Physiological, Epigenetic, and Transcriptome Analyses Provide Insights into the Responses of Wheat Seedling Leaves to Different Water Depths under Flooding Conditions
Abstract
:1. Introduction
2. Results
2.1. The Distinct Effects of FS and HS/WL on Biomass and Photosynthesis
2.2. Physiochemical Changes under the Three Flooding Conditions
2.3. Global Changes in DNA Methylation under the CK, WL, HS, and FS Conditions
2.4. Analysis of DEGs in Wheat in Response to the Three Types of Flooding Stress
2.5. KEGG Enrichment Analysis of the WL-, HS- and FS-Induced DEGs
2.6. GO Enrichment Analysis of the WL-, HS- and FS-Induced DEGs
2.7. Analysis of the DEGs Related to the Photosynthesis Pathway in Response to WL, HS, and FS Stresses
2.8. Analysis of the DEGs Related to Phenylpropanoid Biosynthesis and Antioxidant Pathways in Response to WL, HS, and FS Stresses
2.9. Expression of the Plant Hormone Signal Transduction Pathway and Transcription Factor Genes in Response to Different Flooding Stresses
3. Discussion
3.1. The Submergence of Functional Leaves Was the Key Factor Determining Photosynthetic Efficiency after Submergence
3.2. The Role of Antioxidant Mechanisms in Response to the Three Types of Flooding Conditions
3.3. Genes Related to Phenylpropanoid Biosynthesis Were Differentially Regulated in Response to Different Flood Stresses in the Wheat Seedling Stage
3.4. Specific Responses of Plant Hormone Signaling Genes to Different Depths of Flooding Stress
3.5. Flooding-Type-Dependent Response Pathways and TFs
3.6. Type-Dependent Alterations in DNA Methylation Levels under the WL, HS, and FS Treatments
4. Materials and Methods
4.1. Plant Material and Flooding Treatments
4.2. Physiological Measurements and Growth Parameters
4.3. Methylation-Sensitive Amplified Polymorphism (MSAP) Analysis
4.4. RNA Extraction, Library Preparation, and Sequencing
4.5. RNA-Seq Read Mapping, Sequence Assembly, and Differential Expression
4.6. Functional Analysis of DEGs
4.7. Quantitative Real-Time PCR (qRT–PCR) Validation
4.8. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Manik, S.M.N.; Quamruzzaman, M.; Livermore, M.; Zhao, C.C.; Johnson, P.; Hunt, I.; Shabala, S.; Zhou, M.X. Impacts of barley root cortical aerenchyma on growth, physiology, yield components, and grain quality under field waterlogging conditions. Field Crops Res. 2022, 279, 108461. [Google Scholar] [CrossRef]
- Sasidharan, R.; Bailey-Serres, J.; Ashikari, M.; Atwell, B.J.; Colmer, T.D.; Fagerstedt, K.; Fukao, T.; Geigenberger, P.; Hebelstrup, K.H.; Hill, R.D. Community recommendations on terminology and procedures used in flooding and low oxygen stress research. New Phytol. 2017, 214, 1403–1407. [Google Scholar] [CrossRef] [PubMed]
- Manik, S.M.; Pengilley, G.; Dean, G.; Field, B.; Shabala, S.; Zhou, M.X. Soil and crop management practices to minimize the impact of waterlogging on crop productivity. Front. Plant Sci. 2019, 10, 140. [Google Scholar] [CrossRef]
- Xiao, Y.S.; Wu, X.L.; Sun, M.X.; Peng, F.T. Hydrogen sulfide alleviates waterlogging-induced damage in peach seedlings via enhancing antioxidative system and inhibiting ethylene synthesis. Front. Plant Sci. 2020, 11, 696. [Google Scholar] [CrossRef] [PubMed]
