Transcriptome Characterization of Hybrid Sturgeon Skin under Alkaline Stress

doi:10.7668/hbnxb.20193330

Abstract

Abstract:

To investigate the effect of alkaline stress on the skin physiology of hybrid sturgeon(Huso dauricus♀×Acipenser schrenckii♂),we investigated the molecular characteristics of the skin tissue of hybrid sturgeon under alkaline stress and normal breeding water conditions by transcriptome sequencing.The total number of differentially expressed genes(DEGs)between control and stress groups was the result showed that was 1 849,of which 1 302 genes were up-regulated genes and 547 genes were down-regulated in the skin tissue of the stress group.GO clustering of differentially expressed genes showed that they were mainly enriched in seven GO terms,including regulation of cytoplasmic calcium ion concentration,muscle contraction,troponin complex,troponin T binding,and troponin C binding.KEGG enrichment analysis revealed that glycine,serine and threonine metabolism,protein digestion and absorption,starch and sucrose metabolism were significantly enriched pathways.Interaction network analysis of metabolic pathways revealed that the core metabolic pathways of hybrid sturgeon skin under alkaline stress were the adherent patch,protein digestion and absorption and platelet activation,complement and coagulation cascade and hypoxia-inducible factor-1 signaling pathways as the main efficient pathways.Interaction network analysis of metabolic pathways indicated that the core metabolic pathways of hybrid sturgeon skin under alkaline stress were the adherent patch,protein digestion and absorption and platelet activation,complement and coagulation cascade and hypoxia-inducible factor-1 signaling pathways as the main efficient pathways.The results of histological sections showed that the skin and kidney tissues of hybrid sturgeon were severely damaged by alkaline stress,and the glomeruli and tubules were significantly wrinkled,especially the atrophy of the distal tubules,and the epithelial cells of the glomeruli were reduced in size,and the walls of the tubules were thinned or even detached;the number of mucous cells in the skin tissues increased with the increase of alkalinity,and the nuclei of rod-shaped cells were solidified and arranged more closely under alkaline stress.

Key words: Hybrid sturgeon(Huso dauricus♀×Acipenser schrenckii♂), Alkaline stress, Transcriptome, Skin, Histological sections, Metabolic pathway networks

LIU Xiafei, YANG Helin, WANG Nianmin, LÜ Weihua, XU Wei, CAO Dingchen, ZHANG Ying. Transcriptome Characterization of Hybrid Sturgeon Skin under Alkaline Stress[J]. Acta Agriculturae Boreali-Sinica, 2023, 38(2): 206-216. doi: 10.7668/hbnxb.20193330.

/ / Recommend / Download Citations

URL: http://www.hbnxb.net/EN/10.7668/hbnxb.20193330

http://www.hbnxb.net/EN/Y2023/V38/I2/206

Figures/Tables 12

Tab.1 Primers and sequences

基因名称 Gene name	引物序列(5'-3') Primer sequence(5'-3')
ALOXE3	F:CTGGTGGAAATGGTCTGCCT R:GCAATATCCTCCGGCAGACA
EEF2K	F:AACAGCCCCCTGATCAACAC R:GCCGATCTTCTTCTCCAGCA
TNNI2	F:ATGCTCCAGATTGCCAAGGC R:TACCCAAGGACAGTGGAGGG
ASPH	F:CGATGGCGATGGTGACTTTG R:AAGCTCCTCCTCCACCAAGA
CAPN3	F:CACTTCCAGTTCTGGCGCTA R:GTTCACCAAGTCTGCGGAGA
JIP3	F:GCAACATCACAAGAGCCAGA R:CCAGGCTGAGAACAGAGTCC
MAPK1	F:TGGCAGAGATGCTGTCAAAC R:TCTGTTCCAGGGAACTTTGC
β-actin	F:ATCGCCGCACTGGTTGTTGA R:ATGCCGTGCTCGATGGGATA

Tab.2 Summary of RAN-seq dates

样品名 Sample	过滤后序列/M Clean reads	过滤后碱基数/G Clean bases	Q30/%	GC/%
C1	48.06	6.90	96.29	47.03
C2	46.24	6.65	95.92	48.82
C3	46.09	6.59	96.12	47.10
D1	50.61	7.27	96.09	48.27
D2	49.23	7.12	95.76	47.95
D3	48.16	6.97	96.06	46.99

Tab.3 Statistics of transcript splicing results

Unigene	N50	总长度/bp Total length	最大长度/bp Max length	最小长度/bp Min length
80 422	1 759	88 658 788	32 175	301

Tab.4 Comparison results statistics of Clean reads and Unigene

样品名 Sample	总比对率 Total mapped reads	多位点比对率 Multiple mapped	单一位点比对率 Uniquely mapped
C1	42 597 958(88.64%)	11 942 715(24.85%)	30 655 243(63.79%)
C2	42 117 652(91.09%)	11 320 775(24.48%)	30 796 877(66.61%)
C3	41 046 870(89.07%)	11 562 511(25.09%)	29 484 359(63.98%)
D1	45 961 299(90.81%)	14 489 614(28.63%)	31 471 685(62.18%)
D2	44 622 929(90.64%)	13 121 244(26.65%)	31 501 685(63.99%)
D3	43 158 248(89.61%)	12 327 576(25.60%)	30 830 672(64.02%)

