Transcriptome analysis of gene expression profiling in the suspension cells of Populus tomentosa treated by histone deacetylase inhibitor TSA
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摘要:
组蛋白去乙酰化酶HDAC具有调节细胞增殖、诱导细胞分化、凋亡的作用, 是近年生物学研究热点之一, 而在木本植物方面的作用却鲜有报道。 目的本实验用组蛋白去乙酰化酶抑制剂曲古抑菌素A(Trichostatin A, TSA)对杨树悬浮细胞进行处理, 通过改变细胞的组蛋白乙酰化水平, 来探讨其对基因表达谱变化的影响。 方法用0.5 μmol/L的TSA处理悬浮细胞, 10 d后收集材料用于RNA-Seq分析, 比较经过TSA处理与对照组的悬浮细胞之间转录组表达差异情况。 结果通过显微镜观察发现, 对照组细胞呈均匀椭圆形, 而经过TSA处理后的细胞出现圆形及长条形细胞。通过转录组分析得到4 465个差异表达基因(DEGs), 其中2 363个基因上调, 2 102个基因下调。差异表达基因主要富集在细胞周期、苯丙素生物合成、细胞壁结构成分和乙酰化相关等途径。 结论通过分析TSA处理和对照组的悬浮细胞基因表达差异, 发现TSA通过影响组蛋白乙酰化水平直接或间接影响细胞生长、细胞壁组分和细胞周期的相关基因, 为认识组蛋白乙酰化对植物生长发育的影响提供依据。 Abstract:Histone deacetylase (HDAC), which regulates cell proliferation, cell diferentiation and apoptosis, is one of the hot topics in biology in recent years, but rarely reported in woody plants. ObjectiveIn this study, the change of gene expression profile was investigated by treating the poplar suspension cells with TSA to change the level of histone acetylation in cells. MethodThe suspension cells were treated with 0.5 μmol/L TSA for ten days and were collected for RNA-Seq analysis. Then the gene expression differences were compared between TSA-treated cells and control group suspension cells. ResultThe cells in the control group were homogeneous and oval, while the cells after TSA treatment were round and elongated by microscope observation. 4 465 differentially expressed genes (DEGs) were obtained by the transcriptome analysis, of which 2 363 genes were up-regulated and 2 102 genes were down-regulated. Differentially expressed genes were mainly enriched in cell cycle, phenylpropanoid biosynthesis, cell wall structure and acetylation. ConclusionBy analyzing the difference of gene expression between TSA-treated and control group suspension cells, our results suggest that TSA can directly or indirectly affect genes that regulate cell growth, cell wall structure and lignin synthesis pathway through affecting the level of histone acetylation, which provide evidence for understanding of histone acetylation on plant growth and development. -
Key words:
- transcriptome /
- suspension cell /
- trichostatin A(TSA) /
- Populus tomentosa /
- histone deacetylation
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图 1 TSA处理和对照组毛白杨悬浮细胞形态观察
A.培养10 d的对照组悬浮细胞；B.TSA处理培养10 d的悬浮细胞；C.对照组悬浮细胞形态图(光镜20x)；D.TSA处理的悬浮细胞形态图(光镜20x)；E.碘化丙啶(PI)染色后对照组悬浮细胞形态图(荧光20x)；F.碘化丙啶(PI)染色后TSA处理的悬浮细胞形态图(荧光20x)。
Figure 1. Cell morphological observation of TSA-treated and control group suspension cells in Populus tomentosa
A, suspension cells cultured for 10 days in the control group; B, suspension cells treated by TSA for 10 days; C, cell morphology of suspension culture in the control group under light microscopy (20x); D, cell morphology of TSA-treated suspension culture under light microscopy (20x); E, cell morphology of suspension culture in the control group stained by PI in control under fluorescence microscopy (20x); F, cell morphology of TSA-treated suspension culture stained by PI under fluorescence microscopy (20x).
图 2 差异表达基因的火山图
x.差异倍数; y.校正后的P值。下表 3同此。
红点表示显著性差异表达的上调基因，绿点表示显著性差异表达的下调基因，蓝点表示无显著性差异表达的基因。Figure 2. Volcano map of differentially expressed genes
Red dots indicate significantly up-regulated differentially expressed genes, green dots indicate significantly down-regulated differentially expressed genes. Blue dots indicate non-significantly differentially expressed genes. x, fold change; y, P-adjusted value. The same below in Tab. 3.
