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      Transcriptomic response to three osmotic stresses in gills of hybrid tilapia ( Oreochromis mossambicus female × O. urolepis hornorum male)

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          Abstract

          Background

          Osmotic stress is a widespread phenomenon in aquatic animal. The ability to cope with salinity stress and alkaline stress is quite important for the survival of aquatic species under natural conditions. Tilapia is an important commercial euryhaline fish species. What’s more tilapia is a good experimental material for osmotic stress regulation research, but the molecular regulation mechanism underlying different osmotic pressure of tilapia is still unexplored.

          Results

          To elucidate the osmoregulation strategy behind its hyper salinity, alkalinity and salinity-alkalinity stress of tilapia, the transcriptomes of gills in hybrid tilapia ( Oreochromis mossambicus ♀ ×  O. urolepis hornorum ♂) under salinity stress (S: 25‰), alkalinity stress(A: 4‰) and salinity-alkalinity stress (SA: S: 15‰, A: 4‰) were sequenced using deep-sequencing platform Illumina/HiSeq-2000 and differential expression genes (DEGs) were identified. A total of 1958, 1472 and 1315 upregulated and 1824, 1940 and 1735 downregulated genes ( P-value < 0.05) were identified in the salt stress, alkali stress and saline-alkali stress groups, respectively, compared with those in the control group. Furthermore, Kyoto Encyclopedia of Genes and Genomes pathway analyses were conducted in the significant different expression genes. In all significant DEGs, some of the typical genes involved in osmoregulation, including carbonic anhydrase (CA), calcium/calmodulin-dependent protein kinase (CaM kinase) II (CAMK2), aquaporin-1(AQP1), sodium bicarbonate cotransporter (SLC4A4/NBC1), chloride channel 2(CLCN2), sodium/potassium/chloride transporter (SLC12A2 / NKCC1) and other osmoregulation genes were also identified. RNA-seq results were validated with quantitative real-time PCR (qPCR), the 17 random selected genes showed a consistent direction in both RNA-Seq and qPCR analysis, demonstrated that the results of RNA-seq were reliable.

          Conclusions

          The present results would be helpful to elucidate the osmoregulation mechanism of aquatic animals adapting to saline-alkali challenge. This study provides a global overview of gene expression patterns and pathways that related to osmoregulation in hybrid tilapia, and could contribute to a better understanding of the molecular regulation mechanism in different osmotic stresses.

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          Most cited references65

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          The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste.

          The fish gill is a multipurpose organ that, in addition to providing for aquatic gas exchange, plays dominant roles in osmotic and ionic regulation, acid-base regulation, and excretion of nitrogenous wastes. Thus, despite the fact that all fish groups have functional kidneys, the gill epithelium is the site of many processes that are mediated by renal epithelia in terrestrial vertebrates. Indeed, many of the pathways that mediate these processes in mammalian renal epithelial are expressed in the gill, and many of the extrinsic and intrinsic modulators of these processes are also found in fish endocrine tissues and the gill itself. The basic patterns of gill physiology were outlined over a half century ago, but modern immunological and molecular techniques are bringing new insights into this complicated system. Nevertheless, substantial questions about the evolution of these mechanisms and control remain.
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            Ion regulation in fish gills: recent progress in the cellular and molecular mechanisms.

            Fish encounter harsh ionic/osmotic gradients on their aquatic environments, and the mechanisms through which they maintain internal homeostasis are more challenging compared with those of terrestrial vertebrates. Gills are one of the major organs conducting the internal ionic and acid-base regulation, with specialized ionocytes as the major cells carrying out active transport of ions. Exploring the iono/osmoregulatory mechanisms in fish gills, extensive literature proposed several models, with many conflicting or unsolved issues. Recent studies emerged, shedding light on these issues with new opened windows on other aspects, on account of available advanced molecular/cellular physiological approaches and animal models. Respective types of ionocytes and ion transporters, and the relevant regulators for the mechanisms of NaCl secretion, Na(+) uptake/acid secretion/NH(4)(+) excretion, Ca(2+) uptake, and Cl(-) uptake/base secretion, were identified and functionally characterized. These new ideas broadened our understanding of the molecular/cellular mechanisms behind the functional modification/regulation of fish gill ion transport during acute and long-term acclimation to environmental challenges. Moreover, a model for the systematic and local carbohydrate energy supply to gill ionocytes during these acclimation processes was also proposed. These provide powerful platforms to precisely study transport pathways and functional regulation of specific ions, transporters, and ionocytes; however, very few model species were established so far, whereas more efforts are needed in other species.
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              Transcriptomic Responses to Salinity Stress in the Pacific Oyster Crassostrea gigas