- Liu, K.; Harrison, M.T.; Shabala, S.; Meinke, H.; Ahmed, I.; Zhang, Y.B.; Tian, X.H.; Zhou, M.X. The state of the art in modeling waterlogging impacts on plants: What do we know and what do we need to know. Earth’s Future 2020, 8, e2020EF001801. [Google Scholar] [CrossRef]
- Liu, K.; Harrison, M.T.; Archontoulis, S.V.; Huth, N.; Yang, R.; Liu, D.L.; Yan, H.L.; Meinke, H.; Huber, I.; Feng, P.Y.; et al. Climate change shifts forward flowering and reduces crop waterlogging stress. Environ. Res. Lett. 2021, 16, 094017. [Google Scholar] [CrossRef]
- Wang, J.; Sun, H.; Sheng, J.J.; Jin, S.R.; Zhou, F.S.; Hu, Z.L.; Diao, Y. Transcriptome, physiological and biochemical analysis of Triarrhena sacchariflora in response to flooding stress. BMC Genet. 2019, 20, 88. [Google Scholar] [CrossRef]
- Li, Y.; Shi, L.C.; Yang, J.; Qian, Z.H.; He, Y.X.; Li, M.W. Physiological and transcriptional changes provide insights into the effect of root waterlogging on the aboveground part of Pterocarya stenoptera. Genomics 2021, 113, 2583–2590. [Google Scholar] [CrossRef]
- Shen, C.W.; Yuan, J.P.; Qiao, H.; Wang, Z.J.; Liu, Y.H.; Ren, X.J.; Wang, F.; Liu, X.; Zhang, Y.; Chen, X.L.; et al. Transcriptomic and anatomic profiling reveal the germination process of different wheat varieties in response to waterlogging stress. BMC Genet. 2020, 21, 93. [Google Scholar] [CrossRef]
- Zeng, N.B.; Yang, Z.J.; Zhang, Z.F.; Hu, L.X.; Chen, L. Comparative transcriptome combined with proteome analyses revealed key factors involved in Alfalfa (Medicago sativa) response to waterlogging stress. Int. J. Mol. Sci. 2019, 20, 1359. [Google Scholar] [CrossRef]
- Keska, K.; Szczesniak, M.W.; Makalowska, I.; Czernicka, M. Long-Term waterlogging as factor contributing to hypoxia stress tolerance enhancement in cucumber: Comparative transcriptome analysis of waterlogging sensitive and tolerant accessions. Genes 2021, 12, 189. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; He, Y.; Zhang, C.B.; Tian, Y.A.; Lei, X.; Li, D.X.; Bai, S.Q.; Deng, X.G.; Lin, H.H. Physiological and transcriptional responses of Phalaris arundinacea under waterlogging conditions. J. Plant Physiol. 2021, 261, 153428. [Google Scholar] [CrossRef]
- Salah, A.; Zhan, M.; Cao, C.G.; Han, Y.L.; Ling, L.; Liu, Z.H.; Li, P.; Ye, M.; Jiang, Y. Gamma-aminobutyric acid promotes chloroplast ultrastructure, antioxidant capacity, and growth of waterlogged maize seedlings. Sci. Rep. 2019, 9, 484. [Google Scholar] [CrossRef]
- Yu, F.; Liang, K.; Fang, T.; Zhao, H.L.; Han, X.S.; Cai, M.J.; Qiu, F.Z. A group VII ethylene response factor gene, ZmEREB180, coordinates waterlogging tolerance in maize seedlings. Plant Biotechnol. J. 2019, 17, 2286–2298. [Google Scholar] [CrossRef] [PubMed]
- Wei, X.N.; Xu, H.J.; Rong, W.; Ye, X.G.; Zhang, Z.Y. 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]
- Wang, W.S.; Qin, Q.; Sun, F.; Wang, Y.X.; Xu, D.D.; Li, Z.K.; Fu, B.Y. Genome-wide differences in DNA methylation changes in two contrasting rice genotypes in response to drought conditions. Front. Plant Sci. 2016, 7, 1675. [Google Scholar] [CrossRef]
