Cite this paper:
CUI Wenxiao, MA Aijun, HUANG Zhihui, WANG Xin'an, SUN Zhibin, LIU Zhifeng, ZHANG Wei, YANG Jingkun, ZHANG Jinsheng, QU Jiangbo. Transcriptomic analysis reveals putative osmoregulation mechanisms in the kidney of euryhaline turbot Scophthalmus maximus responded to hypo-saline seawater[J]. HaiyangYuHuZhao, 2020, 38(2): 467-479

Transcriptomic analysis reveals putative osmoregulation mechanisms in the kidney of euryhaline turbot Scophthalmus maximus responded to hypo-saline seawater

CUI Wenxiao1,2,3, MA Aijun2,3, HUANG Zhihui2,3, WANG Xin'an2,3, SUN Zhibin2,3, LIU Zhifeng2,3, ZHANG Wei2,3, YANG Jingkun2,3, ZHANG Jinsheng2,3, QU Jiangbo4
1 College of Fisheries and Life Science, Shanghai Ocean University, Ministry of Education, Shanghai 201306, China;
2 Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China;
3 Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences; Shandong Key Laboratory of Marine Fisheries Biotechnology and Genetic Breeding; Qingdao Key Laboratory for Marine Fish Breeding and Biotechnology, Qingdao 266071, China;
4 Yantai Tianyuan Aquatic Limited Corporation, Yantai 264003, China
Abstract:
Turbot harbor a relatively remarkable ability to adapt to opposing osmotic challenges and are an excellent model species to study the physiological adaptations of flounder associated with osmoregulatory plasticity. The kidney transcriptome of turbot treated 24 h in water of hypo-salinity (salinity 5) and seawater (salinity 30) was sequenced and characterized. In silico analysis indicated that all unigenes had significant hits in seven databases. The functional annotation analysis of the transcriptome showed that the immune system and biological processes associated with digestion, absorption, and metabolism played an important role in the osmoregulation of turbot in response to hypo-salinity. Analysis of biological processes associated with inorganic channels and transporters indicated that mineral absorption and bile secretion contributed to iono-osmoregulation resulting in cell volume regulation and cell phenotypic plasticity. Moreover, we analyzed and predicted the mechanisms of canonical signaling transduction. Biological processes involved in renin secretion, ECM-receptor interaction, adherens junction, and focal adhesion played an important role in the plasticity phenotype in hypo-stress, while the signal transduction network composed of the MAPK signaling pathway and PI3K-Akt signaling pathway with GABAergic synapse, worked in hypoosmoregulation signal transduction in the turbot. In addition, analysis of the tissue specificity of targeted gene expression using qPCR during salinity stress was carried out. The results showed that the kidney, gill, and spleen were vital regulating organs of osmotic pressure, and the osmoregulation pattern of euryhaline fish differed among species.
Key words:    osmoregulation mechanisms|Scophthalmus maximus|hypo-saline|signal transduction|cell volume regulation|gene expression   
Received: 2019-03-08   Revised: 2019-07-10
Tools
PDF (1180 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by CUI Wenxiao
Articles by MA Aijun
Articles by HUANG Zhihui
Articles by WANG Xin'an
Articles by SUN Zhibin
Articles by LIU Zhifeng
Articles by ZHANG Wei
Articles by YANG Jingkun
Articles by ZHANG Jinsheng
Articles by QU Jiangbo
References:
Alves-Costa F A, Denovan-Wright E M, Thisse C, Thisse B, Wright J M. 2008. Spatio-temporal distribution of fatty acid-binding protein 6 (fabp6) gene transcripts in the developing and adult zebrafish (Danio rerio). FEBS J., 275(13):3 325-3 334.
Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biol., 11(10):R106, https://doi.org/10.1186/gb-2010-11-10-r106.
Arden K C. 2004. FoxO:linking new signaling pathways. Mol.Cell, 14(4):416-418.
