Comparative Transcriptome Analysis of Salt-Tolerant and -Sensitive Soybean Cultivars under Salt Stress
Abstract
:1. Introduction
2. Results
2.1. Phenotypic and Photosynthetic Response of Soybean Seedlings to Salt Stress
2.2. Quality Control, Assembly, and Read Mapping of RNA-Seq Data
2.3. Differential Expression Gene Analysis
2.4. Transcriptome Data Verified by Quantitative Real-Time PCR
2.5. Gene Ontology (GO) Enrichment Analysis for the DEGs
2.6. Kyoto Encyclopedia of Genes and Genomes (KEGG) Enrichment Analysis for the DEGs
2.7. Gene Co-Expression Modules Reveal Diverse Expression Patterns under Salt Stress
3. Discussion
3.1. Photosynthetic Response to Salt Stress by Soybean Seedlings
3.2. Changes in Gene Transcription and Different Pathways of Soybean Seedings under Salt Stress
3.3. Plant Hormone and MAPK Signaling Pathways Are Common Pathways Responding to Salt Stress in Soybean
3.4. The Cultivar-Specific Pathways Revealed the Different Responsive Strategies to Salt Stress between the Salt-Tolerant and Salt-Sensitive Cultivars
4. Materials and Methods
4.1. Plant Materials and Experiment Design
4.2. RNA Sequencing
4.3. Raw Sequencing Data Processing
4.4. Differential Expression Gene Analysis
4.5. GO and KEGG Enrichment Analyses
4.6. Construction of Gene Co-Expression Modules
4.7. qRT-PCR Analysis
4.8. Data Processing and Visualization
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Sedivy, E.J.; Wu, F.; Hanzawa, Y. Soybean domestication: The origin, genetic architecture and molecular bases. New Phytol. 2017, 214, 539–553. [Google Scholar] [CrossRef] [PubMed]
- Lam, H.-M.; Xu, X.; Liu, X.; Chen, W.; Yang, G.; Wong, F.-L.; Li, M.-W.; He, W.; Qin, N.; Wang, B.; et al. Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat. Genet. 2010, 42, 1053–1059. [Google Scholar] [CrossRef]
- Ashraf, M.; Wu, L. Breeding for Salinity Tolerance in Plants. Crit. Rev. Plant Sci. 1994, 13, 17–42. [Google Scholar] [CrossRef]
- Phang, T.-H.; Shao, G.; Lam, H.-M. Salt Tolerance in Soybean. J. Integr. Plant Biol. 2008, 50, 1196–1212. [Google Scholar] [CrossRef]
- Abel, G.H.; MacKenzie, A.J. Salt Tolerance of Soybean Varieties (Glycine max L. Merrill) during Germination and Later Growth. Crop Sci. 1964, 4, 157–161. [Google Scholar] [CrossRef]
- Papiernik, S.K.; Grieve, C.M.; Lesch, S.M.; Yates, S.R. Effects of Salinity, Imazethapyr, and Chlorimuron Application on Soybean Growth and Yield. Commun. Soil Sci. Plant Anal. 2005, 36, 951–967. [Google Scholar] [CrossRef]
- Pathan, M.S.; Lee, J.-D.; Shannon, J.G.; Nguyen, H.T. Recent Advances in Breeding for Drought and Salt Stress Tolerance in Soybean. In Advances in Molecular Breeding Toward Drought and Salt Tolerant Crops; Jenks, M.A., Hasegawa, P.M., Jain, S.M., Eds.; Springer: Dordrecht, The Netherlands, 2007; pp. 739–773. [Google Scholar]
