24-Epibrassinolide (EBR) Confers Tolerance against NaCl Stress in Soybean Plants by Up-Regulating Antioxidant System, Ascorbate-Glutathione Cycle, and Glyoxalase System
Abstract
:1. Introduction
2. Material and Methods
2.1. Growth Estimation
2.2. Assessment of Pigment Content and Chlorophyll Fluorescence
2.3. Gas Exchange Parameters Estimation
2.4. Estimation of Proline and Glycine Betaine (GB)
2.5. Evaluation of Hydrogen Peroxide (H2O2), Malondialdehyde (MDA), and Electrolyte Leakage (EL)
2.6. Estimation of Antioxidant Enzymes’ Activities and Asc-Glu Cycle
2.7. Measurement of Methylglyoxal Content and Activity of GlyI and GlyII
2.8. Estimation of Total Phenols and Total Flavonoids
2.9. Estimation of Mineral Elements
2.10. Statistical Analysis
3. Results
3.1. Growth and Biomass Yield
3.2. Photosynthetic Pigments, Chlorophyll Fluorescence, and Leaf Gas Exchange Parameters
3.3. Proline and GB
3.4. H2O2 and MDA Content and EL
3.5. Activities of Antioxidant Enzymes and Enzymes of Ascorbate-Glutathione Cycle
3.6. Glyoxalase System
3.7. Total Phenols and Total Flavonoid Content
3.8. Mineral Elements
4. Discussion
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Haque, S. Salinity problems and crop production in coastal regions of Bangladesh. Pak. J. Bot. 2006, 38, 1359–1365. [Google Scholar]
- Shalhevet, J. Using water of marginal quality for crop production: major issues. Agric. Water Manag. 1994, 25, 233–269. [Google Scholar] [CrossRef]
- Wang, W.; Vinocur, B.; Altman, A. Plant responses to drought, salinity and extreme temperatures: Towards genetic engineering for stress tolerance. Planta 2003, 218, 1–14. [Google Scholar] [CrossRef] [PubMed]
- Ahanger, M.A.; Qin, C.; Maodong, Q.; Dong, X.X.; Ahmad, P.; Abd_Allah, E.F.; Zhang, L. Spermine application alleviates salinity induced growth and photosynthetic inhibition in Solanum lycopersicum by modulating osmolyte and secondary metabolite accumulation and differentially regulating antioxidant metabolism. Plant Physiol. Biochem. 2019, 144, 1–13. [Google Scholar] [CrossRef] [PubMed]
- Ahanger, M.A.; Agarwal, R. Salinity stress induced alterations in antioxidant metabolism and nitrogen assimilation in wheat (Triticum aestivum L.) as influenced by potassium supplementation. Plant Physiol. Biochem. 2017, 115, 449–460. [Google Scholar] [CrossRef] [PubMed]
- Porcel, R.; Aroca, R.; Ruiz-Lozano, J.M. Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron. Sustain. Dev. 2012, 32, 181–200. [Google Scholar] [CrossRef]
- Ahmad, P.; Abass Ahanger, M.; Nasser Alyemeni, M.; Wijaya, L.; Alam, P.; Ashraf, M. Mitigation of sodium chloride toxicity in Solanum lycopersicum L. by supplementation of jasmonic acid and nitric oxide. J. Plant. Interact. 2018, 13, 64–72. [Google Scholar] [CrossRef]
- Ahmad, P. Growth and antioxidant responses in mustard (Brassica juncea L.) plants subjected to combined effect of gibberellic acid and salinity. Arch. Agron. Soil Sci. 2010, 56, 575–588. [Google Scholar] [CrossRef]
- Ahmad, F.; Singh, A.; Kamal, A. Ameliorative effect of salicylic acid in salinity stressed Pisum sativum by improving growth parameters, activating photosynthesis and enhancing antioxidant defense system. Biosci. Biotechnol. Res. Commun. 2017, 10, 481–489. [Google Scholar] [CrossRef]
- Munns, R.; Tester, M. Mechanisms of Salinity Tolerance. Annu. Rev. Plant. Biol. 2008, 59, 651–681. [Google Scholar] [CrossRef] [Green Version]
- Ashraf, M.; Foolad, M.R. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ. Exp. Bot. 2007, 59, 206–216. [Google Scholar] [CrossRef]
- Murata, N.; Mohanty, P.S.; Hayashi, H.; Papageorgiou, G.C. Glycinebetaine stabilizes the association of extrinsic proteins with the photosynthetic oxygen-evolving complex. FEBS Lett. 1992, 296, 187–189. [Google Scholar] [CrossRef] [Green Version]
- Khan, M.I.R.; Asgher, M.; Khan, N.A. Alleviation of salt-induced photosynthesis and growth inhibition by salicylic acid involves glycinebetaine and ethylene in mungbean (Vigna radiata L.). Plant Physiol. Biochem. 2014, 80, 67–74. [Google Scholar] [CrossRef] [PubMed]
- Ahanger, M.A.; Tyagi, S.R.; Wani, M.R.; Ahmad, P. Drought Tolerance: Role of Organic Osmolytes, Growth Regulators, and Mineral Nutrients. In Physiological Mechanisms and Adaptation Strategies in Plants Under Changing Environment; Ahmad, P., Wani, M.R., Eds.; Springer: New York, NY, USA, 2014; Volume 1, pp. 25–55. [Google Scholar]
