Scientia Agricultura Sinica ›› 2025, Vol. 58 ›› Issue (6): 1065-1082.doi: 10.3864/j.issn.0578-1752.2025.06.003

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

Screening Regulatory Genes Related to Wheat Grain Protein Accumulation Based on Transcriptome and WGCNA Analysis

PAN LiYuan1(), WANG YongJun1, LI HaiJun1, HOU Fu1, LI Jing1, LI LiLi1, SUN SuYang1,2,3()   

  1. 1 Huaiyin Institute of Agricultural Sciences of Xuhuai Region in Jiangsu, Huai’an 223001, Jiangsu
    2 Zhongshan Laboratory of Biological Breeding, Jiangsu Academy of Agricultural Sciences, Nanjing 210014
    3 Jiangsu Provincial Collaborative Innovation Center of Modern Industrial Technology for Grain Crops, Yangzhou University, Yangzhou 225009, Jiangsu
  • Received:2024-08-04 Accepted:2024-09-20 Online:2025-03-25 Published:2025-03-25
  • Contact: SUN SuYang

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Abstract:

【Objective】 Common wheat, as an important food crop, plays a crucial role in global food security. Identifying the gene regulatory networks involved in wheat grain protein synthesis and determining key candidate genes will provide theoretical support for quality breeding and improvement of wheat. 【Method】 The study used wheat grains at six developmental stages (5, 10, 15, 20, 25, and 30 days post-anthesis) as research materials to summarize the pattern of protein accumulation in wheat grains. Transcriptome data and grain protein content phenotypic data were analyzed using the WGCNA (Weighted Gene Co-expression Network Analysis) method to construct weighted gene co-expression networks and identify key hub transcription factor (TFs) genes.【Result】 The accumulation of protein content in wheat grains showed a trend of initial decline followed by an increase, reaching its lowest value (12.16%) at 25 days post-anthesis, with significant differences in protein content between adjacent developmental stages. A total of 25 427 differentially expressed genes (DEGs) were identified between adjacent developmental stages. Cluster analysis divided these DEGs into five groups (A-E), with group B containing the highest number of DEGs (10 906). A total of 1 022 transcription factors (TFs) from 49 families were identified, with the NAC family containing the most TFs (107). WGCNA analysis identified five co-expression modules significantly associated with protein content. The turquoise module showed the highest positive correlation with protein content (r=0.80, P=1×10-⁴). By integrating differentially expressed genes and weighted gene co-expression networks, six positively regulated hub TFs from the MIKC-MADS, TCP, TALE, and CPP families were identified in two modules (turquoise and blue). Further correlation analysis between the protein content phenotype of Huaimai 48 and gene expression levels at different time points revealed that the expression levels of five hub TFs were significantly positively correlated with the protein content phenotype. Specifically, TraesCS5B03G0740100 and TraesCS7D03G0590500 showed specific high expression in spike and grain tissues.【Conclusion】 The study identified important modules (turquoise and blue) related to wheat protein content accumulation, screened six hub TFs, and identified that the expression levels of two hub TFs are significantly positively correlated with protein content and are specifically highly expressed in spike and grain tissues. These genes can serve as candidate genes for regulating protein accumulation in wheat grains.

Key words: common wheat, seed development, protein content, weighted gene co-expression network analysis, transcript factors

Table 1

The primers used for qRT-PCR in this study"

基因ID Gene ID 正向引物 Forward primer (5′-3′) 反向引物 Reverse primer (5′-3′)
TraesCS3A03G0074600 CGGAGATCATTGCGTAGGG GGAATTAGCACGTGTGGCG
TraesCS3A03G0885700 TCTTCCTTCATCGCTTCCATC TCCTCAGGGTGCCATCTATCA
TraesCS3A03G0888300 TACCCAGTTTTAGTAGACGCCC CTCGTTTTGTCCCAGTGTGC
TraesCS3A03G0891600 GAAGTGCGACGTGGATATAAGG GAAGGTACTGAGAGAGGCGAGA
TraesCS3A03G0891900 GAAGGCTTTTGGGGATGCT GCTATCCAATCGCTCTCCTCTT
TraesCS3A03G0892500 TCGTTCGGATGACAGTGCTT CTATCCCACATTTGGAAACAGG
TraesCS4B03G0043800 GAACAAATCCCAGCCATCCA ACGAGTAGGCGTTGGGTATTC
TraesCS4B03G0823800 TCCACCAGATGGCGGAGTT GGCGTGGGGAAGAGCGT
TraesCS6B03G0310500 GGGGAGGCACTATTGCTTTC CCAAAGTAGTCCGAAGCGTATC
TraesCS6B03G0312000 CCTGCTTTGATGGCTGGAC AAGAAGGGGAATGGGGCT
TaActin GGAATGGTCAAGGCTGGTTT CGGAGCTCGTTGTAGAATGTGT

