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Acta Agronomica Sinica ›› 2021, Vol. 47 ›› Issue (9): 1639-1653.doi: 10.3724/SP.J.1006.2021.04223

• RESEARCH PAPERS • Previous Articles     Next Articles

Identification of gene co-expression modules of peanut main stem growth by WGCNA

WANG Ying(), GAO Fang, LIU Zhao-Xin, ZHAO Ji-Hao, LAI Hua-Jiang, PAN Xiao-Yi, BI Chen, LI Xiang-Dong, YANG Dong-Qing*()   

  1. College of Agronomy, Shandong Agricultural University / State Key Laboratory of Crop Biology, Tai’an 271018, Shandong, China
  • Received:2020-10-02 Accepted:2021-01-21 Online:2021-09-12 Published:2021-02-20
  • Contact: YANG Dong-Qing E-mail:15610413063@163.com;chengyang2364@sdau.edu.cn
  • Supported by:
    National Key Research and Development Program of China “Physiological Basis and Agronomic Management for High-quality and High-yield of Field Cash Crops”(2018YFD1000900);Shandong Key Research and Development Program(2018YFJH0601-3);Shandong Agricultural Application Technology Innovation Project(SD2019ZZ11);Shandong Modern Agricultural Industrial Technology System Peanut Innovation Team Chief Expert Special Fund(SDAIT-04-01)

Abstract:

This study was investigated the difference of transcriptome using three different peanut varieties with high main stem by RNA-seq. Transcriptomics combined with weighted gene co-expression network analysis (WGCNA) was used to explore the hub genes related to main stem growth and the molecular mechanisms of morphological formation of peanut stems. Results showed that 5872 differential expressed genes (DEGs) were detected in the Df216 and Huayu 33 comparation group, while 6662 DEGs were detected in the Df216 and Shanhua 108 comparation group. GO analysis suggested that these DEGs were mainly involved in molecular function and biological process, including the primary and secondary cell wall organization and biogenesis, phenylpropanoid biosynthetic and metabolic process, lignin biosynthetic process, and cellulose synthase activity, respectively. There were 33 modules were identified by WGCNA, among which five modules (Grey60, Cyan, Darkolivegreen, Brown, and Blue) were highly significant association with main stem height. According to the connectivity of genes in modules, caffeoyl-CoA O-methyltransferase, transcription factorATAF2, WAT1 (walls are thin1), and GDSL esterase/lipase were the hub genes, respectively. The results of hub gene networks by weighted values indicated that coumaroylquinate 3’-monooxygenase, 4-coumarate-CoA ligase, shikimate O-hydroxycinnamoyltransferase, rapid alkalinization factor,COBRA-like protein, and zinc finger protein had high connections with ADRL3Lin the Grey60 module, while β-1,4-galactosyltransferase, LRR receptor-like serine/threonine-protein kinase, pectin acetylesterase, leucine-rich repeat extensin-like protein had high connections with TZB0A2 in the Brown module. The identification of co-expression modules and their hub genes, and the analysis of gene function and gene networks of key genes will be helpful for revealing the genetic basis of the main height in peanut.

Key words: peanut, plant height, transcriptome, weighted gene co-expression network, hub gene

Fig.1

Phenotypic characterization at 90 days after sowing and changes of main stem height in three cultivars PP333: Shanhua 108 sprayed with paclobutrazol; GA3: Shanhua 108 sprayed with gibberellin. "

Fig. 2

Comparison of differentially expressed genes in three cultivars"

Fig. 3

Comparison and GO classification of differentially expressed genes in three cultivars"

Table 1

Significant GO terms in each different comparison groups"

