The E3 Ligase GmPUB21 Negatively Regulates Drought and Salinity Stress Response in Soybean
Abstract
:1. Introduction
2. Results
2.1. GmPUB21 Is a U-Box E3 Ligase in Soybean
2.2. GmPUB21 Responses to Osmotic Stress and ABA Treatment, Localize to the Nucleus, Cytosol, and Plasma Membrane
2.3. Overexpression of GmPUB21 Inhibits the Seed Germination under Mannitol, NaCl, and ABA Treatment
2.4. Overexpression of GmPUB21 Increases the Sensitivity to Drought and Salinity Stress
2.5. The Stable Genetic Transformation of GmPUB21 Promoted Its Expression in Guard Cells and Increased Stomatal Density
2.6. Knock-Down GmPUB21 in Soybean Improves the Tolerance to Drought and Salinity Stress
3. Discussion
4. Materials and Methods
4.1. Plant Materials and Treatments
4.2. Cloning and Sequence Analysis of GmPUB21
4.3. Quantitative Real-Time PCR Analysis
4.4. Recombinant Protein Expression and Purification
4.5. In Vitro Ubiquitination Analysis
4.6. Subcellular Localization of GmPUB21
4.7. Generation of GmPUB21 Overexpressing Tobacco Plants
4.8. Determination of GmPUB21 Overexpressing Tobacco Plants Seed Germination under Osmotic Stress and ABA Treatment
4.9. Determination of GmPUB21 Overexpressing Tobacco Plant’s Response to Drought and Salt Stress
4.10. DAB and NBT Staining
4.11. Guard Cell Stomatal Aperture Observations and Measurement of Transpiration Rates
4.12. Knock-Down of GmPUB21 in Soybean
4.13. Determination of GmPUB21 Knock-Down Plants to Drought and Salinity Stress
4.14. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
PEG | Polyethylene glycol |
ABA | Abscisic acid |
BiFC | Bimolecular fluorescent complimentary assay |
CDS | Coding sequences |
OE | overexpression |
dpt | days post-treatment |
Ub | Ubiquitin |
E1 | ubiquitin-activating enzyme |
E2 | ubiquitin-conjugating enzyme |
E3 | ubiquitin ligase |
PUB | plant U-box |
N. benthamiana | Nicotiana benthamiana |
ROS | reactive oxygen species |
VIGS | virus-induced gene silencing |
BPMV | bean pod mottle virus |
References
- Ashraf, M. Stress-induced changes in wheat grain composition and quality. Crit. Rev. Food Sci. Nutr. 2014, 54, 1576–1583. [Google Scholar] [CrossRef] [PubMed]
- Golldack, D.; Luking, I.; Yang, O. Plant tolerance to drought and salinity: Stress regulating transcription factors and their functional significance in the cellular transcriptional network. Plant Cell Rep. 2011, 30, 1383–1391. [Google Scholar] [CrossRef] [PubMed]
- Peleg, Z.; Blumwald, E. Hormone balance and abiotic stress tolerance in crop plants. Curr. Opin. Plant Biol. 2011, 14, 290–295. [Google Scholar] [CrossRef] [PubMed]
- Huang, G.T.; Ma, S.L.; Bai, L.P.; Zhang, L.; Ma, H.; Jia, P.; Liu, J.; Zhong, M.; Guo, Z.F. Signal transduction during cold, salt, and drought stresses in plants. Mol. Biol. Rep. 2012, 39, 969–987. [Google Scholar] [CrossRef]
- 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]