Babey M, Kopp P, Robertson G L. 2011. Familial forms of diabetes insipidus:clinical and molecular characteristics.Nat. Rev. Endocrinol., 7(12):701-714.
Bakir B, Sezerman O U. 2006. Functional classification of G-protein coupled receptors, based on their specific ligand coupling patterns. In:Rothlauf F, Branke J, Cagnoni S, Costa E, Cotta C, Drechsler R, Lutton E, Machado P, Moore J H, Romero J, Smith G D, Squillero G, Takagi H eds. Applications of Evolutionary Computing. Springer, Berlin, Heidelberg. p.1-12.
Beyenbach K W. 1986. Secretory NaCl and volume flow in renal tubules. Am. J. Physiol., 250(5):R753-R763.
Beyenbach K W. 2004. Kidneys sans glomeruli. Am. J. Physiol.Renal Physiol., 286(5):F811-F827.
Bhattacharya S. 2004. Handbook of cell signaling. J. Anat., 205(1):77.
Bonni A, Sun Y, Nadal-Vicens M, Bhatt A, Frank D A, Rozovsky I, Stahl N, Yancopoulos G D, Greenberg M E. 1997. Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway. Science, 278(5337):477-483.
Brennan R S, Galvez F, Whitehead A. 2015. Reciprocal osmotic challenges reveal mechanisms of divergence in phenotypic plasticity in the killifish Fundulus heteroclitus.J. Exp. Biol., 218(8):1 212-1 222.
Cutler C P, Cramb G. 2002. Branchial expression of an aquaporin 3 (AQP-3) homologue is downregulated in the European eel Anguilla anguilla following seawater acclimation. J. Exp. Biol., 205(17):2 643-2 651.
Cutler C P, Philips C, Hazon N, Cramb G. 2009. Aquaporin 8(AQP8) intestinal mRNA expression increases in response to salinity acclimation in yellow and silver European eels(Anguilla anguilla). Comp. Biochem. Physiol. A Mol.Integr. Physiol., 153(S2):S78.
Dietz C, Stiller K T, Griese M, Schulz C, Susenbeth A. 2013.Influence of salinity on energy metabolism in juvenile turbot, Psetta maxima (L.). Aquacult. Nutr., 19(S1):135-150.
Edwards S L, Marshall W S. 2012. Principles and patterns of osmoregulation and euryhalinity in fishes. Fish Physiol., 32:1-44.
Ehebauer M, Hayward P, Martinez-Arias A. 2006. Notch signaling pathway. Sci. STKE, 2006(364):cm7.
Farrell A P. 2011. Encyclopedia of Fish Physiology:from Genome to Environment. Academic Press, San Diego.
Fielding C J, Shore V G, Fielding P E. 1972. A protein cofactor of lecithin:cholesterol acyltransferase. Biochem. Biophys.Res. Commun., 46(4):1 493-1 498.
Fiol D F, Kültz D. 2007. Osmotic stress sensing and signaling in fishes. FEBS J., 274(22):5 790-5 798.
Fouchs A, Ollivier H, Haond C, Roy S, Calvès P, PichavantRafini K. 2010. Activation of the MAPKs ERK1/2 by cell swelling in turbot hepatocytes. Biol. Cell, 102(8):447-456.
Götz S, García-Gómez J M, Terol J, Williams T D, Nagaraj S H, Nueda M J, Robles M, Talón M, Dopazo J, Conesa A. 2008. High-throughput functional annotation and data mining with the blast2go suite. Nucleic Acids Res., 36(10):3 420-3 435.
Goward C R, Nicholls D J. 1994. Malate dehydrogenase:a model for structure, evolution, and catalysis. Protein Sci., 3(10):1 883-1 888.
Grabherr M G, Haas B J, Yassour M, Levin J Z, Thompson D A, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q D, Chen Z H, Mauceli E, Hacohen N, Gnirke A, Rhind N, Di Palma F, Birren B W, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A. 2011. Trinity:reconstructing a fulllength transcriptome without a genome from RNA-Seq data. Nat. Biotechnol., 29(7):644-652.
