Abstract
Temperature is a major environmental factor that influences growth, development, metabolism, and physiological performance in fish. Grass carp (Ctenopharyngodon idella) is a highly productive fish in freshwater culture. To understand the molecular mechanism of grass carp under heat stress, we used RNA-Seq to analyze the liver and brain transcriptome of 12 libraries constructed from high-temperature (36 °C) and control (28 °C) groups. We obtained 42.49 and 42.57 GB of clean data from six liver and six brain libraries, respectively, and identified 2,534 genes that were differentially expressed in liver tissue and 1622 in brain tissue (P < 0.05). According to KEGG analysis, significant differences occurred in the expression of genes involved in metabolic and immune pathways, such as the cAMP signaling pathway, apoptosis, calcium signaling pathway, lipid metabolism, and protein processing in endoplasmic reticulum and peroxisome proliferator-activated receptor signaling pathways. This study revealed that high temperature enhanced lipid metabolism, reduced fatty acid synthesis, and disrupted the immune system of grass carp. These results investigated the molecular regulation of heat stress in grass carp and provided valuable information for the healthy culture of grass carp under high temperatures.
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References
Agre P (2004) Aquaporin water channels (Nobel Lecture) (p 4278–4290). Angew Chem Int Ed 43:4278–4290
Anders S, Pyl PT, Huber W (2015) HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics 166–169
Bing LSS, Jian Z, Su Y, Zhang, W, Ge X (2019) Transcriptome profiling and histology changes in juvenile blunt snout bream (Megalobrama amblycephala) liver tissue in response to acute thermal stress. Genomics 111:242–250
Bionaz M, Loor J (2011) Gene Networks driving bovine mammary protein synthesis during the lactation cycle. Bioinform Biol Insights 5:83–98
Bo L, Xie J, Ge X, Xu P, Wang A, He Y, Zhou Q, Pan L, Chen R (2010) Effects of anthraquinone extract from Rheum officinale Bail on the growth performance and physiological responses of Macrobrachium rosenbergii under high temperature stress. Fish Shellfish Immunol 29:49–57
Bolger AM, Marc L, Bjoern U (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120
Brett JR (2015) Energetic Responses of salmon to temperature. a study of some thermal relations in the physiology and freshwater ecology of sockeye salmon (Oncorhynchus nerkd). Am Zool 11:99–113
Budihardjo IB, Oliver H, Lutter M, Luo X, Wang XD, Budihardjo I, Oliver H, Lutter M, Luo X, Wang XD (1999) Biochemical pathways of caspase activation during apoptosis. Annu Rev Cell Dev Biol 15:269–290
Bukau B, Horwich AL, Bakau B (1998) The Hsp70 and Hsp60 review chaperone machines. Cell 92:351–366
Chen M, Wang Y, Huang L, Sandoval H, Liu Y, Wang J (2006) Dendritic cell apoptosis in the maintenance of immune tolerance. Science 311:1160–1164
Cheng C, Yang F, Liao S, Miao Y, Ye C, Wang A, Tan J, Chen X (2015) High temperature induces apoptosis and oxidative stress in pufferfish (Takifugu obscurus) blood cells. J Therm Biol 53:172–179
Cheng C, Guo Z, Luo S, Wang A (2018) Effects of high temperature on biochemical parameters, oxidative stress, DNA damage and apoptosis of pufferfish (Takifugu obscurus). Ecotoxicol Environ Saf 150:190–198
Clarke A, Johnston NM (1999) Scaling of metabolic rate with body mass and temperature in teleost fish. J Anim Ecol 68:893–905
Cui Y, Liu B, Xie J, Xu P, Zhang Y (2013) The effect of hyperthermia on cell viability, oxidative damage, and heat shock protein expression in hepatic cells of grass carp (Ctenopharyngodon idellus). J Therm Biol 40:721–729
Edenhofer PR, Sokona Y, Farahani E, Kadner S, Seyboth K, Adler A, Baum I, Brunner S (2014) IPCC, 2014: Climate Change 2014: mitigation of climate change. Contribution of Working Group III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change 15:1435