- Komivi, D.; Marie, A.M.; Zhou, R.; Zhou, Q.; Yang, M.; Ndiaga, C.; Diaga, D.; Wang, L.H.; Zhang, X.R. The contrasting response to drought and waterlogging is underpinned by divergent DNA methylation programs associated with transcript accumulation in sesame. Plant Sci. 2018, 277, 207–217. [Google Scholar] [CrossRef] [PubMed]
- Pan, R.; Xu, Y.H.; Xu, L.; Zhou, M.X.; Jiang, W.; Wang, Q.; Zhang, W.Y. Methylation changes in response to hypoxic stress in wheat regulated by methyltransferases. Russ. J. Plant Physiol. 2020, 67, 323–333. [Google Scholar] [CrossRef]
- Kumar, S.; Bhushan, B.; Wakchaure, G.; Meena, K.K.; Kumar, M.; Meena, N.L.; Rane, J. Plant phenolics under water-deficit conditions: Biosynthesis, accumulation, and physiological roles in water stress alleviation. In Plant Phenolics in Sustainable Agriculture; Springer: Berlin/Heidelberg, Germany, 2020; pp. 451–465. [Google Scholar]
- Li, B.; Cai, H.Y.; Liu, K.; An, B.Z.; Wang, R.; Yang, F.; Zeng, C.L.; Jiao, C.H.; Xu, Y.H. DNA methylation alterations and their association with high temperature tolerance in rice anthesis. J. Plant Growth Regul. 2022, 42, 780–794. [Google Scholar] [CrossRef]
- Tang, M.Q.; Yue, J.; Huang, Z.; Hu, Y.L.; Li, Z.; Luo, D.J.; Cao, S.; Zhang, H.; Pan, J.; Wu, X.; et al. Physiological and DNA methylation analysis provides epigenetic insights into chromium tolerance in kenaf. Environ. Exp. Bot. 2022, 194, 104684. [Google Scholar] [CrossRef]
- Rao, L.; Li, S.; Cui, X. Leaf morphology and chlorophyll fluorescence characteristics of mulberry seedlings under waterlogging stress. Sci. Rep. 2021, 11, 13379. [Google Scholar] [CrossRef] [PubMed]
- Manzur, M.E.; Grimoldi, A.A.; Striker, G.G. The forage grass Paspalum dilatatum tolerates partial but not complete submergence caused by either deep water or repeated defoliation. Crop Pasture Sci. 2020, 71, 190–198. [Google Scholar] [CrossRef]
- Striker, G.G.; Kotula, L.; Colmer, T.D. Tolerance to partial and complete submergence in the forage legume Melilotus siculus: An evaluation of 15 accessions for petiole hyponastic response and gas-filled spaces, leaf hydrophobicity and gas films, and root phellem. Ann. Bot. 2019, 123, 169–180. [Google Scholar] [CrossRef] [PubMed]
- Appels, R.; Eversole, K.; Stein, N.; Feuillet, C.; Keller, B.; Rogers, J.; Pozniak, C.J.; Choulet, F.; Distelfeld, A. Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 2018, 361, 7191. [Google Scholar]
- Herzog, M.; Fukao, T.; Winkel, A.; Konnerup, D.; Lamichhane, S.; Alpuerto, J.B.; Hasler, S.H.; Pedersen, O. Physiology, gene expression, and metabolome of two wheat cultivars with contrasting submergence tolerance. Plant Cell Environ. 2018, 41, 1632–1644. [Google Scholar] [CrossRef] [PubMed]
- Herzog, M.; Striker, G.G.; Colmer, T.D.; Pedersen, O. Mechanisms of waterlogging tolerance in wheat: A review of root and shoot physiology. Plant Cell Environ. 2016, 39, 1068–1086. [Google Scholar] [CrossRef] [PubMed]
- Wang, W.; Du, J.; Chen, L.; Zeng, Y.; Tan, X.; Shi, Q.; Pan, X.; Wu, Z.; Zeng, Y. Transcriptomic, proteomic, and physiological comparative analyses of flooding mitigation of the damage induced by low-temperature stress in direct seeded early indica rice at the seedling stage. BMC Genom. 2021, 22, 176. [Google Scholar] [CrossRef] [PubMed]