图 3 差异基因GO功能富集
Biological process, 生物过程; Molecular function, 分子功能; Cellular component, 细胞组成; Oxidation-reduction process, 氧化还原过程; Photosynthesis, 光合作用; Negative regulation of peptidase activity, 肽酶活性负调控; Negative regulation of endopeptidase activity, 肽链内切酶活性的负调节; Regulation of endopeptidase activity, 肽链内切酶活性的调节; regulation of peptidase activity, 肽酶活性的调节; Negative regulation of hydrolase activity, 水解酶活性负调控; Negative regulation of proteolysis, 蛋白水解酶活性负调控; Single-organism metabolic process, 单体代谢过程; Response to wounding, 损伤反应; Carbohydrate metabolic process, 糖代谢过程; Negative regulation of cellular protein metabolic process, 细胞蛋白质代谢过程的负调控; Negative regulation of protein metabolic process, 蛋白质代谢过程的负调节; Oxylipin biosynthetic process, 羟脂素生物合成过程; Thylakoid, 类囊体; Thylakoid part, 部分类囊体; Photosynthetic membrane, 光合膜; Photosystem, 光系统; Photosystem II, 光系统II; Thylakoid membrane, 类囊体膜; Photosystem I, 光系统I; Chloroplast thylakoid, 叶绿体类囊体膜; Plastid thylakoid, 质体类囊体; Oxidoreductase activity, 氧化还原酶活性; Endopeptidase inhibitor activity, 肽链内切酶抑制剂活性; Peptidase inhibitor activity, 肽酶抑制剂活性; Endopeptidase regulator activity, 肽链内切酶调节活性; Peptidase regulator activity, 肽酶调节活性; Tetrapyrrole binding, 四吡咯结合; Enzyme inhibitor activity, 酶抑制剂活性; Microtubule-based movement, 微管运动; Movement of cell or subcellular component, 细胞或亚细胞组分的运动; DNA replication initiation, DNA复制起始; Microtubule-based process, 微管过程; Regulation of cell cycle process, 细胞周期过程的调控; Mitotic cell cycle process, 有丝分裂细胞周期过程; Regulation of mitotic cell cycle, 有丝分裂细胞周期调控; Regulation of cell cycle phase transition, 细胞周期进程的调控; Cell cycle process, 细胞周期过程; Mitotic cell cycle phase transition, 有丝分裂细胞周期的转变; Cell cycle phase transition, 细胞周期; Mitotic cell cycle, 有丝分裂细胞周期; Kinesin complex, 驱动蛋白复合体; Microtubule associated complex, 微管相关复合物; Microtubule cytoskeleton, 微管细胞骨架; Intrinsic component of plasma membrane, 内源性质膜组件; Cytoskeletal part, 部分细胞骨架; Cytoskeleton, 细胞骨架; Plasma membrane part, 质膜部分; Integral component of plasma membrane, 质膜整体组分; DNA packaging complex, DNA包装复合物; Protein-DNA complex, 蛋白质- DNA复合物; Microtubule motor activity, 微管运动活性; Motor activity, 肌动活动; Cytoskeletal protein binding, 细胞骨架蛋白结合; Microtubule binding, 微管结合; Tubulin binding, 微管蛋白结合; Adenyl ribonucleotide binding, 腺苷核糖核酸结合; Adenyl nucleotide binding, 腺苷核苷酸结合; Number of genes, 基因数目。
Figure 3. GO function enrichment of differential genes
图 4 差异基因KEGG富集分析
Alanine, aspartate and glutamate metabolism, 丙氨酸、天门冬氨酸和谷氨酸代谢; Biosynthesis of secondary metabolites, 次生代谢产物的生物合成; Cyanoamino acid metabolism, 氰氨基酸代谢; Cysteine and methionine metabolism, 半胱氨酸和蛋氨酸代谢; Degradation of aromatic compounds, 芳香族化合物的降解; Glycine, serine and threonine metabolism, 甘氨酸、丝氨酸和苏氨酸代谢; Glyoxylate and dicarboxylate metabolism, 乙醛酸和二羧酸盐代谢; Isoquinoline alkaloid biosynthesis, 喹啉生物碱生物合成; Linoleic acid metabolism, 亚油酸代谢; Metabolic pathways, 代谢途径; Phenylalanine metabolism, 苯丙氨酸代谢; Phenylpropanoid biosynthesis, 苯丙烷生物合成; Photosynthesis, 光合作用; Photosynthesis-antenna proteins, 光合作用蛋白; Plant hormone signal transduction, 植物激素信号转导; Sesquiterpenoid and triterpenoid biosynthesis, 倍半萜和三萜生物合成; Starch and sucrose metabolism, 淀粉与蔗糖代谢; Tropane, piperidine and pyridine alkaloid biosynthesis, 托烷、哌啶和吡啶生物碱的生物合成; Tyrosine metabolism, 酪氨酸代谢; Ubiquinone and other terpenoid-quinone biosynthesis, 泛醌及其他萜类醌生物合成；Gene number, 基因个数。
