Comparative transcriptome analysis in livers of female and male marine medaka (Oryzias melastigma)
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摘要: 海水青鳉 (Oryzias melastigma) 作为雌雄异体的模式动物，在研究外来污染物毒性效应性别差异上具有优势。运用转录组学技术系统研究了雌、雄海水青鳉肝脏组织中的差异表达基因，结果显示雌、雄青鳉肝脏中共有1 351个显著差异表达基因，其中683个在雌鱼肝脏中高表达，668个在雄鱼肝脏中高表达。雌鱼肝脏中高表达的差异基因主要涉及生殖和性激素合成相关通路，如卵黄蛋白原和雌激素受体。雄鱼肝脏中高表达的差异基因主要涉及能量代谢、细胞骨架和肌肉收缩等相关生物过程，如丙酮酸激酶、肌酸激酶、肌球蛋白和肌钙蛋白等。实时荧光定量PCR验证结果显示，除DNA错配修复蛋白基因以外，其他17个基因差异表达倍数与RNA-seq对应基因差异表达趋势基本一致，表明转录组分析数据基本可靠。研究表明，雌、雄海水青鳉肝脏中基因表达具有差异调控模式，研究获得的差异基因和调控通路将为海水青鳉对外来污染物性别差异响应分子机制研究提供一定的理论基础。Abstract: As a gonochoristic model animal, marine medaka (Oryzias melastigma) is good for studying the sex-specific responses of organisms to xenobiotic pollutants. We used comparative transcriptomics technology to systematically investigate the differentially expressed genes (DEGs) between the liver tissues of female and male medaka. We identified 683 significantly up-regulated DEGs in the females, and 668 DEGs in the males. The high expressed DEGs in the females were involved in the reproductive and sex hormone synthesis pathways, such as vitellogenin and estrogen receptor. The top twenty DEGs in the males were involved in energy metabolism, cytoskeleton and muscle contraction, such as pyruvate kinase, creatine kinase, myosin and troponin. Except for the DNA mismatch repair protein, all the 17 DEGs had similar magnitude and expression trends by both qRT-PCR and RNA-seq analyses, which confirms the reliability of the RNA-seq data. The results demonstrate that the gene expression patterns are different in the livers of female and male medaka, and the DEGs provide a theoretical basis for promoting the molecular mechanism of sex-specific responses of medaka to xenobiotic pollutants.
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Key words:
- Oryzias melastigma /
- Liver /
- Sex /
- Transcriptome /
- Differential expression genes
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图 1 雌、雄海水青鳉肝脏基因差异表达分析火山图
Figure 1. Volcano plot of deferential expressed genes in livers of female and male O. melastigma
图 2 qRT-PCR验证结果
Figure 2. Comparison of relative expression levels between RNA-Seq and qRT-PCR results
表 1 靶基因qRT-PCR引物序列
Table 1. Primer sequences of tested genes used in qRT-PCR
Gene 编号
Gene ID注释结果
Gene description引物序列 (5'—3')
Primer sequence (5'–3')ENSOMEG00000014272 丙酮酸激酶 pyruvate kinase GATGCAGGTTCTTCCGTTAT
GTTTCAGCGTGGTATTCGTGENSOMEG00000023209 肌酸激酶 creatine kinase M-type TACAAGCCCACCGACAAGCA
GCCAGAGCCTCAATGGACAGENSOMEG00000008770 ATP依赖6-磷酸果糖激酶 ATP-dependent 6-phosphofructokinase, muscle type TCCTCCAGGGACATCAGA
CCAGGAAAGCCTCAAAGCENSOMEG00000013229 异柠檬酸脱氢酶 isocitrate dehydrogenase [NADP], mitochondrial ACATTCCTCGGCTTGTTC
ACATTCCTCGGCTTGTTCENSOMEG00000016412 葡萄糖激酶 glucokinase GCGATTTCTTGGCTTTGG
GGAGTACATTTGGTTCGTENSOMEG00000013940 肌球蛋白重链 myosin heavy chain AAGGCTAACAGTGAGGTGG
CTCCACATCAATCATAAGGTCENSOMEG00000022055 肌钙蛋白C troponin C ACTCACCCAAACGGACCCAG
