-15
Katsanidis, E & Addis, PB 1999, Novel HPLC analysis of tocopherols, tocotrienols, and cholesterol in tissue. Free Radical Biology and Medicine, 27: 1137-1140.
Kim, C.H, Kim, E.J & Nam, Y.K 2021, Superoxide dismutase multigene family from a primitive chondrostean sturgeon, Acipenser baerii: Molecular characterization, evolution, and antioxidant defense during development and pathogen infection. Antioxidants, 10: 232.
Kong, X, Jiang, H, Wang, S, Wu, X, Fei, W, Li, L, Nie, G & Li, X 2013, Effects of copper exposure on the hatching status and antioxidant defence at different developmental stages of embryos and larvae of goldfish Carassius auratus. Chemosphere, 92: 1458-1464.
Lavens, P, Lebegue, E, Jaunet, H, Brunel, A, Dhert, P & Sorgeloos, P 1999, Effect of dietary essential fatty acids and vitamins on egg quality in turbot broodstocks. Aquaculture International, 7: 225-240.
Maxime, V 2008, The physiology of triploid fish: current knowledge and comparisons with diploid fish. Fish and Fisheries, 9: 67-78.
Martínez-Álvarez, RM, Morales, AE & Sanz, A 2005, Antioxidant defences in fish: biotic and abiotic factors. Reviews in Fish Biology and Fisheries, 15: 75-88, https://doi.org/10.1007/s11160-005-7846-4.
Mohammed, W, Kadhim Alahmed, SG & Al-Mamoori, AM 2021, The biochemical and molecular markers of Cyprenus carpio L. after chronic exposure to lead. Caspian Journal of Environmental Sciences, 19: 817-824.
Mourente, G, Tocher, DR, Diaz, E, Grau, A & Pastor, E 1999, Relationships between antioxidants, antioxidant enzyme activities and lipid peroxidation products during early development in Dentex dentex eggs and larvae. Aquaculture, 179: 309-324.
Myers, JM, Hershberger, WK & Iwamoto, RN 1986, The induction of tetraploidy in salmonids. Journal of the World Aquaculture Society, 17: 1-7.
Nelis, HJ, Lavens, P, Van Steenberge, MM, Sorgeloos, P, Criel, GR & De Leenheer, AP 1988, Qualitative and quantitative changes in the carotenoids during development of the brine shrimp Artemia. Journal of Lipid Research, 29: 491-499.
Okomoda, VT, Olufeagba, SO, Ataguba, GA, Solomon, SG, Oladimeji, SA, Hassan, A & Abol-Munafi, AB 2021, Tetraploid induction in Clarias gariepinus using cold shock protocol. Aquaculture, 545: 737178.
Packer, L 1991, Protective role of vitamin E in biological systems. The American Journal of Clinical Nutrition, 53: 1050S-1055S.
Palace, VP & Werner, J 2006, Vitamins A and E in the maternal diet influence egg quality and early life stage development in fish: A review. Scientia Marina, 70: 41-57.
Palacios, A, Piergiacomi, VA & Catala, A 1996, Vitamin A supplementation inhibits chemiluminescence and lipid peroxidation in isolated rat liver microsomes and mitochondria. Molecular and Cellular Biochemistry, 154: 77-82.
Pérez, JA, Papadakis, IE, Papandroulakis, N, Cruces, L, Cotou, E, Gisbert, E, Lorenzo, A, Mylonas, CC & Rodríguez, C 2020, The ontogeny of greater amberjack digestive and antioxidant defence systems under different rearing conditions: A histological and enzymatic approach. Aquaculture Nutrition, 26: 1908-1925.
Peters, LD, Porte, C, Albaiges, J & Livingstone, DR 1994, 7-Ethoxyresorufin O-deethylase (EROD) and antioxidant enzyme activities in larvae of sardine (Sardina pilchardus) from the North coast of Spain. Marine Pollution Bulletin, 28: 299-304.
Peters, LD & Livingstone, DR 1996, Antioxidant enzyme activities in embryologic and early larval stages of turbot. Journal of Fish Biology, 49: 986-997.
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: 125-156.
Serigstad, B 1987, Oxygen uptake of developing fish eggs and larvae. Sarsia, 72: 369-371.
Solé, M, Potrykus, J, Fernández-Díaz, C & Blasco, J 2004, Variations on stress defenses and metallothionein levels in the Senegal sole, Solea senegalensis, during early larval stages. Fish Physiology and Biochemistry, 30: 57-66.
Taghipoor, K, Keyvanshokooh, S, Salati, AP, Pasha-Zanoosi, H & Babaheydari, SB 2016, Effects of triploidy induction on antioxidant defence status in rainbow trout (Oncorhynchus mykiss) during early development. Animal Reproduction Science, 171: 108-113.
Trichet, VV 2010, Nutrition and immunity: an update. Aquaculture Research, 41: 356-372.
Ukeda, H, Kawana, D, Maeda, S & Sawamura, M 1999, Spectrophotometric assay for superoxide dismutase based on the reduction of highly water-soluble tetrazolium salts by xanthine-xanthine oxidase. Bioscience, Biotechnology and Biochemistry, 63: 485-488.
Weber, GM, Hostuttler, MA, Cleveland, BM & Leeds TD 2014, Growth performance comparison of intercross-triploid, induced triploid, and diploid rainbow trout. Aquaculture, 433: 85-93.
Weber, GM, Hostuttler, MA, Semmens, KJ & Beers, BA 2015, Induction and viability of tetraploids in brook trout (Salvelinus fontinalis). Canadian Journal of Fisheries and Aquatic Sciences, 72(10):1443-1449.
Xavier, PL, Senhorini, JA, Pereira-Santos, M, Fujimoto, T, Shimoda, E, Silva, LA, Dos Santos, SA & Yasui, GS 2017, A flow cytometry protocol to estimate DNA content in the yellowtail tetra Astyanax altiparanae. Frontiers in Genetics, 8: 131.
Zahmatkesh, A, Karimzadeh, K & Faridnia, M 2020, Effect of dietary selenium nanoparticles and chitosan oligosaccharide on biochemical parameters of Caspian roach (Rutilus caspicus) under malathion stress. Caspian Journal of Environmental Sciences, 18: 59-71.
     Zengin, H, Yılmaz, Ö, Demir, E & Gökçe, Z. 2015, Antioxidant enzymatic defences during embryogenesis of rainbow trout Oncorhynchus mykiss (Walbaum 1792). Turkish Journal of Fisheries and Aquatic Sciences, 15: 443-452.
Caspian Journal of Environmental Sciences
Volume 21, Issue 5
Special Issue: Enviroment & Economy
December 2023
Pages 1005-1016

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