Transcriptome Analysis of Tolerant and Susceptible Maize Genotypes Reveals Novel Insights about the Molecular Mechanisms Underlying Drought Responses in Leaves
Abstract
:1. Introduction
2. Results
2.1. Morphological and Physiological Analysis of CML69 and LX9801 Seedlings in Responses to Drought Stress
2.2. RNA Sequencing (RNA-seq) Analysis and Identification of Differentially Expressed Genes
2.3. Annotation and Differential Analysis of Differentially Expressed Genes
2.4. GO and KEGG Pathway Enrichment Analysis
2.5. Effects of Drought Stress on the Drought-Tolerant Line
2.6. Effects of Drought Stress on the Drought-Susceptible Line
2.7. Validation of DEGs by Quantitative Real-Time PCR (qRT-PCR)
3. Discussion
4. Materials and Methods
4.1. Plant Materials, Growth Conditions, and Drought Stress Treatments
4.2. Physiological and Phenotypic Characterizations
4.3. Total RNA Extraction, cDNA Library Construction and Transcriptome Sequencing
4.4. Sequencing Reads Processing, Mapping, and Gene Expression Quantification
4.5. Functional Annotation of Gene Transcripts
4.6. Gene Ontology (GO) Enrichment and KEGG Pathway Enrichment Analyses
4.7. Quantitative Real-Time (qRT-PCR) Analysis
4.8. Statistical Analysis of Physiological Data
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
DEGs | Differentially expressed genes |
KEGG | Kyoto Encyclopedia of Genes and Genomes |
GO | Gene ontology |
LEA | Late embryogenesis abundant proteins |
ROS | Reactive oxygen species |
AQPs | Aquaporins |
GAs | Gibberellins |
ASR | Abscisic acid stress ripening |
PEPC | Phosphoenolpyruvate carboxylase 1 |
Pi | Inorganic phosphate |
C | Control |
3D | Three days of drought stress |
5D | Five days of drought stress |
TFs | Transcription factors |
MDA | Malondialdehyde |
REL | Relative electrolyte leakage |
BP | Base pairs |
Vs. | Versus |
AA | Amino acid |
Rep | Replicates |
lncRNA | Long noncoding RNA |
TE-lncRNA | Transposable elements long noncoding RNA |
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Inbred Line 1 | Comparison 2 | DEG Number 3 | Upregulated 4 | Downregulated 5 |
---|---|---|---|---|
CML69 | C vs. 3D | 1902 | 745 | 1157 |
C vs. 5D | 5385 | 2511 | 2874 | |
LX9801 | C vs. 3D | 3362 | 1321 | 2041 |
C vs. 5D | 5512 | 2434 | 3078 |
Inbred Line 1 | Comparison 2 | DEG Number 3 | Upregulated 4 | Downregulated 5 |
---|---|---|---|---|
CML69 | C vs. 3D | 1294 | 596 | 698 |
C vs. 5D | 4145 | 2154 | 1991 | |
LX9801 | C vs. 3D | 2488 | 1094 | 1394 |
C vs. 5D | 3996 | 2160 | 1836 |
Inbred Line 1 | Comparison 2 | DEG Number 3 | Upregulated 4 | Downregulated 5 |
---|---|---|---|---|
CML69 | C vs. 3D | 713 | 381 | 332 |
C vs. 5D | 2114 | 1105 | 1009 | |
LX9801 | C vs. 3D | 1350 | 607 | 743 |
C vs. 5D | 2014 | 1072 | 942 |
Gene ID 1 | Log2 Ratio (CML69_C vs. 3D) 2 | Log2 Ratio (LX9801_C vs. 3D) 3 | Best-Hit-A.th 4 | Symbol 5 | Annotation 6 |
---|---|---|---|---|---|
Zm00001d003712 | 1.067078963 | −1.903915782 | - | AASR3 | Abscisic acid stress ripening 3 |
Zm00001d004203 | 1.157175723 | −2.539146896 | AT5G24860.1 | FPF1 | Flowering promoting factor 1 |