- Kotula, L.; Garcia Caparros, P.; Zörb, C.; Colmer, T.D.; Flowers, T.J. Improving crop salt tolerance using transgenic approaches: An update and physiological analysis. Plant Cell Environ. 2020, 43, 2932–2956. [Google Scholar] [CrossRef]
- Wang, J.; Li, C.; Li, L.; Reynolds, M.; Mao, X.; Jing, R. Exploitation of Drought Tolerance-Related Genes for Crop Improvement. Int. J. Mol. Sci. 2021, 22, 10265. [Google Scholar] [CrossRef]
- Mukhopadhyay, D.; Riezman, H. Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 2007, 315, 201–205. [Google Scholar] [CrossRef] [Green Version]
- Ye, Y.; Rape, M. Building ubiquitin chains: E2 enzymes at work. Nat. Rev. Mol. Cell Biol. 2009, 10, 755–764. [Google Scholar] [CrossRef] [Green Version]
- Davis, C.; Spaller, B.L.; Matouschek, A. Mechanisms of substrate recognition by the 26S proteasome. Curr. Opin. Struct. Biol. 2021, 67, 161–169. [Google Scholar] [CrossRef]
- Stone, S.L. The role of ubiquitin and the 26S proteasome in plant abiotic stress signaling. Front. Plant Sci. 2014, 5, 135. [Google Scholar] [CrossRef] [PubMed]
- Yu, F.; Wu, Y.; Xie, Q. Ubiquitin-proteasome system in ABA signaling: From perception to action. Mol. Plant 2016, 9, 21–33. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lyzenga, W.J.; Stone, S.L. Abiotic stress tolerance mediated by protein ubiquitination. J. Exp. Bot. 2012, 63, 599–616. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Duplan, V.; Rivas, S. E3 ubiquitin-ligases and their target proteins during the regulation of plant innate immunity. Front. Plant Sci. 2014, 5, 42. [Google Scholar] [CrossRef] [Green Version]
- Nakada, S. Opposing roles of RNF8/RNF168 and deubiquitinating enzymes in ubiquitination-dependent DNA double-strand break response signaling and DNA-repair pathway choice. J. Radiat. Res. 2016, 57, i33–i40. [Google Scholar] [CrossRef] [Green Version]
- Li, L.; Li, B.; Xie, C.; Zhang, T.; Borassi, C.; Estevez, J.M.; Li, X.; Liu, X. Arabidopsis RAD23B regulates pollen development by mediating degradation of KRP1. J. Exp. Bot. 2020, 71, 4010–4019. [Google Scholar] [CrossRef] [Green Version]
- Chen, M.; Fan, W.; Hao, B.; Zhang, W.; Yan, M.; Zhao, Y.; Liang, Y.; Liu, G.; Lu, Y.; Zhang, G.; et al. EbARC1, an E3 Ubiquitin Ligase Gene in Erigeron breviscapus, Confers Self-Incompatibility in Transgenic Arabidopsis thaliana. Int. J. Mol. Sci. 2020, 21, 1458. [Google Scholar] [CrossRef] [Green Version]
- Kim, D.Y.; Scalf, M.; Smith, L.M.; Vierstra, R.D. Advanced proteomic analyses yield a deep catalog of ubiquitylation targets in Arabidopsis. Plant Cell 2013, 25, 1523–1540. [Google Scholar] [CrossRef] [Green Version]
- Smalle, J.; Vierstra, R.D. The ubiquitin 26S proteasome proteolytic pathway. Annu. Rev. Plant Biol. 2004, 55, 555–590. [Google Scholar] [CrossRef] [PubMed]
- Yee, D.; Goring, D.R. The diversity of plant U-box E3 ubiquitin ligases: From upstream activators to downstream target substrates. J. Exp. Bot. 2009, 60, 1109–1121. [Google Scholar] [CrossRef] [Green Version]
