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Effects of temperature on the transcriptomes of pituitary and liver in Golden Pompano Trachinotus blochii

Abstract

Fish growth can be modulated dynamically through the brain-pituitary-liver regulation axis. In the present study, whole transcriptomes of the pituitary and liver from Golden Pompano Trachinotus blochii were sequenced in seawater at 20 °C (T_low) and 25 °C (T_high). A total of 187,277,583 paired-end reads were assembled to obtain 100,495 transcripts, corresponding to 83,974 genes. These reads were mapped to T. blochii transcripts, and the mapping accuracy ranged from 80.4 to 94.9%. Two lists of differentially expressed genes were obtained by comparisons of pituitary and liver T_low versus T_high groups, comprising 458 and 205 genes, respectively. Of these, 33 differentially expressed genes were common between the two lists. Twelve GO terms were overrepresented for the 458 differentially expressed genes in the pituitary, and it is noteworthy that the GO term galanin receptor activity (GO: 0004966) related to the modulation of appetite and metabolism, whose genes made up half of all assembled genes in the term. For the 205 differentially expressed genes in the liver, 19 overrepresented GO terms were mainly related to immune regulation, digestion, and protein metabolism. Among the common differentially expressed genes, there were 32 genes that had identical changing trends in both pituitary and liver comparisons. Furthermore, two GO terms inorganic diphosphatase activity and MHC protein complex were overrepresented. These results indicate that the brain could regulate pituitary function through galanin signal mechanism and that the metabolism of liver was further optimized to modulate immunity and growth under different temperatures.

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References

  1. Arendt JD (1997) Adaptive intrinsic growth rates: an integration across taxa. Q Rev Biol 72:149–177

  2. Ayles GB (1975) Influence of the genotype and the environment on growth and survival of rainbow trout (Salmo gairdneri) in Central Canadian aquaculture lakes. Aquaculture 6:181–188

  3. Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol 42:517–525

  4. Bauer FE, Ginsberg L, Venetikou M, MacKay DJ, Burrin JM, Bloom SR (1986) Growth hormone release in man induced by galanin, a new hypothalamic peptide. Lancet 2:192–195

  5. Bœuf G, Payan P (2001) How should salinity influence fish growth? Comp Biochem Physiol Part C: Toxicol Pharmacol 130:411–423

  6. Breer H, Rahmann H (1976) Involvement of brain gangliosides in temperature adaptation of fish. J Therm Biol 1:233–235

  7. Brierley AS, Kingsford MJ (2009) Impacts of climate change on marine organisms and ecosystems. Curr Biol 19:R602–R614

  8. Canli M, Atli G (2003) The relationships between heavy metal (Cd, Cr, Cu, Fe, Pb, Zn) levels and the size of six Mediterranean fish species. Environ Pollut 121:129–136

  9. Cardoso CM, Sartorio PV, Machado ASD, Vignardi CP, Rojas DCGC, Passos MJACR, Rocha AJS, van Ngan P, Gomes V (2015) Hsp70 and p53 expressions and behavior of juvenile pompano, Trachinotus carolinus (Perciformes, Carangidae), at controlled temperature increase. J Exp Mar Biol Ecol 470:34–42

  10. Chan JCL (2000) Tropical cyclone activity over the Western North Pacific associated with El Niño and La Niña events. J Clim 13:2960–2972

  11. Chang JP, Johnson JD, Sawisky GR, Grey CL, Mitchell G, Booth M, Volk MM, Parks SK, Thompson E, Goss GG, Klausen C, Habibi HR (2009) Signal transduction in multifactorial neuroendocrine control of gonadotropin secretion and synthesis in teleosts-studies on the goldfish model. Gen Comp Endocrinol 161:42–52

  12. Chang JP, Habibi HR, Yu Y, Moussavi M, Grey CL, Pemberton JG (2012) Calcium and other signalling pathways in neuroendocrine regulation of somatotroph functions. Cell Calcium 51:240–252