- Ahanger, M.A.; Gul, F.; Ahmad, P.; Akram, N.A. Environmental Stresses and Metabolomics—Deciphering the Role of Stress Responsive Metabolites. In Plant Metabolites and Regulation Under Environmental Stress; Elsevier: Amsterdam, The Netherlands, 2018; pp. 53–67. [Google Scholar] [CrossRef]
- Ahmad, P.; Abd_Allah, E.F.; Alyemeni, M.N.; Wijaya, L.; Alam, P.; Bhardwaj, R.; Siddique, K.H.M. Exogenous application of calcium to 24-epibrassinosteroid pre-treated tomato seedlings mitigates NaCl toxicity by modifying ascorbate–glutathione cycle and secondary metabolites. Sci. Rep. 2018, 8, s41598–s41618. [Google Scholar] [CrossRef]
- Ahmad, P.; Jaleel, C.A.; Salem, M.A.; Nabi, G.; Sharma, S. Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress. Crit. Rev. Biotechnol. 2010, 30, 161–175. [Google Scholar] [CrossRef]
- Ahmad, P.; Jaleel, C.A.; Sharma, S. Antioxidant defense system, lipid peroxidation, proline-metabolizing enzymes, and biochemical activities in two Morus alba genotypes subjected to NaCl stress. Russ. J. Plant Physiol. 2010, 57, 509–517. [Google Scholar] [CrossRef]
- Rasool, S.; Ahmad, A.; Siddiqi, T.O.; Ahmad, P. Changes in growth, lipid peroxidation and some key antioxidant enzymes in chickpea genotypes under salt stress. Acta Physiol. Plant. 2013, 35, 1039–1050. [Google Scholar] [CrossRef]
- Ahanger, M.A.; Agarwal, R. Potassium up-regulates antioxidant metabolism and alleviates growth inhibition under water and osmotic stress in wheat (Triticum aestivum L.). Protoplasma 2017, 254, 1471–1486. [Google Scholar] [CrossRef]
- Ahmad, P.; Ahanger, M.A.; Alam, P.; Alyemeni, M.N.; Wijaya, L.; Ali, S.; Ashraf, M. Silicon (Si) Supplementation Alleviates NaCl Toxicity in Mung Bean [Vigna radiata (L.) Wilczek] Through the Modifications of Physio-biochemical Attributes and Key Antioxidant Enzymes. J. Plant. Growth Regul. 2018. [Google Scholar] [CrossRef]
- Sharma, I.; Ching, E.; Saini, S.; Bhardwaj, R.; Pati, P.K. Exogenous application of brassinosteroid offers tolerance to salinity by altering stress responses in rice variety Pusa Basmati-1. Plant Physiol. Biochem. 2013, 69, 17–26. [Google Scholar] [CrossRef]
- Sharma, I.; Pati, P.K.; Bhardwaj, R. Effect of 28-homobrassinolide on antioxidant defence system in Raphanus sativus L. under chromium toxicity. Ecotoxicology 2011, 20, 862–874. [Google Scholar] [CrossRef] [PubMed]
- Sharma, N.; Hundal, G.S.; Sharma, I.; Bhardwaj, R. 28-Homobrassinolide alters protein content and activities of glutathione-S-transferase and polyphenol oxidase in Raphanus sativus L. plants under heavy metal stress. Toxicol. Int. 2014, 21, 44. [Google Scholar] [PubMed]
- Vardhini, B.V.; Anjum, N.A. Brassinosteroids make plant life easier under abiotic stresses mainly by modulating major components of antioxidant defense system. Front. Environ. Sci. 2015, 2, 67. [Google Scholar] [CrossRef]
- Xia, X.-J.; Zhou, Y.-H.; Shi, K.; Zhou, J.; Foyer, C.H.; Yu, J.-Q. Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance. J. Exp. Bot. 2015, 66, 2839–2856. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kanwar, M.K.; Bhardwaj, R.; Chowdhary, S.P.; Arora, P.; Sharma, P.; Kumar, S. Isolation and characterization of 24-Epibrassinolide from Brassica juncea L. and its effects on growth, Ni ion uptake, antioxidant defense of Brassica plants and in vitro cytotoxicity. Acta Physiol. Plant. 2012, 35, 1351–1362. [Google Scholar] [CrossRef]
- Sharma, A.; Thakur, S.; Kumar, V.; Kanwar, M.K.; Kesavan, A.K.; Thukral, A.K.; Bhardwaj, R.; Alam, P.; Ahmad, P. Pre-sowing Seed Treatment with 24-Epibrassinolide Ameliorates Pesticide Stress in Brassica juncea L. through the Modulation of Stress Markers. Front. Plant Sci. 2016, 7. [Google Scholar] [CrossRef] [PubMed]
- Sirhindi, G.; Kaur, H.; Bhardwaj, R.; Sharma, P.; Mushtaq, R. 28-Homobrassinolide potential for oxidative interface in Brassica juncea under temperature stress. Acta Physiol. Plant. 2017, 39, 228. [Google Scholar] [CrossRef]
- Ahanger, M.A.; Ashraf, M.; Bajguz, A.; Ahmad, P. Brassinosteroids Regulate Growth in Plants Under Stressful Environments and Crosstalk with Other Potential Phytohormones. J. Plant. Growth Regul. 2018, 37, 1007–1024. [Google Scholar] [CrossRef]
- Chen, T.H.; Murata, N. Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant. Cell Environ. 2011, 34, 1–20. [Google Scholar] [CrossRef]