比较组
Comparison group
GO本体类型
GO ontology
GO条目
GO term
GO注释
GO annotation
基因数
Count
校正后的P
P-value
花育33号vs. Df216
Huayu 33 vs. Df216
生化过程
Biological process
GO:0009250 葡聚糖生物合成的过程
Glucan biosynthetic process
50 0.041165
生化过程
Biological process
GO:0010411 木葡聚糖代谢过程
Xyloglucan metabolic process
23 0.018282
山花108 vs. Df216
Shanhua 108 vs. Df216
分子功能
Molecular function
GO:0001046 核心启动子序列特异性DNA结合
Core promoter sequence-specific DNA binding
21 0.003117
分子功能
Molecular function
GO:0001047 核心启动子整合
Core promoter binding
21 0.003117
分子功能
Molecular function
GO:0016762 木葡聚糖: 木葡糖基转移酶活性
Xyloglucan:xyloglucosyl transferase activity
21 0.003117
分子功能
Molecular function
GO:0015171 氨基酸跨膜转运蛋白活性
Amino acid transmembrane transporter activity
47 0.025596
生化过程
Biological process
GO:0000271 多糖生物合成的过程
Polysaccharide biosynthetic process
92 0.001366
生化过程
Biological process
GO:0015849 有机酸运输
Organic acid transport
74 0.003012
生化过程
Biological process
GO:0046942 羧酸运输
Carboxylic acid transport
74 0.003012
山花108 vs. 花育33号
Shanhua 108 vs. Huayu 33
细胞组成
Cellular component
GO:0044421 胞外区部分
Extracellular region part
34 0.001703
分子功能
Molecular function
GO:0004185 丝氨酸型羧肽酶活性
Serine-type carboxypeptidase activity
16 0.003464
分子功能
Molecular function
GO:0070008 丝氨酸型外肽酶活性
Serine-type exopeptidase activity
16 0.00394
生化过程
Biological process
GO:0003333 氨基酸跨膜转运
Amino acid transmembrane transport
25 0.001824
生化过程
Biological process
GO:0007267 细胞间信号传导
Cell-cell signaling
13 0.011421
生化过程
Biological process
GO:0098656 阴离子跨膜转运
Anion transmembrane transport
39 0.039813

Table 2

Significant GO terms among different comparison groups"

GO条目
GO term
GO注释
GO annotation
花育33号vs. Df216 Huayu 33 vs. Df216 山花108 vs. Df216
Shanhua 108 vs. Df216
山花108 vs. 花育33号 Shanhua 108 vs. Huayu 33
基因数
Count
校正后的P
P-value
基因数
Count
校正后的P
P-value
基因数
Count
校正后的P
P-value
GO:0031225 膜的锚固成分
Anchored component of membrane
98 4.553E-11 89 0.0001002 67 7.96E-08
GO:0005578 蛋白质的细胞外基质
Proteinaceous extracellular matrix
12 0.004731 12 0.036629 13 8.511E-06
GO:0046658 质膜锚定成分
Anchored component of plasma membrane
55 0.0047443 57 0.0664356 52 5.388E-07
GO:2000652 次生细胞壁生物发生的调控
Regulation of secondary cell wall biogenesis
17 9.805E-05 16 0.0016265 10 0.0185837
GO:1903338 细胞壁组织或生物发生的调节
Regulation of cell wall organization or biogenesis
27 2.636E-05 24 0.0033336 18 0.0013154
GO:0051274 葡聚糖生物合成的过程
Beta-glucan biosynthetic process
42 0.0009383 48 0.0002424 29 0.0068829
GO:0051273 葡聚糖代谢过程
Beta-glucan metabolic process
55 2.754E-05 58 0.0001085 41 6.796E-05
GO:0044042 葡聚糖代谢过程
Glucan metabolic process
90 0.0001556 98 0.000349 66 0.0002696
GO:0034637 细胞碳水化合物的生物合成过程
Cellular carbohydrate biosynthetic process
74 0.0463189 97 9.156E-05 58 0.0042563
GO:0030244 纤维素生物合成的过程
Cellulose biosynthetic process
37 0.0003169 43 3.566E-05 24 0.0114207
GO:0030243 纤维素代谢过程
Cellulose metabolic process
48 2.636E-05 51 5.814E-05 36 5.853E-05
GO条目
GO term
GO注释
GO annotation
花育33号vs. Df216 Huayu 33 vs. Df216 山花108 vs. Df216
Shanhua 108 vs. Df216
山花108 vs. 花育33号 Shanhua 108 vs. Huayu 33
基因数
Count
校正后的P
P-value
基因数
Count
校正后的P
P-value
基因数
Count
校正后的P
P-value
GO:0009834 次生细胞壁生物发生
Secondary cell wall biogenesis
70 1.901E-22 85 2.361E-31 23 0.0430558
GO:0009832 细胞壁生物起源
Cell wall biogenesis
103 3.631E-17 125 2.642E-24 45 0.016437
GO:0009831 植物型细胞壁修饰或参与多维细胞生长
Plant-type cell wall modification
or involved in multidimensional cell growth
13 0.0017006 14 0.0013665 11 0.0007573
GO:0009825 多维细胞生长
Multidimensional cell growth
25 0.0487668 32 0.0017647 23 0.0010804
GO:0009664 细胞壁组织
Cell wall organization
70 1.685E-05 82 2.134E-07 54 5.871E-06
GO:0006865 氨基酸转运
Amino acid transport
40 0.0487668 53 0.0002826 32 0.0077748
GO:0006073 细胞葡聚糖代谢过程
Cellular glucan metabolic process
90 0.0001556 98 0.000349 66 0.0002696

