TRANSCTIPTOMIC RESPONSES TO ACUTE LOW TEMPERATURE STRESS IN GIANT FRESHWATER PRAWN MACROBRACHIUM ROSENBERGII
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摘要: 为探究罗氏沼虾(Macrobrachium rosenbergii)急性低温应激响应的基因表达模式, 研究以罗氏沼虾成虾为研究对象, 分别设置实验组(16℃)和对照组(24℃), 实验组从24℃急性降温(2℃/1h)至16℃后的0、1h、3h、6h、12h、24h和回温至24℃后共7个时间点采集肝胰腺组织进行转录组测序分析。差异表达基因(DEGs)筛选结果显示, 胁迫3h与回温后的DEGs数量(5062个)几乎是1h与回温后的1.5倍(3516个), 随着胁迫时间的延长, 各时间点与回温后的DEGs数量逐渐降低。KEGG富集发现, DEGs显著富集在溶酶体、淀粉和蔗糖代谢、抗原加工与呈递等途径中。此外, 罗氏沼虾在急性低温应激下, 黏着斑、ECM-受体互作、细胞色素P450对异生物质的代谢、谷胱甘肽代谢、氧化磷酸化、p53信号通路等相关基因也发生了显著变化。WGCNA分析发现各组间的共有DEGs聚类在与细胞功能及免疫相关模块和与能量物质代谢相关模块上。另外, 花生四烯酸代谢信号通路中的Cytochrome P450 2L1-like基因、谷胱甘肽代谢信号通路中的NADP-specific isocitrate dehydrogenase基因及淀粉和蔗糖代谢信号通路中的Hexokinase基因等的表达量随低温应激时间增加呈先增后减的趋势。这些通路及基因可能在罗氏沼虾急性低温应激下的能量代谢及免疫调节等活动中起重要作用。研究为揭示罗氏沼虾急性低温应激响应的分子调控机制提供了基础数据。Abstract: The giant freshwater prawn (GFP) Macrobrachium rosenbergii is one of the important economically freshwater shrimp species, and its annual production in China is dominant in the world. However, its tolerance to low temperatures is extremely poor, and acute low temperatures can lead to large-scale deaths and cause huge economic losses. In order to explore genes related to the GFP response to acute low temperature, comparative transcriptomic analyses were performed for the hepatopancreas of adult GFPs exposed to low temperature. The low temperature stress group (16℃) and the control group (24℃) were set up. The water temperature of the stress group was decreased from 24℃ to 16℃ at a rate of around 2℃/h through adding ice cubes. The hepatopancreas were collected for transcriptomic analyses from exposed shrimps respectively at 1h, 3h, 6h, 12h, 24h after acute cooling at 16℃, rewarming to 24℃ and control group. The results of differentially expressed genes (DEGs) showed that 1702 DEGs were identified between samples of cooling for 1h and the control group (M1 vs. C0); the number of DEGs between the stress group and the control group began to increase gradually with stress time, and reached the maximum at 6h (M3 vs. C0, a total of 2899), then gradually decreased, maintaining the homeostasis under low temperature stress. After rewarming to 24℃, the number of DEGs (M6 vs. C0, 1969) returned to the level of 1h stress. Additionally, the DEGs number (5062) between samples of stress for 3h and rewarming to 24℃ (M2 vs. M6) was almost 1.5 times of that (3516) between samples of stress for 1h and rewarming (M1 vs. M6). With the extension of time, the number of DEGs decreased gradually, suggesting that the homeostasis of the GFP had drastic changes in the first 3h of acute low temperature stress, but the adaptability to low temperature gradually increased with stress time, and a steady state under low temperature was established probably after being stressed from 3h to 6h, and after rewarming, the homeostasis returned to the equilibrium of short-term cold stress. KEGG enrichment analysis showed that DEGs was enriched in lysosome, starch and sucrose metabolism, antigen processing and presentation. Adhesion spots, ECM-receptor interaction, metabolism of cytochrome P450 to isobiotic substances, glutathione metabolism, oxidative phosphorylation, and p53 signaling pathway were also involved in the regulation of acute cold stress in the GFP. The common DEGs among all groups were clustered as the cell function and immunity modules and energy metabolism modules. In addition, the up-regulated cytochrome P450 2L1-like gene in the arachidonic acid metabolic signaling pathway was screened, and its expression increased firstly and then decreased with the increase of cold stress time. NADP-specific isocitrate dehydrogenase, an upregulated gene in glutathione metabolic signaling pathway, was firstly reduced and then increased with time. Expression of hexokinase, a down-regulated gene in starch and sucrose metabolic signaling pathways, increased and then decreased over time. The above mentioned enriched pathways indicated that the metabolic function of the GFP might have been seriously affected under acute low temperature stress, with a large amount of reactive oxygen species being produced, the balance of energy circulation being disrupted, and the immune system being also damaged, which was corroborated with the phenomena of fasting, slow movement, susceptibility to diseases and even death of the GFP under acute low temperature. Consequently, these screened pathways and genes may play important roles in energy metabolism and immune regulation during acute cold stress in the GFP. The present study provides basic data for revealing the molecular regulatory mechanism of the response of the GFP to acute low temperature stress, also provides a theoretical basis for the selective breeding of new cold-tolerant GFP varieties.