- Lichtenthaler, H.K.; Wellburn, A.R. Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem. Soc. Trans. 1983, 11, 591–592. [Google Scholar] [CrossRef]
- Li, P.-M.; Cai, R.-G.; Gao, H.-Y.; Peng, T.; Wang, Z.-L. Partitioning of excitation energy in two wheat cultivars with different grain protein contents grown under three nitrogen applications in the field. Physiol. Plant. 2007, 129, 822–829. [Google Scholar] [CrossRef]
- Grieve, C.M.; Grattan, S.R. Rapid assay for determination of water soluble quaternary ammonium compounds. Plant. Soil 1983, 70, 303–307. [Google Scholar] [CrossRef]
- Velikova, V.; Yordanov, I.; Edreva, A. Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Plant. Sci. 2000, 151, 59–66. [Google Scholar] [CrossRef]
- Madhava Rao, K.V.; Sresty, T.V.S. Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan (L.) Millspaugh) in response to Zn and Ni stresses. Plant. Sci. 2000, 157, 113–128. [Google Scholar] [CrossRef]
- Dionisio-Sese, M.L.; Tobita, S. Antioxidant responses of rice seedlings to salinity stress. Plant. Sci. 1998, 135, 1–9. [Google Scholar] [CrossRef]
- Aebi, H. Catalase in vitro. In Methods Enzymol.; Colowick, S., Kaplan, N., Eds.; Elsevier: Gainesville, FL, USA, 1984; Volume 105, pp. 121–126. [Google Scholar]
- Nakano, Y.; Asada, K. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant. Cell Physiol. 1981, 22, 867–880. [Google Scholar]
- Foyer, C.H.; Halliwell, B. The presence of glutathione and glutathione reductase in chloroplasts: A proposed role in ascorbic acid metabolism. Planta 1976, 133, 21–25. [Google Scholar] [CrossRef]
- Miyake, C.; Asada, K. Thylakoid-bound ascorbate peroxidase in spinach chloroplasts and photoreduction of its primary oxidation product monodehydroascorbate radicals in thylakoids. Plant. Cell Physiol. 1992, 33, 541–553. [Google Scholar]
- Yu, J.Q. A role for brassinosteroids in the regulation of photosynthesis in Cucumis sativus. J. Exp. Bot. 2003, 55, 1135–1143. [Google Scholar] [CrossRef]
- Huang, C.; He, W.; Guo, J.; Chang, X.; Su, P.; Zhang, L. Increased sensitivity to salt stress in an ascorbate-deficient Arabidopsis mutant. J. Exp. Bot. 2005, 56, 3041–3049. [Google Scholar] [CrossRef] [Green Version]
- Wild, R.; Ooi, L.; Srikanth, V.; Münch, G. A quick, convenient and economical method for the reliable determination of methylglyoxal in millimolar concentrations: the N-acetyl-l-cysteine assay. Anal. Bioanal. Chem. 2012, 403, 2577–2581. [Google Scholar] [CrossRef] [PubMed]
- Hasanuzzaman, M.; Hossain, M.A.; Fujita, M. Nitric oxide modulates antioxidant defense and the methylglyoxal detoxification system and reduces salinity-induced damage of wheat seedlings. Plant. Biotechnol. Rep. 2011, 5, 353–365. [Google Scholar] [CrossRef]
- Principato, G.B.; Rosi, G.; Talesa, V.; Giovannini, E.; Norton, S.J. A Comparative Study on Glyoxalase II from Vertebrata. Enzyme 1987, 37, 164–168. [Google Scholar] [CrossRef] [PubMed]
- Chun, O.K.; Kim, D.-O.; Lee, C.Y. Superoxide Radical Scavenging Activity of the Major Polyphenols in Fresh Plums. J. Agric. Food Chem. 2003, 51, 8067–8072. [Google Scholar] [CrossRef] [PubMed]
- Zhishen, J.; Mengcheng, T.; Jianming, W. The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem. 1999, 64, 555–559. [Google Scholar] [CrossRef]
- Ahmad, P.; Hashem, A.; Abd-Allah, E.F.; Alqarawi, A.A.; John, R.; Egamberdieva, D.; Gucel, S. Role of Trichoderma harzianum in mitigating NaCl stress in Indian mustard (Brassica juncea L.) through antioxidative defense system. Front. Plant Sci. 2015, 6. [Google Scholar] [CrossRef]
- Mostofa, M.G.; Saegusa, D.; Fujita, M.; Tran, L.-S.P. Hydrogen Sulfide Regulates Salt Tolerance in Rice by Maintaining Na+/K+ Balance, Mineral Homeostasis and Oxidative Metabolism Under Excessive Salt Stress. Front. Plant Sci. 2015, 6. [Google Scholar] [CrossRef]
- Amirjani, M.R. Effect of Salinity Stress on Growth, Mineral Composition, Proline Content, Antioxidant Enzymes of Soybean. Am. J. Plant Physiol. 2010, 5, 350–360. [Google Scholar] [CrossRef]
- Ashraf, M.A.; Ashraf, M.; Ali, Q. Response of two genetically diverse wheat cultivars to salt stress at different growth stages: leaf lipid peroxidation and phenolic contents. Pak. J. Bot 2010, 42, 559–565. [Google Scholar]
- Ahmad, P.; Abdel Latef, A.A.; Hashem, A.; Abd_Allah, E.F.; Gucel, S.; Tran, L.-S.P. Nitric Oxide Mitigates Salt Stress by Regulating Levels of Osmolytes and Antioxidant Enzymes in Chickpea. Front. Plant Sci. 2016, 7. [Google Scholar] [CrossRef]