- Wang, J.; Zhang, Y.X.; Yan, X.R.; Guo, J.P. Physiological and transcriptomic analyses of yellow horn (Xanthoceras sorbifolia) provide important insights into salt and saline-alkali stress tolerance. PLoS ONE 2020, 15, e0244365. [Google Scholar] [CrossRef]
- Cheng, X.X.; Yu, M.; Zhang, N.; Zhou, Z.Q.; Xu, Q.T.; Mei, F.Z.; Qu, L.H. Reactive oxygen species regulate programmed cell death progress of endosperm in winter wheat (Triticum aestivum L.) under waterlogging. Protoplasma 2016, 253, 311–327. [Google Scholar] [CrossRef]
- Gill, M.B.; Zeng, F.; Shabala, L.; Zhang, G.P.; Yu, M.; Demidchik, V.; Shabala, s.; Zhou, M.X. Identification of QTL related to ROS formation under hypoxia and their association with waterlogging and salt tolerance in barley. Int. J. Mol. Sci. 2019, 20, 699. [Google Scholar] [CrossRef]
- Wang, S.Y.; Zhou, H.; Feng, N.J.; Xiang, H.T.; Liu, Y.; Wang, F.; Li, W.; Feng, S.J.; Liu, M.L.; Zheng, D.F. Physiological response of soybean leaves to uniconazole under waterlogging stress at R1 stage. J. Plant Physiol. 2022, 268, 153579. [Google Scholar] [CrossRef]
- Fakih, Z.; Plourde, M.B.; Germain, H. Differential participation of plant ribosomal proteins from the small ribosomal subunit in protein translation under stress. Biomolecules 2023, 13, 1160. [Google Scholar] [CrossRef]
- Liu, Y.; Beyer, A.; Aebersold, R. On the dependency of cellular protein levels on mRNA abundance. Cell 2016, 165, 535–550. [Google Scholar] [CrossRef] [PubMed]
- Cao, B.l.; Li, N.; Xu, K. Crosstalk of phenylpropanoid biosynthesis with hormone signaling in Chinese cabbage is key to counteracting salt stress. Environ. Exp. Bot. 2020, 179, 104209. [Google Scholar] [CrossRef]
- Koramutla, M.K.; Tuan, P.A.; Ayele, B.T. Salicylic acid enhances adventitious root and aerenchyma formation in wheat under waterlogged conditions. Int. J. Mol. Sci. 2022, 23, 1243. [Google Scholar] [CrossRef] [PubMed]
- Nguyen, T.N.; Son, S.; Jordan, M.C.; Levin, D.B.; Ayele, B.T. Lignin biosynthesis in wheat (Triticum aestivum L.): Its response to waterlogging and association with hormonal levels. BMC Plant Biol. 2016, 16, 28. [Google Scholar] [CrossRef] [PubMed]
- Yang, G.; Pan, W.Q.; Zhang, R.Y.; Pan, Y.; Guo, Q.F.; Song, W.N.; Zheng, W.J.; Nie, X.J. Genome-wide identification and characterization of caffeoyl-coenzyme A O-methyltransferase genes related to the Fusarium head blight response in wheat. BMC Genom. 2021, 22, 504. [Google Scholar] [CrossRef]
- Hodgson, K.K.; Perlo, V.; Furtado, A.; Choudhary, H.; Gladden, J.H.; Simmons, B.A.; Botha, F.; Henry, R.J. Association of gene expression with syringyl to guaiacyl ratio in sugarcane lignin. Plant Mol. Biol. 2021, 106, 173–192. [Google Scholar] [CrossRef]
- Wang, D.; Chen, Q.; Chen, W.; Guo, Q.; Xia, Y.; Wang, S.; Jing, D.; Liang, G. Physiological and transcription analyses reveal the regulatory mechanism of melatonin in inducing drought resistance in loquat (Eriobotrya japonica Lindl.) seedlings. Environ. Exp. Bot. 2021, 181, 104291. [Google Scholar] [CrossRef]
- Zhang, Y.; Liu, G.; Dong, H.; Li, C. Waterlogging stress in cotton: Damage, adaptability, alleviation strategies, and mechanisms. Crop J. 2021, 9, 257–270. [Google Scholar] [CrossRef]
