GENOME-WIDE ANALYSIS OF THE TRIPLOPHYSA PAPPENHEIMI HEMOGLOBIN GENE FAMILY AND ITS RESPONSE TO HYPOXIA STRESS
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摘要:
为探究血红蛋白基因家族在黄河高原鳅(Triplophysa pappenheimi)低氧适应中的作用, 研究基于黄河高原鳅基因组数据对血红蛋白基因家族进行了生物信息学分析, 并开展低氧胁迫和基因表达检测。结果显示, 黄河高原鳅血红蛋白基因家族由11个成员组成, 其中包括6个α珠蛋白基因(hbaa1、hbaa2、hbae1、hbae3、hbae4和hbae5)和5个β珠蛋白基因(hbba1、hbba2、hbbe1.1、hbbe1.2和hbbe2)。Motif、Domain 及基因结构分析结果均表明该家族成员具有较高的保守性, 除hbbe2外, 其余基因结构相似。染色体定位分析结果显示, 血红蛋白基因家族成员分布在2条染色体上(Chr_07、Chr_17)。蛋白理化性质分析结果显示, 除hbbe1.2为疏水性不稳定蛋白, 其余基因产物均为疏水性稳定蛋白, 其中hbae3、hbbe1.1、hbbe2为酸性蛋白; 其余8个为碱性蛋白, 其中α-螺旋是主要的二级结构。亚细胞定位预测结果显示, 除hbae4基因产物位于细胞质中, hbae3位于细胞质和细胞外; 其余血红蛋白基因均位于线粒体中。基因表达研究表明, 在急性低氧胁迫12h (0.3±0.1 mg/L)后, hbaa1、hbaa2、hbba1和hbba2基因在肝脏、鳃和血液中的表达量具有上调趋势, 但是差异不显著(P<0.05); 在慢性低氧24h至96h [(3.0±0.1) mg/L]时, hbaa1、hbba1、hbaa2和hbba2基因在肝脏和血液中的表达量达到峰值(P<0.05), 随着胁迫时间延长, 上述基因的表达量均有所下调。在鳃组织中, hbaa1、hbaa2和hbba1的最高表达量出现在慢性低氧后的196h, 而hbba2基因表达峰值出现在24h。研究展示了黄河高原鳅血红蛋白基因家族成员的低氧胁迫表达模式, 为黄河高原鳅的低氧适应机制研究积累科学数据。
Abstract:Triplophysa pappenheimi is a representative species of Nemacheilinae, which can adapt to the aquatic environment of Tibetan Plateau. To investigate the role of hemoglobin gene family in T. pappenheimi adaptation to hypoxia, bioinformatics analysis of hemoglobin gene family was performed based on genome data, followed by an examination of expression changes of hemoglobin genes in response to hypoxia. The hemoglobin gene family to T. pappenheimi consists of 11 members, including six α-globin genes (hbaa1, hbaa2, hbae1, hbae3, hbae4, and hbae5) and five β-globin genes (hbba1, hbba2, hbbe1.1, hbbe1.2, and hbbe2). Motif, domain, and gene structure analysis showed high conservation among these genes; with the exception of hbbe2, the others exhibited similar structure features. Chromosomal localization analysis showed that the members of hemoglobin gene family were distributed on two chromosomes (Chr_07 and Chr_17). The results of physicochemical analysis indicated that all the gene products were stable hydrophobic proteins, except hbbe1.2, among which, hbae3, hbbe1.1, and hbbe2 were classified as acidic proteins, and the other eight were basic proteins, with α-helix is the main secondary structure. Subcellular localization prediction showed that hbae3 and hbae4 were located in the cytoplasm and the other hemoglobin genes were found in the mitochondria. The expression of hbaa1, hbaa2, hbba1 and hbba2 genes in liver, gill and blood showed an up-regulated trend after 12h of acute hypoxia stress, though the difference was not significant (P<0.05). The expression levels of hbaa1, hbba1, hbaa2, and hbba2 genes in liver and blood reached the peak at 24 h to 96h under chronic hypoxia (P<0.05). In gill tissue, the highest expression of hbaa1, hbaa2, and hbba1 appeared at 196h after chronic hypoxia, while hbba2 reached its peak at 24h. This study reveals the role of the hemoglobin gene family in hypoxic environment of T. pappenheimi, accumulating valuable scientific data for its conservation.