Guo J, Zhang M, Wang S, Xu X, Shen Y, Li J (2022) A high-density genetic linkage map and QTL mapping for growth related traits in grass carp (Ctenopharyngodon idella). Aquaculture 552:738041
Handeland SO, Imsland AK, Stefansson SO (2008) The effect of temperature and fish size on growth, feed intake, food conversion efficiency and stomach evacuation rate of Atlantic salmon post-smolts. Aquaculture 283:36–42
Huey RB, Stevenson RD (2015) Integrating Thermal Physiology and Ecology of Ectotherms: A Discussion of Approaches. Am Zool 19:357–366
Huang J, Li Y, Liu Z, Kang Y, Wang J (2018) Transcriptomic responses to heat stress in rainbow trout Oncorhynchus mykiss head kidney. Fish Shellfish Immunol 82:32–40
Huang DY, Ren MC, Liang HL, Ge XP, Xu H, Wu LH (2022) Transcriptome analysis of the effect of high-temperature on nutrient metabolism in juvenile grass carp ( Ctenopharyngodon idellus ). Gene 809:146035
Iranshahi F, Faramarzi M, Kiaalvandi S (2011) The Effect of probiotics on growth performance and body composition of common carp (Cyprinus carpio). J Anim Vet Adv 10:2408–2413
Jeffries KM, Hinch SG, Sierocinski T, Pavlidis P (2013) Transcriptomic responses to high water temperature in two species of Pacific salmon. Evol Appl 7:286–300
Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357-U121
Krebs J, Agellon LB, Michalak M (2015) Ca2+ homeostasis and endoplasmic reticulum (ER) stress: an integrated view of calcium signaling. Biochem Biophys Res Commun 460:114–121
Kregel KC (2002) Invited Review: Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J Appl Physiol 192:2177–2186
Li AJ, Leung P, Bao V, Lui G, Leung K (2015) Temperature-dependent physiological and biochemical responses of the marine medaka Oryzias melastigma with consideration of both low and high thermal extremes. J Therm Biol 54:98–105
Liu F, Wang D, Fu J, Sun G, Shen Y, Dong L, Zhang B, Hu S, Li J (2010) Identification of immune-relevant genes by expressed sequence tag analysis of head kidney from grass carp (Ctenopharyngodon idella). Comp Biochem Physiol Part D Genomics Proteomics 5:116–123
Liu S, Wang X, Sun F, Zhang J, Feng J, Liu H, Sun Y, Zhang Y, Liu Z (2013) RNA-Seq reveals expression signatures of genes involved in oxygen transport, protein synthesis, folding, and degradation in response to heat stress in catfish. Physiol Genomics 45:462–476
Lopes PA, Martins R, Silva I, Madeira MS, Prates J, Soveral G (2018) Modulation of aquaporin gene expression by n-3 long-chain PUFA lipid structures in white and brown adipose tissue from hamsters. Br J Nutr 120:1098–1106
Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550
Lu Z, Tang M, Li Y, Shi F, Zhan F, Zhang M, Zhao L,Li J,Lin L,Qin Z(2021) Molecular cloning and characterization of FADD from the grass carp (Ctenopharyngodon idellus) in response to bacterial infection. Aquaculture 542:736829
Luo SW, Kang H, Kong JR, Xie RC, Liu Y, Wang WN, Xie FX, Wang C, Sun ZM (2017) Molecular cloning, characterization and expression analysis of (B-cell lymphoma-2) Bcl-2 in the orange-spotted grouper (Epinephelus coioides). Dev Comp Immunol 76:150–162
Madeira D, Narciso L, Cabraln HN, Vinagre C, Diniz MS (2013) Influence of temperature in thermal and oxidative stress responses in estuarine fish. Comp Biochem Physiol a: Mol Integr Physiol 166:237–243
Mahanty A, Mohanty S, Mohanty BP (2017) Dietary supplementation of curcumin augments heat stress tolerance through upregulation of nrf-2-mediated antioxidative enzymes and hsps in Puntius sophore. Fish Physiol Biochem 43:1131–1141
Naidoo N (2009) ER and aging—Protein folding and the ER stress response. Ageing Res Rev 8:150–159
Parsell DA, Lindquist S (1993) The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet 27:437–496
Roberts A, Trapnell C, Donaghey J, Rinn JL, Pachter L (2011) Improving RNA-Seq expression estimates by correcting for fragment bias. Genome Biol 12:1–14
Sangwan RS, Tripathi S, Singh J, Narnoliya LK, Sangwan NS (2013) De novo sequencing and assembly of Centella asiatica leaf transcriptome for mapping of structural, functional and regulatory genes with special reference to secondary metabolism. Gene 525:58–76
