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Acta Agronomica Sinica ›› 2022, Vol. 48 ›› Issue (7): 1645-1657.doi: 10.3724/SP.J.1006.2022.14107

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

Identification of regulatory genes related to flavonoids synthesis by weighted gene correlation network analysis in the panicle of foxtail millet

HAN Shang-Ling1(), HUO Yi-Qiong1,2, LI Hui1, HAN Hua-Rui1, HOU Si-Yu1,2,3, SUN Zhao-Xia1,2,3, HAN Yuan-Huai1,2,3, LI Hong-Ying1,2,3,*()   

  1. 1College of Agriculture, Shanxi Agricultural University, Taigu 030801, Shanxi, China
    2Institute of Agricultural Bioengineer, Shanxi Agricultural University, Taigu 030801, Shanxi, China
    3Shanxi Key Laboratory of Germplasm Innovation and Molecular Breeding in Minor Crops, Taigu 030801, Shanxi, China
  • Received:2021-06-22 Accepted:2021-10-19 Online:2022-07-12 Published:2021-11-01
  • Contact: LI Hong-Ying E-mail:1438989621@qq.com;hongying1964@163.com
  • Supported by:
    National Natural Science Foundation of China(31771810);National Natural Science Foundation of China(32070366);National Key Research and Development Project(2018YFD1000705-2);Scientific Research Project of Shanxi Province Outstanding Doctoral Work Award Fund(SXYBKY2019042);Shanxi Graduate Innovation Project(2020SY209);Cultivation Project of Excellent Scientific Research Achievements in Shanxi Universities(2019KJ020);Shanxi Agricultural Valley Construction Research Project(SXNGJSKYZX201702);and the Shanxi Key Laboratory of Minor Crop Germplasm Innovation and Molecular Breeding

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Abstract:

Flavonoids are important secondary metabolites in plants and play significant roles in plant growth and development. They have antioxidant activity and are beneficial to human health. Foxtail millet is rich in nutrients, making it a healthy grain and popular among consumers. The crop is gaining more and more attention as a C4 model plant. However, there are few studies on the metabolic regulatory mechanism of flavonoids in foxtail millet. In this study, the panicles of flavonoid-rich variety JG21 and flavonoid-less variety NMB were analyzed on the flavonoid metabolomic profiles. Transcriptome sequencing was performed on the panicles of JG21 at different developmental stages. Transcription factors involved in regulating flavonoid metabolism were identified by weighted gene correlation network analysis (WGCNA). The expression patterns of these genes were verified by qRT-PCR. The results showed that the main flavonoid components enriched in the spikelets of foxtail millet were apigenin, vitexin, and naringenin, accounting for more than 79% of the total flavonoids. The flavonoid-related network of JG21 contained 38,921 genes, which were divided into 32 modules. Among them, the turquoise module, green module, and magenta module were significantly correlated with flavonoid metabolism. A total of 27 transcription factor families related to the regulation of flavonoid metabolism were identified by using differentially expressed genes related to flavonoid metabolism pathway as the hubs, and 11 transcription factors were obtained through promoter binding motif analysis. Pearson correlation analysis showed that 7 out of the 11 transcription factors might be involved in flavonoid metabolism, which were WRKY38, MYB4a, PI, WRKY15, WRKY62, MYB46, and WRKY23, respectively. The above results provide new candidate genes for studying the transcriptional regulation mechanism of flavonoids and lay a foundation for further investigation of the flavonoid metabolism regulation mechanism in foxtail millet.

Key words: foxtail millet, flavonoids, WGCNA, transcription factor

Fig. 1

Different developmental stages (S1, S3, and S5) of representative variety JG21 panicle S1: the panicles are bright green in appearance, and the inclusions are milky; S3: the panicles are yellow-green or light green in appearance, nutrients are accumulated, and the inclusions are solidified, embryo, and powdery inclusions can be separated; S5: appearance is dark yellow or off-white, palea husk becomes dry crisp, mature kernels."