- Abbas, S.; Latif, H.; Elsherbiny, E.A. Effect of 24-epibrassinolide on the physiological and genetic changes on two varieties of pepper under salt stress conditions. Pak. J. Bot 2013, 45, 1273–1284. [Google Scholar]
- Shahid, M.; Pervez, M.; Balal, R.; Mattson, N.; Rashid, A.; Ahmad, R.; Ayyub, C.; Abbas, T. Brassinosteroid (24-Epibrassinolide) Enhances Growth and Alleviates the Deleterious Effects Induced by Salt Stress in Pea (‘Pisum sativum’ L.). Aust. J. Crop. Sci. 2011, 5, 500. [Google Scholar]
- Hayat, S.; Hasan, S.A.; Yusuf, M.; Hayat, Q.; Ahmad, A. Effect of 28-homobrassinolide on photosynthesis, fluorescence and antioxidant system in the presence or absence of salinity and temperature in Vigna radiata. Environ. Exp. Bot. 2010, 69, 105–112. [Google Scholar] [CrossRef]
- Cerana, R.; Bonetti, A.; Marre, M.T.; Romani, G.; Lado, P.; Marre, E. Effects of a brassinosteroid on growth and electrogenic proton extrusion in Azuki bean epicotyls. Physiol. Plant. 1983, 59, 23–27. [Google Scholar] [CrossRef]
- Ahmad, P.; Ahanger, M.A.; Egamberdieva, D.; Alam, P.; Alyemeni, M.N.; Ashraf, M. Modification of Osmolytes and Antioxidant Enzymes by 24-Epibrassinolide in Chickpea Seedlings Under Mercury (Hg) Toxicity. J. Plant. Growth Regul. 2017, 37, 309–322. [Google Scholar] [CrossRef]
- Neelam, S.; Subramanyam, R. Alteration of photochemistry and protein degradation of photosystem II from Chlamydomonas reinhardtii under high salt grown cells. J. Photochem. Photobiol. B: Biol. 2013, 124, 63–70. [Google Scholar] [CrossRef]
- Sun, S.; An, M.; Han, L.; Yin, S. Foliar application of 24-epibrassinolide improved salt stress tolerance of perennial ryegrass. HortScience 2015, 50, 1518–1523. [Google Scholar] [CrossRef]
- Li, X.-J.; Guo, X.; Zhou, Y.-H.; Shi, K.; Zhou, J.; Yu, J.-Q.; Xia, X.-J. Overexpression of a brassinosteroid biosynthetic gene Dwarf enhances photosynthetic capacity through activation of Calvin cycle enzymes in tomato. BMC Plant. Biol. 2016, 16, s12870–s13016. [Google Scholar] [CrossRef]
- Rahman, A.; Nahar, K.; Hasanuzzaman, M.; Fujita, M. Calcium Supplementation Improves Na+/K+ Ratio, Antioxidant Defense and Glyoxalase Systems in Salt-Stressed Rice Seedlings. Front. Plant Sci. 2016, 7. [Google Scholar] [CrossRef]
- Ali, B.; Hayat, S.; Ahmad, A. 28-Homobrassinolide ameliorates the saline stress in chickpea (Cicer arietinum L.). Environ. Exp. Bot. 2007, 59, 217–223. [Google Scholar] [CrossRef]
- Choudhary, S.P.; Kanwar, M.; Bhardwaj, R.; Yu, J.-Q.; Tran, L.-S.P. Chromium Stress Mitigation by Polyamine-Brassinosteroid Application Involves Phytohormonal and Physiological Strategies in Raphanus sativus L. PLoS ONE 2012, 7, e33210. [Google Scholar] [CrossRef] [PubMed]
- Gururani Mayank, A.; Venkatesh, J.; Tran, L.S.P. Regulation of Photosynthesis during Abiotic Stress-Induced Photoinhibition. Mol. Plant. 2015, 8, 1304–1320. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Choi, H.G.; Moon, B.Y.; Kang, N.J. Correlation between Strawberry (Fragaria ananassa Duch.) Productivity and Photosynthesis-Related Parameters under Various Growth Conditions. Front. Plant Sci. 2016, 7. [Google Scholar] [CrossRef] [PubMed]
- Wani, A.S.; Hayat, S.; Ahmad, A.; Tahir, I. Efficacy of brassinosteroid analogues in the mitigation of toxic effects of salt stress in Brassica juncea plants. J. Environ. Biol. 2017, 38, 27–36. [Google Scholar] [CrossRef]
- Wu, X.; Zhu, Z.; Li, X.; Zha, D. Effects of cytokinin on photosynthetic gas exchange, chlorophyll fluorescence parameters and antioxidative system in seedlings of eggplant (Solanum melongena L.) under salinity stress. Acta Physiol. Plant. 2012, 34, 2105–2114. [Google Scholar] [CrossRef]
- Lima, J.V.; Lobato, A.K.S. Brassinosteroids improve photosystem II efficiency, gas exchange, antioxidant enzymes and growth of cowpea plants exposed to water deficit. Physiol. Mol. Biol. Plants 2017, 23, 59–72. [Google Scholar] [CrossRef]
- Megdiche, W.; Hessini, K.; Gharbi, F.; Jaleel, C.A.; Ksouri, R.; Abdelly, C. Photosynthesis and photosystem 2 efficiency of two salt-adapted halophytic seashore Cakile maritima ecotypes. Photosynthetica 2008, 46, 410–419. [Google Scholar] [CrossRef]
