EFFECTS OF SALINITY STRESS ON ANSCRIPTION AND EXPRESSION IN JUVENILE HIPPOCAMPUS KUDA BLEEKER
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摘要: 为探究大海马(Hippocampus kuda Bleeker)幼体在高盐、低盐胁迫条件下的基因表达水平的变化规律, 对实验条件下的大海马幼体的肝脏样品进行了转录组测序。对照组(CK, 25‰)、高盐(HS-test, 31‰)和低盐 (LS-test, 17‰)胁迫组共获得71794个单基因簇(Unigenes), N50为1780 bp, 平均长度为820.71 bp。高盐胁迫组与对照组比较, 共获得2740个差异表达基因 (DEGs), 其中495个DEGs上调, 2245个DEGs下调; 与对照组相比, 低盐胁迫组共获得3715个DEGs, 其中1854个DEGs上调, 1861个DEGs下调。高/低盐胁迫组DEGs经 KEGG 数据库富集发现, 高/低盐度胁迫均能导致大海马幼体体内氨基酸代谢、免疫代谢、能量和脂肪酸代谢相关基因受到影响。其中, 低盐胁迫时能量代谢和氨基酸代谢的相关基因显著上调, 高盐胁迫时脂肪酸代谢的相关基因显著下调, 而高/低盐胁迫时免疫代谢的相关基因都显著上调。从经过盐度胁迫的大海马幼体的肝脏转录组中分别筛选到免疫相关基因Gst、Hsp70、Hsp90、Sod、Bcl-2、Gadd45α、Tcrβ、Tap2和Traf3, 脂肪酸代谢相关基因Fadsd6、Fas、Sqle、Cyp51、Elovl6和Slc27a6, 能量代谢相关基因Vlcad、Pdha1、Mdh1、Idh3b、G6pd和Sdhd, 及一些氨基酸代谢相关基因Gldc、Atp6v1e1、Sms、Fadh、Asl、Ass1和Glud1等, 可作为大海马幼体响应环境盐度变化应激的候选基因。研究结果为盐度胁迫下大海马幼体的稳态调控机制的研究奠定了一定基础, 有助于在养殖实践中预防极端的盐度改变对大海马幼体所造成的影响。Abstract: Salinity is an important environmental factor that affects the life cycle of aquatic organisms, including their growth, development and reproduction. In fish, acute salinity changes cause a series of physiological responses. Hippocampus kuda is an important economic resource and can adapt to a wide range of salinity levels, while the juveniles are highly sensitive to salinity stress, which may cause pathological signs or diseases by alleviating the immune roles and then lead to mass mortality. The survival rate of cultivated H. kuda is low in China because of the toxic effects of salinity stress on juvenile seahorse. To understand molecular mechanisms of its low survival rate, this study used high-throughput sequencing technology to analyze differentially expressed genes (DEGs) in juvenile seahorse hepatopancreatic tissues treated with normal-salinity water (CK, salinity=25‰), low-salinity water (LS-test, salinity=17‰), and high-salinity water (HS-test, salinity=31‰) respectively for 12h. According to the result of RNA-Seq, a total of 71794 unigenes were produced among control group, high-salinity stress group and low-salinity stress group, and the sequence N50 value was 1780 bp, with an average length of 820.71 bp. Compared with the control group, there were 2740 differently expressed genes selected in high salinity group, of which 495 genes were up-regulated and 2245 were down-regulated. On the other hand, 3715 differently expressed genes were selected in low-salinity group, of which 1854 genes were up-regulated and 1861 genes were down-regulated. Ten dysregulated DEGs (Gst, Bcl-2, Fas, Vlcad, Pdha1, Mdh1, Idh3b, G6pd, Gadd45α and SOD) were confirmed by qRT-PCR. According to the result of Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis, the DEGs were mainly related to metabolism and immune responses. With respect to metabolism, the low-salinity group had enhanced energy and amino acid metabolism, while high-salinity group had reduced lipid metabolism related genes expression. Both high- and low-salinity group had enhanced immune metabolism pathways. Based on our results, we collected the lipid metabolism related genes (Fadsd6, Fas, Sqle, Cyp51, Elovl6 and Slc27a6), amino acid metabolism related genes (Gldc, Atp6v1e1, Sms, Fadh, Asl, Ass1 and Glud1), energy metabolism related genes (Vlcad, Pdha1, Mdh1, Idh3b, G6pd and Sdhd) and immune related genes (Gst, Hsp70, Hsp90, Sod, Bcl-2, Gadd45α, Tcrβ, Tap2 and Traf3) of H. kuda as genetic indicators to identify the stressor. This study will promote the discovery of the molecular mechanism of salt stress adaptation of aquatic organisms, and provides a reference for ambient salinity control in aquaculture.