Figure 4. KEGG enrichment analysis of differentially expressed genes
图 5 苯丙素的生物代谢途径
Caffeoyl-CoA, 咖啡酰辅酶A; P-Coumaroyl-CoA, P-香豆酰辅酶A; 4-Coumaroyl-CoA, 4-香豆酸; Trans-Cinnamate, 反式肉桂酸; Phenylpyruvate, 苯丙酮酸; L-Phenylalanine, L-苯丙氨酸; Feruloyl-Coa, 阿魏酰辅酶A; 2-Hydroxy-3-phenylpropenoate, 2-羟基-3-苯基丙酸酯; Phenylacetaldehyde, 苯乙醛; 2- Phenyl acetamide, 2-苯基乙酰胺; Caffeoyl-CoA O-methyltransferase, 咖啡酰辅酶A甲基转移酶; Phenylalanine ammonia-lyase, 苯丙氨酸解氨酶; Trans-cinnamate 4-monooxygenase, 肉桂酸4-加氧酶; Trans-feruloyl-CoA synthase, 反式阿魏酰辅酶A合成酶; MIF family protein, MIF蛋白家族; Transaminase, 转氨酶; Peroxidase, 过氧化物酶; Amine oxidase, 胺氧化酶
蓝色方框代表上调和下调的基因；红色方框代表上调基因；绿色方框代表下调基因。Figure 5. Phenylalanine metabolism pathway
The blue block indicates up and down regulated genes, the red block indicates up-regulated genes, and the green block indicates down-regulated genes.
表 1 转录组测序数据基本情况
Table 1. Details of transcriptome raw data
样本名称Sample name WT TSA Raw reads 78 359 688 56 834 686 Clean reads 76 174 698 55 525 586 Clean reads percentage/% 97.2 97.7 Clean bases 11.43G 8.33G Error rate/% 0.01 0.01 Q20/% 98.27 98.69 Q30/% 95.61 96.49 GC content/% 44.09 44.39 FPKM Interval(0~1) 17 990(43.20%) 17 828(42.81%) FPKM Interval(1~3) 3 675(8.83%) 3 773(9.06%) FPKM Interval(3~15) 10 137(24.34%) 10 086(24.22%) FPKM Interval(15~60) 7 526(18.07%) 7 651(18.37%) FPKM Interval(>60) 2 314(5.56%) 2 304(5.53%) 注 Notes:Raw reads, 原始序列数据; Clean reads, 过滤后数据; Clean reads percentage，过滤后数据百分比；Clean bases, 转化数据; Error rate, 误码率; Q20(Q30), Phred数值大于20、30的碱基百分比; GC content, G和C数量占总碱基百分比; FPKM Interval, expected number of fragments per kilobase of transcript sequence per millions base pairs sequenced，是每百万fragments中来自某一基因每千碱基长度的fragments数目，按照不同表达水平区间统计。 
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表 2 显著性差异表达基因的统计分析
Table 2. Statistical analysis of significantly differentialby expressed genes
log2x 上调基因数目
Up-regulated gene number/%下调基因数目
Down-regulated gene number/%>2 2 363 2 102 2~5 1 680(71.1%) 1 735(82.5%) 5~10 623(26.4%) 346(16.4%) 10 60(2.5%) 21(1.0%)
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表 3 差异表达的部分基因的功能分析
Table 3. Functional analysis of differentially expressed genes
类别 Category 基因ID Gene ID log2x P值 P value 描述 Description 下调转录因子
Down-regulate transcription factorsAP2-EREBP POPTR_0002s16900 -5.096 41 1.89×10-16 pathogenesis-related transcriptional factor/ERF POPTR_0003s13910 -2.269 73 6.91×10-7 ethylene-responsive transcription factor POPTR_0003s17830 -2.639 41 2.53×10-8 ethylene-responsive transcription factor ERF003 POPTR_0006s10510 -4.754 64 3.82×10-16 pathogenesis-related transcriptional factor/ERF POPTR_0006s27710 -2.946 40 1.28×10-10 pathogenesis-related transcriptional factor/ERF