Characterization of the Regulatory Network under Waterlogging Stress in Soybean Roots via Transcriptome Analysis
<p>Physiological responses of soybean roots to waterlogging stress and heat-map of differentially expressed genes. Plants at the V2 stage were exposed to waterlogging stress for 10 days and allowed to recover for 15 days (<b>A</b>–<b>C</b>). Each of the images indicates before waterlogging (<b>A</b>), after 10 days of waterlogging (<b>B</b>), and 15 days of recovery (<b>C</b>). Scale bar = 5 cm. N = 3 for (<b>A</b>–<b>C</b>). Quantitative data of the root length (<b>D</b>) and the number of adventitious roots (<b>E</b>) are illustrated. Genes differentially expressed in roots during waterlogging stress were identified (<b>F</b>). Processing RNA-seq data under the criteria of FPKM > 4, <span class="html-italic">p</span>-value < 0.05, and |log2(fold change)| over 2 for roots exposed to waterlogging vs. mock-treated soybean roots (control) identified 1999 differentially expressed genes (DEGs). In the left panel, red indicates upregulation in the waterlogging/control comparison and green indicates downregulation in the waterlogging/control comparison. The right panel shows the average normalized FPKM values from RNA-seq experiments; blue indicates the lowest expression level and yellow indicates the highest level. Detailed data for the RNA-seq analysis are presented in <a href="#app1-plants-13-02538" class="html-app">Supplementary Table S2</a>.</p> "> Figure 2
<p>Gene Ontology (GO) enrichment analysis in the “biological process” category for genes up- and downregulated in response to waterlogging. Overall, 21 GO terms were highly over-represented, and in the downregulated gene group, 15 GO terms were significantly enriched (<span class="html-italic">p</span> < 0.05 and fold-enrichment values of >2 log2-fold). Details of the GO assignments are presented in <a href="#app1-plants-13-02538" class="html-app">Supplementary Table S3</a>.</p> "> Figure 3
<p>MapMan analysis of genes associated with the response to waterlogging. Overviews: (<b>A</b>) metabolism; (<b>B</b>) cellular response. Red and blue boxes indicate up- and downregulated genes, respectively; green boxes highlight the pathways related to waterlogging stress response. Detailed information is presented in <a href="#app1-plants-13-02538" class="html-app">Supplementary Table S4</a>.</p> "> Figure 4
<p>Expression analysis of major transcription factors in DEGs. Among the transcription factors, the number of upregulated genes is presented in light gray, and the number of downregulated genes is presented in dark gray (<b>A</b>). The expression of four randomly selected genes from the up- or downregulated genes was compared (<b>B</b>). C: control (light gray), WL: waterlogging (dark gray). *** <span class="html-italic">p</span> < 0.001.</p> "> Figure 5