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图 1 罗氏沼虾急性低温应激差异表达基因统计
比较组合进行差异表达基因筛选的阈值为DESeq2 pval<0.05 |log2FoldChange|>0
Figure 1. Statistics of differentially expressed genes in M. rosenbergii with acute low temperature stress
The threshold for the differential gene screening of the comparison combination is DESeq2 pval<0.05 |log2FoldChange|>0
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图 2 罗氏沼虾急性低温应激差异表达基因热图
Figure 2. Heatmap of differentially expressed genes in M. rosenbergii with acute low temperature stress
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图 3 罗氏沼虾急性低温应激差异表达基因GO 富集分析气泡图
FDR的大小用点的颜色来表示, FDR越小则颜色越接近红色, 每个GO term下包含的差异表达基因的多少用点的大小来表示
Figure 3. Bubble diagram of GO enrichment analysis of differentially expressed genes in M. rosenbergii with acute low temperature stress
The size of FDR is represented by the color of dots. The smaller the FDR, the closer the color is to red. The number of differentially expressed genes contained in each GO term is represented by the size of dots
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图 4 罗氏沼虾急性低温应激差异表达基因KEGG 富集分析气泡图
Q-value 的大小用点的颜色来表示, Q-value 越小则颜色越接近红色, 每个pathway 下包含的差异表达基因的多少用点的大小来表示
Figure 4. Bubble diagram of KEGG enrichment analysis of the differentially expressed genes in M. rosenbergii
The size of Q-value is represented by the color of dots. The smaller the Q-value, the closer the color is to red. The number of differentially expressed genes contained in each pathway is represented by the size of dots
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图 5 罗氏沼虾急性低温应激共有差异表达基因样本聚类及基因模块热图
基因聚类树的每一个分支对应一个模块
Figure 5. Clustering and gene module heatmap of public differentially expressed genes in M. rosenbergii under acute cold stress
Each branch of the gene clustering tree corresponds to a module
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图 6 低温下罗氏沼虾差异表达基因的qRT-PCR验证
Figure 6. qRT-PCR verification of differentially expressed genes in M. rosenbergii under low temperature
表 1 用于罗氏沼虾急性低温胁迫qPCR分析的基因引物
Table 1 Gene primers for qPCR analysis of acute low temperature stress in M. rosenbergii
引物名称
Primer name基因名称
Gene name产物长度
Product length (bp)序列
Sequence (5′—3′)Cluster-33315.45697F 假定蛋白: LOC113813141
Uncharacterized protein: LOC113813141160 ACACAAGCAGGTCGCATAGAGC Cluster-33315.45697R CGCCAAATCCACAGTCCAGGTA Cluster-33315.46133F β-N-乙酰氨基葡萄糖苷酶
Beta-N-acetylglucosaminidase185 TCCTCCAGTTCATCTGCGGTTG Cluster-33315.46133R TCGTCGCTGCTCCACTTATCTG Cluster-33315.45505F γ AMP 活化蛋白激酶亚基
γ AMP-activated protein kinase subunit gamma194 TGTCCTTGGTCCTGCTGGTGAA Cluster-33315.45505R CGTGCTTGGTGGGTAGTTCTCC Cluster-33315.44357F 细胞色素 P450 2L1 样Cytochrome P450 2L1-like 160 CGTTGGCGAACAATACGAGGAG Cluster-33315.44357R GATGGCGTAGCTCTGTGTCTGT Cluster-33315.43475F 反式-1, 2-二氢苯-1, 2-二醇脱氢酶
Trans-1, 2-dihydrobenzene-1, 2-diol dehydrogenase150 CCAGTTTCGGGCAGCCAATAGG Cluster-33315.43475R GACCACCACCCACAACCTTCAC Cluster-33315.43078F 谷胱甘肽 S-转移酶 μ 1 样
Glutathione S-transferase μ 1-like108 TGCCTTTGCTGGAAGCCTTCAT Cluster-33315.43078R CGAGGTATCCTGCTAGGTGGGT Cluster-33315.44900F 细胞周期蛋白G2
Cyclin G2183 CATTGGCAACTTGGGCGTCATC Cluster-33315.44900R GCTGGTATCTCCGAAGGCTTCA Cluster-33315.44571F 醇脱氢酶 3类
Alcohol dehydrogenase class-3140 CGCTGCTTGAAGGTGTGGTATG Cluster-33315.44571R CAGGACAGATGGAAGGCACTCA Cluster-33315.42081F Ras 相关 C3 肉毒杆菌毒素底物 1 样亚型 X5
Ras-related C3 botulinum toxin substrate 1-like isoform X5136 CGCAGGCGACCAATACTGTGAA Cluster-33315.42081R GTGGCTTGAACGGCTTCTGAGA Cluster-33315.45323F 热休克蛋白70