POPTR_0010s22320 -4.569 17 3.88×10-10 ethylene-responsive transcription factor POPTR_0014s01260 -2.150 90 7.90×10-6 AP2-like ethylene-responsive transcription factor POPTR_0014s09020 -2.835 97 1.14×10-5 pathogenesis-related transcriptional factor/ERF POPTR_0001s18800 -3.404 59 2.42×10-5 pathogenesis-related transcriptional factor/ERF POPTR_0004s05110 -4.306 81 5.75×10-5 pathogenesis-related transcriptional factor/ERF POPTR_0017s04540 -2.237 32 2.56×10-7 pathogenesis-related transcriptional factor/ERF AUX/IAA POPTR_0002s10880 -2.836 41 1.22×10-10 putative indoleacetic acid-induced protein 8 (IAA8) POPTR_0006s06550 -10.671 2 1.78×10-19 aux/IAA protein POPTR_0008s16100 -5.260 87 2.35×10-24 aux/IAA protein POPTR_0010s08890 -3.235 68 1.65×10-12 aux/IAA protein POPTR_0018s14300 -4.437 79 1.83×10-19 auxin response factor POPTR_0008s17220 -3.372 51 3.01×10-12 aux/IAA protein POPTR_0018s12790 -3.539 40 5.30×10-12 aux/IAA protein POPTR_0001s17780 -8.999 63 2.45×10-10 aux/IAA protein POPTR_0013s03860 -4.137 51 5.19×10-18 putative auxin-induced protein IAA4 bHLH POPTR_0001s09450 -2.155 17 5.94×10-7 Helix--loop-helix DNA-binding POPTR_0002s05510 -3.028 3 1.42×10-9 transcription factor TT8 POPTR_0005s06220 -4.140 25 2.93×10-16 transcription factor HEC3 POPTR_0006s03560 -2.099 8 3.58×10-6 Helix--loop-helix DNA-binding POPTR_0006s07440 -2.278 97 4.65×10-7 Helix--loop-helix DNA-binding POPTR_0004s05490 -3.654 06 2.25×10-11 Helix--loop-helix DNA-binding POPTR_0001s31250 -8.825 50 1.84×10-9 Helix--loop-helix DNA-binding POPTR_0001s19250 -3.213 79 2.87×10-9 Helix--loop-helix DNA-binding POPTR_0017s07520 -2.338 43 7.97×10-8 Helix--loop-helix DNA-binding POPTR_0008s19510 -4.875 90 6.40×10-7 Helix--loop-helix DNA-binding POPTR_0018s13840 -3.509 27 1.12×10-5 Helix--loop-helix DNA-binding POPTR_0006s05640 -2.208 79 5.49×10-5 Helix--loop-helix DNA-binding POPTR_0018s13850 -4.660 67 9.43×10-18 Helix-loop-helix DNA-binding MYB POPTR_0018s10390 -9.739 11 5.66×10-14 SANT domain, DNA binding; transcription regulator HTH, MYB-type POPTR_0003s14420 -4.532 38 5.50×10-10 SANT domain, DNA binding; transcription regulator HTH, MYB-type POPTR_0002s18170 -3.791 69 1.08×10-15 MYB-related transcription factor LHY POPTR_0003s11360 -3.745 86 3.77×10-12 putative MYB family transcription factor (MYB85) POPTR_0019s07760 -3.707 5 1.80×10-14 putative transcription factor MYB101 POPTR_0015s13180 -2.902 47 2.73×10-6 MYB-like DNA-binding protein POPTR_0012s14540 -2.768 56 1.14×10-7 transcription regulator HTH, Myb-type, DNA-binding POPTR_0006s25840 -2.751 47 4.98×10-9 putative C-MYB-like transcription factor (MYB3R2) POPTR_0002s13030 -2.661 68 1.21×10-6 MYB-like DNA-binding domain POPTR_0006s09860 -2.535 63 9.87×10-7 MYB-like DNA-binding domain POPTR_0006s18620 -2.363 55 2.33×10-6 MYB-like DNA-binding domain POPTR_0007s15110 -2.262 71 5.78×10-7 MYB-CC type transcription factor POPTR_0012s03530 -3.690 53 3.23×10-13 MYB-like DNA-binding domain MYB-like DNA-binding domain POPTR_0011s04010 -7.828 