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Interplay Between Antioxidant Enzymes and Brassinosteroids in Control of Plant Development and Stress Tolerance

  • Mohammad YusufEmail author
  • Qazi Fariduddin
  • Tanveer Alam Khan
  • Mohammad Faizan
  • Ahmad Faraz
Chapter

Abstract

Brassinosteroids (BRs) is a naturally occurring phytohormone of steroidal nature, which take part in the regulation of growth and development of plants through their life cycle. In the present era, availability of a larger number of biotic and abiotic factors restrict the gross production of principal crops. Handful of literature revealed that BRs play vital role in modulating the plant response to various abiotic stresses through alteration in the activities of antioxidant enzymes and proline metabolism by inducing expression of genes involved in defense and antioxidant responses in plants. This plant steroid also found to be very successful in mitigating the damage caused by the oxidative stress under varied unfavorable environmental conditions. These days most debatable part in the BRs research field is the molecular mechanisms associated with the enhanced activities of antioxidant enzymes and proline accumulation in plants under various developmental and environmental cues. Here, we will shed lights on the action mechanisms by which BRs enhanced the activities of antioxidant enzymes and proline accumulation under both stress and stress-free conditions and cross talk with other plant hormones. Therefore, understanding the physiological, biochemical and molecular aspects of BRs would help in developing abiotic stress tolerance in plants in a more significant manner.

Keywords

Abiotic stress Antioxidant system Brassinosteroids Plant Tolerance 

Notes

Acknowledgements

MY is very grateful to Chair, Biology Department, College of Science, UAE University, Al Ain, UAE for providing all the necessary facilities to compile this chapter.

References

  1. Abbas, S., Latif, H. H., & Elsherbiny, E. A. (2013). Effect of 24-epibrassinolide on the physiological and genetic changes on two varieties of pepper under salt stress conditions. Pakistan Journal of Botany, 45, 1273–1284.Google Scholar
  2. Aghdam, M. S., & Mohammadkhani, N. (2014). Enhancement of chilling stress tolerance of tomato fruit by postharvest brassinolide treatment. Food and Bioprocess Technology, 7, 909–914.CrossRefGoogle Scholar
  3. Akram, A. A., & Abdel-Fattah, R. I. (2006). Osmolytes-antioxidant behaviour in Phaseolus vulgaris and Hordeum vulgare with Brassinosteroid under salt stress. Journal of Agronomy, 5(1), 167–174.CrossRefGoogle Scholar
  4. Ali, B., Hayat, S., & Ahmad, A. (2007). 28-Homobrassinolide ameliorates the saline stress in Cicer arietinum L. Environmental and Experimental Botany, 59, 217–223.CrossRefGoogle Scholar
  5. Ali, B., Hayat, S., Fariduddin, Q., & Ahmad, A. (2008). 24-Epibrassinolide protects against the stress generated by salinity and nickel in Brassica juncea. Chemosphere, 72, 1387–1392.PubMedCrossRefGoogle Scholar
  6. Anjum, S. A., Wang, L. C., Farooq, M., Hussain, M., Xue, L. L., & Zou, C. M. (2011). Brassinolide application improves the drought tolerance in maize through modulation of enzymatic antioxidants and leaf gas exchange. Journal of Agronomy and Crop Science, 197, 177–185.CrossRefGoogle Scholar
  7. Anuradha, S., & Rao, S. S. R. (2001). Effect of brassinosteroids on salinity stress induced inhibition of germination and seedling growth of rice (Oryza sativa L.). Plant Growth Regulation, 33, 151–153.CrossRefGoogle Scholar
  8. Anuradha, S., & Rao, S. S. R. (2003). 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 Regulation, 40, 29–32.CrossRefGoogle Scholar
  9. Anuradha, S., & Rao, S. S. R. (2007). Effect of 24-epibrassinolide on the growth and antioxidant enzyme activities in radish seedlings under lead toxicity. Indian Journal of Plant Physiology, 12, 396–400.Google Scholar
  10. Arora, N., Bhardwaj, R., Sharma, P., & Arora, H. K. (2008). Effects of 28-homobrassinolide on growth, lipid peroxidation and antioxidative enzyme activities in seedlings of Zea mays L. under salinity stress. Acta Physiologiae Plantarum, 30, 833–839.CrossRefGoogle Scholar
