Regulatory Dynamics of Plant Hormones and Transcription Factors under Salt Stress
Abstract
:Simple Summary
Abstract
1. Introduction
1.1. Overview of Salt Stress in Plants
1.2. Importance of Understanding Plant Responses to Salt Stress
1.3. Significance of Transcriptional Factors and Hormonal Networks in Salt-Stress Response
2. Transcriptional Factors in Salt-Stress Regulation
2.1. Role of TFs in Gene Expression Regulation
2.2. Key Transcriptional Factors Involved in Salt-Stress Response
2.3. Role of Stress-Responsive Transcription Factors in Enhancing Abiotic Stress Tolerance in Plants
3. Major TF Families
4. Mechanisms of TF Activation during Salt-Stress
5. Hormonal Networks in Salt-Stress Response
5.1. Overview of Plant Hormones Involved in Salt-Stress Response
5.2. Interplay between ABA, Salicylic Acid (SA), Jasmonic Acid (JA) and Other Hormones
5.3. Hormonal Crosstalk in Salt-Stress Adaptation
6. Crosstalk between Transcriptional Factors and Hormonal Networks
6.1. Interaction between TFs and Hormone Signaling Pathways
6.2. Feedback Mechanisms Regulating TFs and Hormonal Responses
6.3. Coordinated Regulation of Gene Expression during Salt Stress
7. Regulation of Salt-Stress-Related Genes
7.1. Molecular Mechanisms Controlling the Expression of Salt-Responsive Genes
7.2. Epigenetic Modifications and Chromatin Remodeling
7.3. Post-Transcriptional and Post-Translational Modifications of Proteins
8. Conclusions
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Wani, S.H.; Kumar, V.; Khare, T.; Guddimalli, R.; Parveda, M.; Solymosi, K.; Suprasanna, P.; Kavi Kishor, P. Engineering salinity tolerance in plants: Progress and prospects. Planta 2020, 251, 76. [Google Scholar] [CrossRef]
- Wang, G.; Shen, W.; Zhang, Z.; Guo, S.; Hu, J.; Feng, R.; Zhao, Q.; Du, J.; Du, Y. The Effect of Neutral Salt and Alkaline Stress with the Same Na+ Concentration on Root Growth of Soybean (Glycine max (L.) Merr.) Seedlings. Agronomy 2022, 12, 2708. [Google Scholar] [CrossRef]
- Antunes, J.; Paz, A.M.; Castanheira, N.; Gonçalves, M.C.; Cortez, N. Study of the influence of the standing time in the electrical conductivity of the saturated soil paste in three soils. Rev. De Ciências Agrárias 2023, 46, 93–98. [Google Scholar]
- Gupta, A.; Rico-Medina, A.; Caño-Delgado, A.I. The physiology of plant responses to drought. Science 2020, 368, 266–269. [Google Scholar] [CrossRef] [PubMed]
- Dutta, D. Interplay between membrane proteins and membrane protein-lipid pertaining to plant salinity stress. Cell Biochem. Funct. 2023, 41, 399–412. [Google Scholar] [CrossRef]
- Hussain, N.; Sohail, Y.; Shakeel, N.; Javed, M.; Bano, H.; Gul, H.S.; Zafar, Z.U.; Frahat Zaky Hassan, I.; Ghaffar, A.; Athar, H.-u.-R. Role of mineral nutrients, antioxidants, osmotic adjustment and PSII stability in salt tolerance of contrasting wheat genotypes. Sci. Rep. 2022, 12, 12677. [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]
- Hualpa-Ramirez, E.; Carrasco-Lozano, E.C.; Madrid-Espinoza, J.; Tejos, R.; Ruiz-Lara, S.; Stange, C.; Norambuena, L. Stress salinity in plants: New strategies to cope with in the foreseeable scenario. Plant Physiol. Biochem. 2024, 108507. [Google Scholar] [CrossRef] [PubMed]
- Flowers, T.J.; Munns, R.; Colmer, T.D. Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes. Ann. Bot. 2015, 115, 419–431. [Google Scholar] [CrossRef]
- Wu, H.; Fan, S.; Gong, H.; Guo, J. Roles of salicylic acid in selenium-enhanced salt tolerance in tomato plants. Plant Soil 2023, 484, 569–588. [Google Scholar] [CrossRef]
- Slama, I.; Abdelly, C.; Bouchereau, A.; Flowers, T.; Savouré, A. Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Ann. Bot. 2015, 115, 433–447. [Google Scholar] [CrossRef]
- 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]
- Çulha, Ş.; Çakirlar, H. Tuzluluğun bitkiler üzerine etkileri ve tuz tolerans mekanizmaları. Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Derg. 2011, 11, 11–34. [Google Scholar]
- Suo, J.; Zhao, Q.; David, L.; Chen, S.; Dai, S. Salinity response in chloroplasts: Insights from gene characterization. Int. J. Mol. Sci. 2017, 18, 1011. [Google Scholar] [CrossRef] [PubMed]
- Shelden, M.C.; Munns, R. Crop root system plasticity for improved yields in saline soils. Front. Plant Sci. 2023, 14. [Google Scholar] [CrossRef]
- Bouhraoua, S.; Ferioun, M.; Nassira, S.; Boussakouran, A.; Akhazzane, M.; Belahcen, D.; Hammani, K.; Louahlia, S. Biomass partitioning and physiological responses of four Moroccan barley varieties subjected to salt stress in a hydroponic system. J. Plant Biotechnol. 2023, 50, 115–126. [Google Scholar] [CrossRef]
- Dabravolski, S.A.; Isayenkov, S.V. The regulation of plant cell wall organisation under salt stress. Front. Plant Sci. 2023, 14, 1118313. [Google Scholar] [CrossRef]
- Abbas, A.; Mansha, S.; Waheed, H.; Siddiq, Z.; Hayyat, M.U.; Zhang, Y.-J.; Alwutayd, K. NaCl stress, tissue specific Na+ and K+ up-take and their effect on growth and physiology of Helianthus annuus L. and Solanum lycopersicum L. Sci. Hortic. 2024, 326, 112454. [Google Scholar] [CrossRef]
- Wang, B.; Wang, J.; Yang, T.; Wang, J.; Dai, Q.; Zhang, F.; Xi, R.; Yu, Q.; Li, N. The transcriptional regulatory network of hormones and genes under salt stress in tomato plants (Solanum lycopersicum L.). Front. Plant Sci. 2023, 14, 1115593. [Google Scholar] [CrossRef]
- Shaffique, S.; Kang, S.-M.; Hoque, M.I.U.; Imran, M.; Aaqil khan, M.; Lee, I.-J. Research progress in soybean by phytohormone modulation and metal chelation over the past decade. Agriculture 2023, 13, 1325. [Google Scholar] [CrossRef]
- Shaffique, S.; Hussain, S.; Kang, S.-M.; Imran, M.; Injamum-Ul-Hoque, M.; Khan, M.A.; Lee, I.-J. Phytohormonal modulation of the drought stress in soybean: Outlook, research progress, and cross-talk. Front. Plant Sci. 2023, 14, 1237295. [Google Scholar] [CrossRef]
- Kumar, P.; Kumar, P.; Suniti; Kumar, U.; Avni; Mann, A. Transcriptional Regulatory Network Involved in Drought and Salt Stress Response in Rice. In Salinity and Drought Tolerance in Plants: Physiological Perspectives; Springer: Berlin/Heidelberg, Germany, 2023; pp. 237–274. [Google Scholar]
- Pan, L.; Ma, J.; Li, J.; Yin, B.; Fu, C. Advances of salt stress-responsive transcription factors in plants. Sheng Wu Gong Cheng Xue Bao = Chin. J. Biotechnol. 2022, 38, 50–65. [Google Scholar]
- 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]
- Lan Thi Hoang, X.; Du Nhi, N.H.; Binh Anh Thu, N.; Phuong Thao, N.; Phan Tran, L.-S. Transcription factors and their roles in signal transduction in plants under abiotic stresses. Curr. Genom. 2017, 18, 483–497. [Google Scholar]
- Kumar, J.; Singh, S.; Singh, M.; Srivastava, P.K.; Mishra, R.K.; Singh, V.P.; Prasad, S.M. Transcriptional regulation of salinity stress in plants: A short review. Plant Gene 2017, 11, 160–169. [Google Scholar] [CrossRef]
- Fernando, V.D. Major transcription factor families involved in salinity stress tolerance in plants. Transcr. Factors Abiotic Stress Toler. Plants 2020, 99–109. [Google Scholar]
- Zhang, T.; Zhou, Y. Plant transcription factors and salt stress. In Plant Transcription Factors; Elsevier: Amsterdam, The Netherlands, 2023; pp. 369–381. [Google Scholar]
- Liu, H.; Tang, X.; Zhang, N.; Li, S.; Si, H. Role of bZIP Transcription Factors in Plant Salt Stress. Int. J. Mol. Sci. 2023, 24, 7893. [Google Scholar] [CrossRef] [PubMed]
- Ray-Jones, H.; Spivakov, M. Transcriptional enhancers and their communication with gene promoters. Cell. Mol. Life Sci. 2021, 78, 6453–6485. [Google Scholar] [CrossRef]
- Hussain, Q.; Asim, M.; Zhang, R.; Khan, R.; Farooq, S.; Wu, J. Transcription factors interact with ABA through gene expression and signaling pathways to mitigate drought and salinity stress. Biomolecules 2021, 11, 1159. [Google Scholar] [CrossRef]
- Chauhan, D.; Singh, D.; Pandey, H.; Khan, Z.; Srivastava, R.; Dhiman, V.K.; Dhiman, V.K. Chapter 13 - Impact of transcription factors in plant abiotic stress: A recent advancement for crop improvement. In Plant Transcription Factors; Srivastava, V., Mishra, S., Mehrotra, S., Upadhyay, S.K., Eds.; Academic Press: Cambridge, MA, USA, 2023; pp. 271–286. [Google Scholar]
- Kimotho, R.N.; Baillo, E.H.; Zhang, Z. Transcription factors involved in abiotic stress responses in Maize (Zea mays L.) and their roles in enhanced productivity in the post genomics era. PeerJ 2019, 7, e7211. [Google Scholar] [CrossRef]
