Comprehensive Analysis of Rice Seedling Transcriptome during Dehydration and Rehydration
Abstract
1. Introduction
2. Results
2.1. Characterization of Rice Seedling Responses to Dehydration and Rehydration
2.2. Identification of Differentially Expressed Genes by Dehydration and Rehydration
2.3. Clustering Analysis of the Differentially Expressed Genes during Dehydration and Rehydration
2.4. Differential Expression of Nitrogen Metabolism Related Genes during Dehydration and Rehydration
2.5. Differential Expression of Hormone-Responsive Genes and Hormone Metabolism-Related Genes during Dehydration and Rehydration
2.6. Differential Expression of Transcription Factor Genes during Dehydration and Rehydration
3. Discussion
4. Materials and Methods
4.1. Plant Growth Conditions and Stress Treatment
4.2. Measurements of Chlorophyll Fluorescence
4.3. RNA-Seq Library Construction and Sequencing
4.4. Bioinformatic Analyses of RNA-Seq Data
4.5. Quantitiative RT-PCR
4.6. Statistical Analyses
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Panda, D.; Mishra, S.S.; Behera, P.K. Drought Tolerance in Rice: Focus on Recent Mechanisms and Approaches. Rice Sci. 2021, 28, 119–132. [Google Scholar] [CrossRef]
- Gupta, A.; Rico-Medina, A.; Cano-Delgado, A.I. The physiology of plant responses to drought. Science 2020, 368, 266–269. [Google Scholar] [CrossRef] [PubMed]
- Zhang, H.; Zhu, J.; Gong, Z.; Zhu, J.K. Abiotic stress responses in plants. Nat. Rev. Genet. 2022, 23, 104–119. [Google Scholar] [CrossRef] [PubMed]
- Zhou, J.; Wang, X.; Jiao, Y.; Qin, Y.; Liu, X.; He, K.; Chen, C.; Ma, L.; Wang, J.; Xiong, L.; et al. Global genome expression analysis of rice in response to drought and high-salinity stresses in shoot, flag leaf, and panicle. Plant. Mol. Biol. 2007, 63, 591–608. [Google Scholar] [CrossRef][Green Version]
- Chung, P.J.; Jung, H.; Jeong, D.H.; Ha, S.H.; Choi, Y.D.; Kim, J.K. Transcriptome profiling of drought responsive noncoding RNAs and their target genes in rice. BMC Genom. 2016, 17, 563. [Google Scholar] [CrossRef][Green Version]
- Joshi, R.; Wani, S.H.; Singh, B.; Bohra, A.; Dar, Z.A.; Lone, A.A.; Pareek, A.; Singla-Pareek, S.L. Transcription Factors and Plants Response to Drought Stress: Current Understanding and Future Directions. Front. Plant. Sci. 2016, 7, 1029. [Google Scholar] [CrossRef][Green Version]
- Maruyama, K.; Urano, K.; Yoshiwara, K.; Morishita, Y.; Sakurai, N.; Suzuki, H.; Kojima, M.; Sakakibara, H.; Shibata, D.; Saito, K.; et al. Integrated analysis of the effects of cold and dehydration on rice metabolites, phytohormones, and gene transcripts. Plant. Physiol. 2014, 164, 1759–1771. [Google Scholar] [CrossRef][Green Version]
- Han, M.L.; Lv, Q.Y.; Zhang, J.; Wang, T.; Zhang, C.X.; Tan, R.J.; Wang, Y.L.; Zhong, L.Y.; Gao, Y.Q.; Chao, Z.F.; et al. Decreasing nitrogen assimilation under drought stress by suppressing DST-mediated activation of Nitrate Reductase 1.2 in rice. Mol. Plant. 2022, 15, 167–178. [Google Scholar] [CrossRef]
- Cutler, S.R.; Rodriguez, P.L.; Finkelstein, R.R.; Abrams, S.R. Abscisic acid: Emergence of a core signaling network. Annu. Rev. Plant. Biol. 2010, 61, 651–679. [Google Scholar] [CrossRef][Green Version]