- González-Guzmán, M.; Gómez-Cadenas, A.; Arbona, V. Abscisic acid as an emerging modulator of the responses of plants to low oxygen conditions. Front. Plant Sci. 2021, 12, 661789. [Google Scholar] [CrossRef]
- Bui, L.T.; Shukla, V.; Giorgi, F.M.; Trivellini, A.; Perata, P.; Licausi, F.; Giuntoli, B. Differential submergence tolerance between juvenile and adult Arabidopsis plants involves the ANAC017 transcription factor. Plant J. 2020, 104, 979–994. [Google Scholar] [CrossRef]
- Yang, Y.Y.; Gao, S.W.; Su, Y.C.; Lin, Z.L.; Guo, J.L.; Li, M.J.; Wang, Z.T.; Que, Y.X.; Xu, L.P. Transcripts and low nitrogen tolerance: Regulatory and metabolic pathways in sugarcane under low nitrogen stress. Environ. Exp. Bot. 2019, 163, 97–111. [Google Scholar] [CrossRef]
- Ateeq, M.; Khan, A.H.; Zhang, D.; Alam, S.M.; Shen, W.; Wei, M.; Meng, J.; Shen, X.; Pan, J.; Zhu, K.; et al. Comprehensive physio-biochemical and transcriptomic characterization to decipher the network of key genes under waterlogging stress and its recuperation in Prunus persica. Tree Physiol. 2023, 43, 1265–1283. [Google Scholar] [CrossRef] [PubMed]
- Kim, Y.H.; Hwang, S.J.; Waqas, M.; Khan, A.L.; Lee, J.H.; Lee, J.D.; Nguyen, H.T.; Lee, I.J. Comparative analysis of endogenous hormones level in two soybean (Glycine max L.) lines differing in waterlogging tolerance. Front. Plant Sci. 2015, 6, 714. [Google Scholar] [CrossRef]
- Chen, H.; Wu, Q.; Ni, M.; Chen, C.; Han, C.; Yu, F.Y. Transcriptome analysis of endogenous hormone response mechanism in roots of Styrax tonkinensis under waterlogging. Front. Plant Sci. 2022, 13, 896850. [Google Scholar] [CrossRef]
- Zhang, Y.J.; Kong, X.Q.; Dai, J.L.; Luo, Z.; Li, Z.H.; Lu, H.Q.; Xu, S.Z.; Tang, W.; Zhang, D.M.; Li, W.J.; et al. Global gene expression in cotton (Gossypium hirsutum L.) leaves to waterlogging stress. PLoS ONE 2017, 12, e0185075. [Google Scholar] [CrossRef]
- Osthoff, A.; Dalle, R.P.D.; Baldauf, J.A.; Piepho, H.P.; Hochholdinger, F. Transcriptomic reprogramming of barley seminal roots by combined water deficit and salt stress. BMC Genom. 2019, 20, 325. [Google Scholar] [CrossRef]
- Luo, D.; Zhou, Q.; Wu, Y.G.; Chai, X.T.; Liu, W.X.; Wang, Y.R.; Yang, Q.C.; Wang, Z.Y.; Liu, Z.P. Full-length transcript sequencing and comparative transcriptomic analysis to evaluate the contribution of osmotic and ionic stress components towards salinity tolerance in the roots of cultivated alfalfa (Medicago sativa L.). BMC Plant Biol. 2019, 19, 32. [Google Scholar] [CrossRef] [PubMed]
- Sharmin, R.A.; Karikari, B.; Chang, F.G.; Al Amin, G.M.; Bhuiyan, M.R.; Hina, A.; Lv, W.; Chunting, Z.; Begum, N.; Zhao, T.J. Genome-wide association study uncovers major genetic loci associated with seed flooding tolerance in soybean. BMC Plant Biol. 2021, 21, 497. [Google Scholar] [CrossRef]
- Kim, J.M.; Sasaki, T.; Ueda, M.; Sako, K.; Seki, M. Chromatin changes in response to drought, salinity, heat, and cold stresses in plants. Front. Plant. Sci. 2015, 6, 114. [Google Scholar] [CrossRef] [PubMed]
- Kim, J.H. Multifaceted chromatin structure and transcription changes in plant stress response. Int. J. Mol. Sci. 2021, 22, 2013. [Google Scholar] [CrossRef]