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图 1 GO 统计柱状图
1. 细胞过程; 2. 代谢过程; 3. 生物调节; 4. 生物过程调节; 5. 刺激反应; 6. 多细胞生物过程; 7. 发育过程; 8. 细胞部分组织或生物合成; 9. 定位; 10. 信号; 11. 生物过程的正调控; 12. 定位的建立; 13. 生物过程的负调控; 14. 免疫系统反应; 15. 移动; 16. 生物黏附; 17. 多机体过程; 18. 生长; 19. 生殖; 20. 生殖过程; 21. 行为; 22. 节律过程; 23. 细胞杀伤; 24. 细胞聚集; 25. 解毒; 26. 生物相; 27. 细胞; 28. 细胞部分; 29. 细胞器; 30. 膜; 31. 细胞器部分; 32. 膜部分; 33. 含蛋白复合物; 34. 细胞间区域组分; 35. 膜结合腔体; 36. 细胞间区域组分; 37. 胞间连丝; 38. 超分子纤维; 39. 突触; 40. 突触部分; 41. 细胞外基质; 42. 细胞外基质成分; 43. 核体; 44. 病毒粒子; 45. 其他组织; 46. 其他组织部分; 47. 病毒粒子部分; 48. 共质体; 49. 结合功能; 50. 催化活性; 51. 分子功能调节剂; 52. 转运因子活性; 53. 信号传导活性; 54. 酶调节剂活性; 55. 分子感应器活性; 56. 结构分子活性; 57. 转录因子活性, 蛋白质结合; 58. 受体调节剂活性; 59. 电子传递活性; 60. 通道调节器活动; 61. 抗氧化活性; 62. 化学排斥因子活性; 63. 翻译调控因子活性; 64. 趋化因子活性; 65. 蛋白标签; 66. 金属伴侣蛋白活性; 67. 形态发生素活性
Figure 1. GO statistics histogram
1. cellular process; 2. metabolic process; 3. biological regulation; 4. regulation of biological process; 5. response to stimulus; 6. multicellular organismal process; 7. developmental process; 8. cellular component organization or biogenesis; 9. localization; 10. signaling; 11. positive regulation of biological process; 12. establishment of localization; 13. negative regulation of biological process; 14. immune system process; 15. locomotion; 16. biological adhesion; 17. multi-organism process; 18. growth; 19. reproduction; 20. reproductive process; 21. behavior; 22. rhythmic process; 23. cell killing; 24. cell aggregation; 25. detoxification; 26. biological phase; 27. cell; 28. cell part; 29. organelle; 30. membrane; 31. organelle part; 32. membrane part; 33. protein-containing complex; 34. extracellular region; 35. membrane-enclosed lumen; 36. extracellular region part; 37. cell junction; 38. supramolecular fiber; 39. synapse; 40. synapse part; 41. extracellular matrix; 42. extracellular matrix component; 43. nucleoid; 44. virion; 45. other organism; 46. other organism part; 47. virion part; 48. symplast; 49. binding; 50. catalytic activity; 51. molecular function regulator; 52. transporter activity; 53. signal transducer activity; 54. enzyme regulator activity; 55. molecular transducer activity; 56. structural molecule activity; 57. transcription factor activity, protein binding; 58. receptor regulator activity; 59. electron transfer activity; 60. channel regulator activity; 61. antioxidant activity; 62. chemorepellent activity; 63. translation regulator activity; 64. chemoattractant activity; 65. protein tag; 66. metallochaperone activity; 67. morphogen activity
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图 3 大海马肝脏转录组中差异表达基因个数统计图
Figure 3. Statistical diagram of differentially expressed genes in liver transcriptome of H. kuda
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图 4 大海马肝脏转录组中差异基因韦恩图
Figure 4. Venn diagram of differential gene in liver transcriptome of H. kuda
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图 5 高盐胁迫组 (HS-test) RT-qPCR 及 RNA-Seq 的比较分析
Figure 5. Comparative analysis of RT-qPCR and RNA-Seq in HS-test
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图 6 低盐胁迫组 (LS-test) RT-qPCR 及 RNA-Seq 的比较分析