Tab.5 Annotation results of NR,NT,KEGG,Swiss-Prot,Pfam,KOG and GO

注释数据库 Anno database	注释基因数量 Annotated number	300≤长度<1 000 300≤Length<1 000	长度≥1 000 Length≥1 000
NR	31 078(38.64%)	12 073(15.01%)	19 005(23.63%)
Swissprot	26 691(33.19%)	9 061(11.27%)	17 630(21.92%)
KEGG	18 262(22.71%)	6 270(7.80%)	11 992(14.91%)
KOG	19 546(24.30%)	6 387(7.94%)	13 159(16.36%)
eggNOG	28 686(35.67%)	10 447(12.99%)	18 239(22.68%)
GO	24 153(30.03%)	8 176(10.17%)	15 977(19.87%)
Pfam	20 427(25.40%)	5 075(6.31%)	15 352(19.09%)

Fig.1 Volcano plot of differential gene expression between control and stress groups The red balls represent up regulated gene; the green balls represent down regulated gene.

Fig.2 Heatmap of differential gene expression between control and stress groups

Fig.3 Significant enrichment of Go in skin differential gene metabolic pathway 1.Regulation of cytosolic calcium ion concentration;2.Muscle contraction;3.Protein side chain deglutamylation;4.Skeletal muscle contraction;5.C-terminal protein deglutamylation;6.Positive regulation of ryanodine-sensitive calcium-release channel;7.Regulation of muscle contraction;8.Regulation of release of sequestered calcium ion into cytosol by;9.Cardiac muscle contraction;10.Response to ATP;11.Troponin complex;12.Junctional sarcoplasmic reticulum membrane;13.Myosin filament;14.Myofibril;15.Respiratory chain;16.Striated muscle thin filament;17.Collagen trimer;18.Z disc;19.Sarcomere;20.Calcium channel complex;21.Troponin T binding;22.Troponin C binding;23.Troponin Ⅰ binding;24.5-aminolevulinate synthase activity;25.Structural constituent of muscle;26.Calcium ion binding;27.Metallocarboxypeptidase activity;28.Neurotransmitter:sodium symporter activity;29.Channel activity;30.Structural constituent of ribosome.

Fig.4 The significantly enriched pathways and corresponding DEGs number of each pathway 1.Dilated cardiomyopathy;2.Hypertrophic cardiomyopathy(HCM);3.Thyroid cancer;4.Staphylococcus aureus infection;5.Prion diseases;6.Protein digestion and absorption;7.Platelet activation;8.Complement and coagulation cascades;9. Gap junction;10.Tight junction;11.ECM-receptor interaction;12.Focal adhesion;13.Adrenergic signaling in cardiomyocytes;14.Cardiac muscle contraction;15.Calcium signaling pathway;16.Ribosome;17.Porphyrin and chlorophyll metabolism;18.Starch and sucrose metabolism;19.Glycine, serine and threonine metabolism;20.Glycolysis/Gluconeogenesis.The color gradient is from red to green and the corresponding enrichment is from high to low;the size of the sphere represents the number of significantly enriched genes.

Fig.5 Validation of RNA-Seq data using qPCR The vertical coordinate is log₂(Fold Change)of the difference multiplier.

Fig.6 Effects of different alkalinity on kidney A-D.Group C,T1,T2 and T3 respectively;Gl.Glomerulus;CS.Cervical segment;DCT.Distal convoluted tubule;PCT.Proximal convoluted tubule.

Fig.7 Effects of different alkalinity on skin A-D.Group C,T1,T2 and T3; BL.Basal layer of epidermis;BV.Blood vessel;CL.Rod cells;SL.Superficial layer of epidermis;EC.Epithelial cells; MC.Mucous cells;ML.Middlelayer of epidermis;P.Pigment;SC.Dermis compactum;SF.Subcutaneous fat;SS.Dermis spongiosum.