- Cohen, I.; Zandalinas, S.I.; Huck, C.; Fritschi, F.B.; Mittler, R. Meta-analysis of drought and heat stress combination impact on crop yield and yield components. Physiol. Plant. 2021, 171, 66–76. [Google Scholar]
- Jia, J.; Zhao, P.; Cheng, L.; Yuan, G.; Yang, W.; Liu, S.; Chen, S.; Qi, D.; Liu, G.; Li, X. MADS-box family genes in sheepgrass and their involvement in abiotic stress responses. BMC Plant Biol. 2018, 18, 42. [Google Scholar] [CrossRef]
- Sarkar, B.; Bandyopadhyay, P.; Das, A.; Pal, S.; Hasanuzzaman, M.; Adak, M.K. Abscisic acid priming confers salt tolerance in maize seedlings by modulating osmotic adjustment, bond energies, ROS homeostasis, and organic acid metabolism. Plant Physiol. Biochem. 2023, 202, 107980. [Google Scholar] [CrossRef] [PubMed]
- Quint, M.; Gray, W.M. Auxin signaling. Curr. Opin. Plant Biol. 2006, 9, 448–453. [Google Scholar] [CrossRef]
- 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] [PubMed]
- Yin, L.; Zander, M.; Huang, S.-s.C.; Xie, M.; Song, L.; Guzmán, J.P.S.; Hann, E.; Shanbhag, B.K.; Ng, S.; Jain, S.; et al. Transcription Factor Dynamics in Cross-Regulation of Plant Hormone Signaling Pathways. bioRxiv 2023. [Google Scholar] [CrossRef]
- Wang, H.; Hao, J.; Chen, X.; Hao, Z.; Wang, X.; Lou, Y.; Peng, Y.; Guo, Z. Overexpression of rice WRKY89 enhances ultraviolet B tolerance and disease resistance in rice plants. Plant Mol. Biol. 2007, 65, 799–815. [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] [PubMed]
- Cai, R.; Dai, W.; Zhang, C.; Wang, Y.; Wu, M.; Zhao, Y.; Ma, Q.; Xiang, Y.; Cheng, B. The maize WRKY transcription factor ZmWRKY17 negatively regulates salt stress tolerance in transgenic Arabidopsis plants. Planta 2017, 246, 1215–1231. [Google Scholar] [CrossRef] [PubMed]
- Yang, Z.; Chi, X.; Guo, F.; Jin, X.; Luo, H.; Hawar, A.; Chen, Y.; Feng, K.; Wang, B.; Qi, J. SbWRKY30 enhances the drought tolerance of plants and regulates a drought stress-responsive gene, SbRD19, in sorghum. J. Plant Physiol. 2020, 246, 153142. [Google Scholar] [CrossRef] [PubMed]
- Luo, X.; Li, C.; He, X.; Zhang, X.; Zhu, L. ABA signaling is negatively regulated by GbWRKY1 through JAZ1 and ABI1 to affect salt and drought tolerance. Plant Cell Rep. 2020, 39, 181–194. [Google Scholar] [CrossRef]
- Qin, Z.; Hou, F.; Li, A.; Dong, S.; Wang, Q.; Zhang, L. Transcriptome-wide identification of WRKY transcription factor and their expression profiles under salt stress in sweetpotato (Ipomoea batatas L.). Plant Biotechnol. Rep. 2020, 14, 599–611. [Google Scholar] [CrossRef]
- Chanwala, J.; Satpati, S.; Dixit, A.; Parida, A.; Giri, M.K.; Dey, N. Genome-wide identification and expression analysis of WRKY transcription factors in pearl millet (Pennisetum glaucum) under dehydration and salinity stress. BMC Genom. 2020, 21, 231. [Google Scholar] [CrossRef] [PubMed]
- Song, Y.; Li, J.; Sui, Y.; Han, G.; Zhang, Y.; Guo, S.; Sui, N. The sweet sorghum SbWRKY50 is negatively involved in salt response by regulating ion homeostasis. Plant Mol. Biol. 2020, 102, 603–614. [Google Scholar] [CrossRef]
- Li, W.; Pang, S.; Lu, Z.; Jin, B. Function and mechanism of WRKY transcription factors in abiotic stress responses of plants. Plants 2020, 9, 1515. [Google Scholar] [CrossRef]
- Han, D.; Hou, Y.; Wang, Y.; Ni, B.; Li, Z.; Yang, G. Overexpression of a Malus baccata WRKY transcription factor gene (MbWRKY5) increases drought and salt tolerance in transgenic tobacco. Can. J. Plant Sci. 2018, 99, 173–183. [Google Scholar] [CrossRef]
- Bankaji, I.; Sleimi, N.; Vives-Peris, V.; Gomez-Cadenas, A.; Perez-Clemente, R.M. Identification and expression of the Cucurbita WRKY transcription factors in response to water deficit and salt stress. Sci. Hortic. 2019, 256, 108562. [Google Scholar] [CrossRef]
- Lin, L.; Yuan, K.; Huang, Y.; Dong, H.; Qiao, Q.; Xing, C.; Huang, X.; Zhang, S. A WRKY transcription factor PbWRKY40 from Pyrus betulaefolia functions positively in salt tolerance and modulating organic acid accumulation by regulating PbVHA-B1 expression. Environ. Exp. Bot. 2022, 196, 104782. [Google Scholar] [CrossRef]
- Zhu, L.; Li, S.; Ouyang, M.; Yang, L.; Sun, S.; Wang, Y.; Cai, X.; Wu, G.; Li, Y. Overexpression of watermelon ClWRKY20 in transgenic Arabidopsis improves salt and low-temperature tolerance. Sci. Hortic. 2022, 295, 110848. [Google Scholar] [CrossRef]
- Han, D.; Xu, T.; Han, J.; Liu, W.; Wang, Y.; Li, X.; Sun, X.; Wang, X.; Li, T.; Yang, G. Overexpression of MxWRKY53 increased iron and high salinity stress tolerance in Arabidopsis thaliana. Vitr. Cell. Dev. Biol.-Plant 2021, 266–278. [Google Scholar] [CrossRef]
- Han, D.; Han, J.; Xu, T.; Li, T.; Yao, C.; Wang, Y.; Luo, D.; Yang, G. Isolation and preliminary functional characterization of MxWRKY64, a new WRKY transcription factor gene from Malus xiaojinensis Cheng et Jiang. Vitr. Cell. Dev. Biol.-Plant 2021, 57, 202–213. [Google Scholar] [CrossRef]
- Zhu, H.; Jiang, Y.; Guo, Y.; Huang, J.; Zhou, M.; Tang, Y.; Sui, J.; Wang, J.; Qiao, L. A novel salt inducible WRKY transcription factor gene, AhWRKY75, confers salt tolerance in transgenic peanut. Plant Physiol. Biochem. 2021, 160, 175–183. [Google Scholar] [CrossRef]
- Xiang, X.-Y.; Chen, J.; Xu, W.-X.; Qiu, J.-R.; Song, L.; Wang, J.-T.; Tang, R.; Chen, D.; Jiang, C.-Z.; Huang, Z. Dehydration-induced WRKY transcriptional factor MfWRKY70 of Myrothamnus flabellifolia enhanced drought and salinity tolerance in Arabidopsis. Biomolecules 2021, 11, 327. [Google Scholar] [CrossRef] [PubMed]
- Fu, Q.-T.; Yu, D.-Q. Expression profiles of AtWRKY25, AtWRKY26 and AtWRKY33 under abiotic stresses. Yi Chuan = Hered. 2010, 32, 848–856. [Google Scholar] [CrossRef] [PubMed]
- Zhou, L.; Wang, N.-N.; Gong, S.-Y.; Lu, R.; Li, Y.; Li, X.-B. Overexpression of a cotton (Gossypium hirsutum) WRKY gene, GhWRKY34, in Arabidopsis enhances salt-tolerance of the transgenic plants. Plant Physiol. Biochem. 2015, 96, 311–320. [Google Scholar] [CrossRef] [PubMed]
- Yao, J.; Shen, Z.; Zhang, Y.; Wu, X.; Wang, J.; Sa, G.; Zhang, Y.; Zhang, H.; Deng, C.; Liu, J. Populus euphratica WRKY1 binds the promoter of H+-ATPase gene to enhance gene expression and salt tolerance. J. Exp. Bot. 2020, 71, 1527–1539. [Google Scholar] [CrossRef]
- Singh, D.; Debnath, P.; Sane, A.P.; Sane, V.A. Tomato (Solanum lycopersicum) WRKY23 enhances salt and osmotic stress tolerance by modulating the ethylene and auxin pathways in transgenic Arabidopsis. Plant Physiol. Biochem. 2023, 195, 330–340. [Google Scholar] [CrossRef]
- Liu, J.X.; Srivastava, R.; Che, P.; Howell, S.H. Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling. Plant J. 2007, 51, 897–909. [Google Scholar] [CrossRef]
- Huang, C.; Zhou, J.; Jie, Y.; Xing, H.; Zhong, Y.; Yu, W.; She, W.; Ma, Y.; Liu, Z.; Zhang, Y. A ramie bZIP transcription factor BnbZIP2 is involved in drought, salt, and heavy metal stress response. DNA Cell Biol. 2016, 35, 776–786. [Google Scholar] [CrossRef]
- Lee, S.C.; Choi, H.W.; Hwang, I.S.; Choi, D.S.; Hwang, B.K. Functional roles of the pepper pathogen-induced bZIP transcription factor, CAbZIP1, in enhanced resistance to pathogen infection and environmental stresses. Planta 2006, 224, 1209–1225. [Google Scholar] [CrossRef]
- Gai, W.-X.; Ma, X.; Qiao, Y.-M.; Shi, B.-H.; ul Haq, S.; Li, Q.-H.; Wei, A.-M.; Liu, K.-K.; Gong, Z.-H. Characterization of the bZIP transcription factor family in pepper (Capsicum annuum L.): CabZIP25 positively modulates the salt tolerance. Front. Plant Sci. 2020, 11, 139. [Google Scholar] [CrossRef]
- Yang, Y.; Yu, T.-F.; Ma, J.; Chen, J.; Zhou, Y.-B.; Chen, M.; Ma, Y.-Z.; Wei, W.-L.; Xu, Z.-S. The soybean bZIP transcription factor gene GmbZIP2 confers drought and salt resistances in transgenic plants. Int. J. Mol. Sci. 2020, 21, 670. [Google Scholar] [CrossRef] [PubMed]
- Nakagawa, H.; Ohmiya, K.; Hattori, T. A rice bZIP protein, designated OSBZ8, is rapidly induced by abscisic acid. Plant J. 1996, 9, 217–227. [Google Scholar] [CrossRef] [PubMed]
- Zhang, L.; Xie, J.; Wang, L.; Si, L.; Zheng, S.; Yang, Y.; Yang, H.; Tian, S. Wheat TabZIP8, 9, 13 participate in ABA biosynthesis in NaCl-stressed roots regulated by TaCDPK9-1. Plant Physiol. Biochem. 2020, 151, 650–658. [Google Scholar] [CrossRef]
- Zhang, L.; Zhang, L.; Xia, C.; Gao, L.; Hao, C.; Zhao, G.; Jia, J.; Kong, X. A novel wheat C-bZIP gene, TabZIP14-B, participates in salt and freezing tolerance in transgenic plants. Front. Plant Sci. 2017, 8, 710. [Google Scholar] [CrossRef] [PubMed]
