Research Progress of Cold Tolerance Mechanism and Functional Genes in Fish

doi:10.13560/j.cnki.biotech.bull.1985.2018-0098

Abstract

Abstract: The ability of fish to adapt to ambient temperature varies broadly,as a result of long-drawn adaptation to habitat environment and evolution. The suffertibility of different fish species to cold stress is the manifestation of the specific expression of genetic information,as well as the reflection of differences in physiological and biochemical performance. Currently,fish physiology responses under low temperature have been in-depth researched while the underlying molecular mechanisms attract increasing interest. The low cost and extensive application of high-throughput sequencing technologies together with bioinformatics analysis allow researchers using omics method to study the metabolic and molecular signaling pathways of the fish under cold stress. The biological molecular mechanisms and related functional genes of fish to cold stress are thus enabled to be further explored. Recent studies prove that many polar fishes have evolved with functional genes gain,loss and large-scale amplification during the long-term adaption to low temperature. The transcription and regulation patterns in fish are conservative to a certain extent while possess obvious specificity in species and tissues under cold stress. Some proteins including antifreeze（glycoprotein）protein,chaperone,metabolic enzyme and transmembrane channel protein are involved in cold-responsive process in fish. However,the corresponding genes characterization and function research remain jagged. This review summarized the molecular mechanisms of fish adaption and tolerance to low temperature from the perspectives of evolution,the genetic expression and epigenetics. Then,cold tolerance related genes were classified and introduced according to their molecular function. Last but not least,we predicted potential research focus in mechanisms,gene mining and application of fish under cold stress,hoping to provide background and reference for researchers and those interested in the field.

Key words: fish, cold stress, genetic evolution, transcriptomics, cold-tolerant genes

LIU Li-li, ZHU Hua, YAN Yan-chun, WANG Xiao-wen, ZHANG Rong, ZHU Jian-ya. Research Progress of Cold Tolerance Mechanism and Functional Genes in Fish[J]. Biotechnology Bulletin, 2018, 34(8): 50-57.

