HAO Tian, TANG Xianhu, JIANG Shouwen, WU Zhichao, XU Qianghua. Transcriptome comparative analysis of liver tissues of three plateau Schizothoracinae fish species[J]. South China Fisheries Science, 2024, 20(3): 92-100. DOI: 10.12131/20230204
Citation: HAO Tian, TANG Xianhu, JIANG Shouwen, WU Zhichao, XU Qianghua. Transcriptome comparative analysis of liver tissues of three plateau Schizothoracinae fish species[J]. South China Fisheries Science, 2024, 20(3): 92-100. DOI: 10.12131/20230204

Transcriptome comparative analysis of liver tissues of three plateau Schizothoracinae fish species

More Information
  • Received Date: October 23, 2023
  • Revised Date: February 25, 2024
  • Accepted Date: March 20, 2024
  • Available Online: March 31, 2024
  • The extreme environmental features of low temperature and low oxygen on the Qinghai-Tibet Plateau provide a natural laboratory for the evolution of biological adaptability. The subfamily Schizothoracinae are widely distributed in the water bodies surrounding the Qinghai-Tibet Plateau, and has adapted to the unique highland environment through long-term evolutionary process. In this study, we focused on two high-altitude (>3 000 m) Schizothoracinae fish species (Schizothorax macropogon and S. waltoni) and one low-altitude (<1 000 m) ancestral Schizothoracinae fish species (S. prenanti) to conduct a transcriptome sequencing comparative analysis regarding the liver tissues, which is the main energy metabolism organ in fish species. This analysis reveals the key signaling pathways involved in the adaptation of highland Schizothoracinae to high-altitude environment. Comparing the liver transcriptomes of high-altitude with those of low-altitude Schizothoracinae, we identified 106 genes that shared differential changes in expression between the two high-altitude species. Among these genes, 66 were upregulated and 40 were downregulated. GO and KEGG enrichment analysis reveals that the most important pathways for high-altitude adaptation in Schizothoracinae include oxidation-reduction processes, pathways related to blood development, amino acid metabolism and steroid biosynthesis. Among them, genes related to oxidation-reduction and blood development (faxdc2, cpox, cyp51, and NADH-cytochrome b5 reductase 2) with high expression levels might play a crucial role in high-altitude adaptation. The study provides new insights into the molecular mechanisms underlying the adaptation of fish to high-altitude environment.

  • [1]
    李廷栋. 青藏高原隆升的过程和机制[J]. 地球学报: 中国地质科学院院报, 1995(1): 1-9.
    [2]
    高红山, 潘保田, 李吉均, 等. 青藏高原隆升过程与环境变化[J]. 青岛大学学报 (工程技术版), 2004(4): 40-47.
    [3]
    CAO Y B, CHEN X Q, WANG S, et al. Evolution and regulation of the downstream gene of hypoxia-inducible factor-1α in naked carp (Gymnocypris przewalskii) from Lake Qinghai, China[J]. J Mol Evol, 2008, 67(5): 570-580. doi: 10.1007/s00239-008-9175-4
    [4]
    FORTELIUS M, ERONEN J T, KAYA F, et al. Evolution of neogene mammals in Eurasia: environmental forcing and biotic interactions[J]. ANNU REV EARTH PL SC, 2014, 42: 579-604. doi: 10.1146/annurev-earth-050212-124030
    [5]
    西藏自治区水产局. 西藏鱼类及其资源[M]. 北京: 中国农业出版社, 1995: 10-13.
    [6]
    LI G N, SUN S K, LIU H T, et al. Schizothorax prenanti swimming behavior in response to different flow patterns in vertical slot fishways with different slot positions[J]. Sci Total Environ, 2021, 754: 142142. doi: 10.1016/j.scitotenv.2020.142142
    [7]
    SAAD M J, SANTOS A, PRADA P O. Linking gut microbiota and inflammation to obesity and insulin resistance[J]. Physiol Behav, 2016, 31(4): 283-293.
    [8]
    王维政, 曾泽乾, 黄建盛, 等. 低氧胁迫对军曹鱼幼鱼抗氧化、免疫能力及能量代谢的影响[J]. 海洋学报, 2020, 40(9): 12-18.