References 71

[2]	Sun D J, Zhang Y, Ma G J. A review of sturgeon caviar production and international trade[J]. Chinese Journal of Fisheries, 2014, 27(1):1-7.
[3]	张颖, 曲秋芝, 王斌, 夏永涛, 许式见, 孙大江. 人工养殖下施氏鲟(Acipenser schrenckii)、达氏鳇(Huso dauricus)及其杂交后代的繁殖特性[J]. 水产学杂志, 2016, 29(3):25-29,34.doi:10.3969/j.issn.1005-3832.2016.03.005. doi: 10.3969/j.issn.1005-3832.2016.03.005
	Zhang Y, Qu Q Z, Wang B, Xia Y T, Xu S J, Sun D J. Comparison of reproductive characteristics among Amur sturgeon(Acipenser schrenckii),Kaluga sturgeon (Huso dauricus♂)and their hybrid (Kaluga Sturgeon♀×Amur Sturgeon 8 )[J]. Chinese Journal of Fisheries, 2016, 29(3):25-29,34.
[4]	何志辉, 赵文. 三北地区内陆盐水生物资源及其渔业利用[J]. 大连水产学院学报, 2002, 17(3):157-166.doi:10.16535/j.cnki.dlhyxb.2002.03.001. doi: 10.16535/j.cnki.dlhyxb.2002.03.001
	He Z H, Zhao W. Biological resource in inland saline waters in North China[J]. Journal of Dalian Fisheries University, 2002, 17(3):157-166.
[5]	吴丽华, 徐赟, 王东旗, 孙国庆, 郑永利. 盐碱地黄颡鱼健康养殖技术[J]. 河南水产, 2015(3):13-14.
	Wu L H, Xu Y, Wang D Q, Sun G Q, Zheng Y L. Healthy breeding technology of Pelteobagrus fulvidraco in saline areas[J]. Henan Fisheries, 2015(3):13-14.
[6]	杨广, 王心华, 胡玉花, 田梦园, 胡少迪, 席梦丹, 苗建新, 刘金兰. 乌苏里拟鲿对盐度、碱度的适应性[J]. 天津农学院学报, 2012, 19(3):32-35.doi:10.3969/j.issn.1008-5394.2012.03.009. doi: 10.3969/j.issn.1008-5394.2012.03.009
	Yang G, Wang X H, Hu Y H, Tian M Y, Hu S D, Xi M D, Miao J X, Liu J L. Adaptability of Pseudobagrus ussuriensis to salinity and alkalinity[J]. Journal of Tianjin Agricultural College, 2012, 19(3):32-35.
[7]	魏玉众, 张人铭, 宋明波, 时春明, 阿达可白克·可尔江. 欧鲇幼鱼对盐碱的耐受性[J]. 新疆农业科学, 2019, 56(7):1335-1343.doi:10.6048/j.issn.1001-4330.2019.07.018. doi: 10.6048/j.issn.1001-4330.2019.07.018
	Wei Y Z, Zhang R M, Song M B, Shi C M, Adakebaike K. Studies on the tolerance of Silurus glaris Linnaeus fingerlings to salinity and alkalinity[J]. Xinjiang Agricultural Sciences, 2019, 56(7):1335-1343.
[8]	王龙涛, 葛晨霞, 高春山, 于鹏, 卢怡婷, 张蕾, 王建军, 李月红. 不同浓度盐碱胁迫对异育银鲫的慢性损伤效应[J]. 中国兽医杂志, 2019, 55(7):84-87.
	Wang L T, Ge C X, Gao C S, Yu P, Lu Y T, Zhang L, Wang J J, Li Y H. Effect of different concentrations of saline-alkali stress on the chronic injury of Carassius auratus gibelio[J]. Chinese Journal of Veterinary Medicine, 2019, 55(7):84-87.
[9]	张蕾, 郭曦尧, 马世宏, 程义, 王建军, 楚冲之, 李月红. 不同浓度盐碱胁迫对异育银鲫的慢性损伤效应[J]. 中国兽医杂志, 2018, 54(12):106-109.
	Zhang L, Guo X Y, Ma S H, Cheng Y, Wang J J, Chu C Z, Li Y H. The chronic injury of Hallucinogenic crucial carp with different concentrations of saline-alkali stress[J]. Chinese Journal of Veterinary Medicine, 2018, 54(12):106-109.
[10]	吕富, 黄金田, 王爱民. 碱度对异育银鲫摄食·生长和存活的影响[J]. 安徽农业科学, 2007, 35(22):6789-6790.doi:10.13989/j.cnki.0517-6611.2007.22.107. doi: 10.13989/j.cnki.0517-6611.2007.22.107
	Lü F, Huang J T, Wang A M. Effects of alkalinity on the food consumption,growth and survival of allogynogemetic crucian carp[J]. Journal of Anhui Agricultural Sciences, 2007, 35(22):6789-6790.
[11]	王信海, 姜爱兰, 蔺玉华, 吴学军. 不同盐度和碱度对卡拉白鱼精子活力和受精率的影响[J]. 江西农业学报, 2020, 32(5):93-98.doi:10.19386/j.cnki.jxnyxb.2020.05.17. doi: 10.19386/j.cnki.jxnyxb.2020.05.17
	Wang X H, Jiang A L, Lin Y H, Wu X J. Effects of different salinity and alkalinity on sperm motility and fertilization rate of Chalcalburnus chalcoides aralensis[J]. Acta Agriculturae Jiangxi, 2020, 32(5):93-98.
[12]	姚娜, 宋勇, 王帅, 陈生熬, 阿达可, 刘洁雅, 谢从新. 盐度和碱度对塔里木河叶尔羌高原鳅毒性的研究[J]. 西南农业学报, 2018, 31(2):423-428.doi:10.16213/j.cnki.scjas.2018.2.034. doi: 10.16213/j.cnki.scjas.2018.2.034