- Ji, X.; Liu, G.; Liu, Y.; Zheng, L.; Nie, X.; Wang, Y. The bZIP protein from Tamarix hispida, ThbZIP1, is ACGT elements binding factor that enhances abiotic stress signaling in transgenic Arabidopsis. BMC Plant Biol. 2013, 13, 151. [Google Scholar] [CrossRef]
- Bi, C.; Yu, Y.; Dong, C.; Yang, Y.; Zhai, Y.; Du, F.; Xia, C.; Ni, Z.; Kong, X.; Zhang, L. The bZIP transcription factor TabZIP15 improves salt stress tolerance in wheat. Plant Biotechnol. J. 2021, 19, 209. [Google Scholar] [CrossRef]
- Wang, Z.; Zhu, J.; Yuan, W.; Wang, Y.; Hu, P.; Jiao, C.; Xia, H.; Wang, D.; Cai, Q.; Li, J. Genome-wide characterization of bZIP transcription factors and their expression patterns in response to drought and salinity stress in Jatropha curcas. Int. J. Biol. Macromol. 2021, 181, 1207–1223. [Google Scholar] [CrossRef]
- Ma, H.; Liu, C.; Li, Z.; Ran, Q.; Xie, G.; Wang, B.; Fang, S.; Chu, J.; Zhang, J. ZmbZIP4 contributes to stress resistance in maize by regulating ABA synthesis and root development. Plant Physiol. 2018, 178, 753–770. [Google Scholar] [CrossRef]
- Orellana, S.; Yanez, M.; Espinoza, A.; Verdugo, I.; Gonzalez, E.; RUIZ-LARA, S.; Casaretto, J.A. The transcription factor SlAREB1 confers drought, salt stress tolerance and regulates biotic and abiotic stress-related genes in tomato. Plant Cell Environ. 2010, 33, 2191–2208. [Google Scholar] [CrossRef]
- Zhao, P.; Ye, M.; Wang, R.; Wang, D.; Chen, Q. Systematic identification and functional analysis of potato (Solanum tuberosum L.) bZIP transcription factors and overexpression of potato bZIP transcription factor StbZIP-65 enhances salt tolerance. Int. J. Biol. Macromol. 2020, 161, 155–167. [Google Scholar] [CrossRef]
- Wang, Q.; Guo, C.; Li, Z.; Sun, J.; Wang, D.; Xu, L.; Li, X.; Guo, Y. Identification and analysis of bZIP family genes in potato and their potential roles in stress responses. Front. Plant Sci. 2021, 12, 637343. [Google Scholar] [CrossRef] [PubMed]
- Liu, B.; Zhang, L.; Sun, Y.; Xue, J.; Gao, C.; Yuan, L.; Wang, J.; Jia, X.; Li, R. Genome-wide characterization of bZIP transcription factors in foxtail millet and their expression profiles in response to drought and salt stresses. Chin. Bull. Bot. 2016, 51, 473. [Google Scholar]
- Qu, D.; Wu, F.; Zhao, X.; Zhu, D.; Gu, L.; Yang, L.; Zhao, W.; Sun, Y.; Yang, J.; Tian, W. A bZIP transcription factor VabZIP12 from blueberry induced by dark septate endocyte improving the salt tolerance of transgenic Arabidopsis. Plant Sci. 2022, 315, 111135. [Google Scholar] [CrossRef]
- Jiang, M.; Wang, Z.; Ren, W.; Yan, S.; Xing, N.; Zhang, Z.; Li, H.; Ma, W. Identification of the bZIP gene family and regulation of metabolites under salt stress in Isatis indigotica. Front. Plant Sci. 2022, 13, 1011616. [Google Scholar] [CrossRef] [PubMed]
- Kang, C.; Zhai, H.; He, S.; Zhao, N.; Liu, Q. A novel sweetpotato bZIP transcription factor gene, IbbZIP1, is involved in salt and drought tolerance in transgenic Arabidopsis. Plant Cell Rep. 2019, 38, 1373–1382. [Google Scholar] [CrossRef] [PubMed]
- Tang, Y.; Bao, X.; Zhi, Y.; Wu, Q.; Guo, Y.; Yin, X.; Zeng, L.; Li, J.; Zhang, J.; He, W. Overexpression of a MYB family gene, OsMYB6, increases drought and salinity stress tolerance in transgenic rice. Front. Plant Sci. 2019, 10, 168. [Google Scholar] [CrossRef]
- Xiong, H.; Li, J.; Liu, P.; Duan, J.; Zhao, Y.; Guo, X.; Li, Y.; Zhang, H.; Ali, J.; Li, Z. Overexpression of OsMYB48-1, a novel MYB-related transcription factor, enhances drought and salinity tolerance in rice. PLoS ONE 2014, 9, e92913. [Google Scholar] [CrossRef]
- Yoo, J.H.; Park, C.Y.; Kim, J.C.; Do Heo, W.; Cheong, M.S.; Park, H.C.; Kim, M.C.; Moon, B.C.; Choi, M.S.; Kang, Y.H. Direct interaction of a divergent CaM isoform and the transcription factor, MYB2, enhances salt tolerance in Arabidopsis. J. Biol. Chem. 2005, 280, 3697–3706. [Google Scholar] [CrossRef]
- Zhang, L.; Liu, G.; Zhao, G.; Xia, C.; Jia, J.; Liu, X.; Kong, X. Characterization of a wheat R2R3-MYB transcription factor gene, TaMYB19, involved in enhanced abiotic stresses in Arabidopsis. Plant Cell Physiol. 2014, 55, 1802–1812. [Google Scholar] [CrossRef]
- Liao, Y.; Zou, H.-F.; Wang, H.-W.; Zhang, W.-K.; Ma, B.; Zhang, J.-S.; Chen, S.-Y. Soybean GmMYB76, GmMYB92, and GmMYB177 genes confer stress tolerance in transgenic Arabidopsis plants. Cell Res. 2008, 18, 1047–1060. [Google Scholar] [CrossRef]
- Zhao, K.; Cheng, Z.; Guo, Q.; Yao, W.; Liu, H.; Zhou, B.; Jiang, T. Characterization of the poplar R2R3-MYB gene family and over-expression of PsnMYB108 confers salt tolerance in transgenic tobacco. Front. Plant Sci. 2020, 11, 571881. [Google Scholar] [CrossRef]
- Zhang, X.; Chen, L.; Shi, Q.; Ren, Z. SlMYB102, an R2R3-type MYB gene, confers salt tolerance in transgenic tomato. Plant Sci. 2020, 291, 110356. [Google Scholar] [CrossRef] [PubMed]
- Cheng, L.; Li, X.; Huang, X.; Ma, T.; Liang, Y.; Ma, X.; Peng, X.; Jia, J.; Chen, S.; Chen, Y. Overexpression of sheepgrass R1-MYB transcription factor LcMYB1 confers salt tolerance in transgenic Arabidopsis. Plant Physiol. Biochem. 2013, 70, 252–260. [Google Scholar] [CrossRef] [PubMed]
- Nulu, J.K.; AM, A.J.; Venkatesh, B.; Jayamma, N.; Reddy, B.M.; Pandurangaiah, M. R2R3 MYB Transcription Factor, AhMYB94 Plays a Crucial Role in Stress adaptation of a Salt Susceptible Groundnut Cultivar-K6. 2022; preprint. [Google Scholar] [CrossRef]
- Wu, J.; Jiang, Y.; Liang, Y.; Chen, L.; Chen, W.; Cheng, B. Expression of the maize MYB transcription factor ZmMYB3R enhances drought and salt stress tolerance in transgenic plants. Plant Physiol. Biochem. 2019, 137, 179–188. [Google Scholar] [CrossRef] [PubMed]
- Dong, W.; Liu, X.; Li, D.; Gao, T.; Song, Y. Transcriptional profiling reveals that a MYB transcription factor MsMYB4 contributes to the salinity stress response of alfalfa. PLoS ONE 2018, 13, e0204033. [Google Scholar] [CrossRef]
- Ren, C.; Li, Z.; Song, P.; Wang, Y.; Liu, W.; Zhang, L.; Li, X.; Li, W.; Han, D. Overexpression of a grape MYB transcription factor gene VhMYB2 increases salinity and drought tolerance in Arabidopsis thaliana. Int. J. Mol. Sci. 2023, 24, 10743. [Google Scholar] [CrossRef]
- Wang, Y.; Zhang, Y.; Fan, C.; Wei, Y.; Meng, J.; Li, Z.; Zhong, C. Genome-wide analysis of MYB transcription factors and their responses to salt stress in Casuarina equisetifolia. BMC Plant Biol. 2021, 21, 328. [Google Scholar] [CrossRef]
- Ullah, A.; Ul Qamar, M.T.; Nisar, M.; Hazrat, A.; Rahim, G.; Khan, A.H.; Hayat, K.; Ahmed, S.; Ali, W.; Khan, A. Characterization of a novel cotton MYB gene, GhMYB108-like responsive to abiotic stresses. Mol. Biol. Rep. 2020, 47, 1573–1581. [Google Scholar] [CrossRef]
- ZHANG, Y.-b.; Wei, T.; WANG, L.-h.; HU, Y.-w.; LIU, X.-w.; LIU, Y.-s. Kiwifruit (Actinidia chinensis) R1R2R3-MYB transcription factor AcMYB3R enhances drought and salinity tolerance in Arabidopsis thaliana. J. Integr. Agric. 2019, 18, 417–427. [Google Scholar] [CrossRef]
- Shan, H.; Chen, S.; Jiang, J.; Chen, F.; Chen, Y.; Gu, C.; Li, P.; Song, A.; Zhu, X.; Gao, H. Heterologous expression of the chrysanthemum R2R3-MYB transcription factor CmMYB2 enhances drought and salinity tolerance, increases hypersensitivity to ABA and delays flowering in Arabidopsis thaliana. Mol. Biotechnol. 2012, 51, 160–173. [Google Scholar] [CrossRef]
- Shen, X.; Guo, X.; Guo, X.; Zhao, D.; Zhao, W.; Chen, J.; Li, T. PacMYBA, a sweet cherry R2R3-MYB transcription factor, is a positive regulator of salt stress tolerance and pathogen resistance. Plant Physiol. Biochem. 2017, 112, 302–311. [Google Scholar] [CrossRef] [PubMed]
- Cao, Z.-H.; Zhang, S.-Z.; Wang, R.-K.; Zhang, R.-F.; Hao, Y.-J. Genome wide analysis of the apple MYB transcription factor family allows the identification of MdoMYB121 gene confering abiotic stress tolerance in plants. PLoS ONE 2013, 8, e69955. [Google Scholar] [CrossRef] [PubMed]
- Liu, M.; Li, K.; Sheng, S.; Wang, M.; Hua, P.; Wang, Y.; Chen, P.; Wang, K.; Zhao, M.; Wang, Y. Transcriptome analysis of MYB transcription factors family and PgMYB genes involved in salt stress resistance in Panax ginseng. BMC Plant Biol. 2022, 22, 479. [Google Scholar] [CrossRef] [PubMed]
- Yong, Y.; Zhang, Y.; Lyu, Y. A MYB-related transcription factor from Lilium lancifolium L.(LlMYB3) is involved in anthocyanin biosynthesis pathway and enhances multiple abiotic stress tolerance in Arabidopsis thaliana. Int. J. Mol. Sci. 2019, 20, 3195. [Google Scholar] [CrossRef] [PubMed]