  11. Arteca, R. N. (1995). In P. J. Davies (Ed.), Brassinosteroids in plant hormones: Physiology, biochemistry, and molecular biology (pp. 206–213). Dordrecht: Kluwer Academic Publishers.Google Scholar
  12. Bajguz, A. (2000). Effect of brassinosteroids on nucleic acid and protein content in cultured cell of Chlorella vulgaris. Plant Physiology and Biochemistry, 38, 209–215.CrossRefGoogle Scholar
  13. Bajguz, A. (2007). Metabolism of brassinosteroids in plants. Plant Physiology and Biochemistry, 45, 95–107.PubMedCrossRefGoogle Scholar
  14. Bajguz, A., & Hayat, S. (2009). Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiology and Biochemistry, 47, 1–8.PubMedCrossRefGoogle Scholar
  15. Bajguz, A., & Piotrowska-Niczyporuk, A. (2014). Interactive effect of brassinosteroids and cytokinins on growth, chlorophyll, monosaccharide and protein content in the green alga Chlorella vulgaris (Trebouxiophyceae). Plant Physiology and Biochemistry, 80, 176–183.PubMedCrossRefGoogle Scholar
  16. Cao, Y. Y., & Zhao, H. (2007). Protective roles of brassinolide in rice seedlings under heat stress. Zhongguo Shuidao Kexue (China Rice Science), 21, 525–529.Google Scholar
  17. Cao, S., Xu, Q., Cao, Y., Qian, K., An, K., Zhu, Y., Hu, B. Z., Zhao, H. F., & Kuai, B. K. (2005). Loss-of-function mutations in DET2 gene lead to an enhanced resistance to oxidative stress in Arabidopsis. Physiologia Plantarum, 123, 57–66.CrossRefGoogle Scholar
  18. Choudhary, S. P., Kanwar, M., Bhardwaj, R., Yu, J. Q., & Tran, L. S. (2012a). Chromium stress mitigation by polyamine–brassinosteroid application involves phytohormonal and physiological strategies in Raphanus sativus L. PLoS One, 7, 33210.CrossRefGoogle Scholar
  19. Choudhary, S. P., Yu, J. Q., Yamaguchi-Shinozaki, K., Shinozaki, K., & Tran, L. S. (2012b). Benefits of brassinosteroid crosstalk. Trends in Plant Science, 17, 594–605.PubMedCrossRefGoogle Scholar
  20. Clouse, S. D., & Sasse, J. M. (1998). Brassinosteroids: Essential regulators of plant growth and development. Annual Review of Plant Physiology and Plant Molecular Biology, 49, 427–451.PubMedCrossRefPubMedCentralGoogle Scholar
  21. Clouse, S. D., Langford, M., & McMorris, T. C. (1996). A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiology, 111, 671–678.PubMedPubMedCentralCrossRefGoogle Scholar
  22. Cui, J. X., Zhou, Y. H., Ding, J. G., Xia, X. J., Shi, K., Chen, S. C., Asami, T., Chen, Z., & Yu, J. Q. (2011). Role of nitric oxide in hydrogen peroxide-dependent induction of abiotic stress tolerance by brassinosteroids in cucumber. Plant, Cell & Environment, 34, 347–358.CrossRefGoogle Scholar
  23. De Vleesschauwer, D., Van Buyten, E., Satoh, K., Balidion, J., Mauleon, R., Choi, I. R., Vera-Cruz, C., Kikuchi, S., & Hofte, M. (2012). Brassinosteroids antagonize gibberellin– and salicylate-mediated root immunity in rice. Plant Physiology, 158, 1833–1846.PubMedPubMedCentralCrossRefGoogle Scholar
  24. Deng, X. G., Zhu, T., Zhang, D. W., & Lin, H. H. (2015). The alternative respiratory pathway is involved in brassinosteroid-induced environmental stress tolerance in Nicotiana benthamiana. Journal of Experimental Botany, 66, 6219–6232.PubMedPubMedCentralCrossRefGoogle Scholar
  25. Dhaubhadel, S., Chaundhary, S., Dobinson, K. F., & Krishna, P. (1999). Treatment with 24-epibrassinolide, a brassinosteroid, increases the basic thermotolerance of Brassica napus and tomato seedlings. Plant Molecular Biology, 40, 333–342.PubMedCrossRefGoogle Scholar
  26. Diener, A. C., Li, H., Zhou, W. X., Whoriskey, W. J., Nes, W. D., & Fink, G. R. (2000). Sterol methyltransferase 1 controls the level of cholesterol in plants. Plant Cell, 12, 853–870.PubMedPubMedCentralCrossRefGoogle Scholar
  27. Ding, H. D., Zhu, X. H., Zhu, Z. W., Yang, S. J., Zha, D. S., & Wu, X. X. (2012). Amelioration of salt-induced oxidative stress in eggplant by application of 24-epibrassinolide. Biologia Plantarum, 56, 767–770.CrossRefGoogle Scholar