Grant S, Qiao L, Dent P. 2002. Roles of ERBB family receptor tyrosine kinases, and downstream signaling pathways, in the control of cell growth and survival. Front Biosci., 7:d376-389.
Hoffmann E K, Lambert I H, Pedersen S F. 2009. Physiology of cell volume regulation in vertebrates. Physiol. Rev., 89(1):193-277.
Hummel C S, Lu C, Loo D D F, Hirayama B A, Voss A A, Wright E M. 2011. Glucose transport by human renal Na+/D-glucose cotransporters SGLT1 and SGLT2. Am. J.Physiol. Cell Physiol., 300(1):C14-C21.
Imsland A K, Foss A, Gunnarsson S, Berntssen M H G, FitzGerald R, Bonga S W, v Ham E, Nævdal G, Stefansson S O. 2001. The interaction of temperature and salinity on growth and food conversion in juvenile turbot(Scophthalmus maximus). Aquaculture, 198(3-4):353-367.
Inokuchi M, Hiroi J, Watanabe S, Lee K M, Kaneko T. 2008.Gene expression and morphological localization of NHE3, NCC and NKCC1a in branchial mitochondria-rich cells of mozambique tilapia (Oreochromis mossambicus)acclimated to a wide range of salinities. Comp. Biochem.Physiol. A Mol. Integr. Physiol., 151(2):151-158.
Kalujnaia S, McWilliam I S, Zaguinaiko V A, Feilen A L, Nicholson J, Hazon N, Cutler C P, Cramb G. 2007.Transcriptomic approach to the study of osmoregulation in the European eel Anguilla anguilla. Physiol. Genomics, 31(3):385-401.
Karaica D, Breljak D, Brzica H, Lončar J, Herak-Kramberger C M, Micek V, Vrhovac I, Ivković D J, Mihaljević I, Marić P, Smital T, Burckhardt B C, Burckhardt G, Sabolić I. 2015. CFEX (slc26a6) in rat kidneys, liver, and small intestine in an experimental model of oxalate nephrolitiasis. Arch. Ind. Hyg. Toxicol., 66(3):228.
Kasprowicz A. 2011. Osmosensing. In:Wojtaszek P ed.Mechanical Integration of Plant Cells and Plants. Springer, Berlin, Heidelberg. p.225-240.
Kültz D, Avila K. 2001. Mitogen-activated protein kinases are in vivo transducers of osmosensory signals in fish gill cells. Comp. Biochem. Physiol. B Biochem. Mol. Biol., 129(4):821-829.
Kültz D, Burg M. 1998. Evolution of osmotic stress signaling via MAP kinase cascades. J. Exp. Biol., 201(22):3 015-3 021.
Kültz D. 2015. Physiological mechanisms used by fish to cope with salinity stress. J. Exp. Biol., 218(12):1 907-1 914.
Kurt B, Kurtz L, Sequeira-Lopez M L, Gomez R A, Willecke K, Wagner C, Kurtz A. 2011. Reciprocal expression of connexin 40 and 45 during phenotypical changes in reninsecreting cells. Am. J. Physiol. Renal Physiol., 300(3):F743-F748.
Kurtz A, Wagner C. 1999. Cellular control of renin secretion.J. Exp. Biol., 202(3):219-225.
Lam S H, Lui E Y, Li Z J, Cai S J, Sung W K, Mathavan S, Lam T J, Ip Y K. 2014. Differential transcriptomic analyses revealed genes and signaling pathways involved in ionoosmoregulation and cellular remodeling in the gills of euryhaline mozambique tilapia, Oreochromis mossambicus.BMC Genomics, 15(1):921.
Lee K M, Kaneko T, Katoh F, Aida K. 2006. Prolactin gene expression and gill chloride cell activity in fugu Takifugu rubripes exposed to a hypoosmotic environment. Gen.Comp. Endocrinol., 149(3):285-293.