- Zhou, J.; Hu, Y.; Li, J.; Yu, Z.; Guo, Q. Genome-Wide Identification and Expression Analysis of the Plant U-Box Protein Gene Family in Phyllostachys edulis. Front. Genet. 2021, 12, 710113. [Google Scholar] [CrossRef]
- Metzger, M.B.; Pruneda, J.N.; Klevit, R.E.; Weissman, A.M. RING-type E3 ligases: Master manipulators of E2 ubiquitin-conjugating enzymes and ubiquitination. Biochim. Biophys. Acta 2013, 1843, 47–60. [Google Scholar] [CrossRef] [Green Version]
- Kong, L.; Cheng, J.; Zhu, Y.; Ding, Y.; Meng, J.; Chen, Z.; Xie, Q.; Guo, Y.; Li, J.; Yang, S.; et al. Degradation of the ABA co-receptor ABI1 by PUB12/13 U-box E3 ligases. Nat. Commun. 2015, 6, 8630. [Google Scholar] [CrossRef] [Green Version]
- Seo, D.H.; Lee, A.; Yu, S.G.; Cui, L.H.; Min, H.J.; Lee, S.E.; Cho, N.H.; Kim, S.; Bae, H.; Kim, W.T. OsPUB41, a U-box E3 ubiquitin ligase, acts as a negative regulator of drought stress response in rice (Oryza sativa L.). Plant Mol. Biol. 2021, 106, 463–477. [Google Scholar] [CrossRef]
- Wiborg, J.; O’Shea, C.; Skriver, K. Biochemical function of typical and variant Arabidopsis thaliana U-box E3 ubiquitin-protein ligases. Biochem. J. 2008, 413, 447–457. [Google Scholar] [CrossRef] [Green Version]
- Zeng, L.R.; Park, C.H.; Venu, R.C.; Gough, J.; Wang, G.L. Classification, expression pattern, and E3 ligase activity assay of rice U-box-containing proteins. Mol. Plant 2008, 1, 800–815. [Google Scholar] [CrossRef] [Green Version]
- Wang, N.; Liu, Y.; Cong, Y.; Wang, T.; Zhong, X.; Yang, S.; Li, Y.; Gai, J. Genome-Wide Identification of Soybean U-Box E3 Ubiquitin Ligases and Roles of GmPUB8 in Negative Regulation of Drought Stress Response in Arabidopsis. Plant Cell Physiol. 2016, 57, 1189–1209. [Google Scholar] [CrossRef] [Green Version]
- Cho, S.K.; Ryu, M.Y.; Song, C.; Kwak, J.M.; Kim, W.T. Arabidopsis PUB22 and PUB23 are homologous U-Box E3 ubiquitin ligases that play combinatory roles in response to drought stress. Plant Cell 2008, 20, 1899–1914. [Google Scholar] [CrossRef] [Green Version]
- Liu, Y.C.; Wu, Y.R.; Huang, X.H.; Sun, J.; Xie, Q. AtPUB19, a U-Box E3 Ubiquitin Ligase, Negatively Regulates Abscisic Acid and Drought Responses in Arabidopsis thaliana. Mol. Plant 2011, 4, 938–946. [Google Scholar] [CrossRef]
- Adler, G.; Konrad, Z.; Zamir, L.; Mishra, A.K.; Raveh, D.; Bar-Zvi, D. The Arabidopsis paralogs, PUB46 and PUB48, encoding U-box E3 ubiquitin ligases, are essential for plant response to drought stress. BMC Plant Biol. 2017, 17, 8. [Google Scholar] [CrossRef] [Green Version]
- Chen, X.X.; Wang, T.T.; Rehman, A.U.; Wang, Y.; Qi, J.S.; Li, Z.; Song, C.P.; Wang, B.S.; Yang, S.H.; Gong, Z.Z. Arabidopsis U-box E3 ubiquitin ligase PUB11 negatively regulates drought tolerance by degrading the receptor-like protein kinases LRR1 and KIN7. J. Integr. Plant Biol. 2021, 63, 494–509. [Google Scholar] [CrossRef]
- Zhang, M.; Zhao, J.F.; Li, L.; Gao, Y.N.; Zhao, L.L.; Patil, S.B.; Fang, J.; Zhang, W.; Yang, Y.; Li, M.; et al. The Arabidopsis U-box E3 ubiquitin ligase PUB30 negatively regulates salt tolerance by facilitating BRI1 kinase inhibitor 1 (BKI1) degradation. Plant Cell Environ. 2017, 40, 2831–2843. [Google Scholar] [CrossRef]