GCCCAGCATCCTCATCACCTENSOMEG00000017631 卵黄蛋白原1 vitellogenin-1 ACCCTCTACTCTGTCAACGA
TATCTTCTGGCACTCCTCACENSOMEG00000017938 卵黄蛋白原2 vitellogenin-2 TGAAAGATGTACCGAGTGCG
TCAATGGGTGTTTGGAGGAGENSOMEG00000015512 3-β-羟基类固醇异构酶 3-beta-hydroxysteroid-Delta (8), Delta (7)-isomerase TGGAGTTCCGTGTTTGAGTT
GGTCATTAGCCACATAGTTAGGENSOMEG00000010141 17-β-羟基类固醇脱氢酶 17-beta-hydroxysteroid dehydrogenase 7 GTGCTGCCAAAGAAATCAAA
ACATAGAAGAGGCTCCAACTENSOMEG00000009991 雌激素受体 estrogen receptor ATCAGCCCAGCCTCCTCA
GGGTCCGTTCGTCTCCATENSOMEG00000011913 脂肪酸脱羧酶2 fatty acid desaturase 2 CGGCACTGCTGGCAACTT
GGCTGAACGGCTCCTAAAENSOMEG00000009600 细胞色素P450 cytochrome P4502K1 ACGAGCCAACGAGACAATAC
TAGCAGTCCACAAATCCCCTENSOMEG00000011275 DNA复制许可因子 DNA replication licensing factor MCM6 CCACGGAAACGACGAGGTA
TTTGGCGGTACTCGGGTCTENSOMEG00000001336 DNA错配修复蛋白 DNA mismatch repair protein GGCGTCGCATCATAGTAGCT
CCCTTCTTCCTCCTCCTCTTENSOMEG00000001928 DNA修复蛋白 DNA repair protein RAD51 homolog 1 CGAGTTTGGTGTTGCCGTAG
AGGTCAGATTTCCCAGCGTCENSOMEG00000014847 DNA聚合酶 DNA polymerase epsilon subunit 2 GTGCCCAGATACATTTACAACG
GTGACCATCCCGAGTACGATTA18S核糖体RNA 18S ribosomal RNA GACAAATCGCTCCACCAACT
CCTGCGGCTTAATTTGACCC
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表 2 海水青鳉肝脏转录组测序结果统计
Table 2. Statistics of liver transcriptome of O. melastigma
样品名称
Sample原始数据
Raw reads净序列
Clean reads错误率
Errorrate/%质量值大于30
Q30/%比对到基因组上的序列
Total mapped reads to genome/%CF1 46 032 406 42 172 460 0.02 94.30 91.89 CF2 46 965 052 43 062 498 0.03 93.76 91.71 CF3 45 711 652 41 474 580 0.03 93.90 91.92 CM1 44 214 558 41 630 522 0.03 93.70 90.06 CM2 47 037 770 44 496 970 0.03 93.99 86.77 CM3 47 890 610 44 474 994 0.03 94.00 87.79
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表 3 雌雄海水青鳉肝脏基因表达变化倍数最高的前20个基因
Table 3. Top twenty significantly up-regulated genes in livers of female and male O. melastigma
基因ID
Gene ID变化倍数
log2 fold change基因注释
Gene description雌鱼 Female ENSOMEG00000001115 10.20 溶质载体家族41成员 solute carrier family 41 member 1 ENSOMEG00000003787 10.05 WAP型 (乳清酸性蛋白质) 四二硫核心 WAP-type (Whey Acidic Protein) 'four-disulfide core' ENSOMEG00000009600 9.90 细胞色素 P450 cytochrome P450 2K1 novel.1314 9.90 卵黄蛋白原1 vitellogenin-1 ENSOMEG00000017631 9.80 卵黄蛋白原1 vitellogenin-1 ENSOMEG00000003805 9.69 WAP型 (乳清酸性蛋白质) 四二硫核心 WAP-type (Whey Acidic Protein) 'four-disulfide core' ENSOMEG00000014709 9.65 卵黄蛋白原1 vitellogenin-1 ENSOMEG00000017938 9.63 卵黄蛋白原2 vitellogenin-2 ENSOMEG00000016745 9.35 脑特异性血管生成抑制因子1 brain-specific angiogenesis inhibitor 1 ENSOMEG00000014656 9.31 卵黄蛋白原1 vitellogenin-1 ENSOMEG00000012102 9.20 蛋白赖氨酸6-氧化酶 protein-lysine 6-oxidase ENSOMEG00000016916 9.11 神经元正五肽受体 neuronal pentraxin receptor ENSOMEG00000013237 8.76 cornichon同源蛋白3 protein cornichon homolog 3 ENSOMEG00000017881 8.73 ras相关蛋白 ras-related protein Rab-39B ENSOMEG00000014740 8.73 卵黄蛋白原1 vitellogenin-1 ENSOMEG00000016835 8.67 细胞外丝氨酸/苏氨酸蛋白激酶 extracellular serine/threonine protein kinase FAM20C