	Yao N, Song Y, Wang S, Chen S A, A D A, Liu J Y, Xie C X. Toxicity of salinity and alkalinity to Triplophysa(Hedinichthys)yarkandensis(Day)of tarim river[J]. Southwest China Journal of Agricultural Sciences, 2018, 31(2):423-428.
[13]	章征忠, 张兆琪, 董双林. 淡水白鲳幼鱼盐碱耐受性的初步研究[J]. 青岛海洋大学学报(自然科学版), 1998, 28(3):54-59.doi:10.16441/j.cnki.hdxb.1998.03.008. doi: 10.16441/j.cnki.hdxb.1998.03.008
	Zhang Z Z, Zhang Z Q, Dong S L. Preliminary studies on the tolerance of Colossoma brachypomum fingerlings to salinity and alkalinity[J]. Journal of Ocean University of Qingdao, 1998, 28(3):54-59.
[14]	祝少华. 鲟鱼养殖技术之一:沿黄流域低洼盐碱地池塘养殖匙吻鲟技术[J]. 中国水产, 2007(12):41-43.doi:10.3969/j.issn.1002-6881.2007.12.020. doi: 10.3969/j.issn.1002-6881.2007.12.020
	Zhu S H. One of the sturgeon breeding techniques:Sturgeon breeding technology in low-lying saline ponds along the Yellow Basin[J]. China Fisheries, 2007(12):41-43.
[15]	魏域玲, 冯志云, 蔡原, 赵生国. 西北高原地区地下盐碱水在鲟鱼发眼卵培育中的研究与应用[J]. 甘肃畜牧兽医, 2018, 48(9):64-67,69.doi:10.15979/j.cnki.cn62-1064/s.2018.09.022. doi: 10.15979/j.cnki.cn62-1064/s.2018.09.022
	Wei Y L, Feng Z Y, Cai Y, Zhao S G. Research and application of subsurface saline water in the northwest plateau area for sturgeon hairy-eye egg cultivation[J]. Gansu Animal Husbandry and Veterinary, 2018, 48(9):64-67,69.
[16]	Sanahuja I, Fernández-Alacid L, Ordóñez-Grande B, Sánchez-Nuño S, Ramos A, Araujo R M, Ibarz A. Comparison of several non-specific skin mucus immune defences in three piscine species of aquaculture interest[J]. Fish & Shellfish Immunology, 2019, 89:428-436.doi:10.1016/j.fsi.2019.04.008. doi: 10.1016/j.fsi.2019.04.008
[17]	Soltanian S, Gholamhosseini A. Skin non-specific immune parameters in Palomino rainbow trout[J]. Bulgarian Journal of Veterinary Medicine, 2018, 21(3):292-300.doi:10.15547/bjvm.1086. doi: 10.15547/bjvm.1086 URL
[18]	张艳敏, 杨国坤, 李克克, 孟晓林. 鱼类黏膜层微生物研究进展[J]. 水产学报, 2022, 46(6):1117-1127.doi:10.11964/jfc.20210512856. doi: 10.11964/jfc.20210512856
	Zhang Y M, Yang G K, Li K K, Meng X L. Research progress of mucosal microorganisms of fish[J]. Journal of Fisheries of China, 2022, 46(6):1117-1127.
[19]	吕伟华, 马波, 尹家胜, 杨建, 高雪, 徐伟, 张颖. 施氏鲟皮肤的组织学观察[J]. 水产学杂志, 2021, 34(1):7-11.doi:10.3969/j.issn.1005-3832.2021.01.002. doi: 10.3969/j.issn.1005-3832.2021.01.002
	Lü W H, Ma B, Yin J S, Yang J, Gao X, Xu W, Zhang Y. Histological microscopic observation of skin in amur sturgeon(Acipenser schrenckii)[J]. Chinese Journal of Fisheries, 2021, 34(1):7-11.
[20]	黄智慧, 马爱军, 汪岷. 鱼类体表黏液分泌功能与作用研究进展[J]. 海洋科学, 2009, 33(1):90-94.doi:10.1016/s1874-8651(10)60079-8. doi: 10.1016/s1874-8651(10)60079-8
	Huang Z H, Ma A J, Wang M. Research progression in secretion of fish skin mucous and its function[J]. Marine Sciences, 2009, 33(1):90-94.
[21]	Mehner T, Wieser W. Energetics and metabolic correlates of starvation in juvenile perch(Perca fluviatilis)[J]. Journal of Fish Biology, 1994, 45(2):325-333.doi:10.1111/j.1095-8649.1994.tb01311.x. doi: 10.1111/j.1095-8649.1994.tb01311.x URL
[22]	Nan F R, Feng J, Lü J P, Liu Q, Xie S L. Transcriptome analysis of the typical freshwater rhodophytes Sheathia arcuata grown under different light intensities[J]. PLoS One, 2018, 13(5):e0197729.doi:10.1371/journal.pone.0197729. doi: 10.1371/journal.pone.0197729 URL
[23]	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. Full-length transcriptome assembly from RNA-Seq data without a reference genome[J]. Nature Biotechnology, 2011, 29(7):644-652.doi:10.1038/nbt.1883. doi: 10.1038/nbt.1883 pmid: 21572440
