Skip to main content
SpringerLink
Log in

Characterization and dietary regulation of glutamate dehydrogenase in different ploidy fishes

  • Original Article
  • Published:
Amino Acids Aims and scope Submit manuscript

Abstract

Glutamate dehydrogenase (GDH) plays a crucial role in amino acid deamination and has been used as an inductor of nutrients metabolism. In this study, we cloned and analyzed the GDH cDNAs in diploids (red crucian carp), triploids and tetraploids and characterized their expression profiles upon dietary treatments. Results showed a high sequence similarity of GDH among the three kinds of ploidy fishes and other vertebrates. Expression analysis revealed that GDH exhibited a distinct spatial pattern of expression in different types of fishes. The triploids and tetraploids had higher levels of expression than diploids in heart, liver, gill, muscle, fore-gut and mid-gut. The GDH expression was also developmentally regulated with a stronger expression around blastula stage. The maternal GDH transcripts were first detected from eggs and their expression dropped down from the gastrula stage to heart beat stage. Adult triploids showed the highest levels of GDH expression in liver during breeding season which may contribute to the good appetite and fast growth. In addition, triploids exhibited high growth rates and excess GDH expression compared with other two types of fishes. The liver GDH enzyme activities were also higher in triploids than red crucian carp and tetraploids. Moreover, GDH expression is regulated by dietary protein levels. Fish fed with either high or low protein diets showed higher levels of GDH expression. In summary, our results demonstrated for the first time that the different ploidy fishes had different patterns of GDH mRNA expression during development, breeding and non-breeding seasons, and as well dietary effects from different protein levels in diet. These data indicate that abundant GDH expression may play an important role in growth rates in triploids.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Alexis MN, Papaparaskeva-Papoutsoglou E (1986) Aminotransferase activity in the liver and white muscle of Mugil capito fed diets containing different levels of protein and carbohydrate. Comp Biochem Physiol B Biochem Mol Biol 83(1):245–249. doi:10.1016/0305-0491(86)90361-5

    CAS  Google Scholar 

  • Allen L (1994) Nutritional influences on linear growth: a general review. Eur J Clin Nutr 48(1):75–89

    Google Scholar 

  • Babiak I, Dobosz S, Goryczko K, Kuzminski H, Brzuzan P et al (2002) Androgenesis in rainbow trout using cryopreserved spermatozoa: the effect of processing and biological factors. Theriogenology 57(4):1229–1249. doi:10.1016/S0093-691X(02)00631-3

    Article  PubMed  CAS  Google Scholar 

  • Boris G (2003) Chromosome set manipulation and sex control in common carp: a review. Aquat Living Resour 16(5):408–415. doi:10.1016/s0990-7440(03)00085-8

    Article  Google Scholar 

  • Boutry C, Matsumoto H, Bos C et al (2012) Decreased glutamate, glutamine and citrulline concentrations in plasma and muscle in endotoxemia cannot be reversed by glutamate or glutamine supplementation: a primary intestinal defect. Amino Acids 1–14. doi:10.1007/s00726-012-1221-2

  • Cambier S, Gonzalez P, Mesmer-Dudons N et al (2012) Effects of dietary methylmercury on the zebrafish brain: histological, mitochondrial, and gene transcription analyses. Biometals 25(1):165–180. doi:10.1007/s10534-011-9494-6

    Article  PubMed  CAS  Google Scholar 

  • Chu WY, Chen J, Zhou RX et al (2011) Characterization and ontogenetic expression analysis of the myosin light chains from the fast white muscle of mandarin fish Siniperca chuatsi. J Fish Biol 78(4):1225–1238. doi:10.1111/j.1095-8649.2011.02929.x

    Article  PubMed  CAS  Google Scholar 

  • Cowey C, Walton M (1989) Intermediary metabolism. In: Halver JE (ed) Fish nutrition. Academic Press, New York

    Google Scholar 

  • Cowey C, Knox D, Walton M et al (1977) The regulation of gluconeogenesis by diet and insulin in rainbow trout (Salmo gairdneri). Br J Nutr 38:463–470