- Shahid, M.A.; Sarkhosh, A.; Khan, N.; Balal, R.M.; Ali, S.; Rossi, L.; Gómez, C.; Mattson, N.; Nasim, W.; Garcia-Sanchez, F. Insights into the physiological and biochemical impacts of salt stress on plant growth and development. Agronomy 2020, 10, 938. [Google Scholar] [CrossRef]
- Zhao, J.-Y.; Lu, Z.-W.; Sun, Y.; Fang, Z.-W.; Chen, J.; Zhou, Y.-B.; Chen, M.; Ma, Y.-Z.; Xu, Z.-S.; Min, D.-H. The ankyrin-repeat gene GmANK114 confers drought and salt tolerance in Arabidopsis and soybean. Front. Plant Sci. 2020, 11, 584167. [Google Scholar] [CrossRef]
- Yan, D.; Wang, J.; Lu, Z.; Liu, R.; Hong, Y.; Su, B.; Wang, Y.; Peng, Z.; Yu, C.; Gao, Y. Melatonin-mediated enhancement of photosynthetic capacity and photoprotection improves salt tolerance in wheat. Plants 2023, 12, 3984. [Google Scholar] [CrossRef]
- Qu, Y.; Guan, R.; Yu, L.; Berkowitz, O.; David, R.; Whelan, J.; Ford, M.; Wege, S.; Qiu, L.; Gilliham, M. Enhanced reactive oxygen detoxification occurs in salt-stressed soybean roots expressing GmSALT3. Physiol. Plant. 2022, 174, e13709. [Google Scholar] [CrossRef]
- Feng, C.; Gao, H.; Zhou, Y.; Jing, Y.; Li, S.; Yan, Z.; Xu, K.; Zhou, F.; Zhang, W.; Yang, X.; et al. Unfolding molecular switches for salt stress resilience in soybean: Recent advances and prospects for salt-tolerant smart plant production. Front. Plant Sci. 2023, 14, 1162014. [Google Scholar] [CrossRef]
- Chen, H.; He, H.; Yu, D. Overexpression of a novel soybean gene modulating Na+ and K+ transport enhances salt tolerance in transgenic tobacco plants. Physiol. Plant. 2011, 141, 11–18. [Google Scholar] [CrossRef]
- Chen, H.; Chen, X.; Gu, H.; Wu, B.; Zhang, H.; Yuan, X.; Cui, X. GmHKT1;4, a novel soybean gene regulating Na+/K+ ratio in roots enhances salt tolerance in transgenic plants. Plant Growth Regul. 2014, 73, 299–308. [Google Scholar] [CrossRef]
- Sun, T.; Ma, N.; Wang, C.; Fan, H.; Wang, M.; Zhang, J.; Cao, J.; Wang, D. A Golgi-Localized Sodium/Hydrogen Exchanger Positively Regulates Salt Tolerance by Maintaining Higher K+/Na+ Ratio in Soybean. Front. Plant Sci. 2021, 12, 638340. [Google Scholar] [CrossRef]
- Verma, V.; Ravindran, P.; Kumar, P.P. Plant hormone-mediated regulation of stress responses. BMC Plant Biol. 2016, 16, 86. [Google Scholar] [CrossRef]
- Yu, Z.; Duan, X.; Luo, L.; Dai, S.; Ding, Z.; Xia, G. How Plant Hormones Mediate Salt Stress Responses. Trends Plant Sci. 2020, 25, 1117–1130. [Google Scholar] [CrossRef]
- Hu, J.; Zhuang, Y.; Li, X.; Li, X.; Sun, C.; Ding, Z.; Xu, R.; Zhang, D. Time-series transcriptome comparison reveals the gene regulation network under salt stress in soybean (Glycine max) roots. BMC Plant Biol. 2022, 22, 157. [Google Scholar] [CrossRef]
- Liu, A.; Xiao, Z.; Li, M.-W.; Wong, F.-L.; Yung, W.-S.; Ku, Y.-S.; Wang, Q.; Wang, X.; Xie, M.; Yim, A.K.-Y.; et al. Transcriptomic reprogramming in soybean seedlings under salt stress. Plant Cell Environ. 2019, 42, 98–114. [Google Scholar] [CrossRef]