67 1.09×10-5 MYB-like DNA-binding domain MYB-like DNA-binding domain POPTR_0004s08480 -4.162 95 4.56×10-12 MYB-like DNA-binding domain POPTR_0010s13290 -4.807 59 3.48×10-9 MYB-like DNA-binding domain POPTR_0009s01270 -2.384 50 6.88×10-6 MYB-like DNA-binding domain POPTR_0002s11440 -2.047 54 3.90×10-6 MYB-like DNA-binding domain WRKY POPTR_0012s10290 -2.007 31 7.54×10-6 WRKY transcription factor 75 POPTR_0014s15320 -2.914 72 2.59×10-10 DNA-binding WRKY POPTR_0005s08720 -2.860 66 2.57×10-9 DNA-binding WRKY POPTR_0005s05700 -2.077 97 4.79×10-6 DNA-binding WRKY 下调基因
Down-regulate genes乙酰化相关 POPTR_0009s07820 -11.523 24 4.84×10-25 GNAT5-related n-acetyltransferase (GNAT) family protein; similar to GNAT family Acetylation related POPTR_0019s01520 -5.006 67 9.72×10-18 shikimate O-hydroxycinnamoyl transferase POPTR_0004s05280 -2.038 49 1.85×10-6 transferase family protein; similar to elicitor inducible gene product EIG-i24 木质素合成 POPTR_0014s14310 -5.919 72 1.52×10-27 xyloglucan endo-transglycosylase, C-terminal Lignin synthesis POPTR_0008s03810 -2.516 21 7.35×10-9 phenylalanine ammonia-lyase POPTR_0019s14590 -5.195 90 1.12×10-25 xyloglucan endotransglucosylase/hydrolase POPTR_0004s02030 -2.352 01 2.70×10-6 xyloglucan endotransglucosylase/hydrolase POPTR_0013s14860 -2.062 34 1.41×10-6 xyloglucan endotransglucosylase/hydrolase POPTR_0010s23100 -2.013 57 6.39×10-6 phenylalanine/histidine ammonia-lyases, active site; phenylalanine ammonia-lyase 纤维素合成 POPTR_0003s14230 -2.656 26 2.28×10-9 cellulose synthase Cellulose synthesis POPTR_0002s20130 -3.850 09 1.20×10-8 cellulose synthase POPTR_0014s12000 -2.448 48 3.08×10-7 cellulose synthase 上调转录因子
Up-regulate transcription factorsAP2-EREBP POPTR_0003s15060 3.926 373 1.82×10-13 ethylene-responsive transcription factor ERF106 POPTR_0003s07910 6.005 648 9.03×10-30 pathogenesis-related transcriptional factor/ERF POPTR_0001s15390 2.893 319 1.39×10-10 pathogenesis-related transcriptional factor/ERF POPTR_0006s23480 4.311 008 5.06×10-10 pathogenesis-related transcriptional factor/ERF POPTR_0009s10470 4.597 455 1.10×10-9 pathogenesis-related transcriptional factor/ERF POPTR_0015s13830 4.803 138 3.96×10-8 pathogenesis-related transcriptional factor/ERF POPTR_0002s08610 2.231 947 4.25×10-7 pathogenesis-related transcriptional factor/ERF POPTR_0003s13610 3.464 754 2.20×10-6 pathogenesis-related transcriptional factor/ERF POPTR_0001s15550 3.183 902 5.26×10-6 pathogenesis-related transcriptional factor/ERF POPTR_0014s09540 9.120 961 1.63×10-11 pathogenesis-related transcriptional factor/ERF POPTR_0006s14100 4.137 601 1.77×10-8 pathogenesis-related transcriptional factor/ERF POPTR_0002s06620 2.297 645 1.35×10-7 pathogenesis-related transcriptional factor/ERF POPTR_0017s08250 2.551 527 2.38×10-6 pathogenesis-related transcriptional factor/ERF POPTR_0012s13880 2.173 311 4.10×10-5 pathogenesis-related transcriptional factor/ERF POPTR_0005s08940 2.850 637 1.40×10-9 pathogenesis-related transcriptional factor/ERF bHLH POPTR_0005s22870 