  28. Divi, U. K., Rahman, T., & Krishna, P. (2010). Research article Brassinosteroid-mediated stress tolerance in Arabidopsis shows interactions with abscisic acid, ethylene and salicylic acid pathways. BMC Plant Biology, 10, 151.PubMedPubMedCentralCrossRefGoogle Scholar
  29. Duan, J. J., Lundgren, J. G., Naranjo, S., & Marvier, M. (2010). Extrapolating non-target risk of Bt crops from laboratory to field. Biology Letters, 6, 74–77.PubMedCrossRefGoogle Scholar
  30. Duan, Y., Shi, X., Li, S., Sun, X., & He, X. (2014). Nitrogen use efficiency as affected by phosphorus and potassium in long-term rice and wheat experiments. Journal of Integrative Agriculture, 13, 588–596.CrossRefGoogle Scholar
  31. El-Khallal, S. M., Hathout, T. A., Ashour, A. E. R. A., & Kerrit, A. A. A. (2009). Brassinolide and salicylic acid induced antioxidant enzymes, hormonal balance and protein profile of maize plants grown under salt stress. Research Journal of Agriculture and Biological Sciences, 5, 391–402.Google Scholar
  32. El-Mashad, A., & Mohamed, H. (2012). Brassinolide alleviates salt stress and increases antioxidant activity of cowpea plants (Vigna sinensis). Protoplasma, 249, 625–635.PubMedCrossRefGoogle Scholar
  33. Fariduddin, Q., Khanam, S., Hasan, S. A., Ali, B., Hayat, S., & Ahmad, A. (2009). Effect of 28-homobrassinolide on drought stress induced changes in photosynthesis and antioxidant system of Brassica juncea L. Acta Physiologiae Plantarum, 31, 889–897.CrossRefGoogle Scholar
  34. Fariduddin, Q., Yusuf, M., Chalkoo, S., Hayat, S., & Ahmad, A. (2011). 28-Homobrassinolide improves growth and photosynthesis in Cucumis sativus L. through an enhanced antioxidant system in the presence of chilling stress. Photosynthetica, 49, 55–64.CrossRefGoogle Scholar
  35. Fariduddin, Q., Khalil, R. R., Mir, B. A., Yusuf, M., & Ahmad, A. (2013). 24-Epibrassinolide regulates photosynthesis, antioxidant enzyme activities and proline content of Cucumis sativus under salt and/or copper stress. Environmental Monitoring and Assessment, 185, 7845–7856.PubMedCrossRefPubMedCentralGoogle Scholar
  36. Fariduddin, Q., Mir, B. A., Yusuf, M., & Ahmad, A. (2014). 24-epibrassinolide and/or putrescine trigger physiological and biochemical responses for the salt stress mitigation in Cucumis sativus L. Photosynthetica, 52, 464–474.CrossRefGoogle Scholar
  37. Fariduddin, Q., Ahmed, M., Mir, B. A., Yusuf, M., & Khan, T. A. (2015). 24-Epibrassinolide mitigates the adverse effects of manganese induced toxicity through improved antioxidant system and photosynthetic attributes in Brassica juncea. Environmental Science and Pollution Research, 22, 11349–11359.PubMedCrossRefGoogle Scholar
  38. Farooq, M., Wahid, A., Kobayashi, N., Fujita, D., & Basra, S. M. A. (2009). Plant drought stress: Effects, mechanisms and management. Agronomy for Sustainable Development, 29, 185–212.CrossRefGoogle Scholar
  39. Farooq, M., Wahid, A., Lee, D. J., Cheema, S. A., & Aziz, T. (2010). Comparative time course action of the foliar applied glycinebetaine, salicylic acid, nitrous oxide, brassinosteroids and spermine in improving drought resistance of rice. Journal of Agronomy and Crop Science, 196, 336–345.CrossRefGoogle Scholar
  40. Gendron, J. M., & Wang, Z. Y. (2007). Multiple mechanisms modulate brassinosteroid signaling. Current Opinion in Plant Biology, 10, 436–441.PubMedPubMedCentralCrossRefGoogle Scholar
  41. Goda, H., Shimada, Y., Asami, T., Fujioka, S., & Yoshida, S. (2002). Microarray analysis of brassinosteroid-regulated genes in Arabidopsis. Plant Physiology, 130, 1319–1334.PubMedPubMedCentralCrossRefGoogle Scholar
  42. Gomes, M. M. A. (2011). Physiological effects related to brassinosteroid application in plants. In S. Hayat & A. Ahmad (Eds.), Brassinosteroids: A class of plant hormones (pp. 193–242). Dordrecht: Springer.CrossRefGoogle Scholar
  43. Gomes, M. M. A., Torres Netto, A., Campostrini, E., Bressan-Smith, R., Zullo, M. A. T., Ferraz, T. M., Siqueira, L. N., Leal, N. R., & Nunez-Vazquez, M. (2013). Brassinosteroid analogue affects the senescence in two papaya genotypes submitted to drought stress. Theoretical and Experimental Plant Physiology, 25, 186–195.Google Scholar