              Background Low salinity is one of the main factors limiting the distribution and survival of marine species. As a euryhaline species, the Pacific oyster Crassostrea gigas is considered to be tolerant to relative low salinity. The genes that regulate C. gigas responses to osmotic stress were monitored using the next-generation sequencing of whole transcriptome with samples taken from gills. By RNAseq technology, transcript catalogs of up- and down-regulated genes were generated from the oysters exposed to low and optimal salinity seawater. Methodology/Principal Findings Through Illumina sequencing, we reported 1665 up-regulated transcripts and 1815 down-regulated transcripts. A total of 45771 protein-coding contigs were identified from two groups based on sequence similarities with known proteins. As determined by GO annotation and KEGG pathway mapping, functional annotation of the genes recovered diverse biological functions and processes. The genes that changed expression significantly were highly represented in cellular process and regulation of biological process, intracellular and cell, binding and protein binding according to GO annotation. The results highlighted genes related to osmoregulation, signaling and interactions of osmotic stress response, anti-apoptotic reactions as well as immune response, cell adhesion and communication, cytoskeleton and cell cycle. Conclusions/Significance Through more than 1.5 million sequence reads and the expression data of the two libraries, the study provided some useful insights into signal transduction pathways in oysters and offered a number of candidate genes as potential markers of tolerance to hypoosmotic stress for oysters. In addition, the characterization of C. gigas transcriptome will not only provide a better understanding of the molecular mechanisms about the response to osmotic stress of the oysters, but also facilitate research into biological processes to find underlying physiological adaptations to hypoosmotic shock for marine invertebrates.
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                Author and article information

                Contributors
                zhhping2000@163.com
                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central (London )
                1471-2164
                31 January 2020
                31 January 2020
                2020
                : 21
                : 110
                Affiliations
                [1 ]ISNI 0000 0000 9413 3760, GRID grid.43308.3c, Key Laboratory of Tropical and Subtropical Fishery Resource Application and Cultivation, Ministry of Agriculture and Rural Affairs, Pearl River Fisheries Research Institute, , Chinese Academy of Fishery Science, ; No. 1, Xingyu Road, Liwan District, Guangzhou City, 510380 China
                [2 ]ISNI 0000 0000 9833 2433, GRID grid.412514.7, Shanghai Ocean University, College of Fisheries and Life Science, ; Shanghai, 201306 China
                Author information
                http://orcid.org/0000-0002-6026-4441
                Article
                6512
                10.1186/s12864-020-6512-5
                6995152
                32005144
                29ad448e-d0bb-47d5-8862-cd9611bff2e6
                © The Author(s). 2020

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 31 January 2019
                : 20 January 2020
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100004000, Guangzhou Science and Technology Program key projects;
                Award ID: 201803020034
                Award Recipient :
                Funded by: Central Public-interest Scientific Institution Basal Research Fund, CAFS
                Award ID: 2019KQ - 003
                Award Recipient :
                Funded by: the Guangdong Provincial Special Fund For Modern Agriculture Industry Technology Innovation Teams
                Award ID: 2019KJ150
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: 31001108
                Award Recipient :
                Funded by: National Freshwater Genetic Resource Center
                Award ID: 2019DKA30470
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2020

                Genetics
                tilapia,transcriptome,osmoregulation,osmotic stress
                Genetics
                tilapia, transcriptome, osmoregulation, osmotic stress

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