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Acta Agronomica Sinica ›› 2021, Vol. 47 ›› Issue (12): 2423-2439.doi: 10.3724/SP.J.1006.2021.02084


Prediction of drought and salt stress-related genes in rice based on multi-platform gene expression data

LIU Ya-Wen1(), ZHANG Hong-Yan1,2,*(), CAO Dan2, LI Lan-Zhi2   

  1. 1College of Information and Intelligence, Hunan Agricultural University, Changsha 410128, Hunan, China
    2Hunan Engineering and Technology Research Centre for Agricultural Big Data Analysis and Decision-making, Hunan Agricultural University, Changsha 410128, Hunan, China
  • Received:2020-11-30 Accepted:2021-04-26 Online:2021-12-12 Published:2021-06-02
  • Contact: ZHANG Hong-Yan E-mail:lyw20201022@163.com;hongyan_zhang@hunau.edu.cn
  • Supported by:
    Key Scientific Research Project of Hunan Education Department(18A105);Special Commissioner Project of Changsha City for Industrial Science and Technology(201845);“Double First-class” Construction Project of Hunan Agricultural University(SYL2019075)


Mining stress-related genes based on multi-platform gene expression data in rice can increase the reliability of key genes prediction and obtain more universally meaningful results. In this study, 94 affymetrix microarray data and 42 RNA-seq transcriptome data related to rice abiotic stress were collected from NCBI databases. First, multiple datasets related to the same stress on the same type were fused by data conversion method to obtain the affymetrix data set D_affy and RNA-seq data set D_rnaseq related to drought stress, and the affymetrix data set S_affy and the RNA-seq data set S_rnaseq related to salt stress. Then, the four datasets were analyzed by the classical WGCNA method based on Pearson's linear correlation coefficient and the improved WGCNA method based on the MIC nonlinear correlation coefficient respectively, and the eight Hub gene sets related to stress were obtained. Further, the integration analysis of stress-related Hub genes yielded the final 1936 drought stress-related Hub genes and 1504 salt stress-related Hub genes. Finally, the biological significance of Hub gene was analyzed from multiple perspectives, including prediction performance, enrichment analysis, literature report, STRING online interaction analysis, and Cytoscape visualization analysis. The results revealed that the overall prediction performance of Hub genes was better, and most of them were enriched in the pathways related to drought/salt stress. Among them, there were 31 drought stress response genes and 22 salt stress response genes reported in the literatures. In addition, 11 drought stress candidate genes and 5 salt stress candidate genes were predicted using the interaction analysis of Hub genes. In conclusion, This study provides a new idea for the effective analysis of “high-dimensional, small-sample” crop gene sequencing data, and the experimental results provide a reference for the study of stress-resistant rice varieties.

Key words: rice, multi-platform, drought stress, salt stress, WGCNA-MIC

Fig. 1

Process of rice affy data processing"

Table S1

Affymetrix microarray data from NCBI"

GEO关联 GEO accession 测序平台
Samples (control/stress)
GSE6901 Affymetrix Rice Genome Array (GPL2025) N = 6 (3/3 drought)
GSE21651 Affymetrix Rice Genome Array (GPL2025) N = 8 (4/4 drought)
GSE23211 Affymetrix Rice Genome Array (GPL2025) N = 12 (6/6 drought)
GSE26280 Affymetrix Rice Genome Array (GPL2025) N = 36 (18/18 drought)

GSE6901 Affymetrix Rice Genome Array (GPL2025) N = 6 (3/3 salt)
GSE14403 Affymetrix Rice Genome Array (GPL2025) N = 18 (9/9 salt)
GSE16108 Affymetrix Rice Genome Array (GPL2025) N = 8 (4/4 salt)

Table S2

RNA-seq data from NCBI"