- Tong, S.F.; Chen, N.N.; Wang, D.Y.; Ai, F.D.; Liu, B.; Ren, L.W.; Chen, Y.; Zhang, J.L.; Lou, S.L.; Liu, H.H.; et al. The U-box E3 ubiquitin ligase PalPUB79 positively regulates ABA-dependent drought tolerance via ubiquitination of PalWRKY77 in Populus. Plant Biotechnol. J. 2021, 19, 2561–2575. [Google Scholar] [CrossRef]
- Wang, N.; Liu, Y.D.; Cai, Y.Y.; Tang, J.J.; Li, Y.; Gai, J.Y. The soybean U-box gene GmPUB6 regulates drought tolerance in Arabidopsis thaliana. Plant Physiol. Biochem. 2020, 155, 284–296. [Google Scholar] [CrossRef]
- Park, J.J.; Yi, J.Y.; Yoon, J.; Cho, L.H.; Ping, J.; Jeong, H.J.; Cho, S.K.; Kim, W.T.; An, G. OsPUB15, an E3 ubiquitin ligase, functions to reduce cellularoxidative stress during seedling establishment. Plant J. 2011, 65, 194–205. [Google Scholar] [CrossRef]
- Byun, M.Y.; Cui, L.H.; Oh, T.K.; Jung, Y.J.; Lee, A.; Park, K.Y.; Kang, B.G.; Kim, W.T. Homologous U-box E3 Ubiquitin Ligases OsPUB2 and OsPUB3 Are Involved in the Positive Regulation of Low Temperature Stress Response in Rice (Oryza sativa L.). Front. Plant Sci. 2017, 8, 16. [Google Scholar] [CrossRef]
- Wang, W.L.; Wang, W.Q.; Wu, Y.Z.; Li, Q.X.; Zhang, G.Q.; Shi, R.R.; Yang, J.J.; Wang, Y.; Wang, W. The involvement of wheat U-box E3 ubiquitin ligase TaPUB1 in salt stress tolerance. J. Integr. Plant Biol. 2020, 62, 631–651. [Google Scholar] [CrossRef]
- Li, Q.R.; Li, B.; Wang, J.Y.; Chang, X.P.; Mao, X.G.; Jing, R.L. TaPUB15, a U-Box E3 ubiquitin ligase gene from wheat, enhances salt tolerance in rice. Food Energy Secur. 2021, 10, e250. [Google Scholar] [CrossRef]
- Min, H.J.; Jung, Y.J.; Kang, B.G.; Kim, W.T. CaPUB1, a Hot Pepper U-box E3 Ubiquitin Ligase, Confers Enhanced Cold Stress Tolerance and Decreased Drought Stress Tolerance in Transgenic Rice (Oryza sativa L.). Mol. Cells 2016, 39, 250–257. [Google Scholar]
- Zhao, J.; Zhao, L.; Zhang, M.; Zafar, S.A.; Fang, J.; Li, M.; Zhang, W.; Li, X. Arabidopsis E3 Ubiquitin Ligases PUB22 and PUB23 Negatively Regulate Drought Tolerance by Targeting ABA Receptor PYL9 for Degradation. Int. J. Mol. Sci. 2017, 18, 1841. [Google Scholar] [CrossRef]
- Qin, Q.; Wang, Y.; Huang, L.; Du, F.; Zhao, X.; Li, Z.; Wang, W.; Fu, B. A U-box E3 ubiquitin ligase OsPUB67 is positively involved in drought tolerance in rice. Plant Mol. Biol. 2020, 102, 89–107. [Google Scholar] [CrossRef]
- Zhao, Q.; Liu, L.; Xie, Q. In vitro protein ubiquitination assay. Methods Mol. Biol. 2012, 876, 163–172. [Google Scholar]
- Wang, J.; Qu, B.Y.; Dou, S.J.; Li, L.Y.; Yin, D.D.; Pang, Z.Q.; Zhou, Z.Z.; Tian, M.M.; Liu, G.Z.; Xie, Q.; et al. The E3 ligase OsPUB15 interacts with the receptor-like kinase PID2 and regulates plant cell death and innate immunity. BMC Plant Biol. 2015, 15, 49. [Google Scholar] [CrossRef] [Green Version]