  44. Gratao, P. L., Gomes-Junior, R. A., Delite, F. S., Lea, P. J., & Azevedo, R. A. (2006). Antioxidants stress responses of plants to cadmium. In N. A. Khan & Samiullah (Eds.), Cadmium toxicity and tolerance in plants (pp. 1–34). Oxford: Alpha Science International.Google Scholar
  45. Grove, M. D., Spencer, G. F., Rohwedder, W. K., Mandava, N., Worley, J. F., Warthen, J. D., Steffens, G. L., Flippen-Anderson, J. L., & Cook, J. C. (1979). Brassinolide, a plant growth-promoting steroid isolated from Brassica napus pollen. Nature, 281(5728), 216–217.CrossRefGoogle Scholar
  46. Hansen, M., Chae, H. S., & Kieber, J. (2009). Regulation of ACS protein stability by cytokinin and brassinosteroid. The Plant Journal, 57, 606–614.PubMedCrossRefPubMedCentralGoogle Scholar
  47. Hasan, S. A., Hayat, S., & Ahmad, A. (2011). Brassinosteroids protect photosynthetic machinery against the cadmium induced oxidative stress in two tomato cultivars. Chemosphere, 84, 1446–1451.PubMedCrossRefGoogle Scholar
  48. Hayat, S., Ali, B., Hasan, S. A., & Ahmad, A. (2007). Brassinosteroid enhanced the level of antioxidants under cadmium stress in Brassica juncea. Environmental and Experimental Botany, 60, 33–41.CrossRefGoogle Scholar
  49. Hayat, S., Hasan, S. A., Hayat, Q., & Ahmad, A. (2010). Brassinosteroids protect Lycopersicon esculentum from cadmium toxicity applied as shotgun approach. Protoplasma, 239, 3–14.PubMedCrossRefGoogle Scholar
  50. Hayat, S., Alyemini, M. N., & Hasan, S. A. (2012). Foliar application of brassinosteroids enhances yield and quality of Solanum lycopersicum under cadmium stress. Saudi Journal of Biological Sciences, 19, 325–335.PubMedPubMedCentralCrossRefGoogle Scholar
  51. Hayat, S., Khalique, G., Wani, A. S., Alyemeni, M. N., & Ahmad, A. (2014). Protection of growth in response to 28-homobrassinolide under the stress of cadmium and salinity in wheat. International Journal of Biological Macromolecules, 64, 130–136.PubMedCrossRefGoogle Scholar
  52. Houimli, S. I. M., Denden, M., & Mouhandes, B. D. (2010). Effects of 24-epibrassinolide on growth, chlorophyll, electrolyte leakage and proline by pepper plants under NaCl-stress. European Asian Journal of Biosciences, 4, 96–104.CrossRefGoogle Scholar
  53. Hu, Y. L., Hu, D. N., Xing, X. X., & Guo, X. M. (2011). Effects of different BRs treatments on growth of young forest in Camellia oleifera [J]. Nonwood Forest Research, 1, 10.Google Scholar
  54. Hu, W. H., Yan, X. H., Xiao, Y. A., Zeng, J. J., Qi, H. J., & Ogweno, J. O. (2013). 24-Epibrassinosteroid alleviate drought-induced inhibition of photosynthesis in Capsicum annuum. Scientia Horticulturae, 150, 232–237.CrossRefGoogle Scholar
  55. Jakubowska, D., & Janicka, M. (2017). The role of brassinosteroids in the regulation of the plasma membrane H+- ATPase and NADPH oxidase under cadmium stress. Plant Science: An International Journal of Experimental Botany, 264, 37–47.CrossRefGoogle Scholar
  56. Janeczko, A., Gullner, G., Skoczowski, A., Dubert, F., & Barna, B. (2007). Effects of brassinosteroid infiltration prior to cold treatment on ion leakage and pigment contents in rape leaves. Biologia Plantarum, 51, 355–358.CrossRefGoogle Scholar
  57. Jian, Y. P., Cheng, F., Zhou, Y. H., Xia, X. J., Shi, K., & Yu, J. Q. (2012). Interactive effects of CO2 enrichment and brassinosteroids on CO2 assimilation and photosynthetic electron transport in Cucumis sativus. Environmental and Experimental Botany, 75, 98–106.CrossRefGoogle Scholar
  58. Jiang, Y. P., Huang, L. F., Cheng, F., Zhou, Y. H., Xia, X. J., Mao, W. H., Shi, K., & Yu, J. Q. (2013). Brassinosteroids accelerate recovery of photosynthetic apparatus from cold stress by balancing the electron partitioning, carboxylation and redox homeostasis in cucumber. Physiologia Plantarum, 148, 133–145.PubMedCrossRefGoogle Scholar
  59. Kagale, S., Divi, U. K., Krochko, J. E., Keller, W. A., & Krishna, P. (2007). Brassinosteroids confer resistance to Arabidopsis thaliana and Brassica napus to a range of abiotic stresses. Planta, 225, 353–364.PubMedCrossRefGoogle Scholar
