Volume 37 Issue 3
May  2016
Turn off MathJax
Article Contents
Xin-Jiang LU, Hao ZHANG, Guan-Jun YANG, Ming-Yun LI, Jiong CHEN. Comparative transcriptome analysis on the alteration of gene expression in ayu (Plecoglossus altivelis) larvae associated with salinity change. Zoological Research, 2016, 37(3): 126-135. doi: 10.13918/j.issn.2095-8137.2016.3.126
Citation: Xin-Jiang LU, Hao ZHANG, Guan-Jun YANG, Ming-Yun LI, Jiong CHEN. Comparative transcriptome analysis on the alteration of gene expression in ayu (Plecoglossus altivelis) larvae associated with salinity change. Zoological Research, 2016, 37(3): 126-135. doi: 10.13918/j.issn.2095-8137.2016.3.126

Comparative transcriptome analysis on the alteration of gene expression in ayu (Plecoglossus altivelis) larvae associated with salinity change

doi: 10.13918/j.issn.2095-8137.2016.3.126
Funds:  The project was supported by the Program for the National Natural Science Foundation of China (31201970) and the KC Wong Magna Fund in Ningbo University
More Information
  • Corresponding author: Jiong CHEN
  • Received Date: 2015-12-02
  • Rev Recd Date: 2016-04-29
  • Publish Date: 2016-05-18
  • Ayu (Plecoglossus altivelis) fish, which are an amphidromous species distributed in East Asia, live in brackish water (BW) during their larval stage and in fresh water (FW) during their adult stage. In this study, we found that FW-acclimated ayu larvae exhibited a slower growth ratio compared with that of BW-acclimated larvae. However, the mechanism underlying FW acclimation on growth suppression is poorly known. We employed transcriptome analysis to investigate the differential gene expression of FW acclimation by RNA sequencing. We identified 158 upregulated and 139 downregulated transcripts in FW-acclimated ayu larvae compared with that in BW-acclimated larvae. As determined by Gene Ontology annotation and Kyoto Encyclopedia of Genes and Genomes pathway mapping, functional annotation of the genes covered diverse biological functions and processes, and included neuroendocrinology, osmotic regulation, energy metabolism, and the cytoskeleton. Transcriptional expression of several differentially expressed genes in response to FW acclimation was further confirmed by real-time quantitative PCR. In accordance with transcriptome analysis, iodothyronine deiodinase (ID), pro-opiomelanocortin (POMC), betaine-homocysteine S-methyltransferase 1(BHMT), fructose-bisphosphate aldolase B (aldolase B), tyrosine aminotransferase (TAT), and Na+-K+ ATPase (NKA) were upregulated after FW acclimation. Furthermore, the mRNA expressions of b-type natriuretic peptide (BNP) and transgelin were downregulated after FW acclimation. Our data indicate that FW acclimation reduced the growth rate of ayu larvae, which might result from the expression alteration of genes related to endocrine hormones, energy metabolism, and direct osmoregulation.
  • loading
  • [1]
    Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biology, 11(10):R106.
    Assinder SJ, Stanton JA, Prasad PD. 2009. Transgelin:an actin-binding protein and tumour suppressor. The International Journal of Biochemistry & Cell Biology, 41(3):482-486.
    Avella M, Ducoudret O, Pisani DF, Poujeol P. 2009. Swelling-activated transport of taurine in cultured gill cells of sea bass:physiological adaptation and pavement cell plasticity. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 296(4):R1149-R1160.
    Boeuf G, Payan P. 2001. How should salinity influence fish growth?. Comparative Biochemistry and Physiology Part C:Toxicology & Pharmacology, 130(4):411-423.