[24]	Moriya Y, Itoh M, Okuda S, Yoshizawa A C, Kanehisa M. KAAS:an automatic genome annotation and pathway reconstruction server[J]. Nucleic Acids Research, 2007, 35(2):182-185.doi:10.1093/nar/gkm321. doi: 10.1093/nar/gkm321
[25]	Finn R D, Tate J, Mistry J, Coggill P C, Sammut S J, Hotz H R, Ceric G, Forslund K, Eddy S R, Sonnhammer E L, Bateman A. The Pfam protein families database[J]. Nucleic Acids Research, 2008, 36(1):D281-D288.doi:10.1093/nar/gkm960. doi: 10.1093/nar/gkm960 URL
[26]	Eddy S R. Accelerated profile HMM searches[J]. Plos Computational Biology, 2011, 7(10):e1002195.doi:10.1371/journal.pcbi.1002195. doi: 10.1371/journal.pcbi.1002195 URL
[27]	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. High-throughput functional annotation and data mining with the Blast2GO suite[J]. Nucleic Acids Research, 2008, 36(10):3420-3435.doi:10.1093/nar/gkn176. doi: 10.1093/nar/gkn176 pmid: 18445632
[28]	Li B, Dewey C N. RSEM:accurate transcript quantification from RNA-Seq data with or without a reference genome[J]. BMC Bioinformatics, 2011, 12:323.doi:10.1186/1471-2105-12-323. doi: 10.1186/1471-2105-12-323
[29]	Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y. KEGG for linking genomes to life and the environment[J]. Nucleic Acids Research, 2008, 36:D480-D484.doi:10.1093/nar/gkm882. doi: 10.1093/nar/gkm882 pmid: 18077471
[30]	高珊, 常玉梅, 赵雪飞, 孙博, 张立民, 梁利群, 董志国. 不同NaHCO₃碱度对瓦氏雅罗鱼鳃组织结构的影响[J]. 水生生物学报, 2020, 44(4):736-743.doi:10.7541/2020.088. doi: 10.7541/2020.088
	Gao S, Chang Y M, Zhao X F, Sun B, Zhang L M, Liang L Q, Dong Z G. The effect of different bicarbonate alkalinity on the gill structure of amur ide(Leuciscus waleckii)[J]. Acta Hydrobiologica Sinica, 2020, 44(4):736-743.
[31]	Auffray C, Hood L. Editorial:Systems biology and personalized medicine-the future is now[J]. Biotechnology Journal, 2012, 7(8):938-939.doi:10.1002/biot.201200242. doi: 10.1002/biot.201200242 URL
[32]	Costa V, Angelini C, De Feis I, Ciccodicola A, SantoshKumar. Uncovering the complexity of transcriptomes with RNA-SEQ[J]. Journal of Biomedicine & Biotechnology, 2010(5757): 853916.doi:10.1155/2010/853916. doi: 10.1155/2010/853916
[33]	宋慧. 基于转录组测序技术的大银鱼胚胎盐胁迫适应分子机理研究[D]. 太谷: 山西农业大学, 2014.
	Song H. Molecular mechanism of salt stress adaptation of Pseudosciaena crocea embryos based on transcriptome sequencing technology[D]. Taigu: Shanxi Agricultural University, 2014.
[34]	刘韬, 齐明, 高阳, 刘其根. 青田田鱼幼鱼脑组织在急性低氧胁迫复氧恢复的转录组分析[J]. 上海海洋大学学报, 2023(1):79-88.
	Liu T, Qi M, Gao Y, Liu Q G. Transcriptome analysis of brain tissue of juvenile Qingtian paddy field carp(Cyprinus carpio var.Qingtianensis)during acute changes in dissolved oxygen[J]. Journal of Shanghai Ocean University, 2023(1):79-88.
[35]	寿晨艳. 温度盐度胁迫下褐菖鲉的转录组表达研究[D]. 舟山: 浙江海洋大学, 2021.doi:10.27747/d.cnki.gzjhy.2021.000075. doi: 10.27747/d.cnki.gzjhy.2021.000075.
	Shou C Y. Study on transcriptome expression of Calyx batryticatus under temperature and salinity stress[D]. Zhoushan: Zhejiang Ocean University, 2021.
[36]	徐悦. 瓦氏雅罗鱼鳃、肠组织及原代细胞在碱胁迫下的钙调蛋白表达机制研究[D]. 上海: 上海海洋大学, 2021. doi:10.27314/d.cnki.gsscu.2021.000143. doi: 10.27314/d.cnki.gsscu.2021.000143
	Xu Y.. Study on the expression mechanism of calmodulin in gill, intestine and primary cells of Yarrow vachelli under alkali stress[D]. Shanghai: Shanghai Ocean University, 2021.
[37]	周绪霞, 李卫芬, 许梓荣. 盐度对鱼虾生长性状的影响[J]. 中国饲料, 2004(2):30-33.doi:10.3969/j.issn.1004-3314.2004.02.015. doi: 10.3969/j.issn.1004-3314.2004.02.015
