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Acta Agronomica Sinica ›› 2019, Vol. 45 ›› Issue (2): 161-174.doi: 10.3724/SP.J.1006.2019.83053


Identification of maize flowering gene co-expression modules by WGCNA

Yu-Xin YANG1,Zhi-Qin SANG1,2,Cheng XU1,Wen-Shuang DAI1,Cheng ZOU1,*()   

  1. 1 Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China
    2 Xinjiang Academy of Agricultural and Reclamation Science, Shihezi 832000, Xinjiang, China
  • Received:2018-07-17 Accepted:2018-10-08 Online:2019-02-12 Published:2018-11-08
  • Contact: Cheng ZOU E-mail:zoucheng@caas.cn
  • Supported by:
    This study was supported by the National Key Research and Development Program of China(2016YFD0100303);the National Natural Science Foundation of China(31371638)


Weighted gene co-expression network analysis (WGCNA) is one of the research methods in systematic biology. It can effectively analyze the complex samples, and has been extensively used in the analysis of complicated traits for many samples. Weighted gene co-expression network has the characteristics of scale-free distribution and could construct the scale free network. The genes with similar expression level can be clustered and assigned to a module, then the relationships between co-expression modules and specific tissues can be furtherly analyzed. Our research utilized the transcriptome data of 14 different tissues of maize (Zea mays L.) inbred line B73, and calculated the gene expression level of the whole genome. Through filtering out the genes with low expression level we finally got 22,426 genes with high expression level to construct the gene expression matrix. We utilized the different tissues as the trait to construct the trait matrix. The weighted gene co-expression network analysis packages of R software was used to perform the co-expression network analysis, and 20 co-expression modules were identified. We finally obtained 14 tissue specific modules which were highly correlated with traits (r > 0.65). The enrichment analysis tool Agrigo was taken to perform the GO enrichment of the tissue specific module genes, all the 14 tissues could be enriched in GO terms. Flowering is one of the important agronomic traits in the life cycle of maize controlled by external environment signals and genetic factors. Maize flowering not only represents the transition from the vegetative growth to reproductive growth, also relates to grain yield, plant height and resistance. In our research, we detected eight tissue specific modules, which could be obtained within flowering time related pathways. In addition, 17 flowering genes which have been reported in the literatures were assigned to the co-expression modules, and mainly assigned to the Blue and Darkmagenta modules. Therefore, we focused on the network of Blue and Darkmagenta modules. Our research calculated the gene expression abundances, and detected several flowering time related modules, which will contribute to revealing the genetic mechanism of maize flowering time regulation.

Key words: maize, weighted gene co-expression network, development regulation, flowering, transcriptome

Fig. 1

Determination of soft threshold The abscissa represents the soft threshold (β). A: ordinate corresponds to the index of scale free network model; B: the average link degree of each soft threshold."

Fig. 2

Gene cluster dendrograms and module detecting A: clustering of genes based on the topological overlap. B: the gene modules obtained from the dynamic tree cut. C: the merged modules with similar expression pattern."

Fig. 3

Clustering dendrogram of samples and corresponding tissue information A: the gene cluster tree based on the Euclidean distance. The abscissa represents the different tissues. The ordinate represents the cluster height of genes. B: the association trait heatmap, the white means a low correlation, the red means a high correlation."

Fig. 4

Distribution of number of genes in modules The abscissa represents the modules and the vertical ordinate represents the gene number of each module."

Fig. 5

Heat map of module-trait relationship Each column represents the co-expression module. Red color of each box represents the positive correlation between module and trait. Green color of each box represents the negative relationships between module and trait."

Fig. 6

Enrichment pathway of flowering time Each row corresponds to a GO enrichment pathway, column to a tissue specific module. The point size is calculated by the P-value of multiple check. The Richfactor represent the ratio of input genes to the background genes."

Fig. 7

Gene co-expression network of the blue module"

Fig. 8

Gene co-expression network of the darkmagenta module"

Fig. 9

Gene interaction network of blue module Each node corresponding to a gene, the red node is the hub gene of the network and is the flowering time gene which had reported."

Fig. 10

The gene interaction network of darkmagenta module Each node corresponding to a gene, the red node is the hub gene of the network and is the flowering time gene which had reported."

Table 1

Annotation of candidate flowering gene in Darkmagenta and Blue modules"

Flowering gene
Candidate flowering gene
Homologous gene
in A. thaliana
Gene function
Blue ZCN8 GRMZM2G450273 FPF1 编码调节开花的小蛋白质并参与赤霉素信号传导途径, 在开花的光周期诱导后, 在顶端分生组织中表达
Encodes a small protein that regulates flowering and is involved in gibberellin signalling pathway. It is expressed in apical meristems immediately after the photoperiodic induction of flowering
ZCN7 GRMZM2G455413 PSBA 编码叶绿素结合蛋白D1, 属于光系统II反应中心
Encodes chlorophyll binding protein D1, belonging to photosystem II reaction center core
COL1 GRMZM2G128212 ZFP8 编码锌指蛋白
Encodes a zinc finger protein
PhyB1 GRMZM5G800407 PMAT2 编码消除酚类毒素的丙二酰转移酶
Encodes a malonyltransferase that may play a role in
phenolic xenobiotic detoxification
D8 GRMZM2G338809 AMT2 编码高亲和性的铵转运蛋白
Encodes a high-affinity ammonium transporter
D9 GRMZM2G429322 LHT1 编码一个在细胞间转运氨基酸的高亲和力蛋白
Encoding a high affinity protein that translocation amino acids between cells
ZmCCA1 GRMZM6G435553 PMI1 响应蓝光和渗透压胁迫
Response to blue light and osmotic stress
Darkmagenta GIGZ1B GRMZM2G333183 ABCB1 ATP结合蛋白, 调节生长素转运
ATP-binding protein, regulates the transport of auxin
PhyC2 GRMZM2G038846 AT1G19320 与发病机制相关的超家族蛋白
Pathogenesis-related thaumatin superfamily protein
GIGZ1A GRMZM2G104269 OASC 参与花粉管生长和受精
Involved in pollen tube growth and fertilization
ZmFKF1b GRMZM2G041065 ATAVP3 无机H焦磷酸酶家族蛋白, 在分生组织和花器官原基表达
Inorganic H pyrophosphatase family protein. Expressed in meristems and floral organ primordium
ZmFKF1a GRMZM2G027673 FAB2 植物硬脂酰酰基载体蛋白去饱和酶家族蛋白
Plant stearoyl-acyl-carrier-protein desaturase family protein
ZmPRR59 GRMZM2G107945 FKF1 编码黄素结合的F-box蛋白, 调节花期转变
Encodes flavin-binding F-box protein, regulates transition to flowering
ZmPRR59 GRMZM2G106363 LKP2 编码F-box蛋白, 响应红光和蓝光, 参与光周期途径
Encodes a member of F-box proteins, response to red and blue light, involved in photoperiod pathway