Fig. 4

Significant GO terms in Huayu 33 vs. Df216 (A) and Shanhua 108 vs. Df216 (B) groups"

Table 3

Significantly different expressed genes in different comparison groups"

基因
Gene
基因功能描述
Gene description
花育33号vs. Df216
Huayu 33 vs. Df216
山花108 vs. Df216
Shanhua 108 vs. Df216
差异
倍数
log2 Fold Change
P
P-value
差异
倍数
log2 Fold Change
P
P-value
Arahy.Tifrunner.gnm1.ann1.65D6GP 纤维素合酶A (CESA) Cellulose synthase A (CESA) -5.494 2.564E-06 -5.076 0.0001548
Arahy.Tifrunner.gnm1.ann1.KX036Y 纤维素合酶A (CESA) Cellulose synthase A (CESA) -6.518 2.591E-16 -3.232 3.313E-05
Arahy.Tifrunner.gnm1.ann1.S1R27D 纤维素合酶A (CESA) Cellulose synthase A (CESA) -6.874 7.371E-08 -1.553 0.000396
Arahy.Tifrunner.gnm1.ann1.TQ1ANH 纤维素合酶A (CESA) Cellulose synthase A (CESA) -2.204 1.035E-07 -6.746 4.079E-27
Arahy.Tifrunner.gnm1.ann1.V28JVI 纤维素合酶A (CESA) Cellulose synthase A (CESA) -2.263 7.811E-07 -6.165 1.262E-05
Arahy.Tifrunner.gnm1.ann1.VZR30Z 纤维素合酶A (CESA) Cellulose synthase A (CESA) -5.455 1.812E-15 -2.666 3.491E-05
Arahy.Tifrunner.gnm1.ann1.906G3Q 类COBRA蛋白 COBRA-like protein -2.324 0.0031254 -3.232 3.313E-05
Arahy.Tifrunner.gnm1.ann1.D1AFGR 类COBRA蛋白 COBRA-like protein -2.403 2.538E-06 -1.553 0.000396
Arahy.Tifrunner.gnm1.ann1.TNUB95 类COBRA蛋白 COBRA-like protein -2.270 0.0011721 -6.746 4.079E-27
Arahy.Tifrunner.gnm1.ann1.26LA0S MYB转录因子 Transcription factor MYB -8.816 2.627E-12 -8.747 4.412E-12
Arahy.Tifrunner.gnm1.ann1.9732XC MYB转录因子 Transcription factor MYB -1.108 0.0021535 -1.327 0.0001081
Arahy.Tifrunner.gnm1.ann1.BEF3I8 MYB转录因子 Transcription factor MYB -1.256 0.0003772 -1.329 0.0001474
Arahy.Tifrunner.gnm1.ann1.EHBV2Z MYB转录因子 Transcription factor MYB -2.763 0.0008392 -2.469 0.002727
Arahy.Tifrunner.gnm1.ann1.I7UCTP MYB转录因子 Transcription factor MYB -2.393 0.0001061 -2.336 0.0009775
Arahy.Tifrunner.gnm1.ann1.0B4MFB 苯丙氨酸解氨酶(PAL)
Phenylalanine ammonia-lyase (PAL)
-3.265 6.1E-12 -2.814 1.7409E-11
Arahy.Tifrunner.gnm1.ann1.5H4H17 苯丙氨酸解氨酶(PAL) Phenylalanine ammonia-lyase -2.331 0.003147 -2.474 0.00036061
Arahy.Tifrunner.gnm1.ann1.NB2RRK 苯丙氨酸解氨酶(PAL)
Phenylalanine ammonia-lyase (PAL)
-3.255 7.62E-12 -2.839 1.2212E-11
Arahy.Tifrunner.gnm1.ann1.V1SQAY 苯丙氨酸解氨酶(PAL)
Phenylalanine ammonia-lyase (PAL)
-2.383 5.57E-11 -1.973 4.7356E-09
基因
Gene
基因功能描述
Gene description
花育33号vs. Df216
Huayu 33 vs. Df216
山花108 vs. Df216
Shanhua 108 vs. Df216
差异
倍数
log2 Fold Change