- Shu, S.; Guo, S.-R.; Sun, J.; Yuan, L.-Y. Effects of salt stress on the structure and function of the photosynthetic apparatus in Cucumis sativus and its protection by exogenous putrescine. Physiol. Plant. 2012, 146, 285–296. [Google Scholar] [CrossRef]
- Fariduddin, Q.; Mir, B.A.; Yusuf, M.; Ahmad, A. 24-epibrassinolide and/or putrescine trigger physiological and biochemical responses for the salt stress mitigation in Cucumis sativus L. Photosynthetica 2014, 52, 464–474. [Google Scholar] [CrossRef]
- Fariduddin, Q.; Yusuf, M.; Ahmad, I.; Ahmad, A. Brassinosteroids and their role in response of plants to abiotic stresses. Biol. Plant. 2013, 58, 9–17. [Google Scholar] [CrossRef]
- Shahbaz, M.; Ashraf, M.; Athar, H.-u.-R. Does exogenous application of 24-epibrassinolide ameliorate salt induced growth inhibition in wheat (Triticum aestivum L.). Plant. Growth Regul. 2008, 55, 51–64. [Google Scholar] [CrossRef]
- Lu, Q.; Lu, C. Photosynthetic pigment composition and photosystem II photochemistry of wheat ears. Plant Physiol. Biochem. 2004, 42, 395–402. [Google Scholar] [CrossRef] [PubMed]
- Parveen, N.; Ashraf, M. Role of silicon in mitigating the adverse effects of salt stress on growth and photosynthetic attributes of two maize (Zea mays L.) cultivars grown hydroponically. Pak. J. Bot. 2010, 42, 1675–1684. [Google Scholar]
- Wang, S.; Liu, P.; Chen, D.; Yin, L.; Li, H.; Deng, X. Silicon enhanced salt tolerance by improving the root water uptake and decreasing the ion toxicity in cucumber. Front. Plant Sci. 2015, 6. [Google Scholar] [CrossRef] [PubMed]
- Mahmood, S.; Daur, I.; Al-Solaimani, S.G.; Ahmad, S.; Madkour, M.H.; Yasir, M.; Hirt, H.; Ali, S.; Ali, Z. Plant Growth Promoting Rhizobacteria and Silicon Synergistically Enhance Salinity Tolerance of Mung Bean. Front. Plant Sci. 2016, 7. [Google Scholar] [CrossRef] [PubMed]
- Hu, W.-H.; Yan, X.-H.; Xiao, Y.-A.; Zeng, J.-J.; Qi, H.-J.; Ogweno, J.O. 24-Epibrassinosteroid alleviate drought-induced inhibition of photosynthesis in Capsicum annuum. Sci. Hort. 2013, 150, 232–237. [Google Scholar] [CrossRef]
- Sinha, S.K.; Srivastava, H.S.; Tripathi, R.D. Influence of some growth regulators and cations on inhibition of chlorophyll biosynthesis by lead in maize. Bull. Environ. Contam. Toxicol. 1993, 51. [Google Scholar] [CrossRef]
- Iqbal, N.; Umar, S.; Khan, N.A. Nitrogen availability regulates proline and ethylene production and alleviates salinity stress in mustard (Brassica juncea). J. Plant Physiol. 2015, 178, 84–91. [Google Scholar] [CrossRef]
- Per, T.S.; Khan, N.A.; Reddy, P.S.; Masood, A.; Hasanuzzaman, M.; Khan, M.I.R.; Anjum, N.A. Approaches in modulating proline metabolism in plants for salt and drought stress tolerance: Phytohormones, mineral nutrients and transgenics. Plant Physiol. Biochem. 2017, 115, 126–140. [Google Scholar] [CrossRef]
- Khan, M.N.; Siddiqui, M.H.; Mohammad, F.; Naeem, M.; Khan, M.M.A. Calcium chloride and gibberellic acid protect linseed (Linum usitatissimum L.) from NaCl stress by inducing antioxidative defence system and osmoprotectant accumulation. Acta Physiol. Plant. 2010, 32, 121–132. [Google Scholar] [CrossRef]
- Ahmad, P.; Ozturk, M.; Sharma, S.; Gucel, S. Effect of sodium carbonate-induced salinity–alkalinity on some key osmoprotectants, protein profile, antioxidant enzymes, and lipid peroxidation in two mulberry (Morus alba L.) cultivars. J. Plant. Interact. 2014, 9, 460–467. [Google Scholar] [CrossRef]
- Hasanuzzaman, M.; Alam, M.M.; Rahman, A.; Hasanuzzaman, M.; Nahar, K.; Fujita, M. Exogenous Proline and Glycine Betaine Mediated Upregulation of Antioxidant Defense and Glyoxalase Systems Provides Better Protection against Salt-Induced Oxidative Stress in Two Rice (Oryza sativa L.) Varieties. BioMed Res. Int. 2014, 2014, 1–17. [Google Scholar] [CrossRef] [PubMed]
- Szabados, L.; Savouré, A. Proline: A multifunctional amino acid. Trends Plant. Sci. 2010, 15, 89–97. [Google Scholar] [CrossRef] [PubMed]
- Reddy, P.S.; Jogeswar, G.; Rasineni, G.K.; Maheswari, M.; Reddy, A.R.; Varshney, R.K.; Kavi Kishor, P.B. Proline over-accumulation alleviates salt stress and protects photosynthetic and antioxidant enzyme activities in transgenic sorghum [Sorghum bicolor (L.) Moench]. Plant Physiol. Biochem. 2015, 94, 104–113. [Google Scholar] [CrossRef] [PubMed]
- Bhaskara, G.B.; Yang, T.-H.; Verslues, P.E. Dynamic proline metabolism: importance and regulation in water limited environments. Front. Plant Sci. 2015, 6. [Google Scholar] [CrossRef] [PubMed]