- Yamaguchi-Shinozaki, K.; Shinozaki, K. Transcriptional Regulatory Networks in Cellular Responses and Tolerance to Dehydration and Cold Stresses. Annu. Rev. Plant. Biol. 2006, 57, 781–803. [Google Scholar] [CrossRef][Green Version]
- Fujita, Y.; Yoshida, T.; Yamaguchi-Shinozaki, K. Pivotal role of the AREB/ABF-SnRK2 pathway in ABRE-mediated transcription in response to osmotic stress in plants. Physiol. Plant. 2013, 147, 15–27. [Google Scholar] [CrossRef]
- Waadt, R.; Seller, C.A.; Hsu, P.K.; Takahashi, Y.; Munemasa, S.; Schroeder, J.I. Plant hormone regulation of abiotic stress responses. Nat. Rev. Mol. Cell. Biol. 2022, 23, 680–694. [Google Scholar] [CrossRef]
- Sun, Y.; Fan, X.Y.; Cao, D.M.; Tang, W.; He, K.; Zhu, J.Y.; He, J.X.; Bai, M.Y.; Zhu, S.; Oh, E.; et al. Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev. Cell. 2010, 19, 765–777. [Google Scholar] [CrossRef][Green Version]
- Huang, X.; Hou, L.; Meng, J.; You, H.; Li, Z.; Gong, Z.; Yang, S.; Shi, Y. The Antagonistic Action of Abscisic Acid and Cytokinin Signaling Mediates Drought Stress Response in Arabidopsis. Mol. Plant. 2018, 11, 970–982. [Google Scholar] [CrossRef][Green Version]
- Shani, E.; Salehin, M.; Zhang, Y.; Sanchez, S.E.; Doherty, C.; Wang, R.; Mangado, C.C.; Song, L.; Tal, I.; Pisanty, O.; et al. Plant Stress Tolerance Requires Auxin-Sensitive Aux/IAA Transcriptional Repressors. Curr. Biol. 2017, 27, 437–444. [Google Scholar] [CrossRef][Green Version]
- Wang, J.; Song, L.; Gong, X.; Xu, J.; Li, M. Functions of Jasmonic Acid in Plant Regulation and Response to Abiotic Stress. Int. J. Mol. Sci. 2020, 21, 1446. [Google Scholar] [CrossRef][Green Version]
- Fu, J.; Wu, H.; Ma, S.; Xiang, D.; Liu, R.; Xiong, L. OsJAZ1 Attenuates Drought Resistance by Regulating JA and ABA Signaling in Rice. Front. Plant. Sci. 2017, 8, 2108. [Google Scholar] [CrossRef][Green Version]
- Seo, J.S.; Joo, J.; Kim, M.J.; Kim, Y.K.; Nahm, B.H.; Song, S.I.; Cheong, J.J.; Lee, J.S.; Kim, J.K.; Choi, Y.D. OsbHLH148, a basic helix-loop-helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice. Plant. J. Cell. Mol. Biol. 2011, 65, 907–921. [Google Scholar] [CrossRef]
- Todaka, D.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Recent advances in the dissection of drought-stress regulatory networks and strategies for development of drought-tolerant transgenic rice plants. Front. Plant. Sci. 2015, 6, 84. [Google Scholar] [CrossRef][Green Version]
- Xiang, Y.; Tang, N.; Du, H.; Ye, H.; Xiong, L. Characterization of OsbZIP23 as a key player of the basic leucine zipper transcription factor family for conferring abscisic acid sensitivity and salinity and drought tolerance in rice. Plant. Physiol. 2008, 148, 1938–1952. [Google Scholar] [CrossRef][Green Version]
- Ito, Y.; Katsura, K.; Maruyama, K.; Taji, T.; Kobayashi, M.; Seki, M.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant. Cell. Physiol. 2006, 47, 141–153. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Nakashima, K.; Tran, L.S.; Van Nguyen, D.; Fujita, M.; Maruyama, K.; Todaka, D.; Ito, Y.; Hayashi, N.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant. J. Cell. Mol. Biol. 2007, 51, 617–630. [Google Scholar] [CrossRef] [PubMed]