References

[1] Petricorena ZLC, Somero GN.Biochemical adaptations of notothenioid fishes:Comparisons between cold temperate South American and New Zealand species and Antarctic species[J]. Comparative Biochemistry and Physiology, Part A, 2007, 147(3):799-807.
[2] Chen L, Devries AL, Cheng CH.Evolution of antifreeze glycoprotein gene from a trypsinogen gene in Antarctic notothenioid fish[J]. Proceedings of the National Academy of Sciences USA, 1997, 94:3811-3816.
[3] Beers JM, Jayasundara N.Antarctic notothenioid fish:what are the future consequences of ‘losses’ and ‘gains’ acquired during long-term evolution at cold and stable temperatures?[J]. Journal of Experimental Biology, 2015, 218(12):1834-1845.
[4] Giordano D, Russo R, Coppola D, et al.‘Cool’adaptations to cold environments:globins in Notothenioidei(Actynopterygii, Perciformes)[J]. Hydrobiologia, 2015, 761(1):293-312.
[5] Chen Z, Cheng C, Zhang J, et al.Transcriptomic and genomic evolution under constant cold in Antarctic notothenioid fish[J]. Proceedings of the National Academy of Sciences USA, 2008, 105(35):12944-12949.
[6] Shin SC, Ahn D, Kim SJ, et al.The genome sequence of the Antarctic bullhead notothen reveals evolutionary adaptations to a cold environment[J]. Genome Biology, 2014(15):468.
[7] Gracey AY, Fraser EJ, Li WZ, et al.Coping with cold:an integrative, multitissue analysis of the transcriptome of a poikilothermic vertebrate[J]. Proceedings of the National Academy of Sciences USA, 2004, 101(48):16970-16975.
[8] Shin SC, Kim SJ, Lee JK, et al.Transcriptomics and comparative analysis of three Antarctic notothenioid fishes[J]. PLoS One, 2012, 7(8):e437628.
[9] Windisch HS, Frickenhaus S, John U, et al.Stress response or beneficial temperature acclimation:transcriptomic signatures in Antarctic fish(Pachycara brachycephalum)[J]. Molecular Ecology, 2014, 23(14):3469-3482.
[10] Long Y, Li L, Li Q, et al.Transcriptomic characterization of temperature stress responses in larval zebrafish[J]. PLoS One, 2012, 7(5):e37209.
[11] 王金凤, 胡鹏, 牛虹博, 等. 低温胁迫对鱼类PI3K/AKT/GSK-3β信号通路的影响[J]. 生物学杂志, 2016(6):24-28.
[12] 何金钊, 陈子桂, 陈诏, 等. 三种品系不同规格红罗非鱼的耐寒性能评价[J]. 淡水渔业, 2017(3):79-83.
[13] Scott GR, Johnston IA.Temperature during embryonic development has persistent effects on thermal acclimation capacity in zebrafish.[J]. Proceedings of the National Academy of Sciences USA, 2012, 109(35):14247-14252.
[14] Qian B, Xue L.Liver transcriptome sequencing and de novo annotation of the large yellow croaker(Larimichthy crocea)under heat and cold stress[J]. Marine Genomics, 2016, 25:95-102.
[15] Mininni AN, Milan M, Ferraresso S, et al.Liver transcriptome analysis in gilthead sea bream upon exposure to low temperature
[J]. BMC Genomics, 2014, 1(15):765.
[16] Rebl A, Verleih M, Köbis JM, et al.Transcriptome profiling of gill Tissue in regionally rred and rlobally farmed rainbow trout strains reveals rifferent strategies for coping with thermal stress[J]. Marine Biotechnology, 2013, 15(4):445-460.
[17] Gerdol M, Buonocore F, Scapigliati G, et al.Analysis and characterization of the head kidney transcriptome from the Antarctic fish Trematomus bernacchii(Teleostea, Notothenioidea):A source for immune relevant genes[J]. Marine Genomics, 2015, 20:13-15.
[18] Papetti C, Harms L, Windisch HS, et al.A first insight into the spleen transcriptome of the notothenioid fish Lepidonotothen nudifrons:Resource description and functional overview[J]. Marine Genomics, 2015, 24:237-239.
[19] Díaz N, Piferrer F.Lasting effects of early exposure to temperature on the gonadal transcriptome at the time of sex differentiation in the European sea bass, a fish with mixed genetic and environmental sex determination[J]. BMC Genomics, 2015, 16:679.
[20] Małachowicz M, Kijewska A, Wenne R.Transcriptome analysis of gill tissue of Atlantic cod Gadus morhua L. from the Baltic Sea[J]. Marine Genomics, 2015, 23:37-40.