- Cadavid, I.C.; Guzman, F.; de Oliveira-Busatto, L.; de Almeida, R.M.C.; Margis, R. Transcriptional analyses of two soybean cultivars under salt stress. Mol. Biol. Rep. 2020, 47, 2871–2888. [Google Scholar] [CrossRef]
- Feng, Z.; Ding, C.; Li, W.; Wang, D.; Cui, D. Applications of metabolomics in the research of soybean plant under abiotic stress. Food Chem. 2020, 310, 125914. [Google Scholar] [CrossRef]
- Wang, F.; Chen, X.; Luo, G.; Han, Q. Mapping of regional soil salinities in Xinjiang and strategies for amelioration and management. Chin. Geogr. Sci. 2015, 25, 321–336. [Google Scholar] [CrossRef]
- Peng, J.; Biswas, A.; Jiang, Q.; Zhao, R.; Hu, J.; Hu, B.; Shi, Z. Estimating soil salinity from remote sensing and terrain data in southern Xinjiang Province, China. Geoderma 2019, 337, 1309–1319. [Google Scholar] [CrossRef]
- Barhoumi, Z.; Djebali, W.; Chaïbi, W.; Abdelly, C.; Smaoui, A. Salt impact on photosynthesis and leaf ultrastructure of Aeluropus littoralis. J. Plant Res. 2007, 120, 529–537. [Google Scholar] [CrossRef]
- Bussotti, F.; Gerosa, G.; Digrado, A.; Pollastrini, M. Selection of chlorophyll fluorescence parameters as indicators of photosynthetic efficiency in large scale plant ecological studies. Ecol. Indic. 2020, 108, 105686. [Google Scholar] [CrossRef]
- Chauhan, J.; Prathibha, M.D.; Singh, P.; Choyal, P.; Mishra, U.N.; Saha, D.; Kumar, R.; Anuragi, H.; Pandey, S.; Bose, B.; et al. Plant photosynthesis under abiotic stresses: Damages, adaptive, and signaling mechanisms. Plant Stress 2023, 10, 100296. [Google Scholar] [CrossRef]
- Loudari, A.; Mayane, A.; Zeroual, Y.; Colinet, G.; Oukarroum, A. Photosynthetic performance and nutrient uptake under salt stress: Differential responses of wheat plants to contrasting phosphorus forms and rates. Front. Plant Sci. 2022, 13, 1038672. [Google Scholar] [CrossRef]
- Fan, X.-D.; Wang, J.-Q.; Yang, N.; Dong, Y.-Y.; Liu, L.; Wang, F.-W.; Wang, N.; Chen, H.; Liu, W.-C.; Sun, Y.-P.; et al. Gene expression profiling of soybean leaves and roots under salt, saline–alkali and drought stress by high-throughput Illumina sequencing. Gene 2013, 512, 392–402. [Google Scholar] [CrossRef] [PubMed]
- Acosta-Motos, J.R.; Ortuño, M.F.; Bernal-Vicente, A.; Diaz-Vivancos, P.; Sanchez-Blanco, M.J.; Hernandez, J.A. Plant Responses to Salt Stress: Adaptive Mechanisms. Agronomy 2017, 7, 18. [Google Scholar] [CrossRef]
- Yang, Y.; Guo, Y. Elucidating the molecular mechanisms mediating plant salt-stress responses. New Phytol. 2018, 217, 523–539. [Google Scholar] [CrossRef]
- Sun, S.; Wang, Y.; Wang, J.; Tan, M.; Yan, H.; So, K.; Zhang, Y. Transcriptome responses to salt stress in roots and leaves of Lilium pumilum. Sci. Hortic. 2023, 309, 111622. [Google Scholar] [CrossRef]
- Jalmi, S.K.; Sinha, A.K. ROS mediated MAPK signaling in abiotic and biotic stress- striking similarities and differences. Front. Plant Sci. 2015, 6, 769. [Google Scholar] [CrossRef] [PubMed]