- Zhang, T.; Cui, Z.; Li, Y.; Kang, Y.; Song, X.; Wang, J.; Zhou, Y. Genome-wide identification and expression analysis of MYB transcription factor superfamily in Dendrobium catenatum. Front. Genet. 2021, 12, 714696. [Google Scholar] [CrossRef]
- Su, Y.; Liu, Y.; Xiao, S.; Wang, Y.; Deng, Y.; Zhao, L.; Wang, Y.; Zhao, D.; Dai, X.; Zhou, Z. Isolation, characterization, and functional verification of salt stress response genes of NAC transcription factors in Ipomoea pes-caprae. Front. Plant Sci. 2023, 14, 1119282. [Google Scholar] [CrossRef]
- Liao, Y.-D.; Lin, K.-H.; Chen, C.-C.; Chiang, C.-M. Oryza sativa protein phosphatase 1a (OsPP1a) involved in salt stress tolerance in transgenic rice. Mol. Breed. 2016, 36, 22. [Google Scholar] [CrossRef]
- Li, M.; Wu, Z.; Gu, H.; Cheng, D.; Guo, X.; Li, L.; Shi, C.; Xu, G.; Gu, S.; Abid, M. AvNAC030, a NAC domain transcription factor, enhances salt stress tolerance in Kiwifruit. Int. J. Mol. Sci. 2021, 22, 11897. [Google Scholar] [CrossRef]
- Liu, X.; Baird, W.V. Differential expression of genes regulated in response to drought or salinity stress in sunflower. Crop Sci. 2003, 43, 678–687. [Google Scholar] [CrossRef]
- Peng, H.; Yu, X.; Cheng, H.; Shi, Q.; Zhang, H.; Li, J.; Ma, H. Cloning and characterization of a novel NAC family gene CarNAC1 from chickpea (Cicer arietinum L.). Mol. Biotechnol. 2010, 44, 30–40. [Google Scholar] [CrossRef]
- Zhong, H.; Guo, Q.-Q.; Chen, L.; Ren, F.; Wang, Q.-Q.; Zheng, Y.; Li, X.-B. Two Brassica napus genes encoding NAC transcription factors are involved in response to high-salinity stress. Plant Cell Rep. 2012, 31, 1991–2003. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; He, M.; Dong, F.; Cai, Y.; Gao, W.; Zhou, Y.; Huang, H.; Dai, S. The Chrysanthemum lavandulifolium ClNAC9 gene positively regulates saline, alkaline, and drought stress in transgenic Chrysanthemum grandiflora. J. Am. Soc. Hortic. Sci. 2019, 144, 280–288. [Google Scholar] [CrossRef]
- Wang, Y.; Cao, S.; Guan, C.; Kong, X.; Wang, Y.; Cui, Y.; Liu, B.; Zhou, Y.; Zhang, Y. Overexpressing the NAC transcription factor LpNAC13 from Lilium pumilum in tobacco negatively regulates the drought response and positively regulates the salt response. Plant Physiol. Biochem. 2020, 149, 96–110. [Google Scholar] [CrossRef] [PubMed]
- Lu, M.; Ying, S.; Zhang, D.-F.; Shi, Y.-S.; Song, Y.-C.; Wang, T.-Y.; Li, Y. A maize stress-responsive NAC transcription factor, ZmSNAC1, confers enhanced tolerance to dehydration in transgenic Arabidopsis. Plant Cell Rep. 2012, 31, 1701–1711. [Google Scholar] [CrossRef]
- Dudhate, A.; Shinde, H.; Yu, P.; Tsugama, D.; Gupta, S.K.; Liu, S.; Takano, T. Comprehensive analysis of NAC transcription factor family uncovers drought and salinity stress response in pearl millet (Pennisetum glaucum). BMC Genom. 2021, 22, 70. [Google Scholar] [CrossRef] [PubMed]
- Wang, S.; Huang, J.; Wang, X.; Dang, H.; Jiang, T.; Han, Y. Expression analysis of the NAC transcription factor family of populus in response to salt stress. Forests 2019, 10, 688. [Google Scholar] [CrossRef]
- Li, M.; Chen, R.; Jiang, Q.; Sun, X.; Zhang, H.; Hu, Z. GmNAC06, a NAC domain transcription factor enhances salt stress tolerance in soybean. Plant Mol. Biol. 2021, 105, 333–345. [Google Scholar] [CrossRef]
- Wei, S.; Gao, L.; Zhang, Y.; Zhang, F.; Yang, X.; Huang, D. Genome-wide investigation of the NAC transcription factor family in melon (Cucumis melo L.) and their expression analysis under salt stress. Plant Cell Rep. 2016, 35, 1827–1839. [Google Scholar] [CrossRef]
- Tak, H.; Negi, S.; Ganapathi, T. Banana NAC transcription factor MusaNAC042 is positively associated with drought and salinity tolerance. Protoplasma 2017, 254, 803–816. [Google Scholar] [CrossRef]
- Yu, X.; Liu, Y.; Wang, S.; Tao, Y.; Wang, Z.; Shu, Y.; Peng, H.; Mijiti, A.; Wang, Z.; Zhang, H. CarNAC4, a NAC-type chickpea transcription factor conferring enhanced drought and salt stress tolerances in Arabidopsis. Plant Cell Rep. 2016, 35, 613–627. [Google Scholar] [CrossRef]
- An, J.P.; Yao, J.F.; Xu, R.R.; You, C.X.; Wang, X.F.; Hao, Y.J. An apple NAC transcription factor enhances salt stress tolerance by modulating the ethylene response. Physiol. Plant. 2018, 164, 279–289. [Google Scholar] [CrossRef] [PubMed]
- Punia, H.; Tokas, J.; Malik, A.; Sangwan, S.; Rani, A.; Yashveer, S.; Alansi, S.; Hashim, M.J.; El-Sheikh, M.A. Genome-wide transcriptome profiling, characterization, and functional identification of NAC transcription factors in sorghum under salt stress. Antioxidants 2021, 10, 1605. [Google Scholar] [CrossRef] [PubMed]
- Han, D.; Du, M.; Zhou, Z.; Wang, S.; Li, T.; Han, J.; Xu, T.; Yang, G. Overexpression of a Malus baccata NAC transcription factor gene MbNAC25 increases cold and salinity tolerance in Arabidopsis. Int. J. Mol. Sci. 2020, 21, 1198. [Google Scholar] [CrossRef]
- Wang, L.; Li, Z.; Lu, M.; Wang, Y. ThNAC13, a NAC transcription factor from Tamarix hispida, confers salt and osmotic stress tolerance to transgenic Tamarix and Arabidopsis. Front. Plant Sci. 2017, 8, 635. [Google Scholar] [CrossRef]
- Min, X.; Jin, X.; Zhang, Z.; Wei, X.; Ndayambaza, B.; Wang, Y.; Liu, W. Genome-Wide Identification of NAC Transcription Factor Family and Functional Analysis of the Abiotic Stress-Responsive Genes in Medicago sativa L. J. Plant Growth Regul. 2020, 39, 324–337. [Google Scholar] [CrossRef]
- Bokolia, M.; Singh, B.; Kumar, A.; Goyal, N.; Singh, K.; Chhabra, R. Genome-wide identification of NAC transcription factors in Avena sativa under salinity stress. Plant Stress 2023, 10, 100276. [Google Scholar] [CrossRef]
- Jia, H.; Wang, C.; Wang, F.; Liu, S.; Li, G.; Guo, X. GhWRKY68 reduces resistance to salt and drought in transgenic Nicotiana benthamiana. PLoS ONE 2015, 10, e0120646. [Google Scholar] [CrossRef]
- Yokotani, N.; Ichikawa, T.; Kondou, Y.; Matsui, M.; Hirochika, H.; Iwabuchi, M.; Oda, K. Tolerance to various environmental stresses conferred by the salt-responsive rice gene ONAC063 in transgenic Arabidopsis. Planta 2009, 229, 1065–1075. [Google Scholar] [CrossRef]
- Nakashima, K.; Ito, Y.; Yamaguchi-Shinozaki, K. Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol. 2009, 149, 88–95. [Google Scholar] [CrossRef]
- Zou, M.; Guan, Y.; Ren, H.; Zhang, F.; Chen, F. Characterization of alternative splicing products of bZIP transcription factors OsABI5. Biochem. Biophys. Res. Commun. 2007, 360, 307–313. [Google Scholar] [CrossRef]
- Chaudhry, U.K.; Gökçe, Z.N.Ö.; Gökçe, A.F. The influence of salinity stress on plants and their molecular mechanisms. Biol. Life Sci. Forum 2021, 11, 31. [Google Scholar]
- Guan, Y.; Hwarari, D.; Korboe, H.M.; Ahmad, B.; Cao, Y.; Movahedi, A.; Yang, L. Low temperature stress-induced perception and molecular signaling pathways in plants. Environ. Exp. Bot. 2023, 207, 105190. [Google Scholar] [CrossRef]
- Long, L.; Gu, L.; Wang, S.; Cai, H.; Wu, J.; Wang, J.; Yang, M. Progress in the understanding of WRKY transcription factors in woody plants. Int. J. Biol. Macromol. 2023, 242, 124379. [Google Scholar] [CrossRef]
- Kamali, S.; Singh, A. Genomic and transcriptomic approaches to developing abiotic stress-resilient crops. Agronomy 2023, 13, 2903. [Google Scholar] [CrossRef]
- Samarina, L.; Wang, S.; Malyukova, L.; Bobrovskikh, A.; Doroshkov, A.; Koninskaya, N.; Shkhalakhova, R.; Matskiv, A.; Fedorina, J.; Fizikova, A. Long-term cold, freezing and drought: Overlapping and specific regulatory mechanisms and signal transduction in tea plant (Camellia sinensis (L.) Kuntze). Front. Plant Sci. 2023, 14, 1145793. [Google Scholar] [CrossRef] [PubMed]
- Ha, C.V.; Nasr Esfahani, M.; Watanabe, Y.; Tran, U.T.; Sulieman, S.; Mochida, K.; Van Nguyen, D.; Tran, L.-S.P. Genome-wide identification and expression analysis of the CaNAC family members in chickpea during development, dehydration and ABA treatments. PLoS ONE 2014, 9, e114107. [Google Scholar] [CrossRef] [PubMed]
- Barbosa, E.G.G.; Leite, J.P.; Marin, S.R.R.; Marinho, J.P.; de Fátima Corrêa Carvalho, J.; Fuganti-Pagliarini, R.; Farias, J.R.B.; Neumaier, N.; Marcelino-Guimarães, F.C.; de Oliveira, M.C.N. Overexpression of the ABA-dependent AREB1 transcription factor from Arabidopsis thaliana improves soybean tolerance to water deficit. Plant Mol. Biol. Report. 2013, 31, 719–730. [Google Scholar] [CrossRef]