P
P-value
差异
倍数
log2 Fold Change
P
P-value
Arahy.Tifrunner.gnm1.ann1.AYA1A5 肉桂酸-4-单加氧酶(CYP73A)
Trans-cinnamate 4-monooxygenase (CYP73A)
-1.393 0.000882 -1.173 0.00020608
Arahy.Tifrunner.gnm1.ann1.K1LFJJ 肉桂酸-4-单加氧酶(CYP73A)
Trans-cinnamate 4-monooxygenase (CYP73A)
-1.766 2.92E-05 -1.497 8.6362E-06
Arahy.Tifrunner.gnm1.ann1.SGZ2CH 肉桂酸-4-单加氧酶(CYP73A)
Trans-cinnamate 4-monooxygenase (CYP73A)
-2.124 3.62E-28 -1.839 1.1701E-27
Arahy.Tifrunner.gnm1.ann1.NC09XL 4-香豆酸辅酶A连接酶(4CL)
4-coumarate-CoA ligase (4CL)
-2.127 6.10E-13 -1.695 1.9119E-09
Arahy.Tifrunner.gnm1.ann1.ST1ALI 4-香豆酸辅酶A连接酶(4CL)
4-coumarate-CoA ligase (4CL)
-2.222 9.10E-18 -1.600 9.8676E-12
Arahy.Tifrunner.gnm1.ann1.DXZI51 肉桂酰辅酶A还原酶(CCR)
Cinnamoyl-CoA reductase(CCR)
-2.881 2.05E-05 -3.467 4.0937E-06
Arahy.Tifrunner.gnm1.ann1.FW0QWP 肉桂酰辅酶A还原酶(CCR)
Cinnamoyl-CoA reductase (CCR)
-3.016 4.02E-07 -3.442 1.4653E-05
Arahy.Tifrunner.gnm1.ann1.ULUR0X 肉桂酰辅酶A还原酶(CCR)
Cinnamoyl-CoA reductase (CCR)
-2.552 9.27E-24 -1.880 3.7164E-13
Arahy.Tifrunner.gnm1.ann1.AJ1Q9U 莽草酸香豆酯/奎酸酯3’-羟化酶(C3’H)
Coumaroyl shikimate/quinate 3’-hydroxylases (C3’H)
-1.828 5.243E-12 -1.324 7.724E-08
Arahy.Tifrunner.gnm1.ann1.555M2B 咖啡酸3-O-甲基转移酶(COMT)
Caffeic acid 3-O-methyltransferase (COMT)
-1.438 9.47E-05 -1.014 0.00374356
Arahy.Tifrunner.gnm1.ann1.GM134S 咖啡酸3-O-甲基转移酶(COMT)
Caffeic acid 3-O-methyltransferase (COMT)
-1.765 7.80E-07 -1.447 8.2856E-06
Arahy.Tifrunner.gnm1.ann1.I1E7E1 咖啡酸3-O-甲基转移酶(COMT)
Caffeic acid 3-O-methyltransferase
-2.028 0.005323 -1.957 0.00818603
Arahy.Tifrunner.gnm1.ann1.MG688V 阿魏酸5-羟化酶(F5H) Ferulate-5-hydroxylase (F5H) -2.550 5.69E-25 -1.689 2.8239E-08
Arahy.Tifrunner.gnm1.ann1.PFDI3N 阿魏酸5-羟化酶(F5H) Ferulate-5-hydroxylase (F5H) -2.441 1.78E-17 -1.547 2.4651E-06
Arahy.Tifrunner.gnm1.ann1.ADRL3L 咖啡酰辅酶A-O-甲基转移酶(CCoAOMT)
Caffeoyl-CoA O-methyltransferase (CCoAOMT)
-1.873 3.96E-08 -1.438 3.3642E-06
Arahy.Tifrunner.gnm1.ann1.QGH881 咖啡酰辅酶A-O-甲基转移酶(CCoAOMT)
Caffeoyl-CoA O-methyltransferase (CCoAOMT)
-1.640 3.20E-08 -1.283 7.9012E-06
Arahy.Tifrunner.gnm1.ann1.WH9NWR 咖啡酰辅酶A-O-甲基转移酶(CCoAOMT)
Caffeoyl-CoA O-methyltransferase (CCoAOMT)
-1.493 1.55E-07 -1.258 1.7761E-06

Fig.5

Genes cluster and soft threshold β of different varieties comparison groups"

Fig. 6

Gene cluster dendrogram and module and its high relationships with plant stem height"

Table 4

Description of hub genes in the modules"