  13. Company R, Astola A, Pendon C, Valdivia MM, Perez-Sanchez J (2001) Somatotropic regulation of fish growth and adiposity: growth hormone (GH) and somatolactin (SL) relationship. Comp Biochem Physiol C Toxicol Pharmacol 130:435–445

  14. Deane EE, Woo NYS (2009) Modulation of fish growth hormone levels by salinity, temperature, pollutants and aquaculture related stress: a review. Rev Fish Biol Fisher 19:97–120

  15. Diez JM, Giannicot G, McLeant E, Donaldson EM (1992) The effect of somatostatins (SRIF-14, 25 and 28), galanin and anti-SRIF on plasma growth hormone levels in Coho salmon (Oncorhynchus kisutch, Walbaum). J Fish Biol 40:887–893

  16. Grey CL, Chang JP (2013) Differential modulation of ghrelin-induced GH and LH release by PACAP and dopamine in goldfish pituitary cells. Gen Comp Endocrinol 191:215–224

  17. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M, MacManes MD, Ott M, Orvis J, Pochet N, Strozzi F, Weeks N, Westerman R, William T, Dewey CN, Henschel R, LeDuc RD, Friedman N, Regev A (2013) De novo transcript sequence reconstruction from RNA-seq using the trinity platform for reference generation and analysis. Nat Protoc 8:1494–1512

  18. Hevroy EM et al (2012) Ghrelin is involved in voluntary anorexia in Atlantic salmon raised at elevated sea temperatures. Gen Comp Endocrinol 175:118–134

  19. Hevroy EM et al (2013) GH-IGF system regulation of attenuated muscle growth and lipolysis in Atlantic salmon reared at elevated sea temperatures. J Comp Physiol B 183:243–259

  20. Iwama GK, Afonso LO, Todgham A, Ackerman P, Nakano K (2004) Are hsps suitable for indicating stressed states in fish? J Exp Biol 207:15–19

  21. Ji W, Ping HC, Wei KJ, Zhang GR, Shi ZC, Yang RB, Zou GW, Wang WM (2015) Ghrelin, neuropeptide Y (NPY) and cholecystokinin (CCK) in blunt snout bream (Megalobrama amblycephala): cDNA cloning, tissue distribution and mRNA expression changes responding to fasting and refeeding. Gen Comp Endocrinol 223:108–119

  22. Jobling M (1983) A short review and critique of methodology used in fish growth and nutrition studies. J Fish Biol 23:685–703

  23. Jory DE, Iversen ES, Lewis RH (1985) Culture of fishes of the genus Trachinotus (Carangidae) in the western Atlantic: prospects and problems. J World Maricult Soc 16:87–94

  24. Lacepède (1801) https://www.fishbase.se/summary/Trachinotus-blochii.html.. Accessed 18 August 2019.

  25. Leone S, Shohreh R, Manippa F, Recinella L, Ferrante C, Orlando G, Salvatori R, Vacca M, Brunetti L (2014) Behavioural phenotyping of male growth hormone-releasing hormone (GHRH) knockout mice. Growth Hormon IGF Res 24:192–197

  26. Lohmus M, Raven PA, Sundstrom LF, Devlin RH (2008) Disruption of seasonality in growth hormone-transgenic coho salmon (Oncorhynchus kisutch) and the role of cholecystokinin in seasonal feeding behavior. Horm Behav 54:506–513

  27. Maere S, Heymans K, Kuiper M (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21:3448–3449

  28. Naslund E, Hellstrom PM (2007) Appetite signaling: from gut peptides and enteric nerves to brain. Physiol Behav 92:256–262

  29. Nyberg F (2000) Growth hormone in the brain: characteristics of specific brain targets for the hormone and their functional significance. Front Neuroendocrinol 21:330–348

  30. O'Kusky J, Ye P (2012) Neurodevelopmental effects of insulin-like growth factor signaling. Front Neuroendocrinol 33:230–251