- Kim, J.-S.; Mizoi, J.; Yoshida, T.; Fujita, Y.; Nakajima, J.; Ohori, T.; Todaka, D.; Nakashima, K.; Hirayama, T.; Shinozaki, K. An ABRE promoter sequence is involved in osmotic stress-responsive expression of the DREB2A gene, which encodes a transcription factor regulating drought-inducible genes in Arabidopsis. Plant Cell Physiol. 2011, 52, 2136–2146. [Google Scholar] [CrossRef]
- Narusaka, Y.; Nakashima, K.; Shinwari, Z.K.; Sakuma, Y.; Furihata, T.; Abe, H.; Narusaka, M.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J. 2003, 34, 137–148. [Google Scholar] [CrossRef]
- Xu, Z.-Y.; Kim, S.Y.; Hyeon, D.Y.; Kim, D.H.; Dong, T.; Park, Y.; Jin, J.B.; Joo, S.-H.; Kim, S.-K.; Hong, J.C. The Arabidopsis NAC transcription factor ANAC096 cooperates with bZIP-type transcription factors in dehydration and osmotic stress responses. Plant Cell 2013, 25, 4708–4724. [Google Scholar] [CrossRef]
- Oh, S.-J.; Song, S.I.; Kim, Y.S.; Jang, H.-J.; Kim, S.Y.; Kim, M.; Kim, Y.-K.; Nahm, B.H.; Kim, J.-K. Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol. 2005, 138, 341–351. [Google Scholar] [CrossRef]
- Wu, Y.; Deng, Z.; Lai, J.; Zhang, Y.; Yang, C.; Yin, B.; Zhao, Q.; Zhang, L.; Li, Y.; Yang, C. Dual function of Arabidopsis ATAF1 in abiotic and biotic stress responses. Cell Res. 2009, 19, 1279–1290. [Google Scholar] [CrossRef] [PubMed]
- Vannini, C.; Campa, M.; Iriti, M.; Genga, A.; Faoro, F.; Carravieri, S.; Rotino, G.L.; Rossoni, M.; Spinardi, A.; Bracale, M. Evaluation of transgenic tomato plants ectopically expressing the rice Osmyb4 gene. Plant Sci. 2007, 173, 231–239. [Google Scholar] [CrossRef]
- Qiu, Y.; Yu, D. Over-expression of the stress-induced OsWRKY45 enhances disease resistance and drought tolerance in Arabidopsis. Environ. Exp. Bot. 2009, 65, 35–47. [Google Scholar] [CrossRef]
- Xiao, F.; Zhou, H. Plant salt response: Perception, signaling, and tolerance. Front. Plant Sci. 2023, 13, 1053699. [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]
- Fahad, S.; Hussain, S.; Matloob, A.; Khan, F.A.; Khaliq, A.; Saud, S.; Hassan, S.; Shan, D.; Khan, F.; Ullah, N. Phytohormones and plant responses to salinity stress: A review. Plant Growth Regul. 2015, 75, 391–404. [Google Scholar] [CrossRef]
- Shinozaki, K.; Yamaguchi-Shinozaki, K. Molecular responses to dehydration and low temperature: Differences and cross-talk between two stress signaling pathways. Curr. Opin. Plant Biol. 2000, 3, 217–223. [Google Scholar] [CrossRef]
- Swamy, P.; Smith, B.N. Role of abscisic acid in plant stress tolerance. Curr. Sci. 1999, 1220–1227. [Google Scholar]
- Zhao, Y.; Zhang, Z.; Gao, J.; Wang, P.; Hu, T.; Wang, Z.; Hou, Y.J.; Wan, Y.; Liu, W.; Xie, S.; et al. Arabidopsis Duodecuple Mutant of PYL ABA Receptors Reveals PYL Repression of ABA-Independent SnRK2 Activity. Cell Rep. 2018, 23, 3340–3351.e3345. [Google Scholar] [CrossRef]
- 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]
- Qin, F.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Achievements and challenges in understanding plant abiotic stress responses and tolerance. Plant Cell Physiol. 2011, 52, 1569–1582. [Google Scholar] [CrossRef] [PubMed]
- Nishiyama, R.; Watanabe, Y.; Leyva-Gonzalez, M.A.; Van Ha, C.; Fujita, Y.; Tanaka, M.; Seki, M.; Yamaguchi-Shinozaki, K.; Shinozaki, K.; Herrera-Estrella, L. Arabidopsis AHP2, AHP3, and AHP5 histidine phosphotransfer proteins function as redundant negative regulators of drought stress response. Proc. Natl. Acad. Sci. USA 2013, 110, 4840–4845. [Google Scholar] [CrossRef] [PubMed]
- Wilkinson, S.; Kudoyarova, G.R.; Veselov, D.S.; Arkhipova, T.N.; Davies, W.J. Plant hormone interactions: Innovative targets for crop breeding and management. J. Exp. Bot. 2012, 63, 3499–3509. [Google Scholar] [CrossRef] [PubMed]
- Rehman, A.; Azhar, M.T.; Hinze, L.; Qayyum, A.; Li, H.; Peng, Z.; Qin, G.; Jia, Y.; Pan, Z.; He, S.; et al. Insight into abscisic acid perception and signaling to increase plant tolerance to abiotic stress. J. Plant Interact. 2021, 16, 222–237. [Google Scholar] [CrossRef]
- Ko, J.H.; Yang, S.H.; Han, K.H. Upregulation of an Arabidopsis RING-H2 gene, XERICO, confers drought tolerance through increased abscisic acid biosynthesis. Plant J. 2006, 47, 343–355. [Google Scholar] [CrossRef]
- Achard, P.; Genschik, P. Releasing the brakes of plant growth: How GAs shutdown DELLA proteins. J. Exp. Bot. 2009, 60, 1085–1092. [Google Scholar] [CrossRef]
- Xi, W.; Liu, C.; Hou, X.; Yu, H. MOTHER OF FT AND TFL1 regulates seed germination through a negative feedback loop modulating ABA signaling in Arabidopsis. Plant Cell 2010, 22, 1733–1748. [Google Scholar] [CrossRef]
- Jusovic, M.; Velitchkova, M.Y.; Misheva, S.P.; Börner, A.; Apostolova, E.L.; Dobrikova, A.G. Photosynthetic responses of a wheat mutant (Rht-B1c) with altered DELLA proteins to salt stress. J. Plant Growth Regul. 2018, 37, 645–656. [Google Scholar] [CrossRef]
- Zhao, C.; Jiang, W.; Zayed, O.; Liu, X.; Tang, K.; Nie, W.; Li, Y.; Xie, S.; Li, Y.; Long, T. The LRXs-RALFs-FER module controls plant growth and salt stress responses by modulating multiple plant hormones. Natl. Sci. Rev. 2021, 8, nwaa149. [Google Scholar] [CrossRef]
- Tao, J.-J.; Chen, H.-W.; Ma, B.; Zhang, W.-K.; Chen, S.-Y.; Zhang, J.-S. The role of ethylene in plants under salinity stress. Front. Plant Sci. 2015, 6, 1059. [Google Scholar] [CrossRef]
- Gieniec, M.; Miszalski, Z.; Rozpądek, P.; Jędrzejczyk, R.J.; Czernicka, M.; Nosek, M. How the Ethylene Biosynthesis Pathway of Semi-Halophytes Is Modified with Prolonged Salinity Stress Occurrence? Int. J. Mol. Sci. 2024, 25, 4777. [Google Scholar] [CrossRef] [PubMed]
- Peng, Z.; He, S.; Gong, W.; Sun, J.; Pan, Z.; Xu, F.; Lu, Y.; Du, X. Comprehensive analysis of differentially expressed genes and transcriptional regulation induced by salt stress in two contrasting cotton genotypes. BMC Genom. 2014, 15, 760. [Google Scholar] [CrossRef] [PubMed]
- Li, J.; Zou, X.; Chen, G.; Meng, Y.; Ma, Q.; Chen, Q.; Wang, Z.; Li, F. Potential Roles of 1-Aminocyclopropane-1-carboxylic Acid Synthase Genes in the Response of Gossypium Species to Abiotic Stress by Genome-Wide Identification and Expression Analysis. Plants 2022, 11, 1524. [Google Scholar] [CrossRef] [PubMed]
- Zhang, F.; Zhang, J.; Chen, L.; Shi, X.; Lui, Z.; Li, C. Heterologous expression of ACC deaminase from Trichoderma asperellum improves the growth performance of Arabidopsis thaliana under normal and salt stress conditions. Plant Physiol. Biochem. 2015, 94, 41–47. [Google Scholar] [CrossRef] [PubMed]
- Cao, W.H.; Liu, J.; Zhou, Q.Y.; Cao, Y.R.; Zheng, S.F.; Du, B.X.; Zhang, J.S.; Chen, S.Y. Expression of tobacco ethylene receptor NTHK1 alters plant responses to salt stress. Plant Cell Environ. 2006, 29, 1210–1219. [Google Scholar] [CrossRef]
- Shen, X.; Wang, Z.; Song, X.; Xu, J.; Jiang, C.; Zhao, Y.; Ma, C.; Zhang, H. Transcriptomic profiling revealed an important role of cell wall remodeling and ethylene signaling pathway during salt acclimation in Arabidopsis. Plant Mol. Biol. 2014, 86, 303–317. [Google Scholar] [CrossRef]
- Ryu, H.; Cho, Y.-G. Plant hormones in salt stress tolerance. J. Plant Biol. 2015, 58, 147–155. [Google Scholar] [CrossRef]
- Saeng-ngam, S.; Takpirom, W.; Buaboocha, T.; Chadchawan, S. The role of the OsCam1-1 salt stress sensor in ABA accumulation and salt tolerance in rice. J. Plant Biol. 2012, 55, 198–208. [Google Scholar] [CrossRef]
- Moons, A.; Bauw, G.; Prinsen, E.; Van Montagu, M.; Van Der Straeten, D. Molecular and physiological responses to abscisic acid and salts in roots of salt-sensitive and salt-tolerant Indica rice varieties. Plant Physiol. 1995, 107, 177–186. [Google Scholar] [CrossRef]
- He, T.; Cramer, G.R. Abscisic acid concentrations are correlated with leaf area reductions in two salt-stressed rapid-cycling Brassica species. Plant Soil 1996, 179, 25–33. [Google Scholar] [CrossRef]
- Cramer, G.R.; Quarrie, S.A. Abscisic acid is correlated with the leaf growth inhibition of four genotypes of maize differing in their response to salinity. Funct. Plant Biol. 2002, 29, 111–115. [Google Scholar] [CrossRef]
- Rao, K.P.; Richa, T.; Kumar, K.; Raghuram, B.; Sinha, A.K. In silico analysis reveals 75 members of mitogen-activated protein kinase kinase kinase gene family in rice. DNA Res. 2010, 17, 139–153. [Google Scholar] [CrossRef]