- Sharma, M.; Pandey, G.K. OsPUB75, an Armadillo/U-box protein interacts with GSK3 kinase and functions as negative regulator of abiotic stress responses. Environ. Exp. Bot. 2019, 161, 388–398. [Google Scholar] [CrossRef]
- Wu, Y.; Wang, W.; Li, Q.; Zhang, G.; Zhao, X.; Li, G.; Li, Y.; Wang, Y.; Wang, W. The wheat E3 ligase TaPUB26 is a negative regulator in response to salt stress in transgenic Brachypodium distachyon. Plant Sci. 2020, 294, 110441. [Google Scholar] [CrossRef]
- Yan, H.; Jia, H.; Chen, X.; Hao, L.; An, H.; Guo, X. The cotton WRKY transcription factor GhWRKY17 functions in drought and salt stress in transgenic Nicotiana benthamiana through ABA signaling and the modulation of reactive oxygen species production. Plant Cell Physiol. 2014, 55, 2060–2076. [Google Scholar] [CrossRef] [Green Version]
- Ren, S.; Lyle, C.; Jiang, G.L.; Penumala, A. Soybean Salt Tolerance 1 (GmST1) Reduces ROS Production, Enhances ABA Sensitivity, and Abiotic Stress Tolerance in Arabidopsis thaliana. Front. Plant Sci. 2016, 7, 445. [Google Scholar] [CrossRef] [Green Version]
- Xiong, L.; Zhu, J.K. Molecular and genetic aspects of plant responses to osmotic stress. Plant Cell Environ. 2002, 25, 131–139. [Google Scholar] [CrossRef] [Green Version]
- Darko, E.; Végh, B.; Khalil, R.; Marček, T.; Szalai, G.; Pál, M.; Janda, T. Metabolic responses of wheat seedlings to osmotic stress induced by various osmolytes under iso-osmotic conditions. PLoS ONE 2019, 14, e0226151. [Google Scholar] [CrossRef]
- Molnár, I.; Gáspár, L.; Sárvári, É.; Dulai, S.; Hoffmann, B.; Molnár-Láng, M.; Galiba, G. Physiological and morphological responses to water stress in Aegilops biuncialis and Triticum aestivum genotypes with differing tolerance to drought. Funct. Plant Biol. 2004, 31, 1149–1159. [Google Scholar] [CrossRef]
- Slama, I.; Ghnaya, T.; Hessini, K.; Messedi, D.; Savouré, A.; Abdelly, C. Comparative study of the effects of mannitol and PEG osmotic stress on growth and solute accumulation in Sesuvium portulacastrum. Environ. Exp. Bot. 2007, 61, 10–17. [Google Scholar] [CrossRef]
- Darko, E.; Janda, T.; Majláth, I.; Szopkó, D.; Dulai, S.; Molnár, I.; Türkösi, E.; Molnár-Láng, M. Salt stress response of wheat–barley addition lines carrying chromosomes from the winter barley “Manas”. Euphytica 2015, 203, 491–504. [Google Scholar] [CrossRef] [Green Version]
- Torabi, S.; Niknam, V. Effects of Iso-osmotic Concentrations of NaCl and Mannitol on some Metabolic Activity in Calluses of Two Salicornia species. Vitr. Cell. Dev. Biol. Plant 2011, 47, 734–742. [Google Scholar] [CrossRef]
- Adler, G.; Mishra, A.K.; Maymon, T.; Raveh, D.; Bar-Zvi, D. Overexpression of Arabidopsis ubiquitin ligase AtPUB46 enhances tolerance to drought and oxidative stress. Plant Sci. 2018, 276, 220–228. [Google Scholar] [CrossRef]
- Zhao, J.; Zhang, W.; da Silva, J.A.T.; Liu, X.; Duan, J. Rice histone deacetylase HDA704 positively regulates drought and salt tolerance by controlling stomatal aperture and density. Planta 2021, 254, 79. [Google Scholar] [CrossRef]