5.416 638 8.03×10-14 helix-loop-helix DNA-binding POPTR_0004s02870 4.947 659 2.29×10-13 helix-loop-helix DNA-binding POPTR_0001s27680 3.088 316 6.92×10-12 helix-loop-helix DNA-binding POPTR_0003s05010 3.544 713 1.26×10-6 helix-loop-helix DNA-binding POPTR_0018s09060 2.513 479 1.75×10-6 helix-loop-helix DNA-binding POPTR_0001s29400 2.408 46 1.85×10-6 helix-loop-helix DNA-binding POPTR_0019s11870 2.055 089 2.34×10-6 helix-loop-helix DNA-binding POPTR_0010s14010 2.599 038 3.95×10-6 helix-loop-helix DNA-binding POPTR_0010s08760 7.719 238 5.45×10-6 helix-loop-helix DNA-binding POPTR_0001s18660 2.835 36 6.24×10-6 helix-loop-helix DNA-binding POPTR_0005s04160 5.664 689 2.00×10-20 transcription factor bHLH99 MYB POPTR_0003s06320 2.583 688 1.47×10-8 MYB-like DNA-binding protein POPTR_0007s14630 3.054 572 3.85×10-10 MYB domain protein 87 POPTR_0017s04890 3.299 653 3.43×10-9 putative MYB transcription factor POPTR_0001s07830 2.490 851 3.49×10-8 MYB-like DNA-binding domain POPTR_0014s11230 2.845 941 1.04×10-7 MYB-like DNA-binding domain POPTR_0007s11470 3.070 633 8.56×10-12 MYB-like DNA-binding domain POPTR_0017s04720 4.004 355 2.89×10-17 MYB-like DNA-binding domain POPTR_0010s18130 4.068 391 1.50×10-12 MYB-like DNA-binding domain POPTR_0001s02010 6.986 829 0.000517 MYB-like DNA-binding domain POPTR_0018s06410 9.007 962 5.84×10-11 MYB-like DNA-binding domain POPTR_0006s15480 2.275 316 2.63×10-5 MYB-like DNA-binding domain POPTR_0005s21420 4.377 921 1.70×10-17 MYB-like DNA-binding domain POPTR_0016s12430 2.263 672 1.01×10-6 MYB-CC type transcription factor POPTR_0006s10190 2.025 607 8.49×10-6 MYB-CC type transcription factor POPTR_0001s22660 5.347 404 1.52×10-10 MYB-CC type transcription factor POPTR_0004s02570 5.778 901 1.25×10-9 MYB-CC type transcription factor POPTR_0006s12400 4.105 249 2.30×10-8 MYB-CC type transcription factor POPTR_0005s24550 2.524 575 3.04×10-8 MYB-CC type transcription factor POPTR_0011s12750 3.745 664 1.47×10-5 MYB-CC type transcription factor POPTR_0002s07440 3.708 866 5.67×10-13 MYB-like DNA-binding protein POPTR_0001s20370 4.142 885 9.88×10-14 MYB-like DNA-binding domain POPTR_0009s03240 4.551 641 1.71×10-16 putative MYB family transcription factor MYB59 POPTR_0008s16660 6.760 851 7.71×10-20 MYB-like DNA-binding domain POPTR_0011s04120 7.339 587 4.98×10-26 MYB transcription factor-related POPTR_0017s04720 4.004 355 2.89×10-17 MYB-like DNA-binding domain POPTR_0009s03990 2.642 05 3.19×10-9 MYB-like DNA-binding domain WRKY POPTR_0001s10490 3.049 334 8.40×10-10 putative WRKY transcription factor 41 POPTR_0001s13600 2.678 04 1.89×10-9 putative WRKY transcription factor 45 POPTR_0001s13610 3.055 109 5.18×10-11 putative WRKY transcription factor POPTR_0002s16590 2.778 68 7.05×10-10 WRKY transcription factor 22 POPTR_0003s13840 3.925 765 1.27×10-14 putative WRKY transcription factor 53 POPTR_0003s18060 4.696 985 2.94×10-21 putative WRKY transcription factor 40 POPTR_0008s09140 4.204 637 2.08×10-16 putative WRKY transcription