- Jung, J.-H.; Park, C.-M. Auxin modulation of salt stress signaling in Arabidopsis seed germination. Plant Signal. Behav. 2011, 6, 1198–1200. [Google Scholar] [CrossRef] [PubMed]
- Marzi, D.; Brunetti, P.; Saini, S.S.; Yadav, G.; Puglia, G.D.; Dello Ioio, R. Role of transcriptional regulation in auxin-mediated response to abiotic stresses. Front. Genet. 2024, 15, 1394091. [Google Scholar] [CrossRef] [PubMed]
- Kazan, K. Auxin and the integration of environmental signals into plant root development. Ann. Bot. 2013, 112, 1655–1665. [Google Scholar] [CrossRef] [PubMed]
- Talaat, N.B. Abiotic stresses-induced physiological alteration in wheat. Wheat Prod. Chang. Environ. Responses Adapt. Toler. 2019, 1–30. [Google Scholar]
- Nishiyama, R.; Watanabe, Y.; Fujita, Y.; Le, D.T.; Kojima, M.; Werner, T.; Vankova, R.; Yamaguchi-Shinozaki, K.; Shinozaki, K.; Kakimoto, T. Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. Plant Cell 2011, 23, 2169–2183. [Google Scholar] [CrossRef]
- Weidemüller, P.; Kholmatov, M.; Petsalaki, E.; Zaugg, J.B. Transcription factors: Bridge between cell signaling and gene regulation. Proteomics 2021, 21, 2000034. [Google Scholar] [CrossRef]
- Khadem, A.; Moshtaghi, N.; Bagheri, A. Regulatory networks of hormone-involved transcription factors and their downstream pathways during somatic embryogenesis of Arabidopsis thaliana. 3 Biotech 2023, 13, 132. [Google Scholar] [CrossRef]
- Altmann, M.; Altmann, S.; Rodriguez, P.A.; Weller, B.; Elorduy Vergara, L.; Palme, J.; Marín-de la Rosa, N.; Sauer, M.; Wenig, M.; Villaécija-Aguilar, J.A. Extensive signal integration by the phytohormone protein network. Nature 2020, 583, 271–276. [Google Scholar] [CrossRef]
- Cluis, C.P.; Mouchel, C.F.; Hardtke, C.S. The Arabidopsis transcription factor HY5 integrates light and hormone signaling pathways. Plant J. 2004, 38, 332–347. [Google Scholar] [CrossRef]
- Jiang, J.; Ma, S.; Ye, N.; Jiang, M.; Cao, J.; Zhang, J. WRKY transcription factors in plant responses to stresses. J. Integr. Plant Biol. 2017, 59, 86–101. [Google Scholar] [CrossRef] [PubMed]
- Depuydt, S.; Hardtke, C.S. Hormone signalling crosstalk in plant growth regulation. Curr. Biol. 2011, 21, R365–R373. [Google Scholar] [CrossRef] [PubMed]
- Khan, N.; Bano, A.; Ali, S.; Babar, M.A. Crosstalk amongst phytohormones from planta and PGPR under biotic and abiotic stresses. Plant Growth Regul. 2020, 90, 189–203. [Google Scholar] [CrossRef]
- Figueroa-Macías, J.P.; García, Y.C.; Núñez, M.; Díaz, K.; Olea, A.F.; Espinoza, L. Plant growth-defense trade-offs: Molecular processes leading to physiological changes. Int. J. Mol. Sci. 2021, 22, 693. [Google Scholar] [CrossRef]
- Yao, J.; Waters, M.T. Perception of karrikins by plants: A continuing enigma. J. Exp. Bot. 2020, 71, 1774–1781. [Google Scholar] [CrossRef] [PubMed]
- Jaillais, Y.; Chory, J. Unraveling the paradoxes of plant hormone signaling integration. Nat. Struct. Mol. Biol. 2010, 17, 642–645. [Google Scholar] [CrossRef] [PubMed]
- Yang, D.-L.; Yao, J.; Mei, C.-S.; Tong, X.-H.; Zeng, L.-J.; Li, Q.; Xiao, L.-T.; Sun, T.-p.; Li, J.; Deng, X.-W. Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade. Proc. Natl. Acad. Sci. USA 2012, 109, E1192–E1200. [Google Scholar] [CrossRef]
- Nemhauser, J.L.; Hong, F.; Chory, J. Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 2006, 126, 467–475. [Google Scholar] [CrossRef]
- Zander, M.; Lewsey, M.G.; Clark, N.M.; Yin, L.; Bartlett, A.; Saldierna Guzmán, J.P.; Hann, E.; Langford, A.E.; Jow, B.; Wise, A. Integrated multi-omics framework of the plant response to jasmonic acid. Nat. Plants 2020, 6, 290–302. [Google Scholar] [CrossRef]
- Clark, N.M.; Nolan, T.M.; Wang, P.; Song, G.; Montes, C.; Valentine, C.T.; Guo, H.; Sozzani, R.; Yin, Y.; Walley, J.W. Integrated omics networks reveal the temporal signaling events of brassinosteroid response in Arabidopsis. Nat. Commun. 2021, 12, 5858. [Google Scholar] [CrossRef]
- Moreno, J.E.; Shyu, C.; Campos, M.L.; Patel, L.C.; Chung, H.S.; Yao, J.; He, S.Y.; Howe, G.A. Negative feedback control of jasmonate signaling by an alternative splice variant of JAZ10. Plant Physiol. 2013, 162, 1006–1017. [Google Scholar] [CrossRef] [PubMed]
- Munns, R.; Tester, M. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 2008, 59, 651–681. [Google Scholar] [CrossRef]
- Liu, T. Use model-based analysis of ChIP-Seq (MACS) to analyze short reads generated by sequencing protein–DNA interactions in embryonic stem cells. Stem Cell Transcr. Netw. Methods Protoc. 2014, 81–95. [Google Scholar]
- Strader, L.; Weijers, D.; Wagner, D. Plant transcription factors—being in the right place with the right company. Curr. Opin. Plant Biol. 2022, 65, 102136. [Google Scholar] [CrossRef]
- Singh, K.B.; Foley, R.C.; Oñate-Sánchez, L. Transcription factors in plant defense and stress responses. Curr. Opin. Plant Biol. 2002, 5, 430–436. [Google Scholar] [CrossRef]
- He, C.; Yan, J.; Shen, G.; Fu, L.; Holaday, A.S.; Auld, D.; Blumwald, E.; Zhang, H. Expression of an Arabidopsis vacuolar sodium/proton antiporter gene in cotton improves photosynthetic performance under salt conditions and increases fiber yield in the field. Plant Cell Physiol. 2005, 46, 1848–1854. [Google Scholar] [CrossRef] [PubMed]
- Tran, L.-S.P.; Nakashima, K.; Sakuma, Y.; Simpson, S.D.; Fujita, Y.; Maruyama, K.; Fujita, M.; Seki, M.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 2004, 16, 2481–2498. [Google Scholar] [CrossRef] [PubMed]
- Nakashima, K.; Tran, L.S.P.; 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. 2007, 51, 617–630. [Google Scholar] [CrossRef]
- Hu, H.; You, J.; Fang, Y.; Zhu, X.; Qi, Z.; Xiong, L. Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice. Plant Mol. Biol. 2008, 67, 169–181. [Google Scholar] [CrossRef]
- Peng, H.; Cheng, H.-Y.; Yu, X.-W.; Shi, Q.-H.; Zhang, H.; Li, J.-G.; Ma, H. Characterization of a chickpea (Cicer arietinum L.) NAC family gene, CarNAC5, which is both developmentally-and stress-regulated. Plant Physiol. Biochem. 2009, 47, 1037–1045. [Google Scholar] [CrossRef]
- Meng, C.; Cai, C.; Zhang, T.; Guo, W. Characterization of six novel NAC genes and their responses to abiotic stresses in Gossypium hirsutum L. Plant Sci. 2009, 176, 352–359. [Google Scholar] [CrossRef]
- Xia, N.; Zhang, G.; Liu, X.-Y.; Deng, L.; Cai, G.-L.; Zhang, Y.; Wang, X.-J.; Zhao, J.; Huang, L.-L.; Kang, Z.-S. Characterization of a novel wheat NAC transcription factor gene involved in defense response against stripe rust pathogen infection and abiotic stresses. Mol. Biol. Rep. 2010, 37, 3703–3712. [Google Scholar] [CrossRef] [PubMed]
- Puranik, S.; Bahadur, R.P.; Srivastava, P.S.; Prasad, M. Molecular cloning and characterization of a membrane associated NAC family gene, SiNAC from foxtail millet [Setaria italica (L.) P. Beauv.]. Mol. Biotechnol. 2011, 49, 138–150. [Google Scholar] [CrossRef] [PubMed]
- Abe, H.; Urao, T.; Ito, T.; Seki, M.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 2003, 15, 63–78. [Google Scholar] [CrossRef] [PubMed]
- Ding, Z.; Li, S.; An, X.; Liu, X.; Qin, H.; Wang, D. Transgenic expression of MYB15 confers enhanced sensitivity to abscisic acid and improved drought tolerance in Arabidopsis thaliana. J. Genet. Genom. 2009, 36, 17–29. [Google Scholar] [CrossRef]
- Archana, K.; Rama, N.; Mamrutha, H.; Nataraja, K.N. Down-Regulation of an Abiotic Stress Related Nicotiana Benthamiana WRKY Transcription Factor Induces Physiological Abnormalities; CSIR: Paris, France, 2009. [Google Scholar]
- Zhou, Q.Y.; Tian, A.G.; Zou, H.F.; Xie, Z.M.; Lei, G.; Huang, J.; Wang, C.M.; Wang, H.W.; Zhang, J.S.; Chen, S.Y. Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. Plant Biotechnol. J. 2008, 6, 486–503. [Google Scholar] [CrossRef]
- Liu, Q.; Kasuga, M.; Sakuma, Y.; Abe, H.; Miura, S.; Yamaguchi-Shinozaki, K.; Shinozaki, K. Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought-and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 1998, 10, 1391–1406. [Google Scholar] [CrossRef]
- Lee, S.-j.; Kang, J.-y.; Park, H.-J.; Kim, M.D.; Bae, M.S.; Choi, H.-i.; Kim, S.Y. DREB2C interacts with ABF2, a bZIP protein regulating abscisic acid-responsive gene expression, and its overexpression affects abscisic acid sensitivity. Plant Physiol. 2010, 153, 716–727. [Google Scholar] [CrossRef]