Fig. 1

The phentotypic distribution of the protein content trait in developing seeds of Huaimai 48 A: Grains of Huaimai 48 at six different developmental stages; B: Graph showing the changes in protein content of Huaimai 48 grains at six different developmental stages. Different letters represent significiant differences at 0.05 level"

Table 2

Transcriptome sequencing quality of samples at different developmental stages"

样本
Sample		 时期
Stage
(d)		 原始reads数
Raw reads		 质控后reads数
Saved reads		 质量分数
High quality rate (%)		 比对率
Reads aligned
(%)		 多次比对率
Multialignment (%)		 单一比对率
Unique alignment (%)
05D.Rep1 5 53494726 53253286 99.55 88.31 6.18 94.49
05D.Rep2 5 41144322 40944134 99.51 88.17 6.22 94.38
05D.Rep3 5 42043100 41848014 99.54 88.55 6.14 94.69
10D.Rep1 10 43073974 42750556 99.25 82.85 6.39 89.23
10D.Rep2 10 45712962 45445466 99.41 85.54 6.37 91.91
10D.Rep3 10 47715540 47273162 99.07 80.03 6.62 86.65
15D.Rep1 15 46401552 45997986 99.13 73.62 8.65 82.27
15D.Rep2 15 40517866 40147604 99.09 72.56 8.86 81.42
15D.Rep3 15 44238716 43790148 98.99 71.59 9.02 80.61
20D.Rep1 20 37942654 37577108 99.04 70.18 10.93 81.11
20D.Rep2 20 41530148 41087334 98.93 68.35 11.76 80.11
20D.Rep3 20 53574728 52925588 98.79 69.67 14.02 83.69
25D.Rep1 25 52320432 51672172 98.76 66.29 14.04 80.34
25D.Rep2 25 46626444 46097376 98.87 66.08 13.96 80.04
25D.Rep3 25 51864528 51434414 99.17 69.34 12.86 82.20
30D.Rep1 30 54570678 53738308 98.47 61.09 16.36 77.44
30D.Rep2 30 51852354 51090038 98.53 67.55 12.04 79.59
30D.Rep3 30 55777132 55100978 98.79 68.56 12.38 80.94
共计/平均Total/Mean 850401856 842173672 99.05 74.35 10.16 84.51

Table 3

Numbers of genes detected in different samples of Huaimai 48"

样本
Sample		 已知基因数
No. of known genes		 新基因数
No. of new genes		 所有基因数
No. of all genes
05D.Rep1 87963 6413 94376
05D.Rep2 86713 6512 93225
05D.Rep3 86541 6394 92935
10D.Rep1 84695 6534 91229
10D.Rep2 87409 6613 94022
10D.Rep3 84971 6509 91480
15D.Rep1 83938 6406 90344
15D.Rep2 80963 6210 87173
15D.Rep3 81302 6156 87458
20D.Rep1 78899 6029 84928
20D.Rep2 78802 5994 84796
20D.Rep3 81241 6308 87549
25D.Rep1 79118 6076 85194
25D.Rep2 79869 6076 85945
25D.Rep3 82747 6337 89084
30D.Rep1 77776 5945 83721
30D.Rep2 81517 6167 87684
30D.Rep3 80690 6187 86877
平均Mean 82509 6270 88779

Fig. 2

Gene expression profiles of Huaimai 48 grain across different developmental stages A: Cluster dendrogram of gene expression profiles during six different developmental stages and under various replicate conditions; B: Principal component analysis (PCA) plot of gene expression levels for samples from six different developmental stages; C: Classification plot of gene expression levels for each developmental stage; D: A venn diagram illustrating the number of expressed genes in samples from six different developmental stages"

Fig. 3

The Correlation analysis of gene expression levels between transcriptomic data and qRT-PCR results"

Fig. 4

Numbers of differently expressed genes (DEGs) during different developmental stages of Huaimai 48 grain"

Fig. 5

Clustering analysis of all DEGs and expression profiles of known genes in Huaimai 48 grains A: Clustering of gene expression patterns for Huaimai 48 grain across six different developmental stages; B: Expression patterns of the reported genes in Huaimai 48"

Table 4

Classification and expression patterns of transcription factors"