Li B, Dewey C N. 2011. Rsem:accurate transcript quantification from RNA-Seq data with or without a reference genome.BMC Bioinformatics, 12:323.
Mao X Z, Cai T, Olyarchuk J G, Wei L P. 2005. Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary.Bioinformatics, 21(19):3 787-3 793.
Marshall W, Grosell M. 2005. Ion transport, osmoregulation, and acid-base balance. In:Evans D H, Claiborne J B eds.The Physiology of Fishes. 3rd ed. CRC Press, Boca Raton.p.177-230.
Narnaware B Y K, Kelly S P, Woo N Y S. 2000. Effect of salinity and ration size on macrophage phagocytosis in juvenile black sea bream (Mylio macrocephalus). J. Appl.Ichthyol., 16(2):86-88.
Nishimoto G, Sasaki G, Yaoita E, Nameta M, Li H, Furuse K, Fujinaka H, Yoshida Y, Mitsudome A, Yamamoto T. 2007.Molecular characterization of water-selective AQP (EbAQP4)in hagfish:insight into ancestral origin of AQP4. Am. J.Physiol. Regul. Integr. Comp. Physiol., 292(1):R644-R651.
Oelkers P, Kirby L C, Heubi J E, Dawson P A. 1997. Primary bile acid malabsorption caused by mutations in the ileal sodium-dependent bile acid transporter gene (SLC10A2).J. Clin. Invest., 99(8):1 880-1 887.
Pereiro P, Balseiro P, Romero A, Dios S, Forn-Cuni G, Fuste B, Planas J V, Beltran S, Novoa B, Figueras A. 2012. Highthroughput sequence analysis of turbot (Scophthalmus maximus) transcriptome using 454-pyrosequencing for the discovery of antiviral immune genes. PLoS One, 7(5):e35369.
Pickford G E, Phillips J G. 1959. Prolactin, a factor in promoting survival of hypophysectomized killifish in fresh water. Science, 130(3373):454-455.
Prodocimo, V, Souza C F, Pessini C, Fernandes L C, Freire C A. 2008. Metabolic substrates are not mobilized from the osmoregulatory organs (gills and kidney) of the estuarine pufferfishes Sphoeroides greeleyi and S. testudineus upon short-term salinity reduction. Neotrop. Ichthyol., 6(4):613-620, https://doi.org/10.1590/S1679-62252008000400009.
Rappolee D A, Armant D R. 2009. Cell signaling. In:Krawetz S ed. Bioinformatics for Systems Biology. Humana Press, New York. p.89-104.
Schmittgen T D, Zakrajsek B A. 2000. Effect of experimental treatment on housekeeping gene expression:validation by real-time, quantitative RT-PCR. J. Biochem. Biophys.Methods, 46(1-2):69-81.
Shibata Y, Kumai M, Nishii K, Nakamura K. 2001. Diversity and molecular anatomy of gap junctions. Med. Electron Microsc., 34(3):153-159.
Tang X M, Sui Z, Tian J B, Wang G F. 2006. Effects of salinity on metabolic rate of juvenile turbot (Scophamus maximus). South China Fish. Sci., 2(4):54-58. (in Chinese with English abstract)
Trapnell C, Williams B A, Pertea G, Mortazavi A, Kwan G, Van Baren M J, Salzberg S L, Wold B J, Pachter L. 2010.
Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol., 28(5):511-515.
Vojtek A B, Der C J. 1998. Increasing complexity of the Ras signaling pathway. J. Biol. Chem., 273(32):19 925-19 928.
Xu Z Z, Gan L, Li T Y, Xu C, Chen K, Wang X D, Qin J G, Chen L Q, Li E C. 2015. Transcriptome profiling and molecular pathway analysis of genes in association with salinity adaptation in Nile tilapia Oreochromis niloticus.PLoS One, 10(8):e0136506.
Young M D, Wakefield M J, Smyth G K, Oshlack A. 2010.Gene ontology analysis for RNA-seq:accounting for selection bias. Genome Biol., 11(2):R14.