Zm00001d042143 | 1.727547967 | −2.192605603 | AT3G57240.1 | BG3 | Beta−1,3-glucanase 3 |
Zm00001d008746 | 10.38729576 | −1.248462466 | AT5G09810.1 | ACT7 | Actin 7 |
Zm00001d013410 | 1.03408084 | −1.525068282 | AT3G12110.1 | ACT11 | Actin-11 |
Zm00001d011734 | 1.100182925 | −2.061333851 | - | - | Inorganic pyrophosphatase 1 |
Zm00001d024027 | 1.480081659 | −1.011948016 | - | PRCW1 | Proline-rich cell wall protein |
Zm00001d016301 | 1.822076998 | −2.04090855 | AT1G17710.1 | PEPC1 | Pyridoxal phosphate phosphatase |
Zm00001d033385 | 1.290037527 | −2.314823007 | AT3G50760.1 | GATL2 | Galacturonosyltransferase |
Zm00001d031875 | 1.621452385 | −2.335532517 | AT3G54700.2 | PHT1;7 | Phosphate transporter 1 |
Zm00001d032850 | 1.505609835 | −1.263658023 | AT2G38940.1 | PHT1;2 | Phosphate transporter 1 |
Zm00001d033241 | 1.03144486 | −2.848924659 | AT4G21120.1 | CAT1 | Cationic amino acid transporter |
Zm00001d033957 | 1.211020519 | −1.721699461 | - | bhlh103 | bHLH-transcription factor 103 |
Zm00001d038151 | 1.335042999 | −1.682288928 | AT1G03220.1 | SAP2 | Aspartic protease 2 |
Zm00001d044157 | 1.827511783 | −1.875850961 | AT3G14690.2 | CYP72A15 | Cytochrome P450 |
Zm00001d047436 | 1.44118319 | −1.335352169 | AT5G40010.1 | AATP1 | AAA-ATPase 1 |
Gene ID 1 | Log2 Ratio (CML69_C vs. 5D) 2 | Log2 Ratio (LX9801_C vs. 5D) 3 | Best-Hit-A.th 4 | Symbol 5 | Annotation 6 |
---|---|---|---|---|---|
Zm00001d007606 | 1.544362812 | −2.045097787 | AT5G41040.2 | ASFT | Aliphatic Suberin feruloyl transferase |
Zm00001d032103 | 1.862733313 | −1.816378054 | AT3G21240.1 | 4CL2 | 4-coumarate-CoA ligase |
Zm00001d047972 | 1.17316282 | −1.327960157 | AT2G01900.1 | t5ptase | Inositol polyphosphate 5-phosphatase |
Zm00001d030285 | 1.064851308 | −1.575733162 | AT5G66150.2 | - | Alpha-mannosidase |
Zm00001d017494 | 1.745450662 | −1.355124162 | AT2G45110.1 | EXPB4 | Expansin B4 |
Zm00001d003091 | 2.535603442 | −2.019264795 | AT1G08280.1 | GALT29A | Glycosyltransferase |
Zm00001d011838 | 1.124191501 | −1.027094089 | AT2G41640.1 | GALT61 | Glycosyltransferase family 61 |
Zm00001d024687 | 1.155209579 | −1.009500907 | AT4G15240.1 | GALT | Glycosyltransferase |
Zm00001d052209 | 3.110619463 | −1.221666072 | AT1G22360.1 | UGT85A2 | UDP-glucosyl transferase |
Zm00001d017249 | 1.211898981 | −2.268909254 | AT1G64780.1 | AMT1;2 | Aammonium transporter 1 |
Zm00001d018751 | 2.227663156 | −2.263570515 | AT5G49630.1 | AAP6 | Amino acid permease 6 |
Zm00001d035717 | 1.506215854 | −1.568896164 | - | WAT1 | Walls are thin 1 |
Zm00001d037515 | 1.689789607 | −1.669586632 | AT5G01790.1 | - | Hypothetical protein |
Zm00001d025724 | 1.855649477 | −1.13455352 | AT1G67600.1 | - | Acid phosphatase haloperoxidase |
Zm00001d028367 | 1.2039208 | −2.231720672 | AT1G14700.1 | PAP3 | Purple acid phosphatase 3 |
Zm00001d017270 | 1.586319405 | −1.991000978 | AT3G04530.1 | PPCK2 | Phosphoenolpyruvate carboxylase kinase |
Zm00001d037783 | 1.167986012 | −1.248374599 | AT3G23000.1 | CIPK7 | Serine/threonine protein kinase |
Zm00001d050164 | 1.109395435 | −2.580502154 | - | WAKL20 | Wall-associated receptor kinase-like 20 |