Table S1

Primers used in this study"

基因
Gene		 上游引物
Forward primer (5'-3')		 下游引物
Reverse primer (5'-3')
Seita.4G268200 ACCTCAAGGACGAACAGCAG TTCACGTTCAGGAGGTACGC
Seita.3G350800 CGGTGGATCAACTACCTCCG GCGATCTGAGACCACCTGTT
Seita.7G284800 CACCGAGGAAGAAGACGACC TTGATCTCGTTGTCCGTCCG
Seita.7G201000 GACCTGACGGGCATCAAGAA TTGGAGCACTTGTCGCACTT
Seita.3G236800 GAGCCTGAGTGCAGAGATCG ATCCTCGCCTTTCAGATGCC
Seita.6G239700 CAGAGGAGCACTCTGCTTCG AGGCCTCTGAAGTCGAGCAT
Seita.5G362000 AGGAGATCAACGGGCACAAG CTCCCCGTAGTAGGCGATCT
Seita.5G361900 AGCATCCCCAGAGAGCAAAC GTGGAAGCTGCACCTGTAGT
Seita.3G164900 TTCTGGACGACGGCTACAAG TCTTCACGTTGCACCCTTCC
Seita.7G203300 AGACGTGCACCGACAAATCT TGATGGCAAGAGTGCCACAT
Seita.1G154200 TCGACGATCTGATGAGCTGC CCATCATTTGCTGCCACGAC

Fig. 2

Flavonoids contents at different panicle development stages in foxtail millet Different lowercase letters above the bars mean significantly different at P < 0.05."

Table 1

Information on transcriptome sequencing"

样本名称
Sample name		 总序列数量
Total reads		 匹配序列数量
Mapped reads		 匹配比例
Mapped ratio
(%)		 GC含量
GC content (%)		 Q30比例
Q30 ratio
(%)		 基因间序列比例
Intergenic ratio
(%)		 外显子序列比例
Exon ratio
(%)		 内含子序列比例
Intron ratio
(%)
JG21-S1-1 47,381,498 43,109,022 90.98 53.30 93.50 9.95 86.55 3.50
JG21-S1-2 49,046,244 44,551,756 90.84 53.49 93.28 10.04 86.50 3.46
JG21-S1-3 46,450,810 41,656,468 89.68 53.54 94.01 10.22 86.35 3.43
JG21-S3-1 43,629,752 41,008,492 93.99 54.21 93.48 10.33 86.91 2.76
JG21-S3-2 51,156,392 48,064,045 93.96 54.11 93.70 10.31 86.91 2.78
JG21-S3-3 47,754,204 44,808,816 93.83 53.96 93.61 10.26 86.87 2.87
JG21-S5-1 45,693,728 38,155,584 83.50 53.90 93.63 11.09 85.30 3.61
JG21-S5-2 43,824,250 36,414,881 83.09 53.78 93.48 11.10 85.30 3.60
JG21-S5-3 46,573,564 38,830,068 83.37 53.93 93.52 11.13 85.32 3.55

Fig. 3

Clustering dendrogram of foxtail millet transcriptome samples based on their expression level Euclidean distance"

Fig. 4

Clustering dendrogram of foxtail millet transcripts with assigned module colors a: genes clustering analysis based on TOM-based dissimilarity. b: module divided by dynamic tree cut, different colors represented different modules."

Fig. 5

Identification of key modules related to the key flavonoids metabolites Each row corresponds to a module, and each column corresponds to a trait. The correlation coefficient and the corresponding P-value are shown in each cell."

Fig. S1

Expression analysis of flavonoid differentially expressed genes"

Table 2

Correlation between the differentially expressed genes related to flavonoid synthesis pathway and the contents of three flavonoids"

基因
Gene		 牡荆素
Vitexin		 柚皮素
Naringenin		 芹菜素
Apigenin
CHIL_Seita.7G301600 0.933** 0.992** -0.436
F3H2_Seita.9G561700 0.391 -0.033 0.858**
F3'H6_Seita.2G219600 0.944** 0.987** -0.398
F3'H8_Seita.3G327200 0.921** 0.994** -0.464
ANR2_Seita.7G249100 0.862** 0.994** -0.567
CHSC2_Seita.8G140200 0.954** 0.984** -0.368
4CL1_Seita.6G093400 -0.688* -0.314 -0.642
4CL5_Seita.6G167900 0.974** 0.965** -0.280
4CL2_Seita.1G283300 0.663 0.917** -0.797*
PAL5_Seita.1G240600 0.928** 0.992** -0.442
PAL3_Seita.1G240400 0.919** 0.946** -0.382
PAL4_Seita.1G240500 0.951** 0.984** -0.373
PAL2_Seita.1G240300 0.956** 0.981** -0.352
PAL1_Seita.1G240200 0.953** 0.983** -0.367
PAL7_Seita.6G181000 0.971** 0.969** -0.296

Fig. 6

Regulatory network of flavonoids synthesis genes based on correlation module in foxtail millet Red circles indicate the differentially expressed flavonoid synthesis genes, blue squares indicate differentially expressed transcription factors that interact with flavonoid synthesis genes. A: turquoise module; B: green module; C: magenta module."