- Hu, H.; Dai, M.; Yao, J.; Xiao, B.; Li, X.; Zhang, Q.; Xiong, L. Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc. Natl. Acad. Sci. USA 2006, 103, 12987–12992. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Jeong, J.S.; Kim, Y.S.; Baek, K.H.; Jung, H.; Ha, S.H.; Do Choi, Y.; Kim, M.; Reuzeau, C.; Kim, J.K. Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant. Physiol. 2010, 153, 185–197. [Google Scholar] [CrossRef][Green Version]
- Jeong, J.S.; Kim, Y.S.; Redillas, M.C.; Jang, G.; Jung, H.; Bang, S.W.; Choi, Y.D.; Ha, S.H.; Reuzeau, C.; Kim, J.K. OsNAC5 overexpression enlarges root diameter in rice plants leading to enhanced drought tolerance and increased grain yield in the field. Plant. Biotechnol. J. 2013, 11, 101–114. [Google Scholar] [CrossRef]
- Lim, C.; Kang, K.; Shim, Y.; Yoo, S.C.; Paek, N.C. Inactivating transcription factor OsWRKY5 enhances drought tolerance through abscisic acid signaling pathways. Plant. Physiol. 2022, 188, 1900–1916. [Google Scholar] [CrossRef]
- Sato, Y.; Takehisa, H.; Kamatsuki, K.; Minami, H.; Namiki, N.; Ikawa, H.; Ohyanagi, H.; Sugimoto, K.; Antonio, B.A.; Nagamura, Y. RiceXPro version 3.0: Expanding the informatics resource for rice transcriptome. Nucleic Acids Res. 2013, 41, D1206–D1213. [Google Scholar] [CrossRef][Green Version]
- Chandran, A.K.N.; Moon, S.; Yoo, Y.H.; Gho, Y.S.; Cao, P.; Sharma, R.; Sharma, M.K.; Ronald, P.C.; Jung, K.H. A web-based tool for the prediction of rice transcription factor function. Database: J. Biol. Databases Curation 2019, 2019, baz061. [Google Scholar] [CrossRef][Green Version]
- Muhammad, I.; Shalmani, A.; Ali, M.; Yang, Q.H.; Ahmad, H.; Li, F.B. Mechanisms Regulating the Dynamics of Photosynthesis Under Abiotic Stresses. Front. Plant. Sci. 2020, 11, 615942. [Google Scholar] [CrossRef]
- Du, Y.; Zhao, Q.; Chen, L.; Yao, X.; Xie, F. Effect of Drought Stress at Reproductive Stages on Growth and Nitrogen Metabolism in Soybean. Agronomy 2020, 10, 302. [Google Scholar] [CrossRef][Green Version]
- Marmagne, A.; Masclaux-Daubresse, C.; Chardon, F. Modulation of plant nitrogen remobilization and postflowering nitrogen uptake under environmental stresses. J. Plant. Physiol. 2022, 277, 153781. [Google Scholar] [CrossRef]
- Huang, L.; Li, M.; Zhou, K.; Sun, T.; Hu, L.; Li, C.; Ma, F. Uptake and metabolism of ammonium and nitrate in response to drought stress in Malus prunifolia. Plant. Physiol. Biochem. PPB 2018, 127, 185–193. [Google Scholar] [CrossRef]
- Zenda, T.; Liu, S.; Wang, X.; Liu, G.; Jin, H.; Dong, A.; Yang, Y.; Duan, H. Key Maize Drought-Responsive Genes and Pathways Revealed by Comparative Transcriptome and Physiological Analyses of Contrasting Inbred Lines. Int. J. Mol. Sci. 2019, 20, 1268. [Google Scholar] [CrossRef][Green Version]
- Ali, M.S.; Baek, K.-H. Jasmonic Acid Signaling Pathway in Response to Abiotic Stresses in Plants. Int. J. Mol. Sci. 2020, 21, 621. [Google Scholar] [CrossRef][Green Version]
- Riemann, M.; Dhakarey, R.; Hazman, M.; Miro, B.; Kohli, A.; Nick, P. Exploring Jasmonates in the Hormonal Network of Drought and Salinity Responses. Front. Plant. Sci. 2015, 6, 1077. [Google Scholar] [CrossRef][Green Version]
- Lackman, P.; Gonzalez-Guzman, M.; Tilleman, S.; Carqueijeiro, I.; Perez, A.C.; Moses, T.; Seo, M.; Kanno, Y.; Hakkinen, S.T.; Van Montagu, M.C.; et al. Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco. Proc. Natl. Acad. Sci. USA 2011, 108, 5891–5896. [Google Scholar] [CrossRef][Green Version]