  60. Kanwar, M. K., Bhardwaj, R., Arora, P., Chowdhary, S. P., Sharma, P., & Kumar, S. (2012). Plant steroid hormones produced under Ni stress are involved in the regulation of metal uptake and oxidative stress in Brassica juncea L. Chemosphere, 86, 41–49.PubMedCrossRefGoogle Scholar
  61. Kanwar, M. K., Bhardwaj, R., Chowdhary, S. P., Arora, P., Sharma, P., & Kumar, S. (2013). 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 Physiologiae Plantarum, 35, 1351–1362.CrossRefGoogle Scholar
  62. Kapoor, D., Rattan, A., Gautam, V., Kapoor, N., & Bharadwaj, R. (2014). 24-Epibrassinolide mediated photosynthetic pigments and antioxidative defense systems of radish seedling under cadmium and mercury stress. Journal of Stress Physiology & Biochemistry, 10, 110–121.Google Scholar
  63. Khan, T. A., Fariduddin, Q., & Yusuf, M. (2015). Lycopersicon esculentum under low temperature stress: An approach toward enhanced antioxidants and yield. Environmental Science and Pollution Research, 22, 14178–14188.PubMedCrossRefGoogle Scholar
  64. Kim, T. W., Chang, S. C., Lee, J. S., Hwang, B., Takatsuto, S., Yokota, T., & Kim, S. K. (2004). Cytochrome P450-catalyzed brassinosteroid pathway activation through synthesis of castasterone in Phaseolus vulgaris. Phytochemistry, 65, 679–689.PubMedCrossRefPubMedCentralGoogle Scholar
  65. Kitanaga, Y., Jian, C., Hasegawa, M., Yazaki, J., Kishimoto, N., Kikuchi, S., Nukamura, H., Chikawa, H., Asami, T., Yoshida, S., Yamaguchi, I., & Suzuk, Y. (2006). Sequential regulation of gibberellin, brassinosteroid, and jasmonic acid biosynthesis occurs in rice coleoptiles to control the transcript levels of anti-microbial thionin genes. Bioscience, Biotechnology, and Biochemistry, 70, 2410–2419.PubMedCrossRefGoogle Scholar
  66. Kumar, M., Sirhindi, G., Bhardwaj, R., Kumar, S., & Jain, G. (2010). Effect of exogenous H2O2 on antioxidant enzymes of Brassica juncea L. seedlings in relation to 24-epibrassinolide under chilling stress. Indian Journal of Biochemistry & Biophysics, 47, 378–382.Google Scholar
  67. Kurepin, L. V., Qaderi, M. M., Back, T. G., Reid, D. M., & Pharis, R. P. (2008). A rapid effect of applied brassinolide on abscisic acid concentrations in Brassica napus leaf tissue subjected to short-term heat stress. Plant Growth Regulation, 55, 165–167.CrossRefGoogle Scholar
  68. Kutschera, U., & Wang, Z. Y. (2012). Brassinosteroid action in flowering plants: A Darwinian perspective. Journal of Experimental Botany, 63, 3511–3522.PubMedPubMedCentralCrossRefGoogle Scholar
  69. Lanza, M., Garcia-Ponce, B., Castrillo, G., Catrecha, P., Sauer, M., Rodriguez-Serrano, M., Paez-Garcia, A., Sanchez-Bermejo, T., T C M, Leo del Puerto, Y., Sandalio, L. M., Paz-Ares, J., & Leyva, A. (2012). Role of actin cytoskeleton in brassinosteroid signaling and in its integration with the auxin response in plants. Developmental Cell, 22, 1275–1285.PubMedCrossRefPubMedCentralGoogle Scholar
  70. Li, L., & Van Staden, J. (1998). Effects of plant growth regulators on drought resistance of two maize cultivars. South Afican Journal of Botany, 64, 116–120.CrossRefGoogle Scholar
  71. Li, J., Nagpal, P., Vitart, V., McMorris, T. C., & Chory, J. (1996). A role for brassinosteroids in light-dependent development of Arabidopsis. Science, 2721, 398–401.CrossRefGoogle Scholar
  72. Li, K. R., Wang, H. H., Han, G., Wang, Q. J., & Fan, J. (2008). Effects of brassinolide on the survival, growth and drought resistance of Robinia pseudoacacia seedlings under water-stress. New Forests, 35, 255–266.CrossRefGoogle Scholar
  73. Li, Y. H., Liu, Y. J., Xu, X. L., Jin, M., An, L. Z., & Zhang, H. (2012). Effect of 24-epibrassinolide on drought stress-induced changes in Chorispora bungeana. Biologia Plantarum, 56, 192–196.CrossRefGoogle Scholar
  74. Lin, D., Nagawa, S., Chen, J., Cao, L., Chen, X., Xu, T., Li, H., Dhonukshe, P., Yamamuro, C., Friml, J., Scheres, B., Fu, Y., & Yand, Z. (2012). A ROP GTPase-dependent auxin signaling pathway regulates the subcellular distribution of PIN2 in Arabidopsis roots. Current Biology, 22, 1319–1325.PubMedCrossRefGoogle Scholar