Figure 6. Comparative analysis of RT-qPCR and RNA-Seq in LS-test
表 1 RT-qPCR所用基因及其引物序列
Table 1 Primers used for RT-qPCR
序号Number 基因ID Gene ID 基因注释Gene annotation 引物序列Primer (5′—3′) 扩增效率Amplificati on efficiency (%) 1 TRINITY_DN21408_c0_g2 谷胱甘肽S-转移酶A样Glutathione S-transferase A-like (GST) AAATGACTCTGTACTGGGGCG
CCCCTGGGGTTAATATCGAGC96 2 TRINITY_DN22446_c2_g4 凋亡调节因子Bcl-2Apoptosis regulator Bcl-2 (Bcl-2) GTGAGGTACGTGCCGATGGT
GGGCTGGGATGCTTTTGTG103 3 TRINITY_DN18527_c0_g2 脂肪酸合酶Fatty acid synthase (Fas) GTCCCATTGTGCTGTTGTGAC
CGGACTCCTGAATATCCAGCC105 4 TRINITY_DN17925_c0_g1 超长链特异性酰基辅酶A脱氢酶Very long-chain specific acyl-CoA dehydrogenase (Vlcad) AAAGTGGCCCAGTCTTCTACG
ACTGCCTGTGTAGCTTGACTC105 5 TRINITY_DN21693_c1_g1 丙酮酸脱氢酶E1成分亚单位α Pyruvate dehydrogenase E1 component subunit alpha (Pdha1) TTGCCCGTCATCTTCATCTG
GACATCCATACCATCCACCCT95 6 TRINITY_DN20289_c6_g1 细胞溶质苹果酸脱氢酶Cytosolic malate dehydrogenase (Mdh1) TCTGCGACCACATGAGGGA
TCTGGACGGGGAAGGAGTAG100 7 TRINITY_DN22605_c1_g1 异柠檬酸脱氢酶3 (NAD+)βIsocitrate dehydrogenase 3 (NAD+) beta (Idh3b) CTGGACCTGTTTGCCAATGTG
AATCACACCGGTCACACTCTC104 8 TRINITY_DN18237_c0_g1 葡萄糖-6-磷酸脱氢酶Glucose-6-phosphate dehydrogenase (G6pd) CATGCACGCAGTTCTGATAGC
GGGTGATCTGGCCAAGAAGAA105 9 TRINITY_DN19718_c0_g6 生长停滞和DNA损伤诱导蛋白GADD45α Growth arrest and DNA damage-inducible protein GADD45 alpha-like (Gadd45α) CTTTGGAAGGGACGTAGGCA
AAACATCCGCAGAGGAGTGAA104 10 TRINITY_DN12165_c0_g1 超氧化物歧化酶Superoxide dismutase (SOD) TCACATACTTCACGGGTTTCG
AGGGAAATGTTCAAGGTACTGC102 11 TRINITY_DN14235_c1_g1 β2-微球蛋白Beta-2 microglobulin (B2M) TACACCCACCAGCCAGGAAA
GGACTCGACGACATCGAACATC100 
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表 2 大海马测序数据的统计汇总
Table 2 Statistic summary of the sequencing data of H. kuda
组别Group 原始序列数
Raw reads number过滤后序列数
Clean reads number过滤后碱基数
Clean bases number过滤后序列质量大于30的
碱基数比例Q30 (%)对照组CK 55510236 54453888 7749733968 97.80 高盐胁迫组HS-test 58040146 56489512 8126998064 95.88 低盐胁迫组LS-test 55840746 54407308 7888244898 95.84
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表 3 组装结果统计表
Table 3 Statistics of assembly results
序列长度
Length (bp)组装的转录本
Trinity单基因簇
Unigenes200—600 74243 48867 600—1000 18364 7154 1000—2000 29552 7801 >2000 32271 7972 总计Count 154430 71794 最小长度Min length 201 201 最大长度Max length 15866 15866 平均长度Mean length 1234.69 820.71 N50 2318 1780 N90 476 278 注: N50代表序列从大到小排列, 当其累计长度刚刚超过全部序列总长度50%时, 最后一个序列的大小即为N50的大小。N90代表序列从大到小排列, 当其累计长度刚刚超过全部序列总长度90%时, 最后一个序列的大小即为N90的大小Note: N50 means that the sequence is distributed from large to small, and when the extension length just exceeds 50% of the total length of the entire sequence, the size of the last sequence is the size of N50. N90 means that the sequence is distributed from large to small, and when the extension length just exceeds 90% of the total length of the entire sequence, the size of the last sequence is the size of N90
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表 4 各个数据库的注释汇总表
Table 4 Summary of comments in each database
数据库
Database单基因簇数量
Number of unigenes百分比