- Chen, R.; Jiang, H.; Li, L.; Zhai, Q.; Qi, L.; Zhou, W.; Liu, X.; Li, H.; Zheng, W.; Sun, J.; et al. The Arabidopsis mediator subunit MED25 differentially regulates jasmonate and abscisic acid signaling through interacting with the MYC2 and ABI5 transcription factors. Plant. Cell. 2012, 24, 2898–2916. [Google Scholar] [CrossRef][Green Version]
- Aleman, F.; Yazaki, J.; Lee, M.; Takahashi, Y.; Kim, A.Y.; Li, Z.; Kinoshita, T.; Ecker, J.R.; Schroeder, J.I. An ABA-increased interaction of the PYL6 ABA receptor with MYC2 Transcription Factor: A putative link of ABA and JA signaling. Sci. Rep. 2016, 6, 28941. [Google Scholar] [CrossRef]
- Li, M.; Yu, G.; Cao, C.; Liu, P. Metabolism, signaling, and transport of jasmonates. Plant. Commun. 2021, 2, 100231. [Google Scholar] [CrossRef]
- Jeong, D.-H.; German, M.A.; Rymarquis, L.A.; Thatcher, S.R.; Green, P.J. Abiotic Stress-Associated miRNAs: Detection and Functional Analysis. In Plant MicroRNAs: Methods and Protocols; Meyers, B.C., Green, P.J., Eds.; Humana Press: Totowa, NJ, USA, 2010; pp. 203–230. [Google Scholar]
- Jeong, D.-H.; Park, S.; Zhai, J.; Gurazada, S.G.R.; De Paoli, E.; Meyers, B.C.; Green, P.J. Massive Analysis of Rice Small RNAs: Mechanistic Implications of Regulated MicroRNAs and Variants for Differential Target RNA Cleavage. Plant. Cell. 2011, 23, 4185–4207. [Google Scholar] [CrossRef][Green Version]
- 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] [PubMed][Green Version]
- Bu, D.; Luo, H.; Huo, P.; Wang, Z.; Zhang, S.; He, Z.; Wu, Y.; Zhao, L.; Liu, J.; Guo, J.; et al. KOBAS-i: Intelligent prioritization and exploratory visualization of biological functions for gene enrichment analysis. Nucleic Acids Res. 2021, 49, W317–W325. [Google Scholar] [CrossRef] [PubMed]
- Chen, C.; Chen, H.; Zhang, Y.; Thomas, H.R.; Frank, M.H.; He, Y.; Xia, R. TBtools: An Integrative Toolkit Developed for Interactive Analyses of Big Biological Data. Mol. Plant. 2020, 13, 1194–1202. [Google Scholar] [CrossRef] [PubMed]
- Howe, E.A.; Sinha, R.; Schlauch, D.; Quackenbush, J. RNA-Seq analysis in MeV. Bioinformatics 2011, 27, 3209–3210. [Google Scholar] [CrossRef][Green Version]
- Udvardi, M.K.; Czechowski, T.; Scheible, W.R. Eleven golden rules of quantitative RT-PCR. Plant. Cell. 2008, 20, 1736–1737. [Google Scholar] [CrossRef][Green Version]
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
Park, S.Y.; Jeong, D.-H. Comprehensive Analysis of Rice Seedling Transcriptome during Dehydration and Rehydration. Int. J. Mol. Sci. 2023, 24, 8439. https://doi.org/10.3390/ijms24098439
Park SY, Jeong D-H. Comprehensive Analysis of Rice Seedling Transcriptome during Dehydration and Rehydration. International Journal of Molecular Sciences. 2023; 24(9):8439. https://doi.org/10.3390/ijms24098439
Chicago/Turabian StylePark, So Young, and Dong-Hoon Jeong. 2023. "Comprehensive Analysis of Rice Seedling Transcriptome during Dehydration and Rehydration" International Journal of Molecular Sciences 24, no. 9: 8439. https://doi.org/10.3390/ijms24098439
APA StylePark, S. Y., & Jeong, D.-H. (2023). Comprehensive Analysis of Rice Seedling Transcriptome during Dehydration and Rehydration. International Journal of Molecular Sciences, 24(9), 8439. https://doi.org/10.3390/ijms24098439