<p>Construction and expression validation of co-functional networks associated with transcription factors regulated under waterlogging stress. (<b>A</b>) Co-functional network consists of various transcription factors retrieved from SoyNet. There are 19 AP2/ERF (white nodes), 1 bHLH (pink node), 1 bZIP (orange node), 4 C2H2 (ZF, yellow nodes), 14 NAC (green nodes), 9 WRKY (light blue nodes), 9 MYB (dark blue nodes), and 2 ortholog (gray nodes) in the network. Circular nodes represent upregulated genes; square nodes represent downregulated genes. The raw networks initially created in SoyNet are shown in <a href="#app1-plants-13-02538" class="html-app">Supplementary Figure S2</a>. (<b>B</b>) The expression of nine TF genes was significantly upregulated in a resistant variety, PI 567343, than in Daewonkong under waterlogging stress, as shown by qRT-PCR. The expression levels were normalized to that of <span class="html-italic">Act11</span> using a real-time polymerase chain reaction. DW: Daewonkong (light gray), PI 567343: waterlogging-resistant varieties (dark gray). ** <span class="html-italic">p</span> < 0.01; *** <span class="html-italic">p</span> < 0.001.</p> ">
Abstract
:1. Introduction
2. Materials and Methods
2.1. Experimental Design
2.2. Plant Materials and Waterlogging Stress Treatments
2.3. RNA Sequencing (RNA-Seq) Analysis
2.4. Functional Analysis of DEGs Using Gene Ontology (GO) and MapMan Software
2.5. Ortholog Analysis
2.6. Co-Functional Networks Analysis
2.7. RNA Extraction and Quantitative Real-Time PCR (qRT-PCR) Analysis
3. Results and Discussion
3.1. Physiological Responses of Soybean Roots Exposed to a Waterlogging Stress
3.2. Identification of Differentially Expressed Genes (DEGs) under Waterlogging Stress by RNA-Seq
3.3. Gene Ontology (GO) Enrichment Reveals Biological Processes Associated with Waterlogging Stress in Soybean Roots
3.4. MapMan Analysis of Waterlogging Stress-Related Genes in Soybean Roots
3.5. Expression Analysis of TFs in DEGs
3.6. Ortholog Analysis to Elucidate Flooding Stress-Related Genes in Soybean
3.7. Analysis of Co-Functional Networks of TFs and Orthologs
3.8. Stress Treatment of Waterlogging-Resistant Varieties and Quantitative Real-Time PCR (qRT-PCR) Analysis
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Hou, A.; Chen, P.; Alloatti, J.; Li, D.; Mozzoni, L.; Zhang, B.; Shi, A. Genetic Variability of Seed Sugar Content in Worldwide Soybean Germplasm Collections. Crop Sci. 2009, 49, 903–912. [Google Scholar] [CrossRef]
- Westcott, P.; Hansen, J. USDA Agricultural Projections to 2025. No. (OCE-2016-1); Office of the Chief Economist, World Agricultural Outlook Board: Washington, DC, USA, 2016.
- McFadden, J.; Smith, D.; Wechsler, S.; Wallander, S. Development, Adoption, and Management of Drought-Tolerant Corn in the United States; U.S. Department of Agriculture: Washington, DC, USA, 2019.
- Zhang, X.; Shabala, S.; Koutoulis, A.; Shabala, L.; Johnson, P.; Hayes, D.; Nichols, D.S.; Zhou, M. Waterlogging Tolerance in Barley Is Associated with Faster Aerenchyma Formation in Adventitious Roots. Plant Soil 2015, 394, 355–372. [Google Scholar] [CrossRef]