	Zhou X X, Li W F, Xu Z R. Effect of salinity on growth traits of fish and shrimp[J]. China Feed, 2004(2):30-33.
[38]	施群焰, 袁重桂. 点带石斑鱼对盐度的适应性研究[J]. 福建水产, 2003, 25(4):9-11.doi:10.14012/j.cnki.fjsc.2003.04.003. doi: 10.14012/j.cnki.fjsc.2003.04.003
	Shi Q Y, Yuan C G. Study on the adaptability of Epinephelus awoara to salinity[J]. Journal of Fujian Fisheries, 2003, 25(4):9-11.
[39]	王念民, 杨合霖, 丰超杰, 吕伟华, 曹顶臣, 徐伟, 张颖. 碳酸盐碱度对3月龄杂交鲟(Husodauricus♀×Acipenserschrenckii♂)生长与血清生化指标的影响[J]. 上海海洋大学学报, 2023, 32(1):98-107.
	Wang N M, Yang H L, Feng C J, Lü W H, Cao DC, Xu W, Zhang Y. Effects of different carbonate alkalinity on survival,growth and biochemical indexes in serum of three-month-old hybrid sturgeon(Huso dauricus♀×Acipenser schrenckii♂)[J]. Journal of Shanghai Ocean University, 2023, 32(1):98-107.
[40]	郭雯翡, 么宗利, 来琦芳, 史建全, 周凯, 祁洪芳, 李子牛, 王慧. 盐碱胁迫下青海湖裸鲤鳃基因表达差异[J]. 海洋渔业, 2012, 34(2):137-144.doi:10.13233/j.cnki.mar.fish.2012.02.006.
	Guo W F, Yao Z L, Lai Q F, Shi J Q, Zhou K, Qi H F, Li Z N, Wang H. Differential gene expression of Gymnocypris przewalskii under saline-alkali stress[J]. Marine Fisheries, 2012, 34(2):137-144.
[41]	Tamás P, Hawley S A, Clarke R G, Mustard K J, Green K, Hardie D G, Cantrell D A. Regulation of the energy sensor AMP-activated protein kinase by antigen receptor and Ca²⁺ in T lymphocytes[J]. The Journal of Experimental Medicine, 2006, 203(7):1665-1670.doi:10.1084/jem.20052469. doi: 10.1084/jem.20052469 URL
[42]	晋瑞, 王惠芳. 肌浆/内质网Ca²⁺-ATP酶与糖尿病心肌病[J]. 国际内分泌代谢杂志, 2007, 27(3):181-183.doi:10.3760/cma.j.issn.1673-4157.2007.03.013. doi: 10.3760/cma.j.issn.1673-4157.2007.03.013
	Jin R, Wang H F. Sarcoplasmic/endoplasmic Reticulum calcium ATPases and diabetic cardiomyopathy[J]. International Journal of Endocrinology and Metabolism, 2007, 27(3):181-183.
[43]	Stuenkel E L, Hillyard S D. Effects of temperature and salinity on gill Na⁺-K⁺-ATPase activity in the pupfish Cyprinodon salinus[J]. Comp BiochemPhysiol, 1980, 67(1):179-182.doi:10.1016/0300-9629(80)90426-0. doi: 10.1016/0300-9629(80)90426-0
[44]	曲元刚. NaCl和Na₂CO₃对盐地碱蓬和玉米胁迫效应的比较研究[D]. 济南: 山东师范大学, 2003.
	Qu Y G. Comparison study on stress effects of NaCl and Na₂CO₃ on Suaeda salsa L.and maize[D]. Jinan: Shandong Normal University, 2003.
[45]	夏耀耀, 宾朋, 朱国强, 任文凯. 氨基酸代谢调控猪免疫细胞命运研究进展[J]. 中国科学:生命科学, 2020, 50(9):897-913.doi:10.1360/SSV-2020-0041. doi: 10.1360/SSV-2020-0041
	Xia Y Y, Bin P, Zhu G Q, Ren W K. Amino acid metabolism in fate decision of porcine immune cells:Advances and beyond[J]. Scientia Sinica (Vitae), 2020, 50(9):897-913.
[46]	Kalhan S C, Hanson R W. Resurgence of serine:An often neglected but indispensable amino acid[J]. The Journal of Biological Chemistry, 2012, 287(24):19786-19791.doi:10.1074/jbc.r112.357194. doi: 10.1074/jbc.r112.357194 URL
[47]	Labuschagne C F, van den Broek N J F, Mackay G M, Vousden K H, Maddocks O D K. Serine,but not glycine,supports one-carbon metabolism and proliferation of cancer cells[J]. Cell Reports, 2014, 7(4):1248-1258.doi:10.1016/j.celrep.2014.04.045. doi: 10.1016/j.celrep.2014.04.045 pmid: 24813884
[48]	Locasale J W. Serine,glycine and one-carbon units:Cancer metabolism in full circle[J]. Nature ReviewsCancer, 2013, 13(8):572-583.doi:10.1038/nrc3557. doi: 10.1038/nrc3557
[49]	Li S, Guo Q, Wang Y M, Li Z Y, Kang J D, Yin X J, Zheng X. Glycine treatment enhances developmental potential of porcine oocytes and early embryos by inhibiting apoptosis[J]. Journal of Animal Science, 2018, 96(6):2427-2437.doi:10.1093/jas/sky154. doi: 10.1093/jas/sky154 URL