Percentage (%)非冗余蛋白数据库Nr 26999 37.61 核酸序列数据库Nt 22389 31.19 京都基因与基因组百科全书KEGG 4781 6.66 蛋白质序列数据库Swiss-Prot 22277 31.03 蛋白质家族域数据库Pfam 12391 17.26 基因本体论数据GO 24450 34.06 保守域数据库CDD 15719 21.89 真核生物蛋白相邻类的聚簇KOG 14428 20.1 总单基因簇Total unigenes 71794 100
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表 5 HS-test vs. CK差异基因富集的前20个KEGG代谢通路
Table 5 Top 20 KEGG metabolic pathways enriched for HS-test vs. CK differential genes
通路ID
Pathway ID上调DEGs Up-regulated DEGs 下调DEGs Down-regulated DEGs Q值
Q value代谢通路注释Metabolic pathway annotation ko00100 0 9 0.0023 类固醇生物合成Steroid biosynthesis ko04977 4 3 0.1968 维生素消化吸收Vitamin digestion and absorption ko03320 3 10 0.1968 PPAR信号通路PPAR signaling pathway ko04612 9 1 0.1968 抗原加工提呈Antigen processing and presentation ko00260 3 6 0.1968 甘氨酸、丝氨酸和苏氨酸代谢Glycine, serine and threonine metabolism ko04710 1 8 0.1994 昼夜节律Circadian rhythm ko04711 0 5 0.2081 昼夜节律-果蝇Circadian rhythm-fly ko00564 5 9 0.4242 甘油磷脂代谢Glycerophospholipid metabolism ko00630 3 4 0.4242 乙醛酸和二羧酸代谢Glyoxylate and dicarboxylate metabolism ko00909 0 2 0.5387 倍半萜类化合物和三萜类化合物的生物合成Sesquiterpenoid and triterpenoid biosynthesis ko03060 1 4 0.6468 蛋白质运输Protein export ko04064 8 4 0.6884 NF-κB信号通路NF-kappa B signaling pathway ko04066 2 11 0.7365 HIF-1信号通路HIF-1 signaling pathway ko04976 1 8 0.7687 胆汁分泌Bile secretion ko01040 1 3 0.7687 不饱和脂肪酸的生物合成Biosynthesis of unsaturated fatty acids ko04672 5 0 0.7687 IgA生成的肠道免疫网络Intestinal immune network for IgA production ko00980 2 3 0.8420 细胞色素P450对异生素的代谢Metabolism of xenobiotics by cytochrome P450 ko00440 0 2 0.8420 磷酸盐和次磷酸盐代谢Phosphonate and phosphinate metabolism ko00140 3 2 0.8420 类固醇激素生物合成Steroid hormone biosynthesis ko00534 1 3 0.8420 糖胺聚糖生物合成-硫酸乙酰肝素/肝素Glycosaminoglycan biosynthesis-heparan sulfate/heparin
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表 6 LS-test vs. CK差异基因富集的前20个KEGG代谢通路
Table 6 Top 20 KEGG metabolic pathways enriched for LS-test vs. CK differential genes
通路ID
Pathway ID上调DEGs Up-regulated DEGs 下调DEGs Down-Regulated DEGs Q值
Q value代谢通路注释Metabolic pathway annotation ko03050 24 0 2.27E-07 蛋白酶体Proteasome ko00190 45 1 2.56E-05 氧化磷酸化Oxidative phosphorylation ko00100 2 9 0.0024 类固醇生物合成Steroid biosynthesis ko00020 12 2 0.0290 柠檬酸循环 (TCA循环)Citrate cycle (TCA cycle) ko04612 16 0 0.0394 抗原加工提呈Antigen processing and presentation ko01200 24 5 0.0577 碳代谢Carbon metabolism ko00053 4 4 0.0787 抗坏血酸和藻酸盐代谢Ascorbate and aldarate metabolism ko00982 4 5 0.1366 药物代谢-细胞色素P450Drug metabolism-cytochrome P450 ko00410 8 3 0.1452 β-丙氨酸代谢Beta-Alanine metabolism ko00500 7 4 0.1571 淀粉和蔗糖代谢Starch and sucrose metabolism ko00983 6 5 0.1571 药物代谢-其他酶Drug metabolism-other enzymes ko04721 13 3 0.1571 突触小泡循环Synaptic vesicle cycle ko03008 21 0 0.1689 核糖体在真核生物中的生物发生Ribosome biogenesis in eukaryotes ko04966 8 0 0.2045 收集导管酸分泌Collecting duct acid secretion ko00380 10 3 0.2295 色氨酸代谢Tryptophan metabolism ko03013 34 1 0.2571 RNA转运RNA transport ko03040 29 1 0.2916 剪接体Spliceosome ko00310 11 7 0.3013 赖氨酸降解Lysine degradation ko00300 2 0 0.3219 赖氨酸生物合成Lysine biosynthesis ko00250 7 2 0.3219 丙氨酸、天冬氨酸和谷氨酸代谢Alanine, aspartate and glutamate metabolism
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