- Liu, Q.; Wang, Z.; Yu, S.; Li, W.; Zhang, M.; Yang, J.; Li, D.; Yang, J.; Li, C. Pu-miR172d regulates stomatal density and water-use efficiency via targeting PuGTL1 in poplar. J. Exp. Bot. 2021, 72, 1370–1383. [Google Scholar] [CrossRef]
- Hauser, F.; Li, Z.; Waadt, R.; Schroeder, J.I. SnapShot: Abscisic Acid Signaling. Cell 2017, 171, 1708. [Google Scholar] [CrossRef]
- Zhu, J.K. Abiotic stress signaling and responses in plants. Cell 2016, 167, 313–324. [Google Scholar] [CrossRef] [Green Version]
- Yang, W.; Zhang, W.; Wang, X. Post-translational control of ABA signalling: The roles of protein phosphorylation and ubiquitination. Plant Biotechnol. J. 2017, 15, 4–14. [Google Scholar] [CrossRef]
- Lee, S.C.; Luan, S. ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant Cell Environ. 2012, 35, 53–60. [Google Scholar] [CrossRef]
- An, J.; Li, Q.; Yang, J.; Zhang, G.; Zhao, Z.; Wu, Y.; Wang, Y.; Wang, W. Wheat F-box Protein TaFBA1 Positively Regulates Plant Drought Tolerance but Negatively Regulates Stomatal Closure. Front. Plant Sci. 2019, 10, 1242. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kulathu, Y.; Komander, D. Atypical ubiquitylation—The unexplored world of polyubiquitin beyond Lys48 and Lys63 linkages. Nat. Rev. Mol. Cell Biol. 2012, 13, 508–523. [Google Scholar] [CrossRef] [PubMed]
- Jiang, Y.; Tong, S.; Chen, N.; Liu, B.; Bai, Q.; Chen, Y.; Bi, H.; Zhang, Z.; Lou, S.; Tang, H.; et al. The PalWRKY77 transcription factor negatively regulates salt tolerance and abscisic acid signaling in Populus. Plant J. 2021, 105, 1258–1273. [Google Scholar] [CrossRef] [PubMed]
- Chen, Y.F.; Li, L.Q.; Xu, Q.; Kong, Y.H.; Wang, H.; Wu, W.H. The WRKY6 transcription factor modulates PHOSPHATE1 expression in response to low Pi stress in Arabidopsis. Plant Cell 2009, 21, 3554–3566. [Google Scholar] [CrossRef] [Green Version]
- Cho, S.K.; Chung, H.S.; Ryu, M.Y.; Park, M.J.; Lee, M.M.; Bahk, Y.Y.; Kim, J.; Pai, H.S.; Kim, W.T. Heterologous Expression and Molecular and Cellular Characterization of CaPUB1 Encoding a Hot Pepper U-Box E3 Ubiquitin Ligase Homolog. Plant Physiol. 2006, 142, 1664–1682. [Google Scholar] [CrossRef] [Green Version]
- Chankova, S.; Mitrovska, Z.; Yurina, N. Western Blot Analysis of Chloroplast HSP70B in Chlorella Species. Bio-Protocol 2013, 3, e850. [Google Scholar] [CrossRef]
- Badawi, G.H.; Kawano, N.; Yamauchi, Y.; Shimada, E.; Sasaki, R.; Kubo, A.; Tanaka, K. Over-expression of ascorbate peroxidase in tobacco chloroplasts enhances the tolerance to salt stress and water deficit. Physiol. Plant. 2004, 121, 231–238. [Google Scholar] [CrossRef]
- Li, G.; Tai, F.J.; Zheng, Y.; Luo, J.; Gong, S.Y.; Zhang, Z.T.; Li, X.B. Two cotton Cys2/His2-type zinc-finger proteins, GhDi19-1 and GhDi19-2, are involved in plant response to salt/drought stress and abscisic acid signaling. Plant Mol. Biol. 2010, 74, 437–452. [Google Scholar] [CrossRef]
- Li, S.; Xu, C.H.; Yang, Y.N.; Xia, G.M. Functional analysis of TaDi19A, a salt- responsive gene in wheat. Plant Cell Environ. 2010, 33, 117–129. [Google Scholar]