- Pedersen, O.; Perata, P.; Voesenek, L.A.C.J. Flooding and Low Oxygen Responses in Plants. Funct. Plant Biol. 2017, 44, iii–vi. [Google Scholar] [CrossRef]
- Irfan, M.; Hayat, S.; Hayat, Q.; Afroz, S.; Ahmad, A. Physiological and Biochemical Changes in Plants under Waterlogging. Protoplasma 2010, 241, 3–17. [Google Scholar] [CrossRef]
- Fukao, T.; Barrera-Figueroa, B.E.; Juntawong, P.; Peña-Castro, J.M. Submergence and Waterlogging Stress in Plants: A Review Highlighting Research Opportunities and Understudied Aspects. Front. Plant Sci. 2019, 10, 340. [Google Scholar] [CrossRef]
- Linkemer, G.; Board, J.E.; Musgrave, M.E. Waterlogging Effects on Growth and Yield Components in Late-Planted Soybean. Crop Sci. 1998, 38, 1576–1584. [Google Scholar] [CrossRef]
- Tian, X.-H.; Nakamura, T.; Kokubun, M. The Role of Seed Structure and Oxygen Responsiveness in Pre-Germination Flooding Tolerance of Soybean Cultivars. Plant Prod. Sci. 2005, 8, 157–165. [Google Scholar] [CrossRef]
- Lesk, C.; Rowhani, P.; Ramankutty, N. Influence of Extreme Weather Disasters on Global Crop Production. Nature 2016, 529, 84–87. [Google Scholar] [CrossRef]
- Scott, H.D.; DeAngulo, J.; Daniels, M.B.; Wood, L.S. Flood Duration Effects on Soybean Growth and Yield. Agron. J. 1989, 81, 631–636. [Google Scholar] [CrossRef]
- Tanoue, M.; Hirabayashi, Y.; Ikeuchi, H. Global-Scale River Flood Vulnerability in the Last 50 Years. Sci Rep. 2016, 6, 36021. [Google Scholar] [CrossRef]
- VanToai, T.T.; St. Martin, S.K.; Chase, K.; Boru, G.; Schnipke, V.; Schmitthenner, A.F.; Lark, K.G. Identification of a QTL Associated with Tolerance of Soybean to Soil Waterlogging. Crop Sci. 2001, 41, 1247–1252. [Google Scholar] [CrossRef]
- Cornelious, B.; Chen, P.; Chen, Y.; De Leon, N.; Shannon, J.G.; Wang, D. Identification of QTLs Underlying Water-Logging Tolerance in Soybean. Mol. Breed. 2005, 16, 103–112. [Google Scholar] [CrossRef]
- Nguyen, V.T.; Vuong, T.D.; VanToai, T.; Lee, J.D.; Wu, X.; Mian, M.A.R.; Dorrance, A.E.; Shannon, J.G.; Nguyen, H.T. Mapping of Quantitative Trait Loci Associated with Resistance to Phytophthora Sojae and Flooding Tolerance in Soybean. Crop Sci. 2012, 52, 2481–2493. [Google Scholar] [CrossRef]
- Sayama, T.; Nakazaki, T.; Ishikawa, G.; Yagasaki, K.; Yamada, N.; Hirota, N.; Hirata, K.; Yoshikawa, T.; Saito, H.; Teraishi, M.; et al. QTL Analysis of Seed-Flooding Tolerance in Soybean (Glycine Max [L.] Merr.). Plant Sci. 2009, 176, 514–521. [Google Scholar] [CrossRef] [PubMed]
- Yoo, Y.-H.; Nalini Chandran, A.K.; Park, J.-C.; Gho, Y.-S.; Lee, S.-W.; An, G.; Jung, K.-H. OsPhyB-Mediating Novel Regulatory Pathway for Drought Tolerance in Rice Root Identified by a Global RNA-Seq Transcriptome Analysis of Rice Genes in Response to Water Deficiencies. Front. Plant Sci. 2017, 8, 580. [Google Scholar] [CrossRef]
- Ayaz, A.; Saqib, S.; Huang, H.; Zaman, W.; Lü, S.; Zhao, H. Genome-Wide Comparative Analysis of Long-Chain Acyl-CoA Synthetases (LACSs) Gene Family: A Focus on Identification, Evolution and Expression Profiling Related to Lipid Synthesis. Plant Physiol. Biochem. 2021, 161, 1–11. [Google Scholar] [CrossRef]