模块
Module
核心基因
Hub gene
基因功能描述
Gene description
Black arahy.Tifrunner.gnm1.ann1.Q5T5LU NADH脱氢酶 NADH dehydrogenase
Blue arahy.Tifrunner.gnm1.ann1.Z11ITV 功能未知 Uncharacterized
Brown arahy.Tifrunner.gnm1.ann1.TZB0A2 GDSL酯酶/脂肪酶 GDSL esterase/lipase
Cyan arahy.Tifrunner.gnm1.ann1.X47CQ0 转录因子ATAF2 ATAF2 transcription factor
Darkgreen arahy.Tifrunner.gnm1.ann1.A6Q8V1 功能未知 Uncharacterized
Darkgrey arahy.Tifrunner.gnm1.ann1.1KSV8R 4-香豆酸辅酶A连接酶 (4CL) 4-coumarate-CoA ligase (4CL)
Darkolivegreen arahy.Tifrunner.gnm1.ann1.5B5NV8 薄壁蛋白 WALLS ARE THIN1 (WAT1)
Darkorange arahy.Tifrunner.gnm1.ann1.6255L4 纤维素合酶A Cellulose synthase A
Darkred arahy.Tifrunner.gnm1.ann1.LML9QV 果糖二磷酸醛缩酶 Fructose-bisphosphate aldolase
Darkturquoise arahy.Tifrunner.gnm1.ann1.SHEQ35 质膜ATP酶4 Plasma membrane ATPase 4
Green arahy.Tifrunner.gnm1.ann1.MF538D 光系统I亚基XI Photosystem I subunit XI
Greenyellow arahy.Tifrunner.gnm1.ann1.9WC044 网格蛋白组装蛋白 Clathrin assembly protein
Grey60 arahy.Tifrunner.gnm1.ann1.ADRL3L 咖啡酰辅酶A Caffeoyl-CoA O-methyltransferase
Lightcyan arahy.Tifrunner.gnm1.ann1.FY9BZZ 晚期胚胎富集蛋白, Lea 5 Late embryogenesis abundant protein, Lea 5
Lightgreen arahy.Tifrunner.gnm1.ann1.01T93A FCS类锌蛋白指17 FCS-like zinc finger 17
Lightyellow arahy.Tifrunner.gnm1.ann1.34EHR3 GDSL酯酶/脂肪酶 GDSL esterase/lipase
Magenta arahy.Tifrunner.gnm1.ann1.178YCU 功能未知 Uncharacterized
Midnightblue arahy.Tifrunner.gnm1.ann1.1C5B46 28S核糖体核糖核酸 28S ribosomal RNA
Orange arahy.Tifrunner.gnm1.ann1.1EF43V Iojap蛋白 Protein Iojap
Paleturquoise arahy.Tifrunner.gnm1.ann1.BGN30W 大亚基核糖体蛋白L15 Large subunit ribosomal protein L15
Pink arahy.Tifrunner.gnm1.ann1.3896ZX 脂质体相关蛋白7 Probable plastid-lipid-associated protein 7
Purple arahy.Tifrunner.gnm1.ann1.75V8XQ BAHD酰基转移酶 BAHD acyltransferase DCR
Red arahy.Tifrunner.gnm1.ann1.8M9DZW 脱水早期响应蛋白7 Early-responsive to dehydration 7
Royalblue arahy.Tifrunner.gnm1.ann1.512HAI 五肽重复域含蛋白1 Pentatricopeptide repeat domain-containing protein 1
Saddlebrown arahy.Tifrunner.gnm1.ann1.84UTM8 酪蛋白激酶II亚基-2 Casein kinase II subunit beta-2-like
Salmon arahy.Tifrunner.gnm1.ann1.0ZKW04 膜蛋白PM19L Membrane protein PM19L
Skyblue arahy.Tifrunner.gnm1.ann1.HUVM91 类CASP蛋白质2B2 CASP-like protein 2B2
Steelblue arahy.Tifrunner.gnm1.ann1.XM49AS 功能未知 Uncharacterized
Tan arahy.Tifrunner.gnm1.ann1.EYFM1K 伸展蛋白 Extensin
Turquoise arahy.Tifrunner.gnm1.ann1.EPZ5Z8 功能未知 Uncharacterized
Violet arahy.Tifrunner.gnm1.ann1.P9IGRK 40S核糖体蛋白S19-1 40S ribosomal protein S19-1
White arahy.Tifrunner.gnm1.ann1.R57BTI 核碱基抗坏血酸转运蛋白4 Nucleobase-ascorbate transporter 4
Yellow arahy.Tifrunner.gnm1.ann1.P5C9KT 线粒体GTPase 1 Mitochondrial GTPase 1

Fig.7

Gene networks of hub genes of significant co-expression modules A and B represent Grey60 and Brown modules, respectively."