  75. Lindsey, K., Pullen, M. L., & Topping, J. F. (2003). Importance of plant sterols in pattern formation and hormone signaling. Trends in Plant Science, 8, 521–525.PubMedCrossRefPubMedCentralGoogle Scholar
  76. Liu, J. H., & Moriguchi, T. (2007). Changes in free polyamines titers and expression of polyamines biosynthesis genes during growth of peach in vitro callus. Cell Biology Morphology, 26, 125–131.Google Scholar
  77. Lu, X. M., & Yang, W. (2013). Alleviation effects of brassinolide on cucumber seedlings under NaCl stress. Ying Yong Sheng Tai Xue Bao, 24, 1409–1414.PubMedGoogle Scholar
  78. Mahesh, B., Parshavaneni, B., Ramakrishna, B., & Rao, S. S. R. (2013). Effect of brassinosteroids on germination and seedling growth of radish (Raphanus sativus L.) under PEG-6000 induced water stress. American Journal of Plant Sciences, 4, 2305–2313.CrossRefGoogle Scholar
  79. Marquardt, V., & Adam, G. (1991). Recent advances in brassinosteroid research. In H. Boerner, D. Martin, V. Sjut, H. J. Stan, & J. Stetter (Eds.), Chemistry of plant protection, herbicide resistance-brassinosteroids, gibberellins, plant growth regulators (Vol. 7, pp. 103–139). Berlin: Springer.CrossRefGoogle Scholar
  80. Mazorra, L. M., Nunez, M., Hechavarria, M., Coll, F., & Sanchez-Blanco, M. J. (2002). Influence of brassinosteroids on antioxidant enzymes activity in tomato under different temperatures. Biologia Plantarum, 45, 593–596.CrossRefGoogle Scholar
  81. Meudt, W. J. (1987). Investigations on the mechanism of the brassinosteroid response: VI. Effect of brassinolide on gravitropism of bean hypocotyls. Plant Physiology, 83, 195–198.PubMedPubMedCentralCrossRefGoogle Scholar
  82. Mitchell, J. W., Mandava, N., Worley, J. F., Plimmer, J. R., & Smith, M. V. (1970). Brassins: A new family of plant hormones from rape pollen. Nature, 225, 1065–1066.PubMedCrossRefGoogle Scholar
  83. Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science, 7, 405–410.PubMedCrossRefGoogle Scholar
  84. Mittler, R., Vanderauwera, S., Suzuki, N., Miller, G., Tognetti, V. B., Vandepoele, K., Gollery, M., Shulaev, V., & Van Breusegem, F. (2011). ROS signaling: The new wave. Trends in Plant Science, 16, 300–309.PubMedCrossRefGoogle Scholar
  85. Muday, G. K., Rahman, A., & Binder, B. M. (2012). Auxin and ethylene: Collaborators or competitors? Trends in Plant Science, 17, 181–195.PubMedCrossRefGoogle Scholar
  86. Mussig, C., Fischer, S., & Altamann, T. (2002). Brassinosteroid-regulated gene expression. Plant Physiology, 129, 1241–1251.PubMedPubMedCentralCrossRefGoogle Scholar
  87. Nahar, K., Kyndt, T., Hause, B., Höfte, M., & Gheysen, G. (2013). Brassinosteroids suppress rice defense against root-knot nematodes through antagonism with the jasmonate pathway. Molecular Plant-Microbe Interactions, 26, 106–115.PubMedCrossRefGoogle Scholar
  88. Nakashita, H., Yasuda, M., Nitta, T., Asami, T., Fujioka, S., Arai, Y., Sekimata, K., Takatsuto, S., Yamaguchi, I., & Yoshida, S. (2003). Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. The Plant Journal, 33, 887–898.PubMedCrossRefGoogle Scholar
  89. Nawaz, F., Naeem, M., Zulfiqar, B., Akram, A., Ashraf, M. Y., Raheel, M., Shabbir, R. N., Hussain, R. A., Anwar, I., & Aurangzaib, M. (2017). Understanding brassinosteroid-regulated mechanisms to improve stress tolerance in plants: A critical review. Environmental Science and Pollution Research International, 24, 15959–15975.PubMedCrossRefGoogle Scholar
  90. Nemhauser, J. L., Mockler, C. T., & Chory, J. (2004). Independency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biology, 2, 258.CrossRefGoogle Scholar
  91. Nie, W. F., Wang, M. M., Xia, X. J., Zhou, Y. H., Shi, K., Chen, Z. X., & Yu, J. Q. (2013). Silencing of tomato RBOH1 and MPK2 abolishes brassinosteroid-induced H2O2 generation and stress tolerance. Plant, Cell & Environment, 36, 789–803.CrossRefGoogle Scholar
  92. Nishiyama, A. (2012). NG2 cells (Polydendrocytes). Chapter 10. In H. Kettenmann & B. R. Ransom (Eds.), Neuroglia (3rd ed.). New York: Oxford University Press.Google Scholar
  93. Nunez, M., Mazzafera, P., Mazorra, L. M., Siqueira, W. J., & Zullo, M. A. T. (2003). Influence of a brassinosteroid analog on antioxidant enzymes in rice grown in culture medium with NaCl. Biologia Plantarum, 47, 67–70.CrossRefGoogle Scholar