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图 1 斑马鱼和黄河高原鳅血红蛋白系统进化树
Figure 1. Phylogenetic tree of hemoglobin from Danio rerio and Triplophysa pappenheimi based on the protein sequences
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图 2 黄河高原鳅血红蛋白三级结构模型
Figure 2. Protein tertiary structure model of Hemoglobin in Triplophysa pappenheimi
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图 3 黄河高原鳅血红蛋白基因家族的Motif基序(a)、Domain结构域(b)及基因结构(c)
Figure 3. Motif (a), domain (b), and gene structure (c) of the hemoglobin gene family in Triplophysa pappenheimi
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图 4 黄河高原鳅血红蛋白基因在染色体上的分布
Figure 4. Distribution of hemoglobin gene on chromosomes in Triplophysa pappenheimi
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图 5 血红蛋白基因在不同组织的表达热图
Figure 5. Heat map of hemoglobin gene expression in different tissues
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图 6 血红蛋白各基因在各组织中的表达量
a. 肝脏组织中的相对表达量; b. 鳃组织中的相对表达量; c. 血液中的相对表达量; 相同字母表示差异不显著(P>0.05); 不同字母表示差异显著(P<0.05)
Figure 6. Expression levels of hemoglobin gene in various tissues
a. Relative expression in liver; b. Relative expression in gill; c. Relative expression in blood; The same letter indicates no significant difference (P>0.05), while different letters indicate significant differences (P<0.05)
表 1 用于qRT-PCR 分析的引物序列
Table 1 Primer sequences for qRT-PCR analysis
基因
Gene序列
Sequence (5′—3′)退火温度
Annealing
temperature (℃)β-actin F GAACCCCAAGGCTAACAGAGAA 56.9 β-actin R AGGCATACAGGGACAGCACA 59.1 hbae1 F TGGTGTTGGTGAAGCTGTTGAGAA 58.8 hbae1 R GCCAGAACGACGAGTATGTTGTGA 59.3 hbae3 F GAGCCAGGAACTTATCCACAGACA 58.7 hbae3 R CCTCAGACCAAGACCTACTTCTCC 58.8 hbae4 F CATTTACGCTGCCACGGGAAGAA 60.4 hbae4 R TGCTGAGGTGTGCCAGTGTAGT 61.2 hbae5 F TCTCACTGGAGCGACCTGACAC 61.7 hbae5 R GGAAGAGCATGGCAATCACAACAAG 59.0 hbbe1.1 F TACAACGCCGCCGCCATCAT 63.2 hbbe1.1 R GAGGAGACCACAACAGCGAGGAA 61.6 hbbe1.2 F TACAACGCCGCCGCCATCAT 63.2 hbbe1.2 R AGAGACCACAACAGCGAGGAACTT 60.5 hbbe2 F ACTCAGCGGTACTTCGGCAGTT 61.3 hbbe2 R GCAGCAATCACGATAGTCAGGCAAT 59.8 hbaa1 F GACAAGGACAAGGCTGCCGTAAG 61.0 hbaa1 R TGAGCGAAGTAGGTCTTGGTCTGAG 60.3 hbaa2 F ACGATCTTGTTGGTGGATTGAGCAA 58.7 hbaa2 R AGCAGATACAGCCGACAGGAACT 60.5 hbba1 F TCCACCTTCGGCAACCTGTCA 61.8 hbba1 R AGCGGACACGACCACAGACA 61.9 hbba2 F GCCTTTACGCCAAACTAAGCAAACT 58.1 hbba2 R GCCACGACGACAGACAGGAATT 60.1 
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表 2 黄河高原鳅血红蛋白基因家族成员理化性质
Table 2 Physical and chemical properties of hemoglobin gene family members in Triplophysa pappenheimi
基因
GeneCDS长度
CDS length
(bp)氨基酸数目
Number of