[50]	Ma E H, Bantug G, Griss T, Condotta S, Johnson R M, Samborska B, et al. Serine is an essential metabolite for effector t cell expansion[J]. Cell Metab, 2017, 25(2):345-357.doi:10.1016/j.cmet.2016.12.011. doi: S1550-4131(16)30644-1 pmid: 28111214
[51]	Maddocks O D, Labuschagne C F, Adams P D, Vousden K H. Serine metabolism supports the methionine cycle and DNA/RNA methylation through De Novo ATP synthesis in cancer cells[J]. Molecular Cell, 2016, 61(2):210-221.doi:10.1016/j.molcel.2015.12.014. doi: 10.1016/j.molcel.2015.12.014 pmid: 26774282
[52]	Rodriguez A E, Ducker G S, Billingham L K, Martinez C A, Mainolfi N, Suri V, Friedman A, Manfredi M G, Weinberg S E, Rabinowitz J D, Chandel N S. Serine metabolism supports macrophage IL-1β production[J]. Cell Metabolism, 2019, 29(4):1003-1011.e4.doi:10.1016/j.cmet.2019.01.014. doi: S1550-4131(19)30014-2 pmid: 30773464
[53]	章琼, 蒋高中, 李冰. 水产动物对氨氮胁迫响应的转录组分析研究进展[J]. 江苏农业科学, 2015, 43(3):227-230.doi:10.15889/j.issn.1002-1302.2015.03.074. doi: 10.15889/j.issn.1002-1302.2015.03.074
	Zhang Q, Jiang G Z, Li B. Aquatic animals of ammonia nitrogen stress response of the transcriptome analysis is reviewed[J]. Jiangsu Agricultural Sciences, 2015, 43(3):227-230.
[54]	Kugler K G, Mueller L A J, Graber A, Dehmer M. Integrative network biology:Graph prototyping for co-expression cancer networks[J]. PLoS One, 2011, 6(7):e22843.doi:10.1371/journal.pone.0022843. doi: 10.1371/journal.pone.0022843 URL
[55]	谢从新. 鱼类学[M]. 北京: 中国农业出版社, 2010.
	Xie C X. Ichthyology[M]. Beijing: China Agriculture Press, 2010.
[56]	汪长星. 皮肤免疫应答研究进展[J]. 智慧健康, 2019, 5(28):52-54.doi:10.19335/j.cnki.2096-1219.2019.28.022. doi: 10.19335/j.cnki.2096-1219.2019.28.022
	Wang C X. Process in research on immune response of skin[J]. Smart Healthcare, 2019, 5(28):52-54.
[57]	韩香雨, 靳玮江, 蒋元琳, 张天祥, 张美善, 赵浩汐, 张珂欣, 刘树强, 胡德夫. 补体与凝血级联激活等通路调控麝鼠香腺周期性退化过程[J]. 基因组学与应用生物学, 2022, 41(2):257-270.doi:10.13417/j.gab.041.000257. doi: 10.13417/j.gab.041.000257
	Han X Y, Jin W J, Jiang Y L, Zhang T X, Zhang M S, Zhao H X, Zhang K X, Liu S Q, Hu D F. Complement and coagulation cascades and other pathways regulate the process of periodic degeneration of muskrat scented glands[J]. Genomics and Applied Biology, 2022, 41(2):257-270.
[58]	Boshra H, Li J, Sunyer J O. Recent advances on the complement system of teleost fish[J]. Fish & Shellfish Immunology, 2006, 20(2):239-262.doi:10.1016/j.fsi.2005.04.004. doi: 10.1016/j.fsi.2005.04.004
[59]	徐永胜. 泥鳅补体C3基因的克隆与表达分析[D]. 武汉: 华中农业大学, 2018.
	Xu Y S. Cloning and expression analysis of mudskipper complement C3 gene[D]. Wuhan: Huazhong Agricultural University, 2018.
[60]	Sun Y, Liu W Z, Liu T, Feng X, Yang N, Zhou H F. Signaling pathway of MAPK/ERK in cell proliferation,differentiation,migration,senescence and apoptosis[J]. Journal of Receptor and Signal Transduction Research, 2015, 35(6):600-604.doi:10.3109/10799893.2015.1030412. doi: 10.3109/10799893.2015.1030412 pmid: 26096166
[61]	Chen S P, Zhao L H, Sherchan P, Ding Y, Yu J, Nowrangi D, Tang J P, Xia Y, Zhang J H. Activation of melanocortin receptor 4 with RO27-3225 attenuates neuroinflammation through AMPK/JNK/p38 MAPK pathway after intracerebral hemorrhage in mice[J]. J Neuroinflammation, 2018, 15(1):106.doi:10.1186/s12974-018-1140-6. doi: 10.1186/s12974-018-1140-6