  94. Ogweno, J. O., Song, X. S., Shi, K., Hu, W. H., Mao, W. H., Zhou, Y. H., Yu, J. Q., & Nogues, S. (2008). Brassinosteroids alleviate heat-induced inhibition of photosynthesis by increasing carboxylation efficiency and enhancing antioxidant systems in Lycopersicon esculentum. Journal of Plant Growth Regulation, 27, 49–57.CrossRefGoogle Scholar
  95. Ozdemir, F., Bor, M., Demiral, T., & Turkan, I. (2004). Effects of 24-epibrassinolide on seed germination, seedling growth, lipid peroxidation, proline content and antioxidative system of rice (Oryza sativa L.) under salinity stress. Plant Growth Regulation, 42, 203–211.CrossRefGoogle Scholar
  96. Qayyum, B., Shahbaz, M., & Akram, N. A. (2007). Interactive effect of foliar application of 24-epibrassinolide and root zone salinity on morpho-physiological attributes of wheat (Triticum aestivum L.). International Journal of Agriculture and Biology, 9, 584–589.Google Scholar
  97. Rady, M. M. (2011). Effect of 24-epibrassinolide on growth, yield, antioxidant system and cadmium content of bean (Phaseolus vulgaris L.) plants under salinity and cadmium stress. Scientia Horticulturae, 129, 232–237.CrossRefGoogle Scholar
  98. Rady, M. M., & Osman, A. S. (2012). Response of growth and antioxidative system of heavy metal contaminated tomato plants 24-epibrassinolide. African Journal of Agricultural Research, 7, 3249–3254.Google Scholar
  99. Raghu, K., Mahesh, K., Divya Sri, N., & Rao, S. S. R. (2014). Effect of brassinosteroids on the seed germination and seedling growth of radish (Raphanus sativus L.) under arsenic toxicity stress. International Journal of Development Research, 9, 1929–1933.Google Scholar
  100. Rajewska, I., Talarek, M., & Bajguz, A. (2016). Brassinosteroids and response of plants to heavy metal action. Frontiers in Plant Science, 7, 629.PubMedPubMedCentralCrossRefGoogle Scholar
  101. Ramakrishna, B., & Rao, S. S. R. (2013). Preliminary studies on the involvement of glutathione metabolism and redox status against zinc toxicity in radish seedlings by 28-homobrassinolide. Environmental and Experimental Botany, 96, 52–58.CrossRefGoogle Scholar
  102. Ren, C., Han, C., Peng, W., Huang, Y., Peng, Z., Xiong, X., Zhu, Q., Gao, B., & Xie, D. (2009). A leaky mutation in DWARF4 reveals an antagonistic role of brassinosteroid in the inhibition of root growth by jasmonate in Arabidopsis. Plant Physiology, 151, 1412–1420.PubMedPubMedCentralCrossRefGoogle Scholar
  103. Ruley, A. T., Sharma, N. C., & Sahi, S. V. (2004). Antioxidant defense in a lead accumulating plant, Sesbania drummondii. Plant Physiology and Biochemistry, 42, 899–906.PubMedCrossRefGoogle Scholar
  104. Saini, S., Sharma, I., & Pati, P. K. (2015). Versatile roles of brassinosteroid in plants in the context of its homoeostasis, signaling and crosstalk. Frontiers in Plant Science, 6, 950.PubMedPubMedCentralCrossRefGoogle Scholar
  105. Sasse, J. M. (1991). The case for brassinosteroids as endogenous plant hormones. In H. G. Cutler, T. Yokota, & G. Adam (Eds.), Brassinosteroids: Chemistry, bioactivity and applications (ACS Symposium Series) (Vol. 474, pp. 158–166). Washington, DC: American Chemical Society.CrossRefGoogle Scholar
  106. Savaliya, D. D., Mandavia, C. K., & Mandavia, M. K. (2013). Role of brassinolide on enzyme activities in groundnut under water deficit stress. Indian Journal of Agricultural Biochemistry, 26, 92–96.Google Scholar
  107. Saygideger, S., & Deniz, F. (2008). Effect of 24-epibrassinolide on biomass, growth and free proline concentration in Spirulina platensis (Cyanophyta) under NaCl stress. Plant Growth Regulation, 56, 219–223.CrossRefGoogle Scholar
  108. Shahbaz, M., Ashraf, M., & Athar, H. (2008). Does exogenous application of 24-epibrassinolide ameliorate salt induced growth inhibition in wheat (Triticum aestivum L.). Plant Growth Regulation, 55, 51–64.CrossRefGoogle Scholar
  109. Shang, Q., Song, S., Zhang, Z., & Guo, S. (2006). Exogenous brassinosteroid induced salt resistance of cucumber (Cucumis sativus L.) seedlings. Scientia Agricultura Sinica, 39, 1872–1877.Google Scholar