- Ben Saad, R.; Zouari, N.; Ben Ramdhan, W.; Azaza, J.; Meynard, D.; Guiderdoni, E.; Hassairi, A. Improved drought and salt stress tolerance in transgenic tobacco overexpressing a novel A20/AN1 zinc-finger “AlSAP” gene isolated from the halophyte grass Aeluropus littoralis. Plant Mol. Biol. 2010, 72, 171–190. [Google Scholar] [CrossRef]
- Huo, Y.; Wang, M.; Wei, Y.; Xia, Z. Overexpression of the Maize psbA Gene Enhances Drought Tolerance through Regulating Antioxidant System, Photosynthetic Capability, and Stress Defense Gene Expression in Tobacco. Front. Plant Sci. 2016, 6, 1223. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Negi, N.P.; Shrivastava, D.C.; Sharma, V.; Sarin, N.B. Overexpression of CuZnSOD from Arachis hypogaea alleviates salinity and drought stress in tobacco. Plant Cell Rep. 2015, 34, 1109–1126. [Google Scholar] [CrossRef] [PubMed]
- Kwak, J.M.; Murata, Y.; Baizabal-Aguirre, V.M.; Merrill, J.; Hawke, S.D.; Tallman, G.; Schroeder, J.I. Dominant negative guard cell K+ channel mutants reduce inward-rectifying K+ currents and light-induced stomatal opening in Arabidopsis. Plant Physiol. 2001, 127, 473–485. [Google Scholar] [CrossRef] [PubMed]
- Gao, S.Q.; Chen, M.; Xu, Z.S.; Zhao, C.P.; Li, L.C.; Xu, H.J.; Tang, Y.M.; Zhao, X.; Ma, Y.Z. The soybean GmbZIP1 transcription factor enhances multiple abiotic stress tolerances in transgenic plants. Plant Mol. Biol. 2011, 75, 537–553. [Google Scholar] [CrossRef] [PubMed]
- Liu, W.X.; Zhang, F.C.; Zhang, W.Z.; Song, L.F.; Wu, W.H.; Chen, Y.F. Arabidopsis Di19 functions as a transcription factor and modulates PR1, PR2, and PR5 expression in response to drought stress. Mol. Plant 2013, 6, 1487–1502. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, C.Q.; Bradshaw, J.D.; Whitham, S.A.; Hill, J.H. The Development of an Efficient Multipurpose Bean Pod Mottle Virus Viral Vector Set for Foreign Gene Expression and RNA Silencing. Plant Physiol. 2010, 153, 52–65. [Google Scholar] [CrossRef] [Green Version]
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Yang, Y.; Karthikeyan, A.; Yin, J.; Jin, T.; Ren, R.; Fang, F.; Cai, H.; Liu, M.; Wang, D.; Li, K.; et al. The E3 Ligase GmPUB21 Negatively Regulates Drought and Salinity Stress Response in Soybean. Int. J. Mol. Sci. 2022, 23, 6893. https://doi.org/10.3390/ijms23136893
Yang Y, Karthikeyan A, Yin J, Jin T, Ren R, Fang F, Cai H, Liu M, Wang D, Li K, et al. The E3 Ligase GmPUB21 Negatively Regulates Drought and Salinity Stress Response in Soybean. International Journal of Molecular Sciences. 2022; 23(13):6893. https://doi.org/10.3390/ijms23136893
Chicago/Turabian StyleYang, Yunhua, Adhimoolam Karthikeyan, Jinlong Yin, Tongtong Jin, Rui Ren, Fei Fang, Han Cai, Mengzhuo Liu, Dagang Wang, Kai Li, and et al. 2022. "The E3 Ligase GmPUB21 Negatively Regulates Drought and Salinity Stress Response in Soybean" International Journal of Molecular Sciences 23, no. 13: 6893. https://doi.org/10.3390/ijms23136893