- Du, H.; Zhu, J.; Su, H.; Huang, M.; Wang, H.; Ding, S.; Zhang, B.; Luo, A.; Wei, S.; Tian, X.; et al. Bulked Segregant RNA-Seq Reveals Differential Expression and SNPs of Candidate Genes Associated with Waterlogging Tolerance in Maize. Front. Plant Sci. 2017, 8, 1022. [Google Scholar] [CrossRef]
- van Veen, H.; Vashisht, D.; Akman, M.; Girke, T.; Mustroph, A.; Reinen, E.; Hartman, S.; Kooiker, M.; van Tienderen, P.; Schranz, M.E.; et al. Transcriptomes of Eight Arabidopsis Thaliana Accessions Reveal Core Conserved, Genotype- and Organ-Specific Responses to Flooding Stress. Plant Physiol. 2016, 172, 668–689. [Google Scholar] [CrossRef]
- Zaman, M.S.U.; Malik, A.I.; Erskine, W.; Kaur, P. Changes in Gene Expression during Germination Reveal Pea Genotypes with Either “Quiescence” or “Escape” Mechanisms of Waterlogging Tolerance. Plant Cell Environ. 2019, 42, 245–258. [Google Scholar] [CrossRef]
- Tamang, B.G.; Li, S.; Rajasundaram, D.; Lamichhane, S.; Fukao, T. Overlapping and Stress-Specific Transcriptomic and Hormonal Responses to Flooding and Drought in Soybean. Plant J. 2021, 107, 100–117. [Google Scholar] [CrossRef]
- Lin, Y.; Li, W.; Zhang, Y.; Xia, C.; Liu, Y.; Wang, C.; Xu, R.; Zhang, L. Identification of Genes/Proteins Related to Submergence Tolerance by Transcriptome and Proteome Analyses in Soybean. Sci Rep. 2019, 9, 14688. [Google Scholar] [CrossRef] [PubMed]
- Koo, S.C.; Kim, H.T.; Kang, B.K.; Lee, Y.H.; Oh, K.W.; Kim, H.Y.; Baek, I.Y.; Yun, H.T.; Choi, M.S. Screening of Flooding Tolerance in Soybean Germplasm Collection. Korean J. Breed. Sci. 2014, 46, 129–135. [Google Scholar] [CrossRef]
- Tamang, B.G.; Magliozzi, J.O.; Maroof, M.a.S.; Fukao, T. Physiological and Transcriptomic Characterization of Submergence and Reoxygenation Responses in Soybean Seedlings. Plant Cell Environ. 2014, 37, 2350–2365. [Google Scholar] [CrossRef] [PubMed]
- Bolger, A.M.; Lohse, M.; Usadel, B. Trimmomatic: A Flexible Trimmer for Illumina Sequence Data. Bioinformatics 2014, 30, 2114–2120. [Google Scholar] [CrossRef] [PubMed]
- Kim, D.; Paggi, J.M.; Park, C.; Bennett, C.; Salzberg, S.L. Graph-Based Genome Alignment and Genotyping with HISAT2 and HISAT-Genotype. Nat. Biotech. 2019, 37, 907–915. [Google Scholar] [CrossRef]
- Kovaka, S.; Zimin, A.V.; Pertea, G.M.; Razaghi, R.; Salzberg, S.L.; Pertea, M. Transcriptome Assembly from Long-Read RNA-Seq Alignments with StringTie2. Genome Biol. 2019, 20, 278. [Google Scholar] [CrossRef]
- Tian, T.; Liu, Y.; Yan, H.; You, Q.; Yi, X.; Du, Z.; Xu, W.; Su, Z. agriGO v2.0: A GO Analysis Toolkit for the Agricultural Community, 2017 Update. Nucleic Acids Res. 2017, 45, W122–W129. [Google Scholar] [CrossRef]
- Wickham, H. Ggplot2. WIREs Comp. Stats. 2011, 3, 180–185. [Google Scholar] [CrossRef]
- Thimm, O.; Bläsing, O.; Gibon, Y.; Nagel, A.; Meyer, S.; Krüger, P.; Selbig, J.; Müller, L.A.; Rhee, S.Y.; Stitt, M. Mapman: A User-Driven Tool to Display Genomics Data Sets onto Diagrams of Metabolic Pathways and Other Biological Processes. Plant J. 2004, 37, 914–939. [Google Scholar] [CrossRef]