    [9]
    MA X Y, QIANG J, HE J, et al. Changes in the physiological parameters, fatty acid metabolism, and SCD activity and expression in juvenile GIFT tilapia (Oreochromis niloticus) reared at three different temperatures[J]. Fish Physiol Biochem, 2015, 41(4): 937-950. doi: 10.1007/s10695-015-0059-4
    [10]
    COLLINS J E, WHITE S, SEARLE S M J, et al. Incorporating RNA-seq data into the zebrafish Ensembl genebuild[J]. Genome Res, 2012, 22(10): 2067-2078. doi: 10.1101/gr.137901.112
    [11]
    LIU S K, ZHANG Y, ZHOU Z C, et al. Efficient assembly and annotation of the transcriptome of catfish by RNA-Seq analysis of a doubled haploid homozygote[J]. BMC Genom, 2012,13(1): 595.
    [12]
    ZHOU Y, FU H C, WANG Y Y, et al. The dynamic immune responses of Mandarin fish (Siniperca chuatsi) to ISKNV in early infection based on full-length transcriptome analysis and weighted gene co-expression network analysis[J]. Fish Shellfish Immunol, 2022, 122: 191-205. doi: 10.1016/j.fsi.2022.02.017
    [13]
    车荣波. 基于转录组数据的鮸鱼分子标记筛选及基因差异表达分析[D]. 舟山: 浙江海洋学院, 2015: 15-16.
    [14]
    邓素贞, 韩兆方, 陈小明, 等. 大黄鱼高温适应的转录组学分析[J]. 水产学报, 2018, 42(11): 1673-1683.
    [15]
    BARAT A, SAHOO P K, KUMAR R, et al. Transcriptional response to heat shock in liver of snow trout (Schizothorax richardsonii): a vulnerable Himalayan Cyprinid fish[J]. Siam J Appl Dyn Syst, 2017, 16(2): 203-213.
    [16]
    CHEN X, FENG W R, YAN F Y, et al. Alteration of antioxidant status, glucose metabolism, and hypoxia signal pathway in Eirocheir sinensis after acute hypoxic stress and reoxygenation[J]. Comp Biochem Physiol C, 2023, 268: 109604.
    [17]
    孔庆辉, 刘海平, 刘锁珠, 等. 巨须裂腹鱼水霉菌的分离鉴定及其对脾脏转录组的影响[J]. 水产学报, 2023, 47(8): 135-144.
    [18]
    BOLGER A M, MARC L, BJOERN U. Trimmomatic: a flexible trimmer for Illumina sequence data[J]. Bioinformatics, 2014(15): 2114-2120.
    [19]
    TRAPNELL C, WILLIAMS B A, PERTEA G, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation[J]. NBT, 2010, 28(5): 511-515.
    [20]
    ROBINSON M D, McCARTHY D J, SMYTH G K. edgeR: a bioconductor package for differential expression analysis of digital gene expression data[J]. Bioinformatics, 2010, 26(1): 139-140. doi: 10.1093/bioinformatics/btp616
    [21]
    LYN D C. Dead zones spreading in world oceans[J]. Biosci J, 2005(7): 552-557.
    [22]
    WANG Y, YANG L D, WU B, et al. Transcriptome analysis of the plateau fish (Triplophysa dalaica): implications for adaptation to hypoxia in fishes[J]. Gene, 2015, 565(2): 211-220. doi: 10.1016/j.gene.2015.04.023
    [23]
    MA X H, DAI W, KANG J L, et al. Comprehensive transcriptome analysis of six catfish species from an altitude gradient reveals adaptive evolution in Tibetan fishes[J]. G3, 2016, 6(1): 141-148. doi: 10.1534/g3.115.024448
    [24]
    YANG L D, WANG Y, ZHANG Z L, et al. Comprehensive transcriptome analysis reveals accelerated genic evolution in a Tibet fish, Gymnodiptychus pachycheilus[J]. Genome Biol Evol, 2015, 7(1): 251-261. doi: 10.1093/gbe/evu279
    [25]
    YU M C, ZHANG D S, HU P, et al. Divergent adaptation to Qinghai Tibetan Plateau implicated from transciptome study of Gymnocypris dobula and Schizothorax nukiangensis[J]. Biochem Syst Ecol, 2017, 71: 97-105. doi: 10.1016/j.bse.2017.02.003
    [26]
    YUAN F H, WANG H L, TIAN Y, et al. Fish oil alleviated high-fat diet-induced non-alcoholic fatty liver disease via regulating hepatic lipids metabolism and metaflammation: a transcriptomic study[J]. Lipids Health Dis, 2016, 15: 20. doi: 10.1186/s12944-016-0190-y
    [27]
    COOPER R U, CLOUGH L M, FARWELL M A, et al. Hypoxia-induced metabolic and antioxidant enzymatic activities in the estuarine fish Leiostomus xanthurus[J]. J Exp Mar Biol Ecol, 2002, 279(1): 1-20.