Library name
Library description
Library type
Library layout
Rice genotype
SRR3647331 1-leaf_34_day_Salt RNAseq Single Nipponbare
SRR3647329 1-leaf_34_day_Salt RNAseq Single Nipponbare
SRR3647327 1-leaf_34_day_Salt RNAseq Single Nipponbare
SRR3647330 1-leaf_34_day_Control RNAseq Single Nipponbare
SRR3647328 1-leaf_34_day_Control RNAseq Single Nipponbare
SRR3647326 1-leaf_34_day_Control RNAseq Single Nipponbare
ERR266228 1-Seedling_shoots_2_weeks_1h_Control RNAseq Single Nipponbare
ERR266233 1-Seedling_shoots_2_weeks_1h_Control RNAseq Single Nipponbare
ERR266230 1-Seedling_shoots_2_weeks_1h_Control RNAseq Single Nipponbare
ERR266225 1-Seedling_shoots_2_weeks_24h_Control RNAseq Single Nipponbare
ERR266234 1-Seedling_shoots_2_weeks_24h_Control RNAseq Single Nipponbare
ERR266232 1-Seedling_shoots_2_weeks_24h_Control RNAseq Single Nipponbare
ERR266229 1-Seedling_shoots_2_weeks_5h_Control RNAseq Single Nipponbare
ERR266223 1-Seedling_shoots_2_weeks_5h_Control RNAseq Single Nipponbare
ERR266222 1-Seedling_shoots_2_weeks_5h_Control RNAseq Single Nipponbare
ERR266237 1-Seedling_shoots_2_weeks_1h_Salt RNAseq Single Nipponbare
ERR266236 1-Seedling_shoots_2_weeks_1h_Salt RNAseq Single Nipponbare
ERR266235 1-Seedling_shoots_2_weeks_1h_Salt RNAseq Single Nipponbare
ERR266238 1-Seedling_shoots_2_weeks_24h_Salt RNAseq Single Nipponbare
ERR266226 1-Seedling_shoots_2_weeks_24h_Salt RNAseq Single Nipponbare
ERR266231 1-Seedling_shoots_2_weeks_24h_Salt RNAseq Single Nipponbare
ERR266227 1-Seedling_shoots_2_weeks_5h_Salt RNAseq Single Nipponbare
ERR266224 1-Seedling_shoots_2_weeks_5h_Salt RNAseq Single Nipponbare
ERR266221 1-Seedling_shoots_2_weeks_5h_Salt RNAseq Single Nipponbare
SRR7054183 2-Inflorescence_Control RNAseq Paired Nipponbare
SRR7054182 2-Inflorescence_Control RNAseq Paired Nipponbare
SRR7054181 2-Inflorescence_Control RNAseq Paired Nipponbare
SRR7054180 2-Inflorescence_Control RNAseq Paired Nipponbare
SRR7054179 2-Inflorescence_Drought RNAseq Paired Nipponbare
SRR7054178 2-Inflorescence_Drought RNAseq Paired Nipponbare
SRR7054177 2-Inflorescence_Drought RNAseq Paired Nipponbare
SRR7054176 2-Inflorescence_Drought RNAseq Paired Nipponbare
SRR3051752 Drought stress_rep1 RNAseq Paired Nipponbare
SRR3051753 Drought stress_rep2 RNAseq Paired Nipponbare
SRR3051754 Drought stress_rep3 RNAseq Paired Nipponbare
SRR3051755 Well-water_rep1 RNAseq Paired Nipponbare
SRR3051756 Well-water_rep2 RNAseq Paired Nipponbare
SRR3051757 Well-water_rep3 RNAseq Paired Nipponbare
SRR3051740 Well-water_rep1 RNAseq Paired Nipponbare
SRR3051741 Well-water_rep2 RNAseq Paired Nipponbare
SRR3051742 Well-water_rep3 RNAseq Paired Nipponbare
SRR3051743 Drought stress_rep1 RNAseq Paired Nipponbare
SRR3051744 Drought stress_rep2 RNAseq Paired Nipponbare
SRR3051745 Drought stress_rep3 RNAseq Paired Nipponbare

Fig. 2

Process of rice RNA-seq data processing"

Table 1

Data set of rice"

Data set
No. of genes
Total samples
Control samples
Stress samples
Drought stress-related affymetrix dataset (D_affy)
27,344 62 31 31
Salt stress-related affymetrix dataset (S_affy)
27,344 32 16 16
Drought stress-related RNA-seq dataset (D_rnaseq)
29,828 20 10 10
Salt stress-related RNA-seq dataset (S_rnaseq)
28,425 22 11 11

Fig. 3

WGCNA network analysis of D_affy data A, B: the gene clustering tree and module division based on WGCNA-P and WGCNA-MIC methods, respectively; the Dynamic Tree Cut represents the module divided by the original calculation, the Merged dynamic represents the merged result; C, D: the ME and MS values of each module based on WGCNA-P and WGCNA-MIC methods, respectively; red block indicates that the module is positively correlated with drought stress, and blue indicates that the module is negatively correlated with drought stress."