amino acid分子质量
Molecular
weight (ku)理论等电点
Theoretical
isoelectric point脂溶性指数
Aliphatic
index亲水性平均值
Grand average of
hydropathicity不稳定性指数
Instability
indexhbae1 444 143 15615.17 9.16 103.71 0.064 23.46 hbae3 528 175 19411.69 6.37 112.57 0.245 24.81 hbae4 426 141 15971.74 9.58 94.89 0.040 39.90 hbae5 432 143 15796.51 9.04 101.68 0.121 24.35 hbbe1.1 444 147 16417.94 6.96 96.87 0.083 16.63 hbbe1.2 444 147 16426.95 7.01 96.87 0.085 96.87 hbbe2 444 147 16786.39 6.90 94.22 –0.073 11.10 hbaa1 432 143 15552.07 8.89 99.65 0.129 21.91 hbaa2 432 143 15556.10 9.33 100.98 0.097 16.03 hbba1 444 147 16113.64 7.70 88.98 0.086 20.53 hbba2 444 147 16181.79 8.89 99.52 0.134 9.90
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表 3 黄河高原鳅血红蛋白基因家族成员二级结构和亚细胞定位
Table 3 Secondary structure and subcellular localization of hemoglobin gene family members in Triplophysa pappenheimi
基因
Geneα-螺旋
Alpha-helix (%)β-折叠
Beta-turn (%)无规卷曲
Random coil (%)延伸链
Extended strand (%)亚细胞定位
Subcellular localizationhbae1 66.43 4.20 19.58 9.79 Mitochondrion hbae3 58.29 6.29 22.29 13.14 Cytoplasm, Extracell hbae4 63.83 4.26 22.70 9.22 Cytoplasm hbae5 65.73 4.20 21.68 8.39 Mitochondrion hbbe1.1 65.31 6.80 17.69 10.20 Mitochondrion hbbe1.2 70.75 6.12 17.01 6.12 Mitochondrion hbbe2 63.27 3.40 24.49 8.84 Mitochondrion hbaa1 67.13 4.90 16.78 11.19 Mitochondrion hbaa2 61.54 4.20 25.87 8.39 Mitochondrion hbba1 73.47 6.80 14.97 4.76 Mitochondrion hbba2 70.07 6.12 19.05 4.76 Mitochondrion
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表 4 基于转录组数据的血红蛋白基因在不同组织中的相对表达量
Table 4 The relative expression of hemoglobin genes in different tissues based on RNA-seq data
组织Tissue 时间Time (h) 基因相对表达量 Relative expression of gene hbae4 hbbe1 hbbe2 hbaa1 hbaa2 hbba1 hbba2 肝脏Liver 0 0.06 0.22 0.63 447.34 150.68 447.78 48.50 12 0.07 0.22 0.52 481.01 204.95 676.54 70.12 24 0.12 0.35 0.50 1333.31 554.80 1336.64 177.50 96 0.16 0.31 0.33 1192.53 448.94 1109.33 113.44 168 0.13 0.30 0.62 835.76 354.51 871.58 71.14 鳃Gill 0 0.35 0.51 0.04 2253.08 957.55 2217.45 264.53 12 0.58 2.14 10.16 4603.07 2103.87 6968.25 776.39 24 1.26 1.34 4.46 6961.28 3612.67 6321.26 996.59 96 1.13 2.00 0.58 8994.12 3892.07 8518.22 857.03 168 0.73 1.75 1.82 3693.78 1528.61 4072.82 285.90 血液Blood 0 23.77 42.62 0.40 163575.34 64712.88 189796.58 20481.05 12 15.11 96.02 3.22 187315.80 82866.30 331174.66 39786.25 24 13.01 16.84 9.21 102190.19 43706.21 127182.48 16116.07 96 21.54 58.55 1.13 222169.69 87838.61 226260.85 24392.49 168 29.12 86.19 17.44 201510.76 66919.83 217962.24 19762.22
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