- Jia, W.; Ma, M.; Chen, J.; Wu, S. Plant Morphological, Physiological and Anatomical Adaption to Flooding Stress and the Underlying Molecular Mechanisms. Int. J. Mol. Sci. 2021, 22, 1088. [Google Scholar] [CrossRef]
- Wu, J.; Wang, J.; Hui, W.; Zhao, F.; Wang, P.; Su, C.; Gong, W. Physiology of Plant Responses to Water Stress and Related Genes: A Review. Forests 2022, 13, 324. [Google Scholar] [CrossRef]
- Raudvere, U.; Kolberg, L.; Kuzmin, I.; Arak, T.; Adler, P.; Peterson, H.; Vilo, J. G:Profiler: A Web Server for Functional Enrichment Analysis and Conversions of Gene Lists (2019 Update). Nucleic Acids Res. 2019, 47, W191–W198. [Google Scholar] [CrossRef] [PubMed]
- Kim, E.; Hwang, S.; Lee, I. SoyNet: A Database of Co-Functional Networks for Soybean Glycine Max. Nucleic Acids Res. 2017, 45, D1082–D1089. [Google Scholar] [CrossRef] [PubMed]
- Shannon, P.; Markiel, A.; Ozier, O.; Baliga, N.S.; Wang, J.T.; Ramage, D.; Amin, N.; Schwikowski, B.; Ideker, T. Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks. Genome Res. 2003, 13, 2498–2504. [Google Scholar] [CrossRef] [PubMed]
- Hu, R.; Fan, C.; Li, H.; Zhang, Q.; Fu, Y.-F. Evaluation of Putative Reference Genes for Gene Expression Normalization in Soybean by Quantitative Real-Time RT-PCR. BMC Mol. Biol. 2009, 10, 93. [Google Scholar] [CrossRef]
- Striker, G.G. Flooding Stress on Plants: Anatomical, Morphological and Physiological Responses. Botany 2012, 1, 3–28. [Google Scholar]
- Steffens, B.; Rasmussen, A. The Physiology of Adventitious Roots. Plant Physiol. 2016, 170, 603–617. [Google Scholar] [CrossRef]
- Vidoz, M.L.; Loreti, E.; Mensuali, A.; Alpi, A.; Perata, P. Hormonal Interplay during Adventitious Root Formation in Flooded Tomato Plants. Plant J. 2010, 63, 551–562. [Google Scholar] [CrossRef]
- Zhai, L.; Liu, Z.; Zou, X.; Jiang, Y.; Qiu, F.; Zheng, Y.; Zhang, Z. Genome-Wide Identification and Analysis of microRNA Responding to Long-Term Waterlogging in Crown Roots of Maize Seedlings. Physiol. Plant 2013, 147, 181–193. [Google Scholar] [CrossRef]
- Qi, X.; Li, Q.; Ma, X.; Qian, C.; Wang, H.; Ren, N.; Shen, C.; Huang, S.; Xu, X.; Xu, Q.; et al. Waterlogging-Induced Adventitious Root Formation in Cucumber Is Regulated by Ethylene and Auxin through Reactive Oxygen Species Signalling. Plant Cell Environ. 2019, 42, 1458–1470. [Google Scholar] [CrossRef]
- Cho, H.-Y.; Loreti, E.; Shih, M.-C.; Perata, P. Energy and Sugar Signaling during Hypoxia. New Phytol. 2021, 229, 57–63. [Google Scholar] [CrossRef] [PubMed]
- Perata, P.; Alpi, A. Plant Responses to Anaerobiosis. Plant Sci. 1993, 93, 1–17. [Google Scholar] [CrossRef]
- Bui, L.T.; Novi, G.; Lombardi, L.; Iannuzzi, C.; Rossi, J.; Santaniello, A.; Mensuali, A.; Corbineau, F.; Giuntoli, B.; Perata, P.; et al. Conservation of Ethanol Fermentation and Its Regulation in Land Plants. J. Exp. Bot. 2019, 70, 1815–1827. [Google Scholar] [CrossRef] [PubMed]