Fig. 4

WGCNA network analysis of D_rnaseq data A, B: the gene clustering tree and module division based on WGCNA-P and WGCNA-MIC methods, respectively; the Dynamic Tree Cut represents the module divided by the original calculation, the Merged dynamic represents the merged result; C, D: the ME and MS values of each module based on WGCNA-P and WGCNA-MIC methods, respectively; red block means that the module is positively correlated with drought stress, and blue indicates that the module is negatively correlated with drought stress."

Fig. S1

WGCNA network analysis of S_affy A, B: gene clustering tree and module division of based on WGCNA-P and WGCNA-MIC methods respectively; the Dynamic Tree Cut represents the module divided by the original calculation, the merged dynamic represents the merged result; C, D: the ME and MS values of each module based on WGCNA-P and WGCNA-MIC methods respectively; red indicates that the module is positively correlated with salt stress, and blue indicates that the module is negatively correlated with salt stress."

Fig. S2

WGCNA network analysis of S_rnaseq A, B: gene clustering tree and module division of based on WGCNA-P and WGCNA-MIC methods respectively; the Dynamic Tree Cut represents the module divided by the original calculation, the merged dynamic represents the merged result; C, D: the ME and MS values of each module based on WGCNA-P and WGCNA-MIC methods respectively; red indicates that the module is positively correlated with salt stress, and blue indicates that the module is negatively correlated with salt stress."

Table 2

Classification accuracy of Hub genes"

Hub gene set
Number of genes
Data set
Average accuracy (%)
干旱Drought D_affy_P 220 D_affy 100
D_affy_MIC 104 D_affy 100
D_rnaseq_P 738 D_rnaseq 90.0
D_rnaseq_MIC 1634 D_rnaseq 91.0
D_meta_hub 1936 D_affy 100
D_rnaseq 96.0
盐Salt S_affy_P 470 S_affy 100
S_affy_MIC 293 S_affy 100
S_rnaseq_P 684 S_rnaseq 81.0
S_rnaseq_MIC 331 S_rnaseq 84.6
S_meta_hub 1504 S_affy 100
S_rnaseq 84.6

Table 3

GO enrichment of Hub partial genes"

GO term
Number of genes
GO:0010033 12 BP 对有机物的响应
Response to organic substance
GO:0009719 12 BP 内源性刺激响应
Response to endogenous stimulus
GO:0009725 12 BP 激素刺激响应
Response to hormone stimulus
GO:0006721 8 BP 萜类化合物代谢过程
Terpenoid metabolic process
GO:0007165 37 BP 信号传导Signal transduction 2.20E-05
GO:0009628 15 BP 对非生物刺激的响应
Response to abiotic stimulus
GO:0006970 5 BP 渗透胁迫响应
Response to osmotic stress
GO:0009415 5 BP 对水的响应Response to water 0.006
GO:0004872 22 MF 受体活性 Receptor activity 9.40E-13
GO:0004713 21 MF 蛋白质酪氨酸激酶活性
Protein tyrosine kinase activity
GO:0004722 15 MF 蛋白丝氨酸/苏氨酸磷酸酶活性
Protein serine/threonine phosphatase activity
GO:0008135 12 MF 翻译因子活性, 核酸结合
Translation factor activity, Nucleic acid binding
GO:0044424 1120 CC 细胞内成分 Intracellular part 0
GO:0005737 1011 CC 细胞质Cytoplasm 0
GO:0016020 278 CC 薄膜 Membrane 3.10E-23