Savill J (1997) Apoptosis in resolution of inflammation. J Leukoc Biol 61:375–380
Shen Y, Wang L, Fu J, Xu X, Yue GH, Li J (2019) Population structure, demographic history and local adaptation of the grass carp. BMC Genomics 20:467
Shen Y, Yue G (2018) Current status of research on aquaculture genetics and genomics-information from isga 2018. Aquac Fish 4:43–47
Song L, Zhang J, Li C, Yao J, Jiang C, Li Y, Liu S, Liu Z (2014) Genome-wide identification of Hsp40 Genes in channel catfish and their regulated expression after bacterial infection. PLoS ONE 9:0115752
Srivastava SP, Shi S, Koya D, Kanasaki K (2014) Lipid mediators in diabetic nephropathy. Fibrogenesis & Tissue Repair 7:12–12
Sun S, Wu Y, Yu H, Su Y, Ren M, Zhu J, Ge X (2018) Serum biochemistry, liver histology and transcriptome profiling of bighead carp Aristichthys nobilis following different dietary protein levels. Fish Shellfish Immunol 86:832–839
Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 11:107–184
Tzab C, Amb C, Syb C, Zhb C (2021) Integrated metabolome and transcriptome analyses revealing the effects of thermal stress on lipid metabolism in juvenile turbot Scophthalmus maximus. J Therm Biol 99:102937
Verkman AS (2005) More than just water channels: unexpected cellular roles of aquaporins. J Cell Sci 118:3225
Verma AK, Pal AK, Manush SM, Das T, Dalvi RS, Chandrachoodan PP, Ravi PM, Apte SK (2007) Persistent sub-lethal chlorine exposure augments temperature induced immunosuppression in Cyprinus carpio advanced fingerlings. Fish Shellfish Immunol 22:547–555
Wang F, Dai AY, Tao K, Xiao Q, Huang ZL, Gao M, Li H, Wang X, Cao WX, Feng WL (2015) Heat shock protein-70 neutralizes apoptosis inducing factor in Bcr/Abl expressing cells. Cell Signal 27:1949–1955
Wang J, Scholtens D, Holko M, Ivancic D, Lee O, Hu H, Chatterton RT, Sullivan ME, Hansen N, Bethke K (2013) Lipid metabolism genes in contralateral unaffected breast and estrogen receptor status of breast cancer. Cancer Prev Res 6:321–330
Wang K, Li H, Xu Y, Shao Q, Yi J, Wang R (2019) MFEprimer-3.0: quality control for PCR primers. Nucleic Acids Res 47:W610-W613
Wenning R(2020). THE STATE OF WORLD FISHERIES AND AQUACULTURE (SOFIA) 2020 REPORT. Integrated Environmental Assessment and Management, 16: 800–801.
Xiao L, Yang F (2013) Mediating lipid biosynthesis: implications for cardiovascular disease. Trends Cardiovasc Med 23:269–273
Yang Y, Yu H, Li H, Wang A, Yu HY (2016) Effect of high temperature on immune response of grass carp (Ctenopharyngodon idellus) by transcriptome analysis. Fish Shellfish Immunol 58:89–95
Zhao S, Guo S, Zhu Q, Yuan S, Zheng J (2017) Heat-induced oxidative stress and inflammation involve in cadmium pollution history in the spleen of zebrafish. Fish Shellfish Immunol 72:1–8
Zhao T, Ma A, Huang Z, Liu Z, Sun Z, Zhu C, Yang J, Li Y, Wang Q, Qiao X, Chen Z (2021) Transcriptome analysis reveals that high temperatures alter modes of lipid metabolism in juvenile turbot (Scophthalmus maximus) liver. Comp Biochem Physiol d: Genomics Proteomics 40:100887
Zhi Z, Liu Z, Wang LG (2019) Oxidative stress, apoptosis activation and symbiosis disruption in giant clam Tridacna crocea under high temperature. Fish Shellfish Immunol 84:451–457
Zhou Z, Li Y, Zhang G, Ye H, Luo J (2020) Effects of temperature on the transcriptomes of pituitary and liver in Golden Pompano Trachinotus blochii. Fish Physiol Biochem 46:63–73
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This research was supported by China’s Agricultural Research System (CARS-45–03).
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Zhang, W., Xu, X., Li, J. et al. Transcriptomic Analysis of the Liver and Brain in Grass Carp (Ctenopharyngodon idella) Under Heat Stress. Mar Biotechnol 24, 856–870 (2022). https://doi.org/10.1007/s10126-022-10148-6
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DOI: https://doi.org/10.1007/s10126-022-10148-6