[21] Hung IC, Hsiao YC, Sun HS, et al.MicroRNAs regulate gene plasticity during cold shock in zebrafish larvae[J]. BMC Genomics, 2016(17):922.
[22] Long Y, Song G, Yan J, et al.Transcriptomic characterization of cold acclimation in larval zebrafish[J]. BMC Genomics, 2013
(14):612.
[23] Hu P, Liu M, Liu Y, et al.Transcriptome comparison reveals a genetic network regulating the lower temperature limit in fish[J]. Scientific Reports, 2016(6):28952.
[24] Hu P, Liu M, Zhang D, et al.Global identification of the genetic networks and cis-regulatory elements of the cold response in zebrafish[J]. Nucleic Acids Research, 2015, 43(19):9198-9213.
[25] 朱华平, 卢迈新, 黄樟翰, 等. 低温对罗非鱼基因组DNA甲基化的影响[J]. 水产学报, 2013(10):1460-1467.
[26] Duman JG.Animal ice-binding(antifreeze)proteins and glycolipids:an overview with emphasis on physiological function[J]. Journal of Experimental Biology, 2015, 218(Pt 12):1846-1855.
[27] Evans CW, Hellman L, Middleditch M, et al.Synthesis and recycling of antifreeze glycoproteins in polar fishes[J]. Antarctic Science, 2012, 24(3):259-268.
[28] Hobbs KD.The effect of antifreeze proteins on the cold tolerance of goldfish(Carassius auratus L.)[D]. Ottawa:Memo rial University of Newfoundland, 1999.
[29] Fletcher GL, Shears MA, Yaskowiak ES, et al.Gene transfer:potential to enhance the genome of Atlantic salmon for aquaculture[J]. Australian Journal of Experimental Agriculture, 2004, 44(11):1095.
[30] Hew C, Poon R, Xiong F, et al.Liver-specific and seasonal expression of transgenic Atlantic salmon harboring the winter flounder antifreeze protein gene[J]. Transgenic Research, 1999, 8:405-414.
[31] Evans RP, Fletcher GL.Type I antifreeze proteins expressed in snailfish skin are identical to their plasma counterparts[J]. FEBS J, 2005(272):5327-5336.
[32] Hobbs RS, Fletcher GL.Tissue specific expression of antifreeze protein and growth hormone transgenes driven by the ocean pout(Macrozoarces americanus)antifreeze protein OP5a gene promoter in Atlantic salmon(Salmo salar)[J]. Transgenic Research, 2008, 17(1):33-45.
[33] Bagis H, Aktoprakligil D, Mercan HO, et al.Stable transmission and transcription of newfoundland ocean pout type III fish antifreeze protein(AFP)gene in transgenic mice and hypothermic storage of transgenic ovary and testis[J]. Molecular Reproduction and Development, 2006, 73(11):1404-1411.
[34] Place SP, Hofmann GE.Constitutive expression of a stress-inducible heat shock protein gene, hsp70, in phylogenetically distant Antarctic fish[J]. Polar Biology, 2005, 28(4):261-267.
[35] Teigen LE, Orczewska JI, Mclaughlin J, et al.Cold acclimation increases levels of some heat shock protein and sirtuin isoforms in threespine stickleback[J]. Comparative Biochemistry and Physiology, Part A, 2015, 2015(188):139-147.
[36] Peng G, Zhao W, Shi Z, et al.Cloning HSP70 and HSP90 genes of kaluga(Huso dauricus)and the effects of temperature and salinity stress on their gene expression[J]. Cell Stress and Chaperones, 2016, 21(2):349-359.
[37] Giri SS, Sen SS, Sukumaran V.Role of HSP70 in cytoplasm protection against thermal stress in rohu, Labeo rohita[J]. Fish & Shellfish Immunology, 2014, 41(2):294-299.
[38] Chagoyen M, Carrascosa JL, Pazos F, et al.Molecular determinants of the ATP hydrolysis asymmetry of the CCT chaperonin complex[J]. Proteins, 2014, 82(5):703-707.
[39] Shimon L, Hynes GM, Mccormack EA, et al.ATP-induced allostery in the eukaryotic chaperonin CCT is abolished by the mutation G345D in CCT4 that renders yeast temperature-sensitive for growth[J]. Journal of Molecular Biology, 2008, 377(2):469-477.
[40] 谢建丽, 勇林, 兰曾, 等. 尼罗罗非鱼TCP-1- beta和TCP-1- eta的分子特征及其低温诱导表达[J]. 水生生物学报, 2012, 36(4):634-638.
[41] He YF, Wang LM, Zhu WB, et al.Effects of salinity on cold tolerance of Malaysian red tilapia[J]. Aquaculture International, 2017, 2017(25):777-792.
[42] Kaneko T, Kibayashi K.Mild hypothermia facilitates the expression of cold-inducible RNA-binding protein and heat shock protein 70. 1 in mouse brain[J]. Brain Research, 2012, 1466:128-136.