    [28]
    LI D, YANG Y, WANG T, et al. Liver transcriptome shows differences between acute hypoxia-tolerant and intolerant individuals of greater amberjack (Seriola dumerili)[J]. Animals, 2023, 13: 2717-2717. doi: 10.3390/ani13172717
    [29]
    JIN Q, REN Y, WANG M, et al. Novel function of FAXDC2 in megakaryopoiesis[J]. Blood Cancer J, 2016, 6(9): e478. doi: 10.1038/bcj.2016.87
    [30]
    杨娇艳, 廖明军, 杨劭. 甾醇14α-去甲基化酶 (CYP51) 的研究进展[J]. 生物工程学报, 2008(10): 1681-1688.
    [31]
    YANG Y T, WANG Z, WANG J, et al. Histopathological, hematological, and biochemical changes in high-latitude fish Phoxinus lagowskii exposed to hypoxia[J]. Fish Physiol Biochem, 2021, 47: 919-938. doi: 10.1007/s10695-021-00947-4
    [32]
    SUN J L, ZHAO L L, WU H, et al. Acute hypoxia changes the mode of glucose and lipid utilization in the liver of the largemouth bass (Micropterus salmoides)[J]. Sci Total Environ, 2020, 713: 135157.
    [33]
    LEONARDUZZI G, SOTTERO B, POLI G. Targeting tissue oxidative damage by means of cell signaling modulators: the antioxidant concept revisited[J]. Pharmacol Therapeut, 2010, 128(2): 336-374. doi: 10.1016/j.pharmthera.2010.08.003
    [34]
    ZHAO L L, SUN J L, LIANG J, et al. Enhancing lipid metabolism and inducing antioxidant and immune responses to adapt to acute hypoxic stress in Schizothorax prenanti[J]. Aquaculture, 2020, 519: 734933. doi: 10.1016/j.aquaculture.2020.734933
    [35]
    DASGUPTA S, GIULIO R T D, DROLLETTE B D, et al. Hypoxia depresses CYP1A induction and enhances DNA damage, but has minimal effects on antioxidant sheepshead minnow (Cyprinodon responses in variegatus) larvae exposed to dispersed crude oil[J]. Aquatic Toxicology, 2016, 177: 250-260. doi: 10.1016/j.aquatox.2016.05.022
    [36]
    ELAHIAN F, SEPEHRIZADEH Z, MOGHIMI B, et al. Human cytochrome b5 reductase: structure, function, and potential applications[J]. Crit Rev Biotechnol. 2014, 34(2): 134-143.
    [37]
    JENSEN F B. Red blood cell pH, the Bohr effect, and other oxygenation-linked phenomena in blood O2 and CO2 transport[J]. Society, 2004, 182: 215-227.
    [38]
    HAASE V H. Regulation of erythropoiesis by hypoxia-inducible factors[J]. Blood Rev, 2013, 27(1): 41-53. doi: 10.1016/j.blre.2012.12.003
    [39]
    LEI Y, YANG L D, ZHOU Y, et al. Hb adaptation to hypoxia in high-altitude fishes: fresh evidence from Schizothoracinae fishes in the Qinghai-Tibetan Plateau[J]. Int J Biol Macromol, 2021, 185: 471-484. doi: 10.1016/j.ijbiomac.2021.06.186
    [40]
    NIKINMAA M. Haemoglobin function in vertebrates: evolutionary changes in cellular regulation in hypoxia[J]. Resp Physiol, 2001, 128: 317-329. doi: 10.1016/S0034-5687(01)00309-7
    [41]
    张曦, 付世建, 彭姜岚, 等. 急性低氧对鲫鱼幼鱼血液基础指标的影响[J]. 重庆师范大学学报 (自然科学版), 2011(4): 19-22.