  31. Pakingking R, Mori KI, Bautista NB, de Jesus-Ayson EG, Reyes O (2011) Susceptibility of hatchery-reared snubnose pompano Trachinotus blochii to natural betanodavirus infection and their immune responses to the inactivated causative virus. Aquaculture 311:80–86

  32. Philip AM, Vijayan MM (2015) Stress-immune-growth interactions: cortisol modulates suppressors of cytokine signaling and JAK/STAT pathway in rainbow trout liver. PLoS One 10:e0129299. https://doi.org/10.1371/journal.pone.0129299

  33. Proudan N, Peroski M, Grignol G, Merchenthaler I, Dudas B (2015) Juxtapositions between the somatostatinergic and growth hormone-releasing hormone (GHRH) neurons in the human hypothalamus. Neuroscience 297:205–210

  34. Ramsey MM, Weiner JL, Moore TP, Carter CS, Sonntag WE (2004) Growth hormone treatment attenuates age-related changes in hippocampal short-term plasticity and spatial learning. Neuroscience 129:119–127

  35. Ransangan J, Manin BO, Abdullah A, Roli Z, Sharudin EF (2011) Betanodavirus infection in golden pompano, Trachinotus blochii, fingerlings cultured in deep-sea cage culture facility in Langkawi, Malaysia. Aquaculture 315:327–334

  36. Reinecke M (2010) Influences of the environment on the endocrine and paracrine fish growth hormone-insulin-like growth factor-I system. J Fish Biol 76:1233–1254

  37. Roith DL, Scavo L, Butler A (2001) What is the role of circulating IGF-I? Trends Endocrinol Metab 12:48–52

  38. Schneider-Rivas S, Rivas-Arancibia S, Vazquez-Pereyra F, Vazquez-Sandoval R, Borgonio-Perez G (1995) Modulation of long-term memory and extinction responses induced by growth hormone (GH) and growth hormone releasing hormone (GHRH) in rats. Life Sci 56:PL433–PL441

  39. Seibel BA, Drazen JC (2007) The rate of metabolism in marine animals: environmental constraints, ecological demands and energetic opportunities. Philos Trans R Soc Lond Ser B Biol Sci 362:2061–2078

  40. Silverstein JT, Wolters WR, Shimizu M, Dickhoff WW (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 190:77–88

  41. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and cufflinks. Nat Protoc 7:562–578

  42. Volkoff H, Hoskins LJ, Tuziak SM (2010) Influence of intrinsic signals and environmental cues on the endocrine control of feeding in fish: potential application in aquaculture. Gen Comp Endocrinol 167:352–359

  43. Wynick D, Small CJ, Bacon A, Holmes FE, Norman M, Ormandy CJ, Kilic E, Kerr NCH, Ghatei M, Talamantes F, Bloom SR, Pachnis V (1998) Galanin regulates prolactin release and lactotroph proliferation. Proc Natl Acad Sci U S A 95:12671–12676

  44. Zhou C, Lin H, Huang Z, Wang J, Wang Y, Yu W (2015) Effects of dietary soybean isoflavones on non-specific immune responses and hepatic antioxidant abilities and mRNA expression of two heat shock proteins (HSPs) in juvenile golden pompano Trachinotus ovatus under pH stress. Fish Shellfish Immunol 47:1043–1053

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Acknowledgements

The authors were grateful to all the laboratory members for continuous technical advice and helpful discussion.

Funding

This work was supported by the National Natural Science Foundation of China (NO.31660737), the National Key Research and Development Program of China (No.2018YFD0900704), and Scientific Research Foundation of Hainan University (kyqd1554).

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Correspondence to Jian Luo.

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Zhou, Z., Li, Y., Zhang, G. et al. Effects of temperature on the transcriptomes of pituitary and liver in Golden Pompano Trachinotus blochii. Fish Physiol Biochem 46, 63–73 (2020). https://doi.org/10.1007/s10695-019-00695-6

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Keywords

  • Temperature
  • Transcriptome
  • Trachinotus blochii
  • Adaptation
  • Regulation axis