[43] Juan Y, Wu H, Xie W, et al.Cold-inducible RNA-binding protein mediates airway inflammation and mucus hypersecretion through a post-transcriptional regulatory mechanism under cold stress[J]. International Journal of Biochemistry & Cell Biology, 2016, 78:335-348.
[44] Leong JS, Jantzen SG, von Schalburg KR, et al. Salmo salar and Esox lucius full-length cDNA sequences reveal changes in evolutionary pressures on a post-tetraploidization genome[J]. BMC Genomics, 2010, 11(1):279.
[45] 胡金伟, 尤锋, 王倩, 等. 牙鲆耐寒相关基因CIRP、HMGB1的克隆及表达特征分析[J]. 海洋科学, 2015(1):29-38.
[46] 苗亮, 李明云, 陈莹莹, 等. 大黄鱼冷诱导结合蛋白(CIRP)基因cDNA克隆及低温胁迫对其时空表达的影响[J]. 水产学报, 2017, 41(4):481-489.
[47] Zhang H, Zhang X, Wang Z, et al.Effects of dietary energy level on lipid metabolism-related gene expression in subcutaneous adipose tissue of Yellow breed × Simmental cattle[J]. Animal Science Journal, 2015, 86(4):392-400.
[48] Hsieh SL, Kuo CM.Stearoyl-CoA desaturase expression and fatty acid composition in milkfish(Chanos chanos)and grass carp(Ctenopharyngodon idella)during cold acclimation[J]. Comparative Biochemistry and Physiology, Part B. 2005, 141(1):95-101.
[49] Zerai DB, Fitzsimmons KM, Collier RJ.Transcriptional response of delta-9-desaturase gene to acute and chronic cold Stress in Nile tilapia, Oreochromis niloticus[J]. Journal of the World Aquaculture Society, 2010, 41(5):800-806.
[50] Tiku PE, Gracey AY, Macartney AI, et al.Cold-induced expression of delta 9-desaturase in carp by transcriptional and posttranslational mechanisms[J]. Science, 1996, 271(5250):815-818.
[51] Xu H, Zhang DL, Yu DH, et al.Molecular cloning and expression analysis of scd1 gene from large yellow croaker Larimichthys crocea under cold stress[J]. Gene, 2015, 568(1):100-108.
[52] Heinemann FS, Ozols J.Stearoyl-CoA desaturase, a short-lived protein of endoplasmic reticulum with multiple control mechanisms[J]. Prostaglandins, Leukotrienes and Essential Fatty Acids, 2003, 68(2):123-133.
[53] 刘明丽, 王金凤, 张东, 等. 鳞头犬牙南极鱼atp6v0c基因在HeLa细胞中抗寒功能的研究[J]. 大连海洋大学学报, 2016(1):7-12.
[54] Vergauwen L, Benoot D, Blust R, et al.Long-term warm or cold acclimation elicits a specific transcriptional response and affects energy metabolism in zebrafish[J]. Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology, 2010, 157(2):149-157.
[55] 王倩, 尤锋, 辛梦娇, 等. 斑马鱼GSTM单核苷酸多态性与低温耐受性的相关分析[J]. 海洋科学, 2015(1):1-7.
[56] Maksimov EG, Mironov KS, Trofimova MS, et al.Membrane fluidity controls redox-regulated cold stress responses in cyanobacteria[J]. Photosynthesis Research, 2017, 133(1-3):215-223.
[57] Buemi M, Floccari F, Di Pasquale G, et al.AQP1 in red blood cells of uremic patients during hemodialytic treatment[J]. Nephron, 2002, 92(4):846-852.
[58] Knepper MA.The aquaporin family of molecular water channels[J]. Proceedings of the National Academy of Sciences USA, 1994, 91(14):6255-6258.
[59] 朱华平, 刘玉姣, 刘志刚, 等. 低温胁迫对尼罗罗非鱼水通道蛋白基因(AQP1)表达的影响[J]. 中国水产科学, 2014(6):1181-1189.
[60] Zbikowska HM.Fish can be first - advances in fish transgenesis for commercial applications[J]. Transgenic Research, 2003, 12(4):379-389.
[61] Wang JH.A comprehensive evaluation of the effects and mechanisms of antifreeze proteins during low-temperature preservation[J]. Cryobiology, 2000, 41(1):1-9.
[62] Bang J, Lee J, Murugan R, et al.Antifreeze peptides and glycopeptides, and their derivatives:potential uses in biotechnology[J]. Marine Drugs, 2013, 11(6):2013-2041.
[63] Wu S, Hwang P, Hew C, et al.Effect of antifreeze protein on cold tolerance in juvenile tilapia(Oreochromis mossambicus Peters)and milkfish(Chanos chanos Forsskal)[J]. Zoological Studies, 1998, 1(37):39-44.
[64] Luo S, Wang W, Cai L, et al.Effects of a Dissostichus mawsoni-CaM recombinant proteins feed additive on the juvenile orange-spotted grouper(Epinephelus coioides)under the acute low temperature challenge[J]. Fish Physiology and Biochemistry, 2015, 41(5):1345-1358.