- Chen, T.H.H.; Murata, N. Glycinebetaine: an effective protectant against abiotic stress in plants. Trends Plant Sci. 2008, 13, 499–505. [Google Scholar] [CrossRef]
- Ohnishi, N.; Murata, N. Glycinebetaine Counteracts the Inhibitory Effects of Salt Stress on the Degradation and Synthesis of D1 Protein during Photoinhibition in Synechococcus sp. PCC 7942. Plant Physiol. 2006, 141, 758–765. [Google Scholar] [CrossRef]
- Choudhary, S.P.; Kanwar, M.; Bhardwaj, R.; Gupta, B.D.; Gupta, R.K. Epibrassinolide ameliorates Cr (VI) stress via influencing the levels of indole-3-acetic acid, abscisic acid, polyamines and antioxidant system of radish seedlings. Chemosphere 2011, 84, 592–600. [Google Scholar] [CrossRef]
- Ramakrishna, B.; Rao, S.S.R. 24-Epibrassinolide alleviated zinc-induced oxidative stress in radish (Raphanus sativus L.) seedlings by enhancing antioxidative system. Plant. Growth Regul. 2012, 68, 249–259. [Google Scholar] [CrossRef]
- Yusuf, M.; Fariduddin, Q.; Khan, T.A.; Hayat, S. Epibrassinolide reverses the stress generated by combination of excess aluminum and salt in two wheat cultivars through altered proline metabolism and antioxidants. S. Afr. J. Bot. 2017, 112, 391–398. [Google Scholar] [CrossRef]
- Jaleel, C.A.; Gopi, R.; Sankar, B.; Manivannan, P.; Kishorekumar, A.; Sridharan, R.; Panneerselvam, R. Studies on germination, seedling vigour, lipid peroxidation and proline metabolism in Catharanthus roseus seedlings under salt stress. S. Afr. J. Bot. 2007, 73, 190–195. [Google Scholar] [CrossRef]
- Ali, B.; Hasan, S.A.; Hayat, S.; Hayat, Q.; Yadav, S.; Fariduddin, Q.; Ahmad, A. A role for brassinosteroids in the amelioration of aluminium stress through antioxidant system in mung bean (Vigna radiata L. Wilczek). Environ. Exp. Bot. 2008, 62, 153–159. [Google Scholar] [CrossRef]
- Siddiqui, H.; Hayat, S.; Bajguz, A. Regulation of photosynthesis by brassinosteroids in plants. Acta Physiol. Plant. 2018, 40, s11738–s12018. [Google Scholar] [CrossRef]
- Gao, H.; Zhang, Z.; Lv, X.; Cheng, N.; Peng, B.; Cao, W. Effect of 24-epibrassinolide on chilling injury of peach fruit in relation to phenolic and proline metabolisms. Postharvest Biol. Technol. 2016, 111, 390–397. [Google Scholar] [CrossRef]
- Zheng, Y.; Jia, A.; Ning, T.; Xu, J.; Li, Z.; Jiang, G. Potassium nitrate application alleviates sodium chloride stress in winter wheat cultivars differing in salt tolerance. J. Plant Physiol. 2008, 165, 1455–1465. [Google Scholar] [CrossRef]
- Ahmad, P.; Abdel Latef, A.A.; Abd_Allah, E.F.; Hashem, A.; Sarwat, M.; Anjum, N.A.; Gucel, S. Calcium and Potassium Supplementation Enhanced Growth, Osmolyte Secondary Metabolite Production, and Enzymatic Antioxidant Machinery in Cadmium-Exposed Chickpea (Cicer arietinum L.). Front. Plant Sci. 2016, 7. [Google Scholar] [CrossRef] [PubMed]
- Li, M.; Ahammed, G.J.; Li, C.; Bao, X.; Yu, J.; Huang, C.; Yin, H.; Zhou, J. Brassinosteroid Ameliorates Zinc Oxide Nanoparticles-Induced Oxidative Stress by Improving Antioxidant Potential and Redox Homeostasis in Tomato Seedling. Front. Plant Sci. 2016, 7. [Google Scholar] [CrossRef] [Green Version]
- Song, Y.L.; Dong, Y.J.; Tian, X.Y.; Kong, J.; Bai, X.Y.; Xu, L.L.; He, Z.L. Role of foliar application of 24-epibrassinolide in response of peanut seedlings to iron deficiency. Biol. Plant. 2016, 60, 329–342. [Google Scholar] [CrossRef]
- Manai, J.; Gouia, H.; Corpas, F.J. Redox and nitric oxide homeostasis are affected in tomato (Solanum lycopersicum) roots under salinity-induced oxidative stress. J. Plant Physiol. 2014, 171, 1028–1035. [Google Scholar] [CrossRef]
- Carvalho, L.C.; Vidigal, P.; Amancio, S. Oxidative stress homeostasis in grapevine (Vitis vinifera L.). Front. Environ. Sci. 2015, 3. [Google Scholar] [CrossRef]
- Shahbaz, M.; Ashraf, M. Influence of exogenous application of brassinosteroid on growth and mineral nutrients of wheat (Triticum aestivum L.) under saline conditions. Pak. J. Bot. 2007, 39, 513. [Google Scholar]
- Anuradha, S.; Rao, R.S. Application of brassinosteroids to rice seeds (Oryza sativa L.) reduced the impact of salt stress on growth, prevented photosynthetic pigment loss and increased nitrate reductase activity. Plant Growth Regul. 2003, 40, 29–32. [Google Scholar] [CrossRef]
- El-Mashad, A.A.A.; Mohamed, H.I. Brassinolide alleviates salt stress and increases antioxidant activity of cowpea plants (Vigna sinensis). Protoplasma 2011, 249, 625–635. [Google Scholar] [CrossRef]