  • Related Articles

    [1]REN Xiaoyao, TANG Baojun, ZHENG Hanfeng, LIU Yujia, WEI Tao. Effects of acute hypoxia stress on respiratory metabolism and related gene expression of juvenile Babylonia areolate[J]. South China Fisheries Science, 2025, 21(2): 149-156. DOI: 10.12131/20240205
    [2]ZHANG Linbao, TIAN Fei, CHEN Haigang, ZHANG Zhe, YE Guoling, LI Yitong, TANG Haiwei. Comparative transcriptome analysis in livers of female and male marine medaka (Oryzias melastigma)[J]. South China Fisheries Science, 2023, 19(3): 88-97. DOI: 10.12131/20220250
    [3]JI Yudan, SUN Zhipeng, LYU Weihua, LU Cuiyun, CAO Dingchen, LIU Tianqi, ZHOU Jia, ZHENG Xianhu. Characterization and expression analysis of ho1 from Sander lucioperca under acute hypoxia stress[J]. South China Fisheries Science, 2023, 19(2): 98-106. DOI: 10.12131/20220187
    [4]JIA Huining, SHI Miaomiao, BIAN Yongle, SHI Chongjing, LIU Hengwei, SONG Xuehong, QIN Fenju. Effects of nanometer selenium on immune protection and antioxidant ability of Eriocheir sinensis under hypoxia stress[J]. South China Fisheries Science, 2022, 18(6): 100-109. DOI: 10.12131/20220106
    [5]SONG Ruhao, HU Ruiqin, LI Genfang, ZHANG Zhicong, XU Qianghua. Research on effect of hypoxia stress on liver tissue of zebrafish (Danio rerio) based on transcriptomics technology[J]. South China Fisheries Science, 2022, 18(6): 60-68. DOI: 10.12131/20220038
    [6]SAN Lize, LIU Baosuo, ZHANG Nan, GUO Liang, GUO Huayang, ZHU Kecheng, ZHANG Dianchang. Mining of InDel marker and association analysis of hypoxia tolerance traits in Trachinotus ovatus based on resequencing[J]. South China Fisheries Science, 2022, 18(5): 100-109. DOI: 10.12131/20210347
    [7]GAO Jin, WANG Yongbo, LIU Jinye, GUO Yilan, FU Shuyuan. Transcriptome analysis of Plectropomus leopardus liver under different flow velocity[J]. South China Fisheries Science, 2022, 18(1): 107-117. DOI: 10.12131/20210125
    [8]SUN Yongxu, DONG Hongbiao, WANG Wenhao, CAO Ming, DUAN Yafei, LI Hua, LIU Qingsong, ZHANG Jiasong. Effects of periodic hypoxia stress on intestinal microflora structure of Lateolabrax maculatus[J]. South China Fisheries Science, 2019, 15(4): 46-52. DOI: 10.12131/20190021
    [9]OU Youjun, CHEN Shixi, WANG Pengfei, LI Jia'er, WEN Jiufu, WANG Wen, XIE Mujiao. Study on oxidative stress response and physiological metabolism related indices of Trachinotus ovatus under hyp-oxia stress[J]. South China Fisheries Science, 2017, 13(3): 120-124. DOI: 10.3969/j.issn.2095-0780.2017.03.016
    [10]CHEN Shixi, WANG Pengfei, OU Youjun, LI Jia′er, WEN Jiufu, WANG Wen, XIE Mujiao. Acute and chronic hypoxia effect on gills of golden pompano (Trachinotus ovatus)[J]. South China Fisheries Science, 2017, 13(1): 124-130. DOI: 10.3969/j.issn.2095-0780.2017.01.016

Catalog

    Article views (120) PDF downloads (33) Cited by()
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return