GO:0070887 6 BP 细胞对化学刺激的响应
Cellular response to chemical stimulus
GO:0007275 13 BP 多细胞有机体的发育
Multicellular organismal development
GO:0043436 52 BP 草酸代谢过程
Oxoacid metabolic process
GO:0019752 52 BP 羧酸代谢过程
Carboxylic acid metabolic process
GO:0006082 52 BP 有机酸代谢过程
Organic acid metabolic process
GO:0010033 11 BP 对有机物的响应
Response to organic substance
GO:0009719 11 BP 内源性刺激响应
Response to endogenous stimulus
GO:0009416 6 BP 光刺激响应
Response to light stimulus
GO:0004872 14 MF 受体活性 Receptor activity 5.70E-08
GO:0008135 18 MF 翻译因子活性, 核酸结合
Translation factor activity, nucleic acid binding
GO:0003743 11 MF 翻译起始因子活性
Translation initiation factor activity
GO:0016874 32 MF 连接酶活性 Ligase activity 0.00064
GO:0016020 225 CC 薄膜 Membrane 4.60E-21
GO:0009507 20 CC 叶绿体 Chloroplast 4.30E-15
GO:0005886 18 CC 细胞质膜 Plasma membrane 1.20E-09

Table 4

Hub genes related to stress have been reported"

基因编号RAP_locus 基因符号
Gene symbol
Gene symbol
Os05g0455500 OsP5CS; OsP5CS1; OsALDH18B1 干旱
Os03g0286900 OsRCI2-5
Os02g0766700 OsbZIP23 Os02g0149800 OsPP18
Os08g0112700 OsMADS26 Os03g0267000 OsHSP18.0-CI; OsMSR3; OsSHSP1
Os06g0130100 OsSIK1 Os05g0475400 OsAMTR1
Os09g0552300 OsRPK1 Os08g0408500 OsERF48; OsDRAP1
Os01g0867300 OsABF1; OsbZIP12 Os04g0676700 OsMYB6
Os03g0125100 DSM2 Os12g0597500 OsUAH
Os03g0745000 OsHsfA2a Os06g0316000 Os2H16
Os05g0542500 OsLEA3; OsLEA3-1 Os06g0612800 OsiSAP8
Os02g0671100 MAIF1 Os04g0572400 OsDREB1E
Os06g0211200 OsAREB1; OsbZIP46; OsABF2; ABL1 Os11g0126900 OsNAC10; ONAC122
Os05g0437700 EDT1; OsbZIP40 Os11g0707600 OsGL1-11
Os05g0569300 OsbZIP45 Os03g0805100 SQS
Os08g0196700 OsNF-YA7; OsHAP2A Os05g0213500 OsPYL/RCAR5; OsPYL5; OsPYL11
Os03g0230300 OsSRO1c; BOC1 Os06g0598800 WSL1
Os04g0541700 Oshox22
盐Salt Os03g0348900 OsSRFP1; SDEL2 盐Salt Os02g0121300 OsCYP2; LRT2
Os04g0652400 OsSULTR3; 3;lpa Os03g0272300 OsSDIR1
Os03g0329900 OsPHR1 Os07g0129200 OsPR1a; OsSCP
Os07g0187700 OsPHF1 Os05g0437700 EDT1; OsbZIP40
Os02g0678200 OsSPX-MFS2; OsPSS2 Os08g0557000 OsPIMT1
Os02g0325600 NIGT1 Os06g0693700 OsSIDP366
Os01g0755700 NBIP1 Os04g0676700 OsMYB6
Os10g0545700 OsACR2.1 Os01g0612700 OsLOL2; OsLOL5
Os01g0869900 OsSAPK4; OSPDK Os01g0948400 OsP5CR
Os03g0719900 OsPTR8; OsNPF8.5 Os03g0319300 OsCam1-1
Os09g0434500 OsBIERF1 Os05g0584200 OsLEA5

Fig. 5

Gene interaction network of drought stress"

Fig. 6

Gene interaction network of salt stress"

Table 5

Candidate genes annotation in STRING"