Heat shock protein 70120 ACTCTGTCAGCCTCTGCCCAAG Cluster-33315.45323R ACCACGGAACAAGTCACCACAC 18SF TATACGCTAGTGGAGCTGGAA 18SR GGGGAGGTAGTGACGAAAAAT 
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表 2 急性低温应激下罗氏沼虾转录组测序样本质量
Table 2 Quality of transcriptome sequencing samples of M. rosenbergii under acute low temperature stress
样本Sample 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 (G)错误率
Error rate (%)过滤后序列质量大于
20的碱基数比例Q20 (%)过滤后序列质
量大于30的
碱基数比例Q30 (%)GC含量
GC content (%)C01 23379568 22914824 6.87 0.02 98.32 94.77 43.96 C02 24029340 23579291 7.07 0.02 98.18 94.49 43.52 C03 22762946 22231559 6.67 0.02 98.37 94.91 44.21 M11 21914577 21483440 6.45 0.02 98.27 94.68 44.48 M12 21644434 21168961 6.35 0.02 98.3 94.78 44.01 M13 22306861 21293606 6.39 0.02 98.37 94.93 42.54 M21 22883453 22485963 6.75 0.02 98.36 94.92 44.03 M22 24879818 24430082 7.33 0.02 98.19 94.61 44.06 M23 23238852 22813033 6.84 0.02 98.36 94.93 44.00 M31 22300014 21601471 6.48 0.02 98.29 94.74 43.60 M32 24747603 24102025 7.23 0.02 98.48 95.23 44.91 M33 23994465 23409040 7.02 0.02 98.43 95.09 43.81 M41 22713387 22016757 6.61 0.02 98.32 94.80 43.41 M42 23362302 22918846 6.88 0.02 98.41 95.08 44.36 M43 22886282 22288783 6.69 0.02 98.19 94.56 43.52 M51 26245158 25593705 7.68 0.02 98.33 94.87 44.20 M52 20118392 19681489 5.90 0.02 98.29 94.78 43.89 M53 22748600 22240274 6.67 0.02 98.37 94.93 44.30 M61 22978816 22475617 6.74 0.02 98.42 95.05 43.95 M62 24801163 24256681 7.28 0.02 98.16 94.50 43.24 M63 22036666 21596237 6.48 0.02 98.26 94.73 43.98
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表 3 各数据库注释到的罗氏沼虾急性低温应激基因统计
Table 3 Statistics on the success rate of gene annotation of acute low temperature stress in M. rosenbergii
注释用数据库
Database for annotation注释到的基因数目Number of annotated unigenes 注释到的基因比例
Percentage of annotated unigenes (%)注释到7个数据库
Annotated in all Databases2037 1.50 至少注释到1个数据库
Annotated in at least one Database40236 29.75 注释到GO数据库
Annotated in GO27044 19.99 注释到KO数据库
Annotated in KO8410 6.21 注释到KOG数据库
Annotated in KOG6837 5.05 注释到Nr数据库
Annotated in Nr24826 18.35 注释到Nt数据库
Annotated in Nt8089 5.98 注释到Pfam数据库
Annotated in Pfam27052 20.00 注释到SwissProt数据库Annotated in SwissProt 13446 9.94 所有基因
Total Unigenes135239 100.00
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表 4 用于罗氏沼虾急性低温应激转录组验证的差异表达基因
Table 4 Differentially expressed genes and qRT-PCR results for the validation of the transcriptome of M. rosenbergii acute low temperature stress
基因ID
Gene IDNR注释
Annotated in NRlog2
(差异倍数)
log2
(Fold change)表达模式
RegulationCluster–33315.
45505假定蛋白: LOC113813141
Uncharacterized protein: LOC113813141–1.57
(M1 vs. C0)下调
(down)Cluster–33315.
45697β–N–乙酰氨基葡萄糖苷酶
Beta–N–acetylglucosaminidase–1.81
(M1 vs. C0)下调
(down)Cluster–33315.
46133γ AMP 活化蛋白激酶亚基
γ AMP–activated protein kinase subunit gamma–1.56
(M1 vs. C0)下调
(down)Cluster–33315.43078 细胞色素 P450 2L1 样
Cytochrome
P450 2L1–like1.30
(M1 vs. M4)上调
(up)Cluster–33315.
43475反式–1, 2–二氢苯–1,2–二醇脱氢酶
Trans–1, 2–dihydrobenzene–1, 2–diol dehydrogenase1.09
(M1 vs. M4)上调
(up)Cluster–33315.
44357谷胱甘肽 S–转移酶 μ 1 样
Glutathione S–transferase μ 1–like1.32
(M1 vs. M4)上调
(up)Cluster–33315.
44571细胞周期蛋白G2
Cyclin G2–1.35
(M1 vs. M4)下调
(down)Cluster–33315.
44900醇脱氢酶 3类
Alcohol dehydrogenase class–31.85
(M1 vs. M4)上调
(up)Cluster–33315.
42081Ras 相关 C3 肉毒杆菌毒素底物 1 样亚型 X5
Ras–related C3 botulinum toxin substrate 1–like isoform X5–1.59
(M1 vs. M6)下调
(down)Cluster–33315.
45323热休克蛋白70
Heat shock
protein 70–1.19
(M1 vs. M6)下调
(down)
下载: 导出CSV
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