- Nanjo, Y.; Maruyama, K.; Yasue, H.; Yamaguchi-Shinozaki, K.; Shinozaki, K.; Komatsu, S. Transcriptional Responses to Flooding Stress in Roots Including Hypocotyl of Soybean Seedlings. Plant Mol. Biol. 2011, 77, 129–144. [Google Scholar] [CrossRef] [PubMed]
- Komatsu, S.; Thibaut, D.; Hiraga, S.; Kato, M.; Chiba, M.; Hashiguchi, A.; Tougou, M.; Shimamura, S.; Yasue, H. Characterization of a Novel Flooding Stress-Responsive Alcohol Dehydrogenase Expressed in Soybean Roots. Plant Mol. Biol. 2011, 77, 309–322. [Google Scholar] [CrossRef]
- Jung, K.-H.; An, G. Application of MapMan and RiceNet Drives Systematic Analyses of the Early Heat Stress Transcriptome in Rice Seedlings. J. Plant Biol. 2012, 55, 436–449. [Google Scholar] [CrossRef]
- Wang, J.; Sun, H.; Sheng, J.; Jin, S.; Zhou, F.; Hu, Z.; Diao, Y. Transcriptome, Physiological and Biochemical Analysis of Triarrhena Sacchariflora in Response to Flooding Stress. BMC Genet. 2019, 20, 88. [Google Scholar] [CrossRef]
- Ye, T.; Shi, H.; Wang, Y.; Chan, Z. Contrasting Changes Caused by Drought and Submergence Stresses in Bermudagrass (Cynodon dactylon). Front. Plant Sci. 2015, 6, 951. [Google Scholar] [CrossRef]
- Chiang, C.M.; Chen, L.F.O.; Shih, S.W.; Lin, K.H. Expression of Eggplant Ascorbate Peroxidase Increases the Tolerance of Transgenic Rice Plants to Flooding Stress. J. Plant Biochem. Biotechnol. 2015, 24, 257–267. [Google Scholar] [CrossRef]
- Keya, S.S.; Mostofa, M.G.; Rahman, M.; Das, A.K.; Rahman, A.; Anik, T.R.; Sultana, S.; Khan, A.R.; Islam, R.; Watanabe, Y.; et al. Effects of Glutathione on Waterlogging-Induced Damage in Sesame Crop. Ind. Crops Prod. 2022, 185, 115092. [Google Scholar] [CrossRef]
- Voesenek, L.A.C.J.; Bailey-Serres, J. Flood Adaptive Traits and Processes: An Overview. New Phytol. 2015, 206, 57–73. [Google Scholar] [CrossRef] [PubMed]
- Bui, L.T.; Giuntoli, B.; Kosmacz, M.; Parlanti, S.; Licausi, F. Constitutively Expressed ERF-VII Transcription Factors Redundantly Activate the Core Anaerobic Response in Arabidopsis thaliana. Plant Sci. 2015, 236, 37–43. [Google Scholar] [CrossRef] [PubMed]
- Gasch, P.; Fundinger, M.; Müller, J.T.; Lee, T.; Bailey-Serres, J.; Mustroph, A. Redundant ERF-VII Transcription Factors Bind to an Evolutionarily Conserved Cis-Motif to Regulate Hypoxia-Responsive Gene Expression in Arabidopsis. Plant Cell 2016, 28, 160–180. [Google Scholar] [CrossRef] [PubMed]
- Hattori, Y.; Nagai, K.; Furukawa, S.; Song, X.-J.; Kawano, R.; Sakakibara, H.; Wu, J.; Matsumoto, T.; Yoshimura, A.; Kitano, H.; et al. The Ethylene Response Factors SNORKEL1 and SNORKEL2 Allow Rice to Adapt to Deep Water. Nature 2009, 460, 1026–1030. [Google Scholar] [CrossRef]
- Yu, F.; Liang, K.; Fang, T.; Zhao, H.; Han, X.; Cai, M.; Qiu, F. A Group VII Ethylene Response Factor Gene, ZmEREB180, Coordinates Waterlogging Tolerance in Maize Seedlings. Plant Biotechnol. J. 2019, 17, 2286–2298. [Google Scholar] [CrossRef]