Supplementary table 1

GO enrichment analysis results of tissue specific module (part)"

GO term
Darkorange2 GO: 0009889 BP 生物合成过程调节Regulation of biosynthetic process 6.90E-07
Darkorange2 GO: 0006355 BP DNA依赖的转录调节Regulation of transcription, DNA-dependent 4.40E-07
Darkorange2 GO: 0015267 MF 通道活性Channel activity 0.00068
Darkorange2 GO: 0022838 MF 底物特异性通道活性Substrate-specific channel activity 0.00068
Blue GO: 0009628 BP 非生物刺激的反应Response to abiotic stimulus 3.60E-10
Blue GO: 0009416 BP 光刺激响应Response to light stimulus 1.60E-08
Blue GO: 0003700 MF 转录因子活性Transcription factor activity 0.00017
Blue GO: 0009535 CC 叶绿体类囊体膜Chloroplast thylakoid membrane 0.00022
Darkred GO: 0051186 BP 辅因子代谢过程Cofactor metabolic process 1.20E-19
Darkred GO: 0004252 MF 丝氨酸型肽链内切酶活性Serine-type endopeptidase activity 0.00015
Darkred GO: 0009543 CC 叶绿体类囊体腔 Chloroplast thylakoid lumen 4.40E-13
Darkslateblue GO: 0016051 BP 碳水化合物生物合成过程Carbohydrate biosynthetic process 5.60E-05
Darkslateblue GO: 0016830 MF 碳-碳裂解酶活性Carbon-carbon lyase activity 3.40E-06
Darkslateblue GO: 0042651 CC 类囊体膜Thylakoid membrane 0.00013
Turquoise GO: 0060560 BP 形态发生发育Developmental growth involved in morphogenesis 1.70E-11
Turquoise GO: 0015299 MF 溶质: 氢反向转运蛋白活性Solute: hydrogen antiporter activity 4.60E-05
Turquoise GO: 0031224 CC 内膜Intrinsic to membrane 8.50E-06
Darkmagenta GO: 0010927 BP 涉及形态发生的内膜组装
Cellular component assembly involved in morphogenesis
Darkmagenta GO: 0004553 MF 水解酶活性, 水解O-糖基化合物
Hydrolase activity, hydrolyzing O-glycosyl compounds
Darkmagenta GO: 0030312 CC 高尔基体Golgi apparatus 0.0004
Bisque4 GO: 0042180 BP 细胞酮代谢过程Cellular ketone metabolic process 3.00E-08
Bisque4 GO: 0044281 BP 小分子代谢过程Small molecule metabolic process 9.90E-06
Bisque4 GO: 0042221 BP 相应化学刺激Response to chemical stimulus 0.00032
Darkgrey GO: 0010033 BP 对有机物质的反应Response to organic substance 1.60E-07
Darkgrey GO: 0004553 MF 水解酶活性, 水解O-糖基化合物
Hydrolase activity, hydrolyzing O-glycosyl compounds
Darkgrey GO: 0005740 CC 线粒体包膜Mitochondrial envelope 7.40E-05
Floralwhite GO: 0006412 BP 蛋白质翻译Translation 9.10E-07
Floralwhite GO: 0005198 MF 结构分子活性Structural molecule activity 5.80E-08
Floralwhite GO: 0043227 CC 膜有界细胞器Membrane-bounded organelle 0.0085
Darkolivegreen GO: 0010022 BP 分生组织决定Meristem determinacy 6.10E-07
GO term
Darkolivegreen GO: 0003700 MF 转录因子活性Transcription factor activity 5.50E-05
Orange GO: 0042542 BP 过氧化氢反应Response to hydrogen peroxide 2.90E-05
Orange GO: 0009526 CC 质体Plastid 9.60E-09
Yellow GO: 0009605 BP 响应外界刺激Response to external stimulus 8.40E-10
Yellow GO: 0022892 MF 底物特异性转运体活性Substrate-specific transporter activity 0.00013
Plum2 GO: 0048437 BP 花器官发育Floral organ development 9.20E-05
Plum2 GO: 0005576 CC 胞外区Extracellular region 9.70E-05
Greenyellow GO: 0034220 BP 离子跨膜转运Ion transmembrane transport 5.00E-13
Greenyellow GO: 0032561 MF 鸟苷酸核糖核酸结合Guanyl ribonucleotide binding 2.40E-10
Greenyellow GO: 0043231 CC 内细胞器膜Organelle inner membrane 1.20E-17
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