- Çoban, Ö.; Göktürk Baydar, N. Brassinosteroid effects on some physical and biochemical properties and secondary metabolite accumulation in peppermint (Mentha piperita L.) under salt stress. Ind. Crops Prod. 2016, 86, 251–258. [Google Scholar] [CrossRef]
- Song, S.; Liu, W.; Guo, S.; Shang, Q.; Zhang, Z. Salt resistance and its mechanism of cucumber under effects of exogenous chemical activators. J. Appl. Ecol. 2006, 17, 1871–1876. [Google Scholar]
- Pandey, P.; Singh, J.; Achary, V.M.M.; Reddy, M.K. Redox homeostasis via gene families of ascorbate-glutathione pathway. Front. Environ. Sci. 2015, 3. [Google Scholar] [CrossRef] [Green Version]
- Raja, V.; Majeed, U.; Kang, H.; Andrabi, K.I.; John, R. Abiotic stress: Interplay between ROS, hormones and MAPKs. Environ. Exp. Bot. 2017, 137, 142–157. [Google Scholar] [CrossRef]
- Yuan, L.-Y.; Du, J.; Yuan, Y.-H.; Shu, S.; Sun, J.; Guo, S.-R. Effects of 24-epibrassinolide on ascorbate–glutathione cycle and polyamine levels in cucumber roots under Ca(NO3)2 stress. Acta Physiol. Plant. 2013, 35, 253–262. [Google Scholar] [CrossRef]
- Batth, R.; Singh, K.; Kumari, S.; Mustafiz, A. Transcript Profiling Reveals the Presence of Abiotic Stress and Developmental Stage Specific Ascorbate Oxidase Genes in Plants. Front. Plant Sci. 2017, 8. [Google Scholar] [CrossRef]
- Abd_Allah, E.F.; Alqarawi, A.A.; Hashem, A.; Wirth, S.; Egamberdieva, D. Regulatory roles of 24-epibrassinolide in tolerance of Acacia gerrardii Benth to salt stress. Bioengineered 2017, 9, 61–71. [Google Scholar] [CrossRef]
- Ahammed, G.J.; Choudhary, S.P.; Chen, S.; Xia, X.; Shi, K.; Zhou, Y.; Yu, J. Role of brassinosteroids in alleviation of phenanthrene–cadmium co-contamination-induced photosynthetic inhibition and oxidative stress in tomato. J. Exp. Bot. 2013, 64, 199–213. [Google Scholar] [CrossRef] [PubMed]
- Arora, P.; Bhardwaj, R.; Kanwar, M.K. 24-epibrassinolide regulated diminution of Cr metal toxicity in Brassica juncea L. plants. Braz. J. Plant. Phys. 2010, 22, 159–165. [Google Scholar] [CrossRef]
- Hossain, M.A.; Hossain, M.Z.; Fujita, M. Stress-induced changes of methylglyoxal level and glyoxalase I activity in pumpkin seedlings and cDNA cloning of glyoxalase I gene. Aust. J. Crop. Sci. 2009, 3, 53. [Google Scholar]
- Devanathan, S.; Erban, A.; Perez-Torres, R.; Kopka, J.; Makaroff, C.A. Arabidopsis thaliana Glyoxalase 2-1 Is Required during Abiotic Stress but Is Not Essential under Normal Plant Growth. PLoS ONE 2014, 9, e95971. [Google Scholar] [CrossRef] [PubMed]
- Hoque, T.S.; Hossain, M.A.; Mostofa, M.G.; Burritt, D.J.; Fujita, M.; Tran, L.-S.P. Methylglyoxal: An Emerging Signaling Molecule in Plant Abiotic Stress Responses and Tolerance. Front. Plant Sci. 2016, 7. [Google Scholar] [CrossRef]
- Kalapos, M.P.; Garzó, T.; Antoni, F.; Mandl, J. Accumulation of S-d-lactoylglutathione and transient decrease of glutathione level caused by methylglyoxal load in isolated hepatocytes. Biochim. Biophys. Acta 1992, 1135, 159–164. [Google Scholar] [CrossRef]
- Nahar, K.; Hasanuzzaman, M.; Alam, M.M.; Rahman, A.; Suzuki, T.; Fujita, M. Polyamine and nitric oxide crosstalk: Antagonistic effects on cadmium toxicity in mung bean plants through upregulating the metal detoxification, antioxidant defense and methylglyoxal detoxification systems. Ecotoxicol. Environ. Saf. 2016, 126, 245–255. [Google Scholar] [CrossRef]
- Upadhyaya, C.P.; Venkatesh, J.; Gururani, M.A.; Asnin, L.; Sharma, K.; Ajappala, H.; Park, S.W. Transgenic potato overproducing l-ascorbic acid resisted an increase in methylglyoxal under salinity stress via maintaining higher reduced glutathione level and glyoxalase enzyme activity. Biotechnol. Lett. 2011, 33, 2297–2307. [Google Scholar] [CrossRef]
- Jin, S.H.; Li, X.Q.; Wang, G.G.; Zhu, X.T. Brassinosteroids alleviate high-temperature injury in Ficus concinna seedlings via maintaining higher antioxidant defence and glyoxalase systems. AoB Plants 2015, 7. [Google Scholar] [CrossRef]
- Wahid, A.; Ghazanfar, A. Possible involvement of some secondary metabolites in salt tolerance of sugarcane. J. Plant Physiol. 2006, 163, 723–730. [Google Scholar] [CrossRef]
- Michalak, A. Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Polish J. Environ. Stud. 2006, 15, 523–530. [Google Scholar]