- van Veen, H.; Akman, M.; Jamar, D.C.L.; Vreugdenhil, D.; Kooiker, M.; van Tienderen, P.; Voesenek, L.A.C.J.; Schranz, M.E.; Sasidharan, R. Group VII Ethylene Response Factor Diversification and Regulation in Four Species from Flood-Prone Environments. Plant Cell Environ. 2014, 37, 2421–2432. [Google Scholar] [CrossRef]
- Wei, X.; Xu, H.; Rong, W.; Ye, X.; Zhang, Z. Constitutive Expression of a Stabilized Transcription Factor Group VII Ethylene Response Factor Enhances Waterlogging Tolerance in Wheat without Penalizing Grain Yield. Plant Cell Environ. 2019, 42, 1471–1485. [Google Scholar] [CrossRef]
- Tian, H.; Fan, G.; Xiong, X.; Wang, H.; Zhang, S.; Geng, G. Characterization and Transformation of the CabHLH18 Gene from Hot Pepper to Enhance Waterlogging Tolerance. Front. Plant Sci. 2024, 14, 1285198. [Google Scholar] [CrossRef]
- Rauf, M.; Arif, M.; Fisahn, J.; Xue, G.-P.; Balazadeh, S.; Mueller-Roeber, B. NAC Transcription Factor SPEEDY HYPONASTIC GROWTH Regulates Flooding-Induced Leaf Movement in Arabidopsis. Plant Cell 2013, 25, 4941–4955. [Google Scholar] [CrossRef]
- Tang, H.; Bi, H.; Liu, B.; Lou, S.; Song, Y.; Tong, S.; Chen, N.; Jiang, Y.; Liu, J.; Liu, H. WRKY33 Interacts with WRKY12 Protein to Up-Regulate RAP2.2 during Submergence Induced Hypoxia Response in Arabidopsis Thaliana. New Phytol. 2021, 229, 106–125. [Google Scholar] [CrossRef]
- Liu, Z.; Kumari, S.; Zhang, L.; Zheng, Y.; Ware, D. Characterization of miRNAs in Response to Short-Term Waterlogging in Three Inbred Lines of Zea Mays. PLoS ONE 2012, 7, e39786. [Google Scholar] [CrossRef] [PubMed]
- Xue, T.; Liu, Z.; Dai, X.; Xiang, F. Primary Root Growth in Arabidopsis Thaliana Is Inhibited by the miR159 Mediated Repression of MYB33, MYB65 and MYB101. Plant Sci. 2017, 262, 182–189. [Google Scholar] [CrossRef] [PubMed]
- Dietrich, K.; Weltmeier, F.; Ehlert, A.; Weiste, C.; Stahl, M.; Harter, K.; Dröge-Laser, W. Heterodimers of the Arabidopsis Transcription Factors bZIP1 and bZIP53 Reprogram Amino Acid Metabolism during Low Energy Stress. Plant Cell 2011, 23, 381–395. [Google Scholar] [CrossRef] [PubMed]
- Yao, W.; Li, G.; Yu, Y.; Ouyang, Y. funRiceGenes Dataset for Comprehensive Understanding and Application of Rice Functional Genes. GigaScience 2018, 7, gix119. [Google Scholar] [CrossRef]
- Hinz, M.; Wilson, I.W.; Yang, J.; Buerstenbinder, K.; Llewellyn, D.; Dennis, E.S.; Sauter, M.; Dolferus, R. Arabidopsis RAP2.2: An Ethylene Response Transcription Factor That Is Important for Hypoxia Survival. Plant Physiol. 2010, 153, 757–772. [Google Scholar] [CrossRef]
- Tsuji, H.; Meguro, N.; Suzuki, Y.; Tsutsumi, N.; Hirai, A.; Nakazono, M. Induction of Mitochondrial Aldehyde Dehydrogenase by Submergence Facilitates Oxidation of Acetaldehyde during Re-Aeration in Rice. FEBS Lett. 2003, 546, 369–373. [Google Scholar] [CrossRef]
- Weits, D.A.; Giuntoli, B.; Kosmacz, M.; Parlanti, S.; Hubberten, H.-M.; Riegler, H.; Hoefgen, R.; Perata, P.; van Dongen, J.T.; Licausi, F. Plant Cysteine Oxidases Control the Oxygen-Dependent Branch of the N-End-Rule Pathway. Nat. Commun. 2014, 5, 3425. [Google Scholar] [CrossRef]