    Böhm M, Grässel S. 2012. Role of proopiomelanocortin-derived peptides and their receptors in the osteoarticular system:from basic to translational research. Endocrine Reviews, 33(4):623-651.
    Boivin B, Castonguay M, Audet C, Pavey SA, Dionne M, Bernatchez L. 2015. How does salinity influence habitat selection and growth in juvenile American eels Anguilla rostrata?. Journal of Fish Biology, 86(2):765-784.
    Chen J, Chen Q, Lu XJ, Li CH. 2014. LECT2 improves the outcomes in ayu with Vibrio anguillarum infection via monocytes/macrophages. Fish & Shellfish Immunology, 41(2):586-592.
    Ewing B, Green P. 1998. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Research, 8(3):186-194.
    Gillanders BM, Izzo C, Doubleday ZA, Ye QF. 2015. Partial migration:growth varies between resident and migratory fish. Biology Letters, 11(3):20140850.
    Gonzalez RJ, 2012. The physiology of hyper-salinity tolerance in teleost fish:a review. Journal of Comparative Physiology B, 182(3):321-329.
    Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng QD, Chen ZH, Mauceli E, Hacohen N, Gnirke A, Rhind N, Di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology, 29(7):644-652.
    Hajimoradi M, Hassan ZM, Pourfathollah AA, Daneshmandi S, Pakravan N. 2009. The effect of shark liver oil on the tumor infiltrating lymphocytes and cytokine pattern in mice. Journal of Ethnopharmacology, 126(3):565-570.
    Holmes WN, Donaldson EM. 1969. The body compartments and the distribution of electrolytes. In:Hoar WS, Randall DJ. Fish Physiology. San Diego, CA:Academic Press.
    Huang da W, Sherman BT, Lempicki RA. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols, 4(1):44-57.
    Huang ZA, Chen J, Lu XJ, Shi YH, Li MY. 2011. Alteration on the expression of ayu coagulation factor X gene upon Listonella anguillarum infection. Zoological Research, 32(5):492-498. (in Chinese)
    Hwang PP, Lee TH. 2007. New insights into fish ion regulation and mitochondrion-rich cells. Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology, 148(3):479-497.
    Jorgensen EH, Johnsen HK. 2014. Rhythmic life of the Arctic charr:adaptations to life at the edge. Marine Genomics, 14:71-81.
    Kang CK, Chen YC, Chang CH, Tsai SC, Lee TH. 2015. Seawateracclimation abates cold effects on Na+, K+-ATPase activity in gills of the juvenile milkfish, Chanos chanos. Aquaculture, 446:67-73.
    Langdon JS, Thorpe JE, Roberts RJ. 1984. Effects of cortisol and ACTH on gill Na+/K+-ATPase, SDH and chloride cells in juvenile Atlantic salmon Salmo salar L. Comparative Biochemistry and Physiology Part A:Physiology, 77(1):9-12.
    Li B, Dewey CN. 2011. RSEM:accurate transcript quantification from RNASeq data with or without a reference genome. BMC Bioinformatics, 12(1):323.
    Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT Method. Methods, 25(4):402-408.
    Loretz CA, Pollina C. 2000. Natriuretic peptides in fish physiology. Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology, 125(2):169-187.
    Lu XJ, Chen J, Huang ZA, Shi YH, Wang F. 2010. Proteomic analysis on the alteration of protein expression in gills of ayu (Plecoglossus altivelis) associated with salinity change. Comparative Biochemistry and Physiology Part D:Genomics & Proteomics, 5(3):185-189.
    Lu XJ, Hang XY, Yin L, He YQ, Chen J, Shi YH, Li CH. 2013. Sequencing of the first ayu (Plecoglossus altivelis) macrophage transcriptome and microarray development for investigation the effect of LECT2 on macrophages. Fish & Shellfish Immunology, 34(2):497-504.
    Martinez-Rumayor A, Richards AM, Burnett JC, Januzzi JL. 2008. Biology of the natriuretic peptides. The American Journal of Cardiology, 101(3A):3-8.