- Balasubramaniam, T.; Shen, G.; Esmaeili, N.; Zhang, H. Plants’ Response Mechanisms to Salinity Stress. Plants 2023, 12, 2253. [Google Scholar] [CrossRef] [PubMed]
- Zhou, H.; Shi, H.; Yang, Y.; Feng, X.; Chen, X.; Xiao, F.; Lin, H.; Guo, Y. Insights into plant salt stress signaling and tolerance. J. Genet. Genom. 2024, 51, 16–34. [Google Scholar] [CrossRef] [PubMed]
- Gómez-Gómez, L.; Boller, T. FLS2: An LRR Receptor–like Kinase Involved in the Perception of the Bacterial Elicitor Flagellin in Arabidopsis. Mol. Cell 2000, 5, 1003–1011. [Google Scholar] [CrossRef]
- Zipfel, C.; Robatzek, S.; Navarro, L.; Oakeley, E.J.; Jones, J.D.G.; Felix, G.; Boller, T. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 2004, 428, 764–767. [Google Scholar] [CrossRef] [PubMed]
- Sun, Y.; Li, L.; Macho, A.P.; Han, Z.; Hu, Z.; Zipfel, C.; Zhou, J.-M.; Chai, J. Structural Basis for flg22-Induced Activation of the Arabidopsis FLS2-BAK1 Immune Complex. Science 2013, 342, 624–628. [Google Scholar] [CrossRef]
- Liang, X.; Ding, P.; Lian, K.; Wang, J.; Ma, M.; Li, L.; Li, L.; Li, M.; Zhang, X.; Chen, S.; et al. Arabidopsis heterotrimeric G proteins regulate immunity by directly coupling to the FLS2 receptor. eLife 2016, 5, e13568. [Google Scholar] [CrossRef]
- Zou, Y.; Wang, S.; Zhou, Y.; Bai, J.; Huang, G.; Liu, X.; Zhang, Y.; Tang, D.; Lu, D. Transcriptional Regulation of the Immune Receptor FLS2 Controls the Ontogeny of Plant Innate Immunity. Plant Cell 2018, 30, 2779–2794. [Google Scholar] [CrossRef]
- Gassmann, W.; Appel, H.M.; Oliver, M.J. The interface between abiotic and biotic stress responses. J. Exp. Bot. 2016, 67, 2023–2024. [Google Scholar] [CrossRef]
- Peck, S.; Mittler, R. Plant signaling in biotic and abiotic stress. J. Exp. Bot. 2020, 71, 1649–1651. [Google Scholar] [CrossRef]
- Saijo, Y.; Loo, E.P.-I. Plant immunity in signal integration between biotic and abiotic stress responses. New Phytol. 2020, 225, 87–104. [Google Scholar] [CrossRef] [PubMed]
- Liu, Z.; Guo, C.; Wu, R.; Hu, Y.; Zhou, Y.; Wang, J.; Yu, X.; Zhang, Y.; Bawa, G.; Sun, X. FLS2–RBOHD–PIF4 Module Regulates Plant Response to Drought and Salt Stress. Int. J. Mol. Sci. 2022, 23, 1080. [Google Scholar] [CrossRef] [PubMed]
- Zhang, T.; Liu, Y.; Yang, T.; Zhang, L.; Xu, S.; Xue, L.; An, L. Diverse signals converge at MAPK cascades in plant. Plant Physiol. Biochem. 2006, 44, 274–283. [Google Scholar] [CrossRef]
- Schweighofer, A.; Kazanaviciute, V.; Scheikl, E.; Teige, M.; Doczi, R.; Hirt, H.; Schwanninger, M.; Kant, M.; Schuurink, R.; Mauch, F.; et al. The PP2C-Type Phosphatase AP2C1, Which Negatively Regulates MPK4 and MPK6, Modulates Innate Immunity, Jasmonic Acid, and Ethylene Levels in Arabidopsis. Plant Cell 2007, 19, 2213–2224. [Google Scholar] [CrossRef]