Zm00001d007773 | 1.373813395 | −1.058825309 | AT3G28510.1 | AATP1 | AAA-ATPase ASD mitochondrial |
Zm00001d047436 | 1.511985756 | −1.267657 | AT5G40010.1 | AATP1 | AAA-ATPase 1 |
Zm00001d011734 | 2.245158893 | −1.083662395 | - | - | Inorganic pyrophosphatase 1 |
Zm00001d013565 | 4.481035303 | −1.578440935 | AT4G37810.1 | EPFL2 | Epidermal patterning factor |
Zm00001d016269 | 1.238419504 | −1.361567296 | AT5G25840.1 | DUF1677 | DUF1677 family protein |
Zm00001d016301 | 3.330549142 | −2.375063337 | AT1G17710.1 | PEPC1 | Pyridoxal phosphate phosphatase |
Zm00001d016548 | 2.431505237 | −1.14796758 | AT1G67430.1 | - | - |
Zm00001d025401 | 1.538596646 | −1.066777498 | - | AASR5 | Abscisic acid stress ripening 5 |
Zm00001d037797 | 1.469551335 | −1.783796353 | AT2G24000.2 | SCPL22 | Serine carboxypeptidase |
Zm00001d048947 | 3.3420077 | −1.714779709 | AT3G04720.1 | PR4 | Pathogenesis-related 4 |
Zm00001d044541 | 1.502454541 | −2.085986029 | AT2G45130.1 | SPX3 | SPX domain protein 3 |
Zm00001d052220 | 2.229459236 | −1.898568624 | - | VQ23 | VQ motif-transcription factor |
Zm00001d045537 | 1.133943728 | −2.756015494 | - | - | CYCLOPS |
Zm00001d043665 | 1.599461141 | −1.494855603 | - | - | - |
Gene ID 1 | Log2 Ratio (CML69_C vs. 3D) 2 | Log2 Ratio (LX9801_C vs. 3D) 3 | Best-Hit-A.th 4 | Symbol 5 | Annotation 6 |
---|---|---|---|---|---|
Zm00001d002999 | −1.586466311 | 1.125018924 | AT4G21200.1 | GA2OX8 | Gibberellin 2-oxidase 8 |
Zm00001d012131 | −1.32220827 | 1.195476431 | AT3G62920.1 | - | Zinc metalloproteinase |
Zm00001d017666 | −2.335920246 | 2.562937104 | AT1G32450.1 | NRT1.5 | Nitrate transporter 1.5 |
Zm00001d021781 | −3.589512662 | 1.006168604 | AT1G79360.1 | OCT2 | Organic cation transporter 2 |
Zm00001d039886 | −1.343911524 | 1.867730502 | AT3G54110.1 | PUMP1 | Uncoupling protein PUMP2 |
Zm00001d042730 | −1.845122758 | 2.690906476 | AT5G65360.1 | H3.1 | Histone |
Zm00001d020584 | −10.83217007 | 10.97500245 | AT5G59690.1 | - | Histone |
Zm00001d026106 | −1.39634541 | 1.54543134 | - | Glk41 | G2-like-transcription factor 41 |
Zm00001d031673 | −1.48213493 | 1.180787578 | AT1G43160.1 | RAP2.6 | Related to AP2 6 |
Zm00001d039859 | −1.141107245 | 1.392329759 | AT3G09390.1 | MT2A | Metallothionein |
Zm00001d043795 | −1.222220983 | 1.882006981 | AT1G10360.1 | GSTU18 | Glutathione S-transferase TAU 18 |
Gene ID 1 | Log2 Ratio (CML69_C vs. 5D) 2 | Log2 Ratio (LX9801_C vs. 5D) 3 | Best-hit-A.th 4 | Symbol 5 | Annotation 6 |
---|---|---|---|---|---|
Zm00001d048709 | −1.568831793 | 2.066012833 | - | BX1 | Benzoxazinless 1 |
Zm00001d048710 | −3.193078195 | 1.516375732 | - | BX2 | Benzoxazinone synthesis 2 |
Zm00001d048702 | −2.089702354 | 1.157137323 | - | BX3 | Benzoxazinone synthesis 3 |
Zm00001d018206 | −2.406569277 | 1.214850007 | AT1G37130.1 | NR2 | Nitrate reductase 2 |
Zm00001d033747 | −1.076317875 | 1.504587352 | AT5G37600.1 | GSR 1 | Glutamine synthetase |
Zm00001d043374 | −1.516339733 | 1.240722383 | AT1G52190.1 | NRT1.1 | Nitrate transporter |
Zm00001d017666 | −2.247773905 | 1.220192446 | AT1G32450.1 | NRT1.5 | Nitrate transporter 1.5 |