    Article  PubMed  CAS  Google Scholar 

  • Curthoys NP, Watford M (1995) Regulation of glutaminase activity and glutamine metabolism. Annu Rev Nutr 15(1):133–159. doi:10.1146/annurev.nu.15.070195.001025

    Article  PubMed  CAS  Google Scholar 

  • Ding F, Chu W, Cui P et al (2011) EST-based identification of genes expressed in skeletal muscle of the mandarin fish (Siniperca chuatsi). Genomics, proteomics bioinformatics 9(1–2):30–36. doi:10.1016/s1672-0229(11)60005-3

    Article  PubMed  CAS  Google Scholar 

  • Dowling TE, Secor LC (1997) The role of hybridization and introgression in the diversification of animals. Annu Rev Ecol Syst 28(1):593–619. doi:10.1146/annurev.ecolsys.28.1.593

    Article  Google Scholar 

  • Figueiredo-Silva A, Corraze G, Kaushik S et al (2010) Modulation of blackspot seabream (Pagellus bogaraveo) intermediary metabolic pathways by dispensable amino acids. Amino Acids 39(5):1401–1416. doi:10.1007/s00726-010-0599-y

    Article  PubMed  CAS  Google Scholar 

  • Gómez-Requeni P, Mingarro M, Kirchner S et al (2003) Effects of dietary amino acid profile on growth performance, key metabolic enzymes and somatotropic axis responsiveness of gilthead sea bream (Sparus aurata). Aquaculture 220(1–4):749–767. doi:10.1016/s0044-8486(02)00654-3

    Article  Google Scholar 

  • Hernandez J-P, de-Bashan LE, Rodriguez DJ et al (2009) Growth promotion of the freshwater microalga Chlorella vulgaris by the nitrogen-fixing, plant growth-promoting bacterium Bacillus pumilus from arid zone soils. Eur J Soil Biol 45(1):88–93. doi:10.1016/j.ejsobi.2008.08.004

    Article  CAS  Google Scholar 

  • Kaushik SJ, Seiliez I (2010) Protein and amino acid nutrition and metabolism in fish: current knowledge and future needs. Aquac Res 41(3):322–332. doi:10.1111/j.1365-2109.2009.02174.x

    Article  CAS  Google Scholar 

  • Leggatt RA, Raven PA, Mommsen TP et al (2009) Growth hormone transgenesis influences carbohydrate, lipid and protein metabolism capacity for energy production in coho salmon (Oncorhynchus kisutch). Comp Biochem Physiol B Biochem Mol Biol 154(1):121–133. doi:10.1016/j.cbpb.2009.05.010

    Article  PubMed  CAS  Google Scholar 

  • Li P, Yin YL, Li D et al (2007) Amino acids and immune function. Br J Nutr 98(2):237–252. doi:10.1017/S000711450769936X

    Article  PubMed  CAS  Google Scholar 

  • Li YY, Hu CB, Zheng YJ et al (2008) The effects of dietary fatty acids on liver fatty acid composition and Δ6-desaturase expression differ with ambient salinities in Siganus canaliculatus. Comp Biochem Physiol B Biochem Mol Biol 151(2):183–190. doi:10.1016/j.cbpb.2008.06.013

    Article  PubMed  Google Scholar 

  • Li P, Mai K, Trushenski J et al (2009) New developments in fish amino acid nutrition: towards functional and environmentally oriented aquafeeds. Amino Acids 37:43–53. doi:10.1007/s00726-008-0171-1

    Article  PubMed  Google Scholar 

  • Li F, Yin Y, Tan B et al (2011) Leucine nutrition in animals and humans: mTOR signaling and beyond. Amino Acids 41(5):1185–1193. doi:10.1007/s00726-011-0983-2

    Article  PubMed  CAS  Google Scholar 

  • Liu S ( 2010) Distant hybridization leads to different ploidy fishes. Sci China Life Sci 53(4):416–425. doi:10.1007/s11427-010-0057-9

  • Liu SJ, Feng H, Liu Y et al (1999) The measurement of DNA content of the tetraploid F3–F4 hybrids of red crucian carp (♀) × common carp (♂) and their triploid offspring and other related diploid fish. Acta Sci Nat Univ Norm Hunan 22:61–64