Candidate gene
Name in STRING
干旱Drought Os01g0733200 HSF11 热应激转录因子C-1b; 与热休克启动子元件(HSE)的DNA特异性结合的转录调控因子。
Heat stress transcription factor C-1b; transcriptional regulator that specifically binds DNA of heat shock promoter elements (HSE).
Os07g0178600 HSF5 热应激转录因子A-2b; 转录调控因子, 可特异性结合热休克启动子元件(HSE)的DNA; 属于HSF家族, A类亚科。
Heat stress transcription factor A-2b; transcriptional regulator that specifically binds DNA of heat shock promoter elements (HSE); belongs to the HSF family. Class A subfamily.
Os09g0526600 HSFB2C 热应激转录因子B-2c; 转录调控因子, 可特异性结合热休克启动子元件(HSE)的DNA; 属于HSF家族, B类亚科。
Heat stress transcription factor B-2c; transcriptional regulator that specifically binds DNA of heat shock promoter elements (HSE); belongs to the HSF family. Class B subfamily.
Os01g0583100 OS01T0583100-01 可能的蛋白质磷酸酶2C 6; 属于PP2C家族。
Probable protein phosphatase 2C 6; belongs to the PP2C family.
Os03g0231700 OS03T0231700-02 Os03g0231700蛋白; 角鲨烯单加氧酶, 假定表达; cDNA克隆: J033045D18, 完整插入序列。
Os03g0231700 protein; Squalene monooxygenase, putative, expressed; cDNA clone: J033045D18, full insert sequence.
Os03g0376100 OS03T0376100-01 Os03g0376100蛋白。
Os03g0376100 protein.
Candidate gene
Name in STRING
Os04g0107900 OS04T0107900-02 Os04g0107900蛋白。
Os04g0107900 protein.
Os01g0840100 OsJ_04024 cDNA克隆: J100050G20, 完整插入序列; 70 kD热激蛋白; Os01g0840100蛋白; 假定的HSP70; 未表征的蛋白质。
cDNA, clone: J100050G20, full insert sequence; 70 kD heat shock protein; Os01g0840100 protein; Putative HSP70; uncharacterized protein.
Os03g0277300 OsJ_10337 热休克同源70 kD蛋白, 假定表达。
Heat shock cognate 70 kD protein, putative, expressed.
Os05g0460000 OsJ_18811 Os05g0460000蛋白; 推定的hsp70; cDNA克隆: J090096I11, 完整插入序列; 属于热休克蛋白70家族。
Os05g0460000 protein; Putative hsp70; cDNA, clone: J090096I11, full insert sequence; Belongs to the heat shock protein 70 family.
Os06g0110200 OsJ_19858 cDNA克隆: 002-135-D09, 完整插入序列; Os06g0110200蛋白; 假定的未表征蛋白OSJNBa0004I20.22; 假定的未表征蛋白P0514G12.46。
cDNA clone: 002-135-D09, full insert sequence; Os06g0110200 protein; putative uncharacterized protein OSJNBa0004I20.22; putative uncharacterized protein P0514G12.46.

Os06g0727200 CATB 过氧化氢酶同工酶B; 几乎发生在所有有氧呼吸的生物中, 并保护细胞免受过氧化氢的毒性作用。
Catalase isozyme B; occurs in almost all aerobically respiring organisms and serves to protect cells from the toxic effects of hydrogen peroxide.
Os12g0502300 CYCA2-1 Cyclin-A2-1; 属于细胞周期蛋白家族。Cyclin AB亚家族。
Cyclin-A2-1; belongs to the cyclin family. Cyclin AB subfamily.
Os03g0821100 OsJ_13143 热休克同源70 kD蛋白2, 假定表达; 热休克蛋白同源物70; Os03g0821100蛋白; cDNA克隆: J023030D03, 完整插入序列。
Heat shock cognate 70 kD protein 2, putative, expressed; heat shock protein cognate 70; Os03g0821100 protein; cDNA clone:J023030D03, full insert sequence.
Os10g0491801 OsJ_31995 假定泛素/核糖体蛋白S27a融合蛋白;泛素融合蛋白, 假定表达。
Putative ubiquitin/ribosomal protein S27a fusion protein; ubiquitin fusion protein, putative, expressed.
Os02g0775200 RFC3 复制因子C亚基3; 可能参与DNA复制, 从而调节细胞增殖。
Replication factor C subunit 3; may be involved in DNA replication and thus regulate cell proliferation.
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