- Chu, M.; Chen, P.; Meng, S.; Xu, P.; Lan, W. The Arabidopsis phosphatase PP2C49 negatively regulates salt tolerance through inhibition of AtHKT1;1. J. Integr. Plant Biol. 2021, 63, 528–542. [Google Scholar] [CrossRef] [PubMed]
- Abel, S.; Oeller, P.W.; Theologis, A. Early auxin-induced genes encode short-lived nuclear proteins. Proc. Natl. Acad. Sci. USA 1994, 91, 326–330. [Google Scholar] [CrossRef]
- Dreher, K.A.; Brown, J.; Saw, R.E.; Callis, J. The Arabidopsis Aux/IAA protein family has diversified in degradation and auxin responsiveness. Plant Cell 2006, 18, 699–714. [Google Scholar] [CrossRef]
- Weijers, D.; Benkova, E.; Jäger, K.E.; Schlereth, A.; Hamann, T.; Kientz, M.; Wilmoth, J.C.; Reed, J.W.; Jürgens, G. Developmental specificity of auxin response by pairs of ARF and Aux/IAA transcriptional regulators. EMBO J. 2005, 24, 1874–1885. [Google Scholar] [CrossRef]
- Calderón Villalobos, L.I.A.; Lee, S.; De Oliveira, C.; Ivetac, A.; Brandt, W.; Armitage, L.; Sheard, L.B.; Tan, X.; Parry, G.; Mao, H. A combinatorial TIR1/AFB–Aux/IAA co-receptor system for differential sensing of auxin. Nat. Chem. Biol. 2012, 8, 477–485. [Google Scholar] [CrossRef]
- Lavy, M.; Estelle, M. Mechanisms of auxin signaling. Development 2016, 143, 3226–3229. [Google Scholar] [CrossRef]
- Trenner, J.; Poeschl, Y.; Grau, J.; Gogol-Döring, A.; Quint, M.; Delker, C. Auxin-induced expression divergence between Arabidopsis species may originate within the TIR1/AFB–AUX/IAA–ARF module. J. Exp. Bot. 2017, 68, 539–552. [Google Scholar]
- Luo, J.; Zhou, J.-J.; Zhang, J.-Z. Aux/IAA Gene Family in Plants: Molecular Structure, Regulation, and Function. Int. J. Mol. Sci. 2018, 19, 259. [Google Scholar] [CrossRef]
- Thalmann, M.; Santelia, D. Starch as a determinant of plant fitness under abiotic stress. New Phytol. 2017, 214, 943–951. [Google Scholar] [CrossRef]
- Mathan, J.; Singh, A.; Ranjan, A. Sucrose transport in response to drought and salt stress involves ABA-mediated induction of OsSWEET13 and OsSWEET15 in rice. Physiol. Plant. 2021, 171, 620–637. [Google Scholar] [CrossRef]
- Lemoine, R.; La Camera, S.; Atanassova, R.; Dédaldéchamp, F.; Allario, T.; Pourtau, N.; Bonnemain, J.-L.; Laloi, M.; Coutos-Thévenot, P.; Maurousset, L.; et al. Source-to-sink transport of sugar and regulation by environmental factors. Front. Plant Sci. 2013, 4, 272. [Google Scholar] [CrossRef]
- 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]
- Albert, B.; Kos-Braun, I.C.; Henras, A.K.; Dez, C.; Rueda, M.P.; Zhang, X.; Gadal, O.; Kos, M.; Shore, D. A ribosome assembly stress response regulates transcription to maintain proteome homeostasis. eLife 2019, 8, e45002. [Google Scholar] [CrossRef]
- Shen, Y.; Liu, J.; Geng, H.; Zhang, J.; Liu, Y.; Zhang, H.; Xing, S.; Du, J.; Ma, S.; Tian, Z. De novo assembly of a Chinese soybean genome. Sci. China Life Sci. 2018, 61, 871–884. [Google Scholar] [CrossRef]