- Dubouzet, J.G.; Sakuma, Y.; Ito, Y.; Kasuga, M.; Dubouzet, E.G.; Miura, S.; Seki, M.; Shinozaki, K.; Yamaguchi-Shinozaki, K. OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt-and cold-responsive gene expression. Plant J. 2003, 33, 751–763. [Google Scholar] [CrossRef]
- Wang, Q.; Guan, Y.; Wu, Y.; Chen, H.; Chen, F.; Chu, C. Overexpression of a rice OsDREB1F gene increases salt, drought, and low temperature tolerance in both Arabidopsis and rice. Plant Mol. Biol. 2008, 67, 589–602. [Google Scholar] [CrossRef]
- Xue, G.P.; Loveridge, C.W. HvDRF1 is involved in abscisic acid-mediated gene regulation in barley and produces two forms of AP2 transcriptional activators, interacting preferably with a CT-rich element. Plant J. 2004, 37, 326–339. [Google Scholar] [CrossRef]
- Xu, Z.-S.; Ni, Z.-Y.; Li, Z.-Y.; Li, L.-C.; Chen, M.; Gao, D.-Y.; Yu, X.-D.; Liu, P.; Ma, Y.-Z. Isolation and functional characterization of HvDREB1—a gene encoding a dehydration-responsive element binding protein in Hordeum vulgare. J. Plant Res. 2009, 122, 121–130. [Google Scholar] [CrossRef]
- Qin, F.; Kakimoto, M.; Sakuma, Y.; Maruyama, K.; Osakabe, Y.; Tran, L.S.P.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L. Plant J. 2007, 50, 54–69. [Google Scholar] [CrossRef] [PubMed]
- Agarwal, P.; Agarwal, P.K.; Nair, S.; Sopory, S.; Reddy, M. Stress-inducible DREB2A transcription factor from Pennisetum glaucum is a phosphoprotein and its phosphorylation negatively regulates its DNA-binding activity. Mol. Genet. Genom. 2007, 277, 189–198. [Google Scholar] [CrossRef] [PubMed]
- Lata, C.; Bhutty, S.; Bahadur, R.P.; Majee, M.; Prasad, M. Association of an SNP in a novel DREB2-like gene SiDREB2 with stress tolerance in foxtail millet [Setaria italica (L.)]. J. Exp. Bot. 2011, 62, 3387–3401. [Google Scholar] [CrossRef] [PubMed]
- Hong, J.-P.; Kim, W.T. Isolation and functional characterization of the Ca-DREBLP1 gene encoding a dehydration-responsive element binding-factor-like protein 1 in hot pepper (Capsicum annuum L. cv. Pukang). Planta 2005, 220, 875–888. [Google Scholar] [CrossRef]
- Shen, Y.-G.; Zhang, W.-K.; Yan, D.-Q.; Du, B.-X.; Zhang, J.-S.; Liu, Q.; Chen, S.-Y. Characterization of a DRE-binding transcription factor from a halophyte Atriplex hortensis. Theor. Appl. Genet. 2003, 107, 155–161. [Google Scholar] [CrossRef]
- Li, X.-P.; Tian, A.-G.; Luo, G.-Z.; Gong, Z.-Z.; Zhang, J.-S.; Chen, S.-Y. Soybean DRE-binding transcription factors that are responsive to abiotic stresses. Theor. Appl. Genet. 2005, 110, 1355–1362. [Google Scholar] [CrossRef]
- Chen, M.; Wang, Q.-Y.; Cheng, X.-G.; Xu, Z.-S.; Li, L.-C.; Ye, X.-G.; Xia, L.-Q.; Ma, Y.-Z. GmDREB2, a soybean DRE-binding transcription factor, conferred drought and high-salt tolerance in transgenic plants. Biochem. Biophys. Res. Commun. 2007, 353, 299–305. [Google Scholar] [CrossRef]
- Shukla, R.K.; Raha, S.; Tripathi, V.; Chattopadhyay, D. Expression of CAP2, an APETALA2-family transcription factor from chickpea, enhances growth and tolerance to dehydration and salt stress in transgenic tobacco. Plant Physiol. 2006, 142, 113–123. [Google Scholar] [CrossRef]
- Gupta, K.; Agarwal, P.K.; Reddy, M.; Jha, B. SbDREB2A, an A-2 type DREB transcription factor from extreme halophyte Salicornia brachiata confers abiotic stress tolerance in Escherichia coli. Plant Cell Rep. 2010, 29, 1131–1137. [Google Scholar] [CrossRef]
- Choi, H.-I.; Hong, J.-H.; Ha, J.-O.; Kang, J.-Y.; Kim, S.Y. ABFs, a family of ABA-responsive element binding factors. J. Biol. Chem. 2000, 275, 1723–1730. [Google Scholar] [CrossRef] [PubMed]
- Liao, Y.; Zou, H.-F.; Wei, W.; Hao, Y.-J.; Tian, A.-G.; Huang, J.; Liu, Y.-F.; Zhang, J.-S.; Chen, S.-Y. Soybean GmbZIP44, GmbZIP62 and GmbZIP78 genes function as negative regulator of ABA signaling and confer salt and freezing tolerance in transgenic Arabidopsis. Planta 2008, 228, 225–240. [Google Scholar] [CrossRef]
- Kobayashi, F.; Maeta, E.; Terashima, A.; Kawaura, K.; Ogihara, Y.; Takumi, S. Development of abiotic stress tolerance via bZIP-type transcription factor LIP19 in common wheat. J. Exp. Bot. 2008, 59, 891–905. [Google Scholar] [CrossRef]
- Zou, M.; Guan, Y.; Ren, H.; Zhang, F.; Chen, F. A bZIP transcription factor, OsABI5, is involved in rice fertility and stress tolerance. Plant Mol. Biol. 2008, 66, 675–683. [Google Scholar] [CrossRef]
- Jia, Z.; Lian, Y.; Zhu, Y.; He, J.; Cao, Z.; Wang, G. Cloning and characterization of a putative transcription factor induced by abiotic stress in Zea mays. Afr. J. Biotechnol. 2009, 8. [Google Scholar]
- Hsieh, T.-H.; Li, C.-W.; Su, R.-C.; Cheng, C.-P.; Sanjaya; Tsai, Y.-C.; Chan, M.-T. A tomato bZIP transcription factor, SlAREB, is involved in water deficit and salt stress response. Planta 2010, 231, 1459–1473. [Google Scholar] [CrossRef]
- Nongpiur, R.C.; Singla-Pareek, S.L.; Pareek, A. The quest for osmosensors in plants. J. Exp. Bot. 2020, 71, 595–607. [Google Scholar] [CrossRef] [PubMed]
- Shah, W.H.; Rasool, A.; Saleem, S.; Mushtaq, N.U.; Tahir, I.; Hakeem, K.R.; Rehman, R.U. Understanding the integrated pathways and mechanisms of transporters, protein kinases, and transcription factors in plants under salt stress. Int. J. Genom. 2021, 2021. [Google Scholar] [CrossRef]
- Ci, D.; Song, Y.; Tian, M.; Zhang, D. Methylation of miRNA genes in the response to temperature stress in Populus simonii. Front. Plant Sci. 2015, 6, 921. [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]
- Baulcombe, D.C.; Dean, C. Epigenetic regulation in plant responses to the environment. Cold Spring Harb. Perspect. Biol. 2014, 6, a019471. [Google Scholar] [CrossRef]
- Liu, J.; He, Z. Small DNA methylation, big player in plant abiotic stress responses and memory. Front. Plant Sci. 2020, 11, 595603. [Google Scholar] [CrossRef] [PubMed]
- Song, Y.; Ji, D.; Li, S.; Wang, P.; Li, Q.; Xiang, F. The dynamic changes of DNA methylation and histone modifications of salt responsive transcription factor genes in soybean. PLoS ONE 2012, 7, e41274. [Google Scholar] [CrossRef] [PubMed]
- Ferreira, L.J.; Azevedo, V.; Maroco, J.; Oliveira, M.M.; Santos, A.P. Salt tolerant and sensitive rice varieties display differential methylome flexibility under salt stress. PLoS ONE 2015, 10, e0124060. [Google Scholar] [CrossRef] [PubMed]
- Kumar, S.; Beena, A.S.; Awana, M.; Singh, A. Salt-induced tissue-specific cytosine methylation downregulates expression of HKT genes in contrasting wheat (Triticum aestivum L.) genotypes. DNA Cell Biol. 2017, 36, 283–294. [Google Scholar] [CrossRef]
- Kaldis, A.; Tsementzi, D.; Tanriverdi, O.; Vlachonasios, K.E. Arabidopsis thaliana transcriptional co-activators ADA2b and SGF29a are implicated in salt stress responses. Planta 2011, 233, 749–762. [Google Scholar] [CrossRef]
- Pandey, G.; Sharma, N.; Pankaj Sahu, P.; Prasad, M. Chromatin-based epigenetic regulation of plant abiotic stress response. Curr. Genom. 2016, 17, 490–498. [Google Scholar] [CrossRef]
- Banerjee, A.; Roychoudhury, A. Epigenetic regulation during salinity and drought stress in plants: Histone modifications and DNA methylation. Plant Gene 2017, 11, 199–204. [Google Scholar] [CrossRef]
- Bilichak, A.; Ilnystkyy, Y.; Hollunder, J.; Kovalchuk, I. The progeny of Arabidopsis thaliana plants exposed to salt exhibit changes in DNA methylation, histone modifications and gene expression. PLoS ONE 2012, 7, e30515. [Google Scholar] [CrossRef]
- Tanveer, M.; Shabala, S. Targeting redox regulatory mechanisms for salinity stress tolerance in crops. Salin. Responses Toler. Plants Vol. 1 Target. Sens. Transp. Signal. Mech. 2018, 213–234. [Google Scholar]
- Costa, S.F.; Martins, D.; Agacka-Mołdoch, M.; Czubacka, A.; de Sousa Araújo, S. Strategies to alleviate salinity stress in plants. Salin. Responses Toler. Plants Vol. 1 Target. Sens. Transp. Signal. Mech. 2018, 307–337. [Google Scholar]
- Morton, M.J.; Awlia, M.; Al-Tamimi, N.; Saade, S.; Pailles, Y.; Negrão, S.; Tester, M. Salt stress under the scalpel–dissecting the genetics of salt tolerance. Plant J. 2019, 97, 148–163. [Google Scholar] [CrossRef] [PubMed]
- Bansal, J.; Gupta, K.; Rajkumar, M.S.; Garg, R.; Jain, M. Draft genome and transcriptome analyses of halophyte rice Oryza coarctata provide resources for salinity and submergence stress response factors. Physiol. Plant. 2021, 173, 1309–1322. [Google Scholar] [CrossRef] [PubMed]
- Basu, S.; Roychoudhury, A. Transcript profiling of stress-responsive genes and metabolic changes during salinity in indica and japonica rice exhibit distinct varietal difference. Physiol. Plant. 2021, 173, 1434–1447. [Google Scholar] [CrossRef] [PubMed]