    CAS  Google Scholar 

  • Liu SJ, Hu F, Zhou GJ et al (2000) Gonadal structure of triploid crucian carp produced by crossing allotetraploid hybrids of Carassius auratus red var.(♀) × Cyprinus carpio L.(♂) with Japanese crucian carp (Carassius auratus cuvieri T. et S). Acta Hydrobiol Sin 24:301–306

    Google Scholar 

  • Liu SJ, Liu Y, Zhou GJ et al (2001) The formation of tetraploid stocks of red crucian carp × common carp hybrids as an effect of interspecific hybridization. Aquaculture 192(2–4):171–186. doi:10.1016/s0044-8486(00)00451-8

    Article  Google Scholar 

  • Mommsen T, French C, Hochachka P (1980) Sites and patterns of protein and amino acid utilization during the spawning migration of salmon. Can J Zool 58(10):1785–1799

    Article  CAS  Google Scholar 

  • Moon TW (1983) Metabolic reserves and enzyme activities with food deprivation in immature American eels, Anguilla rostrata (LeSueur). Can J Zool 61(4):802–811. doi:10.1139/z83-106

    Article  CAS  Google Scholar 

  • Moyano FJ, Cardenete G, De la Higuera M (1991) Nutritive and metabolic utilization of proteins with high glutamic acid content by the rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol A Mol Integr Physiol 100(3):759–762. doi:10.1016/0300-9629(91)90404-z

    Google Scholar 

  • Ogata H, Arai S, Alvarez MB (1985) Effect of dietary protein levels on free amino acid contents of juvenile European eel Anguilla anguill. Nippon Suisan Gakkai Shi 5:573–578

    Article  Google Scholar 

  • Otto SP, Whitton J (2000) Polyploid incidence and evolution. Annu Rev Genet 34(1):401–437. doi:10.1146/annurev.genet.34.1.401

    Article  PubMed  CAS  Google Scholar 

  • Pala I, Coelho MM, Schartl M (2008) Dosage compensation by gene-copy silencing in a triploid hybrid fish. Curr Biol 18(17):1344–1348. doi:10.1016/j.cub.2008.07.096

    Article  PubMed  CAS  Google Scholar 

  • Picha ME, Strom CN, Riley LG et al (2009) Plasma ghrelin and growth hormone regulation in response to metabolic state in hybrid striped bass: Effects of feeding, ghrelin and insulin-like growth factor-I on in vivo and in vitro GH secretion. Gen Comp Endocrinol 161(3):365–372. doi:10.1016/j.ygcen.2009.01.026

    Article  PubMed  CAS  Google Scholar 

  • Regnault M (1993) Effect of severe hypoxia on some aspects of nitrogen metabolism in the crab Cancer pagurus. Mar Behav Physiol 22:131–140

    Article  Google Scholar 

  • Rønnestad I, Thorsen A, Finn RN (1999) Fish larval nutrition: a review of recent advances in the roles of amino acids. Aquaculture 177(1–4):201–216. doi:10.1016/s0044-8486(99)00082-4

    Article  Google Scholar 

  • Silverstein JT, Wolters WR, Shimizu M et al (2000) Bovine growth hormone treatment of channel catfish: strain and temperature effects on growth, plasma IGF-I levels, feed intake and efficiency and body composition. Aquaculture 190(1–2):77–88. doi:10.1016/s0044-8486(00)00387-2

    Article  CAS  Google Scholar 

  • Smith MAK (1981) Estimation of growth potential by measurement of tissue protein synthetic rates in feeding and fasting rainbow trout Salmo gairdnerii Richardson. J Fish Biol 19(2):213–220. doi:10.1111/j.1095-8649.1981.tb05825.x

    Article  CAS  Google Scholar 

  • Stelling J, Klamt S, Bettenbrock K et al (2002) Metabolic network structure determines key aspects of functionality and regulation. Nature 420(6912):190–193. doi:10.1038/nature01166