- Love, M.I.; Huber, W.; Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014, 15, 550. [Google Scholar] [CrossRef]
- Yu, G.; Wang, L.-G.; Han, Y.; He, Q.-Y. clusterProfiler: An R package for comparing biological themes among gene clusters. Omics J. Integr. Biol. 2012, 16, 284–287. [Google Scholar] [CrossRef]
- Xie, C.; Mao, X.; Huang, J.; Ding, Y.; Wu, J.; Dong, S.; Kong, L.; Gao, G.; Li, C.Y.; Wei, L. KOBAS 2.0: A web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res. 2011, 39, W316–W322. [Google Scholar] [CrossRef] [PubMed]
- Langfelder, P.; Horvath, S. WGCNA: An R package for weighted correlation network analysis. BMC Bioinform. 2008, 9, 559. [Google Scholar] [CrossRef] [PubMed]
- Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 2001, 25, 402–408. [Google Scholar] [CrossRef] [PubMed]
Modules | XL vs. XLS | XRC vs. XRS | ZLC vs. ZLS | ZRC vs. ZRS |
---|---|---|---|---|
black (2740) a | 125 (5%) b | 892 (33%) | 226 (8%) | 64 (2%) |
turquoise (7815) | 240 (3%) | 354 (5%) | 510 (7%) | 296 (4%) |
blue (4301) | 179 (4%) | 1235 (29%) | 364 (8%) | 263 (6%) |
brown (4287) | 328 (8%) | 298 (7%) | 212 (5%) | 450 (10%) |
yellow (3820) | 175 (5%) | 42 (1%) | 157 (4%) | 1326 (35%) |
green (3586) | 91 (3%) | 1 (0%) | 191 (5%) | 727 (20%) |
red (3413) | 158 (5%) | 1209 (35%) | 151 (4%) | 52 (2%) |
pink (2505) | 135 (5%) | 63 (3%) | 132 (5%) | 984 (39%) |
magenta (1682) | 83 (5%) | 106 (6%) | 344 (20%) | 113 (7%) |
purple (1466) | 66 (5%) | 251 (17%) | 47 (3%) | 198 (14%) |
greenyellow (979) | 174 (18%) | 91 (9%) | 122 (12%) | 89 (9%) |
tan (822) | 103 (13%) | 54 (7%) | 52 (6%) | 66 (8%) |
salmon (675) | 224 (33%) | 55 (8%) | 17 (3%) | 63 (9%) |
midnightblue (467) | 47 (10%) | 11 (2%) | 17 (4%) | 173 (37%) |
cyan (467) | 16 (3%) | 0 (0%) | 17 (4%) | 141 (30%) |
lightcyan (331) | 18 (5%) | 15 (5%) | 5 (2%) | 23 (7%) |
grey60 (312) | 53 (17%) | 105 (34%) | 2 (1%) | 2 (1%) |
lightgreen (291) | 4 (1%) | 15 (5%) | 91 (31%) | 13 (4%) |
lightyellow (282) | 24 (9%) | 7 (2%) | 26 (9%) | 36 (13%) |
royalblue (271) | 5 (2%) | 87 (32%) | 14 (5%) | 2 (1%) |
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. |
© 2024 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
Cheng, Y.; Cheng, X.; Wei, K.; Wang, Y. Comparative Transcriptome Analysis of Salt-Tolerant and -Sensitive Soybean Cultivars under Salt Stress. Int. J. Mol. Sci. 2024, 25, 9818. https://doi.org/10.3390/ijms25189818
Cheng Y, Cheng X, Wei K, Wang Y. Comparative Transcriptome Analysis of Salt-Tolerant and -Sensitive Soybean Cultivars under Salt Stress. International Journal of Molecular Sciences. 2024; 25(18):9818. https://doi.org/10.3390/ijms25189818
Chicago/Turabian StyleCheng, Ye, Xiangqiang Cheng, Kai Wei, and Yan Wang. 2024. "Comparative Transcriptome Analysis of Salt-Tolerant and -Sensitive Soybean Cultivars under Salt Stress" International Journal of Molecular Sciences 25, no. 18: 9818. https://doi.org/10.3390/ijms25189818