- Elnaggar, A.; Mosa, K.A.; Ramamoorthy, K.; El-Keblawy, A.; Navarro, T.; Soliman, S.S. De novo transcriptome sequencing, assembly, and gene expression profiling of a salt-stressed halophyte (Salsola drummondii) from a saline habitat. Physiol. Plant. 2021, 173, 1695–1714. [Google Scholar] [CrossRef] [PubMed]
- Rajkumar, M.S.; Jain, M.; Garg, R. Discovery of DNA polymorphisms via whole genome resequencing and their functional relevance in salinity stress response in chickpea. Physiol. Plant. 2021, 173, 1573–1586. [Google Scholar] [CrossRef]
WRAKY Transcriptional Factors | |||
---|---|---|---|
Plant | Gene | Involved | References |
Fritillaria crassifolia | FcWRAKY70 | Salt stress | [40] |
Glycin max | GmWARKY17 | Salt stress | [41] |
Zea mays | ZmWARKY17 | Salt stress | [42] |
Sorghum bicolor | SbWARKY30 | Salt stress | [43] |
Gossypium barbadense | GbWARKY1 | Salt stress | [44] |
Ipomoea batatas | IbWARKY47 | Salt stress | [45] |
Penicillium glaucum | PgWARKY33/62 | Salt stress | [46] |
Sorghum bicolor | SbWARKY50 | Salt stress | [47] |
Vitis pseudoreticulata | VpWARKY1 and VpWARKY2 | Salt stress | [48] |
Malus baccata | MbWARKY5 | Salt stress | [49] |
Cucurbita pepo | CmWARKY | Salt stress | [50] |
Pyrus betulifolia | PbWARKY40 | Salt stress | [51] |
Citrullus lanatus | ClWARKY20 | Salt stress | [52] |
Malus xiaojinensis | MxWARKY53 | Salt stress | [53] |
Malus xiaojinensis | MxWARKY64 | Salt stress | [54] |
Arachis hypogaea L. | AhWARKY75 | Salt stress | [55] |
Myrothamnus flabellifolia | MfWARKY70 | Salt stress | [56] |
Arabidopsis thaliana | AtWRKY33 | Salt stress | [57] |
Gossypiumhirsutum | GhWRKY34 | Salt stress | [58] |
Populuseuphratica | PeWRKY1 | Salt stress | [59] |
Solanum lycopersicum | SlWRKY23 | Salt stress | [60] |
bZIP Transcriptional Factors | |||
---|---|---|---|
Plant | Gene | Involved | References |
Arabidopsis thaliana | AtbZIP17 | Salt stress | [61] |
Boehmeria nivea | BnbZIP2 | Salt stress | [62] |
Capsicum annuum | CAbZIP1 and CabZIP25 | Salt stress | [63,64] |
Glycine max | GmbZIP2 | Salt stress | [65] |
Oryza sativa | OsbZIP05 | Salt stress | [66] |
Triticum aestivum | TabZIP8 and TabZIP14B | Salt stress | [67,68] |
Tamarix hispida | ThbZIP1 and TabZIP15 | Salt stress | [69,70] |
Jatropha curcas | JcbZIP34, JcbZIP36, JcbZIP49 and JcbZIP50 | Salt stress | [71] |
Zay mays | ZmbZIP4 | Salt stress | [72] |
Solanum lycopersicum | SlbZIP1 | Salt stress | [73] |
Solanum tuberosum | StbZIP25 and StbZIP65 | Salt stress | [74,75] |
Setaria italica | SibZIP35 | Salt stress | [76] |
Vaccinium sp. | VabZIP12 | Salt stress | [77] |
Isatis indigotica | IibZIP | Salt stress | [78] |
Ipomoea batatas | IbbZIP1 | Salt stress | [79] |
MYB Transcriptional Factors | |||
---|---|---|---|
Plant | Gene | Involved | References |
Oryza sativa | OsMYB6 and OsMYB48-1 | Salt stress | [80,81] |
Arabidopsis thaliana | AtMYB44 and AtMYB2 | Salt stress | [82] |
Triticum aestivum L. | TaMYB19-B, | Salt stress | [83] |
Glycine max | GmMYB76 | Salt stress | [84] |
Nicotiana tabacum | PsnMYB108 | Salt stress | [85] |
Solanum lycopersicum | SlMYB102 | Salt stress | [86] |
Leymus chinensis | LcMYB2 | Salt stress | [87] |
Arachis hypogaea | AhMYB94 | Salt stress | [88] |
Zea mays | ZmMYB3R | Salt stress | [89] |
Medicago sativa | MsMYB4 | Salt stress | [90] |
Vitis vinifera | VhMYB2 | Salt stress | [91] |
Casuarina equisetifolia | CeqMYB4 | Salt stress | [92] |
Gossypium hirsutum | GhMYB108 | Salt stress | [93] |
Actinidia chinensis | AcMYB3R | Salt stress | [94] |
Chrysanthemum | CmMYB2 | Salt stress | [95] |
Prunus avium | PacMYBA | Salt stress | [96] |
Malus domestica | MdoMYB121 | Salt stress | [97] |
Betula platyphylla | BplMYB46 | Salt stress | [97] |
Panax ginseng | PgMYB | Salt stress | [98] |
Lilium lancifolium L. | LlMYB3 | Salt stress | [99] |
Dendrobium catenatum | DcMYB | Salt stress | [100] |
NAC Transcriptional Factors | |||
---|---|---|---|
Plant | Gene | Involved | References |
Ipomoea pes-caprae | IpNAC10 | Salt stress | [101] |
Oryza sativa | OsNAC5 and OsNAC6 | Salt stress | [102] |
Actinidia chinensis | AvNAC030 | Salt stress | [103] |
Helianthus annuus | HaNAC-1 | Salt stress | [104] |
Cicer arietinum L. | CarNAC1 | Salt stress | [105] |
Brassica napus | BnNAC5 | Salt stress | [106] |
Chrysanthemum grandiflora | ClNAC9 | Salt stress | [107] |
Lilium pumilum | LpNAC13 | Salt stress | [108] |
Zea mays | ZmSNAC1 | Salt stress | [109] |
Pennisetum glaucum | PgNACs | Salt stress | [110] |
Populus | PtNAC024 and PtNAC182 | Salt stress | [111] |
Glycine max | GmNAC06 | Salt stress | [112] |
Cucumis melo L. | CmNAC14 | Salt stress | [113] |
Musa acuminata | MusaNAC042 | Salt stress | [114] |
Cicer arietinum | CarNAC4 | Salt stress | [115] |
Malus domestica | MdNAC047 | Salt stress | [116] |
Sorghum bicolor (L.) | SbNAC1 | Salt stress | [117] |
Malus baccata | MbNAC25 | Salt stress | [118] |
Tamarix hispida | ThNAC13 | Salt stress | [119] |
Medicago sativa L. | MsNAC058 | Salt stress | [120] |
Vitis vinifera | VvNAC17 | Salt stress | [121] |
Avena sativa | AsNAC9 and AsNAC4 | Salt stress | [121] |
Transcription Factor | Response |
---|---|
WRKY | Reduces harmful ROS levels and ABA signaling positive regulators to protect cell membranes [122] and reduces salt tolerance [41]. |
NAC | Triggers germination/growth rate, higher seed germination under high salinity, and osmotic stress [123]. |
bZIP | Scavenges reactive oxygen species by modifying specific gene expression to improve the salt tolerance of the plant [69]. Involved in ABA response [67,124]. Inhibits seed germination and seedling growth [125]. |
MYB | Response of the transcriptome to osmotic stress and osmolyte formation and maintains root growth under salinity stress [126]. |
Family | DNA-Binding Domains | Cis-Acting Element | Plant Species | Genes Involved in Salt Response | Reference |
---|---|---|---|---|---|
NAC | NAC domain | NAC recognition sequence (TCNACACGCATGT) | Arabidopsis thaliana | AtNAC2 AtNAC019 AtNAC055 AtNAC072 | [193,194] |
Oryza sativa | OsNAC6 SNAC1 SNAC2 | [195,196] | |||
Cicer arietinum | CarNAC5 | [197] | |||
Gossypium hirsutum | GhNAC4 GhNAC6 | [198] | |||
Triticum aestivum | TaNAC4 | [199] | |||
Setaria italica | SiNAC | [200] | |||
MYB | MYB domain | MYBR (TAACNA/G) | Arabidopsis thaliana | AtMYB2 AtMYB4 AtMYB6 AtMYB7 AtMYB44 AtMYB73 | [201,202] |
Glycine max | GmMYB76 GmMYB92 | [84] | |||
WRKY | WRKYGQK domain | W-box (TTGACT/C) | Oryza sativa Nicotiana benthamiana | OsWRKY45 NbWRKY | [139] [203] |
Glycine max | GmWRKY21 GmWRKY54 GmWRKY13 GmMYB177 | [84,204] | |||
ERF/DREB | AP2/ERF domain | DRE sequence, GCC box (AGCCGCC), and (TACCGACAT) | Arabidopsis thaliana | DREB2A DREB2C | [205,206] |
Oryza sativa | OsDREB1A OsDREB1C OsDREB1F OsDREB2A | [207,208] | |||
Hordeum vulgare | HvDRF1 HvDREB1 | [209,210] | |||
Zea mays | ZmDREB2A | [211] | |||
Pennisetum glaucum | PgDREB2A | [212] | |||
Setaria italica | SiDREB2 | [213] | |||
Capsicum annum | CaDREBLP1 | [214] | |||
Artiplex hortensis | AhDREB1 | [215] | |||
Glycine max | GmDREBb GmDREBc GmDREB2 | [216,217] | |||
Cicer arietinum | CAP2 | [218] | |||
Salicornia brachiata | SbDREB2A | [219] | |||
bZIP | bZIP domain | GLM (GTGAGTCAT), ABRE (CCACGTGG), GCN4-like-motif (GTGAGTCAT), | Arabidopsis thaliana | ABF2 ABF3 ABF4 | [220] |
Glycine max | GmbZIP44 GmbZIP62 GmbZIP78 GmbZIP132 | [221] | |||
Triticum aestivum | Wlip19 | [222] | |||
Oryza sativa | OsABI5 OsbZIP23 | [223] | |||
Zea mays | ZmbZIP17 | [224] | |||
Solanum lycopersicum | SlAREB | [225] |
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Aizaz, M.; Lubna; Jan, R.; Asaf, S.; Bilal, S.; Kim, K.-M.; AL-Harrasi, A. Regulatory Dynamics of Plant Hormones and Transcription Factors under Salt Stress. Biology 2024, 13, 673. https://doi.org/10.3390/biology13090673
Aizaz M, Lubna, Jan R, Asaf S, Bilal S, Kim K-M, AL-Harrasi A. Regulatory Dynamics of Plant Hormones and Transcription Factors under Salt Stress. Biology. 2024; 13(9):673. https://doi.org/10.3390/biology13090673
Chicago/Turabian StyleAizaz, Muhammad, Lubna, Rahmatullah Jan, Sajjad Asaf, Saqib Bilal, Kyung-Min Kim, and Ahmed AL-Harrasi. 2024. "Regulatory Dynamics of Plant Hormones and Transcription Factors under Salt Stress" Biology 13, no. 9: 673. https://doi.org/10.3390/biology13090673