家族
Family		 数目
Number		 5种表达模式 Five expression patterns 家族
Family		 数目
Number		 5种表达模式 Five expression patterns
A B C D E A B C D E
AP2 22 4 8 9 1 0 HRT-like 1 0 1 0 0 0
ARF 14 4 9 1 0 0 HSF 24 5 1 15 0 3
ARR-B 11 1 9 0 0 1 LBD 17 5 5 0 0 7
B3 49 4 30 2 5 8 LSD 1 0 1 0 0 0
BES1 2 1 1 0 0 0 MIKC_MADS 37 1 32 0 2 2
bHLH 75 14 38 8 4 11 M-type_MADS 11 2 3 1 0 5
bZIP 59 12 19 10 3 15 MYB 90 22 34 8 2 24
C2H2 37 9 18 5 2 3 MYB_related 28 14 9 1 2 2
C3H 21 7 10 3 1 0 NAC 107 28 22 33 3 21
CAMTA 1 0 1 0 0 0 NF-YA 10 0 0 0 4 6
CO-like 3 0 2 0 0 1 NF-YB 14 6 4 0 0 4
CPP 3 2 1 0 0 0 NF-YC 9 1 8 0 0 0
DBB 8 2 4 0 0 2 Nin-like 3 3 0 0 0 0
Dof 14 1 4 3 1 5 S1Fa-like 1 1 0 0 0 0
E2F/DP 12 5 5 0 0 2 SBP 11 0 10 0 0 1
EIL 4 2 2 0 0 0 SRS 1 0 0 1 0 0
ERF 47 20 11 4 4 8 TALE 13 3 7 2 1 0
FAR1 15 2 3 3 0 7 TCP 22 1 21 0 0 0
G2-like 47 20 17 2 1 7 Trihelix 22 6 10 1 0 5
GATA 4 0 2 0 2 0 Whirly 6 1 5 0 0 0
GeBP 2 1 1 0 0 0 WOX 9 4 1 3 1 0
GRAS 24 8 11 1 2 2 WRKY 34 4 14 1 4 11
GRF 7 0 6 0 1 0 YABBY 9 0 7 2 0 0
HB-other 3 0 2 0 0 1 ZF-HD 11 2 3 6 0 0
HD-ZIP 47 7 35 3 1 1 总计Total 1022 235 447 128 47 165

Fig. 6

Correlation between weighted gene co-expression network and protein content A: Correlation analysis between gene modules and protein content. The first row from the bottom represents WGCNA modules, and the second row represents the correlation between the module and the protein content. The two numbers indicate the correlation coefficient and the P value, respectively. The bar chart at the top shows the number of genes contained in each module; B: Distribution plot of gene significance values across different modules"

Table 5

Canditate TFs for regulating the protein content of wheat grain"

基因ID Gene ID 类别Description 基因连通性值kME 所属模块The modlue
TraesCS2A03G0362900 MADS-box转录因子 MADS-box transcription factor 0.986 青绿色 Turquoise
TraesCS4D03G0036300 TALE转录因子 TALE transcription factor 0.981 青绿色 Turquoise
TraesCS5A03G0079200 TCP转录因子 TCP transcription factor 0.984 青绿色 Turquoise
TraesCS5B03G0740100 MADS-box转录因子 MADS-box transcription factor 0.987 青绿色 Turquoise
TraesCS7D03G0590500 MADS-box转录因子 MADS-box transcription factor 0.981 青绿色 Turquoise
TraesCS5A03G0135400 CPP转录因子 CPP transcription factor 0.981 蓝色 Blue

Fig. 7

Hub transcription factors in the weighted gene co-expression network Only the genes (nodes) with kME>0.98 and top 100 weight value in the positive regulation module were shown. The node size was corresponding with the number of regulated genes. The group of the red nodes represent the hub TF genes. The purple, blue and orange colors indicate this gene regulated by ≥3, 2 and 1 hub transcription factors (hub TFs), respectively"

Fig. 8

The result of GO (A) and KEGG (B) enrichment of the weighted gene co-expression network"

Table 6

Correlation analysis between expression levels of hub TFs and protein content in Huaimai 48 grains during different developmental stages"

表型/基因<BOLD>P</BOLD>henotype/gene 5 d 10 d 15 d 20 d 25 d 30 d 相关性系数r
蛋白质含量GPC (%) 15.59 15.04 14.15 12.81 12.16 13.20
TraesCS2A03G0362900 8.60 5.85 2.99 1.32 0.90 0.56 0.93**
TraesCS4D03G0036300 13.19 7.96 2.72 2.36 1.57 2.39 0.89*
TraesCS5A03G0079200 5.32 3.77 1.95 0.64 0.50 0.54 0.95**
TraesCS5A03G0135400 21.54 48.33 35.01 15.00 11.12 8.03 0.67n.s.
TraesCS5B03G0740100 136.13 83.19 35.66 28.30 19.17 15.06 0.89*
TraesCS7D03G0590500 284.97 153.86 63.75 55.35 33.35 24.53 0.87*

Fig. 9

Expression levels of hub TFs in different tissues from the public database WheatOmics"

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