    McDowall RM. 1992. Diadromy:origins and definitions of terminology. Copeia, 1992(1):248-251.
    Munnich A, Besmond C, Darquy S, Reach G, Vaulont S, Dreyfus JC, Kahn A. 1985. Dietary and hormonal regulation of aldolase B gene expression. The Journal of Clinical Investigation, 75(3):1045-1052.
    Peter MC. 2011. The role of thyroid hormones in stress response of fish. General and Comparative Endocrinology, 172(2):198-210.
    Ramos EJB, Meguid MM, Campos ACL, Coelho JCU. 2005. Neuropeptide Y, α-melanocyte-stimulating hormone, and monoamines in food intake regulation. Nutrition, 21(2):269-279.
    Sakamoto T, McCormick SD. 2006. Prolactin and growth hormone in fish osmoregulation. General and Cmparative Endocrinology, 147(1):24-30.
    Salem M, Rexroad CE, III, Wang JN, Thorgaard GH, Yao JB. 2010. Characterization of the rainbow trout transcriptome using Sanger and 454-pyrosequencing approaches. BMC Genomics, 11:564.
    Schmieder R, Edwards R. 2011. Quality control and preprocessing of metagenomic datasets. Bioinformatics, 27(6):863-864.
    Schwarz DE, Allen PJ. 2014. Effects of salinity on growth and ion regulation of juvenile alligator gar Atractosteus spatula. Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology, 169:44-50.
    Shimakura S, Kojima K, Nakamachi T, Kageyama H, Uchiyama M, Shioda S, Takahashi A, Matsuda K. 2008. Neuronal interaction between melaninconcentrating hormone- and alpha-melanocyte-stimulating hormonecontaining neurons in the goldfish hypothalamus. Peptides, 29(8):1432-1440.
    Subash Peter MC, Lock RAC, Wendelaar Bonga SE. 2000. Evidence for an osmoregulatory role of thyroid hormones in the freshwater Mozambique tilapia Oreochromis mossambicus. General and Comparative Endocrinology, 120(2):157-167.
    Tian JJ, Lu RH, Ji H, Sun J, Li C, Liu P, Lei CX, Chen LQ, Du ZY. 2015. Comparative analysis of the hepatopancreas transcriptome of grass carp(Ctenopharyngodon idellus) fed with lard oil and fish oil diets. Gene, 565(2):Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology, 28(5):511-515.
    Tseng YC, Hwang PP. 2008. Some insights into energy metabolism for osmoregulation in fish. Comparative Biochemistry and Physiology Part C:Toxicology & Pharmacology, 148(4):419-429.
    Wang S, Furmanek T, Kryvi H, Krossoy C, Totland GK, Grotmol S, Wargelius A. 2014. Transcriptome sequencing of Atlantic salmon (Salmo salar L.) notochord prior to development of the vertebrae provides clues to regulation of positional fate, chordoblast lineage and mineralisation. BMC Genomics, 15:141.
    Weng CF, Chiang CC, Gong HY, Chen MH, Lin CJ, Huang WT, Cheng CY, Hwang PP, Wu JL. 2002. Acute changes in gill Na+-K+-ATPase and creatine kinase in response to salinity changes in the euryhaline teleost, tilapia(Oreochromis mossambicus). Physiological and Biochemical Zoology, 75(1):29-36.
    Xiao SJ, Han ZF, Wang PP, Han F, Liu Y, Li JT, Wang ZY. 2015. Functional marker detection and analysis on a comprehensive transcriptome of large yellow croaker by next generation sequencing. PLoS One, 10(4):e0124432.
    Yada T, Tsuruta T, Sakano H, Yamamoto S, Abe N, Takasawa T, Yogo S, Suzuki T, Iguchi K, Uchida K, Hyodo S. 2010. Changes in prolactin mRNA levels during downstream migration of the amphidromous teleost, ayu Plecoglossus altivelis. General and Comparative Endocrinology, 167(2):261-267.
  • 加载中


    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Article Metrics

    Article views (1754) PDF downloads(1635) Cited by()
    Proportional views


    DownLoad:  Full-Size Img  PowerPoint