factor 3 POPTR_0015s07530 2.614 523 3.20×10-9 DNA-binding WRKY POPTR_0015s11130 2.538 428 6.01×10-9 WRKY transcription factor 75 POPTR_0017s11570 3.024 346 1.44×10-10 putative WRKY transcription factor 72 POPTR_0002s21330 5.191 626 1.31×10-12 DNA-binding WRKY POPTR_0003s16750 3.001 877 2.79×10-11 DNA-binding WRKY POPTR_0001s34520 2.472 224 1.91×10-8 DNA-binding WRKY POPTR_0016s13600 2.270 756 2.06×10-7 DNA-binding WRKY POPTR_0002s19630 2.314 696 2.31×10-7 DNA-binding WRKY POPTR_0001s09900 2.442 682 1.90×10-6 DNA-binding WRKY POPTR_0019s14460 2.760 178 5.27×10-10 WRKY transcription factor 25 上调基因
Up-regulate genes乙酰化相关 POPTR_0005s18970 6.099 277 7.99×10-16 GCN5-related N-acetyltransferase (GNAT) domain Acetylation related POPTR_0007s13930 2.380 817 3.83×10-8 Histone H1/H5 POPTR_0006s01190 2.205 723 5.79×10-7 chloramphenicol acetyltransferase-like domain POPTR_0016s11990 2.709 516 4.48×10-6 chloramphenicol acetyltransferase-like domain POPTR_0008s15450 3.704 659 9.50×10-14 GCN5-related N-acetyltransferase (GNAT) domain POPTR_0003s18090 3.476 053 3.90×10-7 GCN5-related N-acetyltransferase (GNAT) domain POPTR_0010s06380 3.686 076 8.04×10-14 chloramphenicol acetyltransferase-like domain POPTR_0010s19360 2.671 295 1.16×10-7 chloramphenicol acetyltransferase-like domain POPTR_0019s14700 2.592 051 1.44×10-6 chloramphenicol acetyltransferase-like domain POPTR_0018s11840 7.567 995 1.27×10-5 chloramphenicol acetyltransferase-like domain POPTR_0010s06390 7.306 48 7.55×10-5 chloramphenicol acetyltransferase-like domain POPTR_0005s11860 2.582 812 3.05×10-9 Histone H5 细胞周期 POPTR_0008s08890 4.544 545 3.32×10-16 cell cycle and apoptosis regulator protein Cell cyclin POPTR_0008s08880 5.080 659 7.40×10-7 cell cycle and apoptosis regulator protein POPTR_0002s12450 2.348 594 8.65×10-8 cyclin-like POPTR_0002s11980 4.406 009 7.55×10-5 cyclin-like POPTR_0001s45630 4.777 505 3.77×10-13 F-box domain, cyclin-like POPTR_0011s01490 3.731 533 3.69×10-12 F-box domain, cyclin-like POPTR_0009s05230 2.808 402 1.65×10-9 F-box domain, cyclin-like POPTR_0006s22490 2.553 471 3.17×10-8 F-box domain, cyclin-like POPTR_0003s19730 2.329 87 6.76×10-8 F-box domain, cyclin-like 木质素合成 POPTR_0006s07060 2.624 056 1.87×10-9 xyloglucan endotransglucosylase/hydrolase Lignin synthesis POPTR_0007s14570 4.197 216 9.25×10-18 xyloglucan endotransglucosylase/hydrolase POPTR_0002s06120 3.670 01 4.53×10-13 xyloglucan endotransglucosylase/hydrolase POPTR_0003s09590 3.004 086 1.75×10-11 xyloglucan endotransglucosylase/hydrolase POPTR_0005s22300 2.032 963 1.03×10-5 xyloglucan endotransglucosylase/hydrolase POPTR_0001s07100 8.394 74 2.93×10-8 xyloglucan fucosyltransferase POPTR_0001s07130 2.411 038 3.25×10-7 xyloglucan fucosyltransferase POPTR_0018s10300 4.105 44 9.51×10-14 xyloglucan endo-transglycosylase, C-terminal 纤维素合成 POPTR_0011s07040 2. 549 334 2.01×10-5 cellulose synthase Cellulose synthesis POPTR_0009s17100 4.878 897 1.65×10-8 cellulose synthase
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