- Samantara, K.; Shiv, A.; De-sousa, L.L.; Sandhu, K.S.; Priyadarshini, P.; Mohapatra, S.R. A comprehensive review on epigenetic mechanisms and application of epigenetic modifications for crop improvement. Environ. Exp. Bot. 2021, 188, 104479. [Google Scholar] [CrossRef]
- Ren, Y.F.; Wang, W.; He, J.Y.; Zhang, L.Y.; Wei, Y.J.; Yang, M. Nitric oxide alleviates salt stress in seed germination and early seedling growth of pakchoi (Brassica chinensis L.) by enhancing physiological and biochemical parameters. Ecotoxicol. Environ. Saf. 2020, 187, 109785. [Google Scholar] [CrossRef] [PubMed]
- Chen, C.J.; Chen, H.; Zhang, Y.; Thomas, H.R.; Frank, M.H.; He, Y.H.; Xia, R. TBtools: An integrative toolkit developed for interactive analyses of big biological data. Mol. Plant 2020, 13, 1194–1202. [Google Scholar] [CrossRef] [PubMed]
MSAP Band Types | Patterns a | CK | WL | HS | FS | |
---|---|---|---|---|---|---|
HpaⅡ | MspⅠ | |||||
Ⅰ | 1 | 1 | 53 | 49 | 30 | 60 |
Ⅱ | 1 | 0 | 136 | 123 | 41 | 134 |
Ⅲ | 0 | 1 | 181 | 151 | 158 | 156 |
IV | 0 | 0 | 83 | 130 | 224 | 103 |
Total amplified bands | 453 | 453 | 453 | 453 | ||
Hemi-methylated ratio (%) b | 30.02% | 27.15% | 9.05% | 29.58% | ||
Full methylated ratio (%) c | 58.28% | 62.03% | 84.33% | 57.17% | ||
Total methylated ratio (%) d | 88.30% | 89.18% | 93.38% | 86.75% |
Description of Groups | CK | Flooding-Treated | WL | HS | FS | ||
---|---|---|---|---|---|---|---|
HpaⅡ | MspⅠ | HpaⅡ | MspⅠ | ||||
No change | 1 | 1 | 1 | 1 | 30 | 16 | 29 |
0 | 0 | 0 | 0 | 100 | 72 | 102 | |
1 | 0 | 1 | 0 | 29 | 22 | 10 | |
0 | 1 | 0 | 1 | 90 | 23 | 79 | |
Total | 249 (56.21%) | 133 (30.50%) | 220 (48.89%) | ||||
Hypomethylation | 1 | 0 | 1 | 1 | 12 | 7 | 16 |
0 | 1 | 1 | 1 | 3 | 3 | 9 | |
0 | 0 | 1 | 1 | 4 | 4 | 6 | |
0 | 1 | 1 | 0 | 5 | 3 | 18 | |
0 | 0 | 1 | 0 | 16 | 11 | 24 | |
0 | 0 | 0 | 1 | 34 | 46 | 43 | |
Total | 74 (16.70%) | 74 (16.97%) | 116 (25.78%) | ||||
Hypermethylation | 0 | 1 | 0 | 0 | 73 | 103 | 52 |
1 | 0 | 0 | 0 | 24 | 89 | 38 | |
1 | 1 | 0 | 0 | 4 | 10 | 3 | |
1 | 1 | 0 | 1 | 7 | 23 | 8 | |
1 | 1 | 1 | 0 | 12 | 4 | 13 | |
Total | 120 (27.09%) | 229 (52.52%) | 114 (25.33%) |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Li, B.; Hua, W.; Zhang, S.; Xu, L.; Yang, C.; Zhu, Z.; Guo, Y.; Zhou, M.; Jiao, C.; Xu, Y. Physiological, Epigenetic, and Transcriptome Analyses Provide Insights into the Responses of Wheat Seedling Leaves to Different Water Depths under Flooding Conditions. Int. J. Mol. Sci. 2023, 24, 16785. https://doi.org/10.3390/ijms242316785
Li B, Hua W, Zhang S, Xu L, Yang C, Zhu Z, Guo Y, Zhou M, Jiao C, Xu Y. Physiological, Epigenetic, and Transcriptome Analyses Provide Insights into the Responses of Wheat Seedling Leaves to Different Water Depths under Flooding Conditions. International Journal of Molecular Sciences. 2023; 24(23):16785. https://doi.org/10.3390/ijms242316785
Chicago/Turabian StyleLi, Bo, Wei Hua, Shuo Zhang, Le Xu, Caixian Yang, Zhanwang Zhu, Ying Guo, Meixue Zhou, Chunhai Jiao, and Yanhao Xu. 2023. "Physiological, Epigenetic, and Transcriptome Analyses Provide Insights into the Responses of Wheat Seedling Leaves to Different Water Depths under Flooding Conditions" International Journal of Molecular Sciences 24, no. 23: 16785. https://doi.org/10.3390/ijms242316785