    Article  PubMed  CAS  Google Scholar 

  • Stumvoll M, Perriello G, Meyer C et al (1999) Role of glutamine in human carbohydrate metabolism in kidney and other tissues. Kidney Int 55(3):778–792. doi:10.1046/j.1523-1755.1999.055003778.x

    Article  PubMed  CAS  Google Scholar 

  • Sun YD, Liu SJ, Zhang C et al (2003) The chromosome number and gonadal structure of F9–F11 allotetraploid crucian-carp. Acta Genet Sin 30:414–418

    Google Scholar 

  • Treberg J, Brosnan M, Brosnan J (2010) The simultaneous determination of NAD(H) and NADP(H) utilization by glutamate dehydrogenase. Mol Cell Biochem 344(1):253–259. doi:10.1007/s11010-010-0549-8

    Article  PubMed  CAS  Google Scholar 

  • Wei JW, Carroll RJ, Harden KK et al (2012) Comparisons of treatment means when factors do not interact in two-factorial studies. Amino Acids 42:2031–2035. doi:10.1007/s00726-011-0924-0

    Article  PubMed  CAS  Google Scholar 

  • Woo NYS, Fung ACY (1981) Studies on the biology of the red sea bream Chrysophrys major—IV. Metabolic effects of starvation at low temperature. Comp Biochem Physiol A Mol Integr Physiol 69(3):461–465. doi:10.1016/0300-9629(81)93005-x

  • Wu G, Bazer FW, Davis TA et al (2007) Important roles for the arginine family of amino acids in swine nutrition and production. Livest Sci 112(1):8–22. doi:10.1016/j.livsci.2007.07.003

    Article  Google Scholar 

  • Wu G, Bazer F, Davis T et al (2009) Arginine metabolism and nutrition in growth, health and disease. Amino Acids 37(1):153–168. doi:10.1007/s00726-008-0210-y

    Article  PubMed  CAS  Google Scholar 

  • Yao K, Yin YL, Chu W et al (2008) Dietary arginine supplementation increases MTOR signaling activity in skeletal muscle of neonatal pigs. J Nutr 138(5):867–872

    PubMed  CAS  Google Scholar 

  • Yin FG, Liu YL, Yin YL et al (2009) Dietary supplementation with Astragalus polysaccharide enhances ileal digestibilities and serum concentrations of amino acids in early weaned piglets. Amino Acids 37:263–270. doi:10.1007/s00726-008-0142-6

    Article  PubMed  CAS  Google Scholar 

  • Zhang G, Chu W, Hu S et al (2011) Identification and analysis of muscle-related protein isoforms expressed in the white muscle of the Mandarin fish (Siniperca chuatsi). Mar Biotechnol 13(2):151–162. doi:10.1007/s10126-010-9275-1

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the National Natural Science Foundation of China (Grant No. 30930071), the National Natural Science Foundation of China for Young Scholars (Grant No.31001114), the Natural Science Fund for Innovative Research Team of Hunan Province (Grant No. 10JJ7004), the National Special Fund for Scientific Research in public benefits (Grant No. 200903046), the Doctoral Fund of Ministry of Education of China (Grant No. 20104306110004), and the Construction Project of Key Discipline of Hunan Province and China.

Author information

Authors and Affiliations

  1. Key Laboratory of Protein Chemistry and Developmental Biology of State Education Ministry of China, College of Life Sciences, Hunan Normal University, Changsha, 410081, China

    Zhen Liu, Yi Zhou, Shaojun Liu, Huan Zhong, Chun Zhang, Xuewei kang & Yun Liu

  2. Department of Biotechnology and Environmental Science, Changsha University, Changsha, 410003, China

    Zhen Liu

Authors
  1. Zhen Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yi Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shaojun Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Huan Zhong
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chun Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xuewei kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yun Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shaojun Liu.

Additional information

Authors Z. Liu and Y. Zhou contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, Z., Zhou, Y., Liu, S. et al. Characterization and dietary regulation of glutamate dehydrogenase in different ploidy fishes. Amino Acids 43, 2339–2348 (2012). https://doi.org/10.1007/s00726-012-1313-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00726-012-1313-z

Keywords

Search

Navigation