ENSOMEG00000016456 8.17 卵黄蛋白原1 vitellogenin-1 ENSOMEG00000017903 7.67 ras相关蛋白 ras-related protein Rab-38 ENSOMEG00000008961 6.89 透明带精子结合蛋白4 zona pellucida sperm-binding protein 4 ENSOMEG00000009991 6.45 雌激素受体 estrogen receptor 雄鱼 Male ENSOMEG00000014272 13.42 丙酮酸激酶 pyruvate kinase PKM ENSOMEG00000015762 11.86 肌酸激酶 creatine kinase M-type ENSOMEG00000018541 11.74 热休克蛋白71 heat shock cognate 71 kDa protein ENSOMEG00000013940 11.72 肌球蛋白重链 myosin heavy chain, fast skeletal muscle ENSOMEG00000021803 11.30 肌球蛋白调节轻链2 myosin regulatory light chain 2, skeletal muscle isoform ENSOMEG00000021829 11.00 磷酸甘油酸突变酶2 phosphoglycerate mutase 2 ENSOMEG00000005322 10.74 肌球蛋白重链 myosin heavy chain, fast skeletal muscle ENSOMEG00000015087 10.60 肥大细胞蛋白酶8 mast cell protease 8 ENSOMEG00000000307 10.56 肌钙蛋白C troponin C, skeletal muscle ENSOMEG00000012484 10.55 蛋白酪氨酸磷酸酶 protein tyrosine phosphatase type IVA 3 ENSOMEG00000007501 10.50 ADP/ATP转位酶 ADP/ATP translocase 1 ENSOMEG00000023209 10.48 肌酸激酶 creatine kinase M-type ENSOMEG00000008770 10.47 ATP依赖6-磷酸果糖激酶 ATP-dependent 6-phosphofructokinase, muscle type ENSOMEG00000002691 10.25 辛肌动蛋白结合重复序列蛋白 Xin actin-binding repeat-containing protein 2 ENSOMEG00000006520 10.24 小清蛋白 parvalbumin beta ENSOMEG00000008672 10.21 LIM结构域结合蛋白 LIM domain-binding protein 3 ENSOMEG00000018391 10.15 肌球蛋白结合蛋白C myosin-binding protein C, fast-type ENSOMEG00000020650 9.98 ryanodine受体 ryanodine receptor 1 ENSOMEG00000001483 9.96 结蛋白 desmin ENSOMEG00000015807 9.96 AMP脱氨酶 AMP deaminase 1
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表 4 差异表达基因显著富集KEGG通路
Table 4. Significantly enriched KEGG pathways
KEGG 通路KEGG pathway 雌鱼Female 雄鱼Male P 通路 IDPathway ID DNA复制与修复过程 DNA replication and repair process DNA复制 DNA replication 20 0 1.91×10−11 ola03030 错配修复 Mismatch repair 11 0 5.03×10−6 ola03430 嘧啶代谢 Pyrimidine metabolism 12 3 3.31×10−3 ola00240 嘌呤代谢 Purine metabolism 10 13 2.52×10−2 ola00230 核苷酸切除修复 Nucleotide excision repair 9 0 3.18×10−2 ola03420 碱基切除修复 Base excision repair 7 1 4.95×10−2 ola03410 脂类代谢过程 Lipid metabolism process 甾体生物合成 Steroid biosynthesis 13 0 2.64×10−7 ola00100 PPAR信号通路 PPAR signaling pathway 8 8 6.39×10−3 ola03320 脂肪酸代谢 Fatty acid metabolism 12 2 1.70×10−2 ola01212 不饱和脂肪酸生物合成 Biosynthesis of unsaturated fatty acids 7 2 2.52×10−2 ola01040 脂肪酸生物合成 Fatty acid biosynthesis 6 0 3.78×10−2 ola00061 萜骨架生物合成 Terpenoid backbone biosynthesis 6 0 3.78×10−2 ola00900 氨基酸与蛋白生物合成 Amino acid and protein biosynthesis 真核生物核糖体生物发生 Ribosome biogenesis in eukaryotes 21 1 2.64×10−7 ola03008 内质网蛋白加工 Protein processing in endoplasmic reticulum 27 3 3.31×10−3 ola04141 精氨酸和脯氨酸代谢 Arginine and proline metabolism 4 8 1.22×10−2 ola00330 氨基酸生物合成 Biosynthesis of amino acids 9 7 1.30×10−2 ola01230 氨酰tRNA生物合成 Aminoacyl-tRNA biosynthesis 10 0 1.31×10−2 ola00970 蛋白质输出 Protein export 7 0 1.81×10−2 ola03060 其他 Others N-聚糖生物合成 N-Glycan biosynthesis 11 0 2.52×10−2 ola00510
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