Table S2

Binding motif analysis of candidate transcription factors and the promoter of flavonoids genes"

转录因子
Transcription factor		 结合基序
Motif ID		 E值
E-value		 靶基因
Target gene		 模板链
Strand		 起始位置
Start		 终止位置
End		 p值
p-value		 q值
q-value		 匹配序列
Matched Sequence
Seita.4G268200 MA0940.1
(AP1)		 3.23722E-30 Seita.7G301600_CHIL - 361 373 0.0000404 0.119 ATAAAAAAATAAA
Seita.7G301600_CHIL + 765 777 0.0000413 0.119 CTAAATAAGAAAA
Seita.7G301600_CHIL + 1004 1016 0.0000417 0.119 ATAAAAATATAAA
Seita.1G240300_PAL2 + 695 707 0.0000676 0.153 ACAGAAAAAAAAA
Seita.7G301600_CHIL - 367 379 0.0000686 0.153 ACTAAAATAAAAA
Seita.2G219600_F3'H6 + 307 319 0.0000880 0.156 ACGAAAAAGGGAA
Seita.3G350800 MA1040.1(MYB46) 3.80676E-67 Seita.7G301600_CHIL - 1790 1797 0.0000179 0.293 GTTAGGTA
Seita.7G301600_CHIL - 1685 1692 0.0000593 0.293 GGTAGGTG
Seita.8G140200_CHSC2 + 1015 1022 0.0000772 0.293 GTTTGGTA
Seita.7G284800 MA1039.1(MYB4a) 1.80221E-92 Seita.7G301600_CHIL - 1685 1692 0.0000121 0.096 GGTAGGTG
Seita.1G240300_PAL2 - 1435 1442 0.0000241 0.096 GGTTGGTG
Seita.1G240300_PAL2 + 93 100 0.0000241 0.096 GGTTGGTG
Seita.2G219600_F3'H6 + 682 689 0.0000241 0.096 GGTTGGTG
Seita.1G240300_PAL2 - 665 672 0.0000535 0.155 GGTTGGTA
Seita.2G219600_F3'H6 + 375 382 0.0000681 0.181 AGTAGGTG
Seita.1G240300_PAL2 + 905 912 0.0000975 0.183 AGTAGGTG
Seita.7G301600_CHIL + 1220 1227 0.0000975 0.183 AGTAGGTG
Seita.7G201000 MA0120.1(id1) 2.69525E-87 Seita.1G240300_PAL2 - 1350 1361 0.0000238 0.185 TGGTCCCTTCCG
Seita.7G301600_CHIL + 553 564 0.0000644 0.232 TTTCCCTTCTCT
Seita.1G240300_PAL2 - 490 501 0.0000684 0.232 TTTTCCCTCTCT
Seita.2G219600_F3'H6 - 308 319 0.0000694 0.232 TTCCCTTTTTCG
Seita.3G236800 MA0559.1(PI) 4.96687E-74 Seita.8G140200_CHSC2 + 1243 1256 0.00000786 0.123 ACAAAACAGGAAAA
Seita.7G301600_CHIL + 1630 1643 0.0000174 0.146 ACAAAACAGGAAAA
Seita.8G140200_CHSC2 + 1261 1274 0.0000234 0.146 ACAAAAATAGAATA
Seita.8G140200_CHSC2 + 499 512 0.0000354 0.172 CTAGAAGAAGAAGG
Seita.8G140200_CHSC2 + 1219 1232 0.0000809 0.172 AAGAATAAGGAAAG
Seita.8G140200_CHSC2 + 710 723 0.0000885 0.172 ACAGAACTAGAAAA
Seita.6G239700 MA1039.1(MYB4) 1.85497E-89 Seita.9G561700_F3H2 + 277 284 0.0000975 0.183 AGTTGGTG
Seita.5G362000 MA1084.1(WRKY38) 2.75933E-17 Seita.6G167900_4CL5 + 176 183 0.0000414 0.660 AGTTGACC
Seita.6G167900_4CL5 - 1533 1540 0.0000828 0.880 CATTGACC
Seita.5G361900 MA1091.1(WRKY62) 1.26504E-15 Seita.6G167900_4CL5 - 177 184 0.0000147 0.468 TGGTCAAC
Seita.3G164900 MA1080.1(WRKY23) 2.98528E-34 Seita.1G240500_PAL4 - 947 954 0.0000593 0.820 AGTCAAAG
Seita.7G203300 MA0990.1(EDT1) 0 Seita.6G167900_4CL5 + 662 671 0.0000346 0.366 AAATAAATGC
Seita.6G167900_4CL5 - 330 339 0.0000779 0.618 CTTTTAATGC
Seita.1G154200 MA1076.1(WRKY15) 3.76677E-45 Seita.1G240500_PAL4 - 955 964 0.0000855 0.907 GAGTCAACTC