- Sauter, M.; Rzewuski, G.; Marwedel, T.; Lorbiecke, R. The Novel Ethylene-regulated Gene OsUsp1 from Rice Encodes a Member of a Plant Protein Family Related to Prokaryotic Universal Stress Proteins. J. Exp. Bot. 2002, 53, 2325–2331. [Google Scholar] [CrossRef]
- Zhou, Z.; de Almeida Engler, J.; Rouan, D.; Michiels, F.; Van Montagu, M.; Van Der Straeten, D. Tissue Localization of a Submergence-Induced 1-Aminocyclopropane-1-Carboxylic Acid Synthase in Rice. Plant Physiol. 2002, 129, 72–84. [Google Scholar] [CrossRef]
- Mitsuya, S.; Yokota, Y.; Fujiwara, T.; Mori, N.; Takabe, T. OsBADH1 Is Possibly Involved in Acetaldehyde Oxidation in Rice Plant Peroxisomes. FEBS Lett. 2009, 583, 3625–3629. [Google Scholar] [CrossRef]
- Valliyodan, B.; Ye, H.; Song, L.; Murphy, M.; Shannon, J.G.; Nguyen, H.T. Genetic Diversity and Genomic Strategies for Improving Drought and Waterlogging Tolerance in Soybeans. J. Exp. Bot. 2017, 68, 1835–1849. [Google Scholar] [CrossRef] [PubMed]
- Urano, K.; Kurihara, Y.; Seki, M.; Shinozaki, K. ‘Omics’ Analyses of Regulatory Networks in Plant Abiotic Stress Responses. Curr. Opin. Plant Biol. 2010, 13, 132–138. [Google Scholar] [CrossRef] [PubMed]
Plants | Initial_Alias (Gene_Id) | Symbol | Ortholog_Name | Description | DEG | Reference |
---|---|---|---|---|---|---|
Arabidopsis | AT1G12010 | ACO | Glyma.15G112700 | 1-aminocyclopropane-1-carboxylate (ACC) oxidase | Down | [67] |
AT1G12010 | ACO | Glyma.09G008400 | 1-aminocyclopropane-1-carboxylate (ACC) oxidase | Down | [67] | |
AT5G39890 | AtPCO2 | Glyma.19G020500 | cysteine oxidase (PCO) | Down | [69] | |
AT5G15120 | AtPCO1 | Glyma.19G020500 | cysteine oxidase (PCO) | Down | [69] | |
Rice | Os07g47620 | OsUsp1 | Glyma.02G155600 | not annotated | Up | [70] |
Os01g09700 | OS-ACS5, OsACS5 | Glyma.05G223000 | 1-aminocyclopropane-1-carboxylate (ACC) synthase | Up | [71] | |
Os01g09700 | OS-ACS5, OsACS5 | Glyma.08G030100 | 1-aminocyclopropane-1-carboxylate (ACC) synthase | Up | [71] | |
Os04g39020 | BAD1, OsBADH1 | Glyma.06G186300 | betaine-aldehyde dehydrogenase | Up | [72] | |
Os02g49720 | ALDH2a, OsALDH2B5 | Glyma.02G034000 | aldehyde dehydrogenase (ALDH2B) | Down | [68] |
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Yoo, Y.-H.; Cho, S.-Y.; Lee, I.; Kim, N.; Lee, S.-K.; Cho, K.-S.; Kim, E.Y.; Jung, K.-H.; Hong, W.-J. Characterization of the Regulatory Network under Waterlogging Stress in Soybean Roots via Transcriptome Analysis. Plants 2024, 13, 2538. https://doi.org/10.3390/plants13182538
Yoo Y-H, Cho S-Y, Lee I, Kim N, Lee S-K, Cho K-S, Kim EY, Jung K-H, Hong W-J. Characterization of the Regulatory Network under Waterlogging Stress in Soybean Roots via Transcriptome Analysis. Plants. 2024; 13(18):2538. https://doi.org/10.3390/plants13182538
Chicago/Turabian StyleYoo, Yo-Han, Seung-Yeon Cho, Inhye Lee, Namgeol Kim, Seuk-Ki Lee, Kwang-Soo Cho, Eun Young Kim, Ki-Hong Jung, and Woo-Jong Hong. 2024. "Characterization of the Regulatory Network under Waterlogging Stress in Soybean Roots via Transcriptome Analysis" Plants 13, no. 18: 2538. https://doi.org/10.3390/plants13182538