[62]	Ichimura K, Mizoguchi T, Yoshida R, Yuasa T, Shinozaki K. Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6[J]. The Plant Journal, 2000, 24(5):655-665.doi:10.1046/j.1365-313x.2000.00913.x. doi: 10.1046/j.1365-313x.2000.00913.x URL
[63]	Hirose S, Kaneko T, Naito N, Takei Y. Molecular biology of major components of chloride cells[J]. Comparative Biochemistry and Physiology Part B, Biochemistry & Molecular Biology, 2003, 136(4):593-620.doi:10.1016/s1096-4959(03)00287-2. doi: 10.1016/s1096-4959(03)00287-2 URL
[64]	Geven E J W, Klaren P H M. The teleost head kidney:Integrating thyroid and immune signalling[J]. Developmental and Comparative Immunology, 2017, 66(1):73-83.doi:10.1016/j.dci.2016.06.025. doi: 10.1016/j.dci.2016.06.025 URL
[65]	Hellio C, Pons A M, Beaupoil C, Bourgougnon N, Gal Y L. Antibacterial,antifungal and cytotoxic activities of extracts from fish epidermis and epidermal mucus[J]. International Journal of Antimicrobial Agents, 2002, 20(3):214-219.doi:10.1016/S0924-8579(02)00172-3. doi: 10.1016/S0924-8579(02)00172-3 URL
[66]	Fast M D, Sims D E, Burka J F, Mustafa A, Ross N W. Skin morphology and humoral non-specific defence parameters of mucus and plasma in rainbow trout,coho and Atlantic salmon[J]. Comparative Biochemistry and Physiology Part A, Molecular & Integrative Physiology, 2002, 132(3):645-657.doi:10.1016/s1095-6433(02)00109-5. doi: 10.1016/s1095-6433(02)00109-5
[67]	张金生, 刘志峰, 马爱军, 崔文晓, 曲江波. 大菱鲆水通道蛋白(AQP1、AQP3)以及离子通道蛋白(CFTR、NHE1)对低盐胁迫的响应[J]. 渔业科学进展, 2020, 41(4):41-49.doi:10.19663/j.issn2095-9869.20190410003. doi: 10.19663/j.issn2095-9869.20190410003.
	Zhang J S, Liu Z F, Ma A J, Cui W X, Qu J B. Response of aquaporin(AQP1,AQP3)and ion channel protein(CFTR,NHE1)of turbot(Scophthalmus maximus)to low-salinity stress[J]. Progress in Fishery Sciences, 2020, 41(4):41-49.
[68]	Yang S H, Tsai J D, Kang C K, Yang W K, Kung H N, Lee T H. The ultrastructural characterization of mitochondria-rich cells as a response to variations in salinity in two types of teleostean pseudobranch:Milkfish(Chanos chanos)and Mozambique tilapia(Oreochromis mossambicus)[J]. Journal of Morphology, 2017, 278(3):390-402.doi:10.1002/jmor.20650. doi: 10.1002/jmor.20650 URL
[69]	Seale A P, Stagg J J, Yamaguchi Y, Breves J P, Soma S, Watanabe S, Kaneko T, Cnaani A, Harpaz S, Lerner D T, Grau E G. Effects of salinity and prolactin on gene transcript levels of ion transporters,ion pumps and prolactin receptors in Mozambique tilapia intestine[J]. General and Comparative Endocrinology, 2014, 206:146-154.doi:10.1016/j.ygcen.2014.07.020. doi: 10.1016/j.ygcen.2014.07.020 URL
[1]	谢忠明, 孙大江. 鲟鱼养殖技术[M]. 北京: 中国农业出版社, 2002:9.
	Xie Z M, Sun D J. Acipenser culture technology[M]. Beijing: China Agriculture Press, 2002:9
[2]	孙大江, 张颖, 马国军. 鲟鱼子酱的生产与国际贸易概况[J]. 水产学杂志, 2014, 27(1):1-7.doi:10.3969/j.issn.1005-3832.2014.01.001. doi: 10.3969/j.issn.1005-3832.2014.01.001
[70]	Tipsmark C K, Breves J P, Rabeneck D B, Trubitt R T, Lerner D T, Grau E G. Regulation of gill claudin paralogs by salinity,cortisol and prolactin in Mozambique tilapia(Oreochromis mossambicus)[J]. Comp Biochem Physiol A Mol Integr Physiol, 2016, 199:78-86.doi:10.1016/j.cbpa.2016.05.014. doi: 10.1016/j.cbpa.2016.05.014 URL
[71]	Tong C, Zhang C F, Zhao K, Zhang R Y. Transcriptome profiling analysis of naked carp(Gymnocypris przewalskii)provides insights into the immune-related genes in highland fish[J]. Fish & Shellfish Immunology, 2015, 46(2):366-377.doi:10.1016/j.fsi.2015.06.025. doi: 10.1016/j.fsi.2015.06.025

Please choose a citation manager

Content to export