Zm00001d026131 | −1.101040846 | 1.057095664 | - | LHT | Lysine histidine transporter-like 7 |
Zm00001d051362 | −1.056763575 | 1.205752805 | AT4G17340.1 | TIP2 | Tonoplast intrinsic protein 2 |
Zm00001d021653 | −2.03788204 | 1.009690798 | AT1G61800.1 | GPT2 | Glucose−6-phosphate translocator 2 |
Zm00001d018056 | −1.257508316 | 1.100290806 | AT1G26945.1 | bHLH30 | bHLH-transcription factor 30 |
Zm00001d026106 | −2.455075759 | 1.96335238 | - | Glk41 | G2-like-transcription factor 41 |
Zm00001d033876 | −1.529425044 | 1.281885695 | AT4G37740.1 | GRF2 | Growth-regulating factor 2 |
Zm00001d034160 | −1.128547313 | 1.256333329 | - | glk44 | G2-like-transcription factor 44 |
Zm00001d006857 | −11.32647816 | 3.296768997 | AT1G20950.1 | - | Phosphofructokinase family |
Zm00001d016444 | −1.518798472 | 1.235047417 | - | - | - |
Zm00001d020584 | −10.83217007 | 11.67180641 | AT5G59690.1 | - | Histone |
Zm00001d020726 | −1.804385564 | 2.404793087 | AT1G47380.1 | PP2C | Protein phosphatase 2C |
Zm00001d021168 | −1.22761115 | 2.022306741 | AT2G43840.1 | UGT74F1 | UDP-glycosyltransferase 74 F1 |
Zm00001d025947 | −1.138375432 | 1.60173917 | AT3G60690.1 | SAUR59 | SAUR-like auxin-responsive |
Zm00001d027861 | −1.422607421 | 1.729671881 | AT4G39660.1 | AGT2 | Alanine: glyoxylate aminotransferase |
Zm00001d028693 | −1.639385828 | 1.098782465 | - | Saf1 | Safener induced 1 |
Zm00001d030348 | −1.953534228 | 1.091478477 | AT1G64710.1 | - | Alcohol dehydrogenase |
Zm00001d034788 | −1.200633487 | 1.688351727 | AT1G77280.2 | - | Kinase protein |
Zm00001d036989 | −1.501992276 | 1.044909155 | AT4G37820.2 | - | Transmembrane protein |
Zm00001d038209 | −1.16700922 | 1.0113365 | AT5G49820.1 | RUS6 | Root UVB sensitive protein |
Zm00001d038695 | −1.789903087 | 2.114447302 | - | GA2ox7 | Gibberellin 2-oxidase |
Zm00001d039859 | −1.549403992 | 2.883195042 | AT3G09390.1 | MT2A | Metallothionein |
Zm00001d050694 | −1.052286015 | 2.30335502 | AT1G43710.1 | EMB1075 | Pyridoxal phosphate (PLP) |
Zm00001d052651 | −1.629711466 | 2.143596379 | AT5G13870.3 | XTH5 | Xyloglucan endotransglucosylase |
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Waititu, J.K.; Zhang, X.; Chen, T.; Zhang, C.; Zhao, Y.; Wang, H. Transcriptome Analysis of Tolerant and Susceptible Maize Genotypes Reveals Novel Insights about the Molecular Mechanisms Underlying Drought Responses in Leaves. Int. J. Mol. Sci. 2021, 22, 6980. https://doi.org/10.3390/ijms22136980
Waititu JK, Zhang X, Chen T, Zhang C, Zhao Y, Wang H. Transcriptome Analysis of Tolerant and Susceptible Maize Genotypes Reveals Novel Insights about the Molecular Mechanisms Underlying Drought Responses in Leaves. International Journal of Molecular Sciences. 2021; 22(13):6980. https://doi.org/10.3390/ijms22136980
Chicago/Turabian StyleWaititu, Joram Kiriga, Xingen Zhang, Tianci Chen, Chunyi Zhang, Yang Zhao, and Huan Wang. 2021. "Transcriptome Analysis of Tolerant and Susceptible Maize Genotypes Reveals Novel Insights about the Molecular Mechanisms Underlying Drought Responses in Leaves" International Journal of Molecular Sciences 22, no. 13: 6980. https://doi.org/10.3390/ijms22136980