Table 3

Function of the candidate transcription factors"

转录因子
Transcription factor		 功能
Function
AP1 拟南芥: 参与花的形成[20⇓-22]
Arabidopsis thaliana: participate in flower formation[20⇓-22]
MYB46 拟南芥: 参与木质素生物合成[23⇓-25]
Arabidopsis thaliana: participate in lignin biosynthesis[23⇓-25]
MYB4a/b 拟南芥: 参与类黄酮生物合成[26]
Arabidopsis thaliana: participate in flavonoid biosynthesis[26]
id1 玉米: 参与开花过程[27-28]
Zea mays: participate in flowering process[27-28]
PI 拟南芥: 参与开花过程[29]
Arabidopsis thaliana: participate in flowering process[29]
WRKY38 拟南芥: 基础防御的负调节剂[30]
Arabidopsis thaliana: negative regulator of basal defense[30]
WRKY62 拟南芥: 基础防御的负调节剂; 参与水杨酸诱导的反应[30-31]
Arabidopsis thaliana: negative regulator of basal defense; participate in the response induced by salicylic acid[30-31]
WRKY23 拟南芥: 介导黄酮醇合成的局部调控, 调节生长素的转运[32]; 参与生长素介导的PIN蛋白的重排[33]
Arabidopsis thaliana: participate in local regulation of flavonol biosynthesis and auxin transport[32]; participate in auxin-mediated PIN polarity rearrangements[33]
EDT1 拟南芥: 增加陆地棉抗旱性和耐盐性[34⇓-36]
Arabidopsis thaliana: increase drought and salt tolerance of upland cotton[34⇓-36]
WRKY15 拟南芥: 调节植物的生长和盐/渗透胁迫反应[37]; 抑制木质部形成期间VND7上游的导管分子分化[38]
Arabidopsis thaliana: modulates plant growth and salt/osmotic stress responses[37]; suppresses tracheary element differentiation upstream of VND7 during xylem formation[38]

Table 4

Correlation between the expression levels of 11 transcription factors and the contents of three flavonoids"

转录因子
Transcription factors		 JG21 NMB
牡荆素
Vitexin		 柚皮素
Naringenin		 芹菜素
Apigenin		 牡荆素
Vitexin		 柚皮素
Naringenin		 芹菜素
Apigenin
WRKY38 0.948** 0.984** -0.378 0.595 0.715 -0.975**
EDT1 0.976** 0.962** -0.275 -0.983** -0.887* 0.993**
AP1 -0.922** -0.975** 0.422 0.927** 0.995** -0.717
MYB4a 0.926** 0.975** -0.401 0.879* 0.811* -0.991**
PI 0.886** 0.997** -0.534 0.805* 0.919* -0.889*
MYB4b -0.051 -0.472 0.994** 0.939** 0.984** -0.936**
WRKY15 0.980** 0.917** -0.136 0.738 0.801* -0.755
id1 -0.969** -0.973** 0.304 0.998** 0.998** -0.976**
WRKY62 0.946** 0.988** -0.392 0.497 0.773 -0.834*
MYB46 0.840** 0.986** -0.605 0.911** 0.915** -0.944**
WRKY23 0.983** 0.944** -0.228 0.874* 0.890* -0.937**
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