- Ben Abdallah, S.; Aung, B.; Amyot, L.; Lalin, I.; Lachâal, M.; Karray-Bouraoui, N.; Hannoufa, A. Salt stress (NaCl) affects plant growth and branch pathways of carotenoid and flavonoid biosyntheses in Solanum nigrum. Acta Physiol. Plant. 2016, 38, s11738–s12016. [Google Scholar] [CrossRef]
- Taïbi, K.; Taïbi, F.; Ait Abderrahim, L.; Ennajah, A.; Belkhodja, M.; Mulet, J.M. Effect of salt stress on growth, chlorophyll content, lipid peroxidation and antioxidant defence systems in Phaseolus vulgaris L. S. Afr. J. Bot. 2016, 105, 306–312. [Google Scholar] [CrossRef]
- Agati, G.; Biricolti, S.; Guidi, L.; Ferrini, F.; Fini, A.; Tattini, M. The biosynthesis of flavonoids is enhanced similarly by UV radiation and root zone salinity in L. vulgare leaves. J. Plant Physiol. 2011, 168, 204–212. [Google Scholar] [CrossRef] [PubMed]
- Nijveldt, R.J.; van Nood, E.; van Hoorn, D.E.C.; Boelens, P.G.; van Norren, K.; van Leeuwen, P.A.M. Flavonoids: a review of probable mechanisms of action and potential applications. Am. J. Clin. Nutr. 2001, 74, 418–425. [Google Scholar] [CrossRef] [PubMed]
- Potapovich, A.; Kostyuk, V. Comparative study of antioxidant properties and cytoprotective activity of flavonoids. Biochemistry (Moscow) 2003, 68, 514–519. [Google Scholar] [CrossRef] [PubMed]
- Raghu, K.; Rao, R. Effect of brassinosteroids on antioxidants content and radical scavenging activity of Tinospora cordifolia (Willd.) Miers ex Hook. F & Thoms. J. Med. Plants 2016, 4, 117–121. [Google Scholar]
- Li, X.; Ahammed, G.J.; Li, Z.-X.; Zhang, L.; Wei, J.-P.; Shen, C.; Yan, P.; Zhang, L.-P.; Han, W.-Y. Brassinosteroids Improve Quality of Summer Tea (Camellia sinensis L.) by Balancing Biosynthesis of Polyphenols and Amino Acids. Front. Plant Sci. 2016, 7. [Google Scholar] [CrossRef]
- Bartwal, A.; Mall, R.; Lohani, P.; Guru, S.K.; Arora, S. Role of Secondary Metabolites and Brassinosteroids in Plant Defense Against Environmental Stresses. J. Plant. Growth Regul. 2012, 32, 216–232. [Google Scholar] [CrossRef]
- Tomar, N.S.; Agarwal, R.M. Influence of Treatment of Jatropha curcas L. Leachates and Potassium on Growth and Phytochemical Constituents of Wheat ( Triticum aestivum L.). Am. J. Plant. Sci. 2013, 04, 1134–1150. [Google Scholar] [CrossRef]
- Mehr, Z.; Khajeh, H.; Bahabadi, S.E.; Sabbagh, S. Changes on proline, phenolic compounds and activity of antioxidant enzymes in Anethum graveolens L. under salt stress. Int. J. Agron. Plant Prod. 2012, 3, 710–715. [Google Scholar]
- Dawood, M.G.; EL-Awadi, M.E. Alleviation of salinity stress on Vicia faba L. plants via seed priming with melatonin. Acta Biol. Colomb. 2015, 20. [Google Scholar] [CrossRef]
- Bhattacharya, A.; Sood, P.; Citovsky, V. The roles of plant phenolics in defence and communication during Agrobacterium and Rhizobium infection. Mol. Plant Pathol. 2010. [Google Scholar] [CrossRef] [PubMed]
- De Leon, T.B.; Linscombe, S.; Gregorio, G.; Subudhi, P.K. Genetic variation in Southern USA rice genotypes for seedling salinity tolerance. Front. Plant Sci. 2015, 6. [Google Scholar] [CrossRef] [PubMed]
- Gu, M.; Li, N.; Shao, T.; Long, X.; Brestič, M.; Shao, H.; Li, J. Accumulation capacity of ions in cabbage (Brassica oleracea L.) supplied with sea water. Plant. Soil Environ. 2016, 62, 314–320. [Google Scholar]
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Alam, P.; Albalawi, T.H.; Altalayan, F.H.; Bakht, M.A.; Ahanger, M.A.; Raja, V.; Ashraf, M.; Ahmad, P. 24-Epibrassinolide (EBR) Confers Tolerance against NaCl Stress in Soybean Plants by Up-Regulating Antioxidant System, Ascorbate-Glutathione Cycle, and Glyoxalase System. Biomolecules 2019, 9, 640. https://doi.org/10.3390/biom9110640
Alam P, Albalawi TH, Altalayan FH, Bakht MA, Ahanger MA, Raja V, Ashraf M, Ahmad P. 24-Epibrassinolide (EBR) Confers Tolerance against NaCl Stress in Soybean Plants by Up-Regulating Antioxidant System, Ascorbate-Glutathione Cycle, and Glyoxalase System. Biomolecules. 2019; 9(11):640. https://doi.org/10.3390/biom9110640
Chicago/Turabian StyleAlam, Pravej, Thamer H. Albalawi, Fahad H. Altalayan, Md Afroz Bakht, Mohammad Abass Ahanger, Vaseem Raja, Muhammad Ashraf, and Parvaiz Ahmad. 2019. "24-Epibrassinolide (EBR) Confers Tolerance against NaCl Stress in Soybean Plants by Up-Regulating Antioxidant System, Ascorbate-Glutathione Cycle, and Glyoxalase System" Biomolecules 9, no. 11: 640. https://doi.org/10.3390/biom9110640