Table 5

Genes associated with hub gene in Grey60 and Brown modules and their function annotations"

模块
Module
关联基因
Associated gene
权重
Weight
基因功能描述
Gene function annotations
Grey60 arahy.Tifrunner.gnm1.ann1.AJ1Q9U 0.1318 莽草酸香豆酯/奎酸酯3’-羟化酶(C3’H)
Coumaroyl shikimate/quinate 3’-hydroxylases (C3’H)
arahy.Tifrunner.gnm1.ann1.QGH881 0.1183 咖啡酰辅酶A-O-甲基转移酶(CCoAOMT)
Caffeoyl-CoA O-methyltransferase (CCoAOMT)
arahy.Tifrunner.gnm1.ann1.NC09XL 0.1175 4-香豆酸辅酶A连接酶(4CL)
4-coumarate-CoA ligase (4CL)
arahy.Tifrunner.gnm1.ann1.AXL13P 0.1169 莽草酸香豆酯/奎酸酯3’-羟化酶(C3'H)
Coumaroyl shikimate/quinate 3’-hydroxylases (C3'H)
arahy.Tifrunner.gnm1.ann1.ST1ALI 0.1109 4-香豆酸辅酶A连接酶(4CL)
4-coumarate-CoA ligase (4CL)
arahy.Tifrunner.gnm1.ann1.M5N13L 0.1086 快速碱化因子(RALF)
Rapid alkalinization factor (RALF)
模块
Module
关联基因
Associated gene
权重
Weight
基因功能描述
Gene function annotations
arahy.Tifrunner.gnm1.ann1.T3N7AF 0.1049 锌指蛋白
Zinc finger protein
arahy.Tifrunner.gnm1.ann1.D1AFGR 0.1046 类COBRA蛋白
COBRA-like protein
arahy.Tifrunner.gnm1.ann1.ND3FHR 0.1034 羟基肉桂酰辅酶A莽草酸/奎尼酸羟基肉桂酰转移(HCT)
Shikimate O-hydroxycinnamoyltransferase (HCT)
arahy.Tifrunner.gnm1.ann1.N9L63V 0.1027 鼠李半乳糖醛酸聚糖裂解酶(RGL)
Rhamnogalacturonan lyase (RGL)
Brown arahy.Tifrunner.gnm1.ann1.WKJE7A 0.1711 半乳聚糖β-1,4-半乳糖基转移酶(GALS3)
Galactan beta-1,4-galactosyltransferase (GALS3)
arahy.Tifrunner.gnm1.ann1.XNX4G2 0.1556 LRR受体样丝氨酸/苏氨酸蛋白激酶(FEI1)
LRR receptor-like serine/threonine-protein kinase (FEI1)
arahy.Tifrunner.gnm1.ann1.ZIW1BH 0.1548 果胶乙酰酯酶(PAE)
Pectin acetylesterase (PAE)
arahy.Tifrunner.gnm1.ann1.U9FET0 0.1529 类成蛋白1
Formin-like protein 1
arahy.Tifrunner.gnm1.ann1.V8PY6L 0.1521 富含亮氨酸重复序列的类伸展蛋白(LRXs)
Leucine-rich repeat extensin-like protein (LRXs)
arahy.Tifrunner.gnm1.ann1.Y1E6HX 0.1434 葡聚糖内切1,3-β-葡糖苷酶13
Glucan endo-1,3-beta-glucosidase 13
arahy.Tifrunner.gnm1.ann1.ZES6QF 0.1421 碱性亮氨酸拉链蛋白(bZIP34)
Basic leucine zipper 34
arahy.Tifrunner.gnm1.ann1.X0GQC6 0.1416 磷酸糖转运蛋白
Sugar phosphate/phosphate translocator
arahy.Tifrunner.gnm1.ann1.UC02TM 0.1403 RR型类受体丝氨酸/苏氨酸蛋白激酶
LRR receptor-like serine/threonine-protein kinase
arahy.Tifrunner.gnm1.ann1.Z92X92 0.1399 羟脯氨酸O-半乳糖基转移酶HPGT1
Hydroxyproline O-galactosyltransferase HPGT1
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