  110. Sharma, P., & Dubey, R. S. (2005). Modulation of nitrate reductase activity in rice seedlings under aluminium toxicity and water stress: Role of osmolytes as enzyme protectant. Journal of Plant Physiology, 162, 854–864.PubMedCrossRefGoogle Scholar
  111. Sharma, N., Hundal, G. S., Sharma, I., & Bharadwaj, R. (2012). Effect of 24-epibrssinolide on protein content and activities of glutathione-S-transferase and poly phenol oxidase in Raphanus sativus L. plants under cadmium and mercury metal stress. Terrestrial and Aquatic Toxicology, 6, 1–7.Google Scholar
  112. Sharma, I., Ching, E., Saini, S., Bhardwaj, R., & Pati, P. K. (2013). Exogenous application of brassinosteroid offers tolerance to salinity by altering stress responses in rice variety Pusa Basmati-1. Plant Physiology and Biochemistry, 69, 17–26.PubMedCrossRefPubMedCentralGoogle Scholar
  113. Shimada, Y., Goda, H., Nakamura, A., Takatsuto, S., Fujioka, S., & Yoshida, S. (2003). Organ-specific expression of brassinosteroid-biosynthetic genes and distribution of endogenous brassinosteroids in Arabidopsis. Plant Physiology, 131, 287–297.PubMedPubMedCentralCrossRefGoogle Scholar
  114. Simonovicova, M., Tamas, L., Huttova, J., & Mistrik, I. (2004). Effect of aluminum on oxidative stress related enzymes activities in barley roots. Biologia Plantarum, 48, 261–266.CrossRefGoogle Scholar
  115. Steber, C. M., & McCourt, P. (2001). A role for brassinosteroids in germination in Arabidopsis. Plant Physiology, 125, 76.CrossRefGoogle Scholar
  116. Szekeres, M., Nemeth, K., Koncz-kalman, Z., Mathur, J., Kauschmann, A., Altmann, T., Redei, G. P., Nagy, F., Schell, J., & Koncz, C. (1996). Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell, 851, 171–182.CrossRefGoogle Scholar
  117. Taiz, L., & Zeiger, E. (2006). Plant physiology (4th ed.). Sunderland: Sinauer Associates.Google Scholar
  118. Takahashi, T., & Kakehi, J. I. (2010). Polyamines: Ubiquitous polycations with unique roles in growth and stress responses. Annals of Botany, 105, 1–6.PubMedCrossRefGoogle Scholar
  119. Upreti, K. K., & Murti, G. S. R. (2004). Effects of brassinosteroids on growth, nodulation, phytohormone content and nitrogenase activity in French bean under water stress. Biologia Plantarum, 48, 407–411.CrossRefGoogle Scholar
  120. Vardhini, B. V. (2011). Studies on the effect of brassinolide on the antioxidative system of two varieties of sorghum grown in saline soils of Karaikal. Asian and Australasian Journal of Plant Science and Biotechnology, 5, 31–34.Google Scholar
  121. Vardhini, B. V., & Rao, S. S. R. (2003). Amelioration of osmotic stress by brassinosteroids on seed germination and seedling growth of three varieties of sorghum. Plant Growth Regulation, 41, 21–31.Google Scholar
  122. Vercruyssen, L., Gonzalez, N., Werner, T., Schmülling, T., & Inze, D. (2011). Combining enhanced root and shoot growth reveals cross talk between pathways that control plant organ size in Arabidopsis. Plant Physiology, 155, 1339–1352.PubMedPubMedCentralCrossRefGoogle Scholar
  123. Wang, Q., Lai, T. F., Qin, G. Z., & Tian, S. P. (2009). Response of jujube fruits to exogenous oxalic acid treatment based on proteomic analysis. Plant & Cell Physiology, 50, 230–242.CrossRefGoogle Scholar
  124. Wang, Q., Ding, T., Gao, L., Pang, J., & Yang, N. (2012). Effect of brassinolide on chilling injury of green bell pepper in storage. Scientia Horticulturae, 144, 195–200.CrossRefGoogle Scholar
  125. Wang, X. H., Shu, C., Li, H. Y., Hu, X. Q., & Wang, Y. X. (2014). Effects of 0.01% brassinolide solution application on yield of rice and its resistance to autumn low-temperature damage. Acta Agriculturae Jiangxi, 26, 36–38.Google Scholar
  126. Wani, A. S., Hayat, S., Ahmad, A., & Tahir, I. (2017). Efficacy of brassinosteroid analogues in the mitigation of toxic effects of salt stress in Brassica juncea plants. Journal of Environmental Botany, 38, 27–36.Google Scholar
  127. Werner, T., Nehnevajova, E., Kollmer, I., Novak, O., Strnad, M., Kramer, U., & Schmulling, T. (2010). Root-specific reduction of cytokinin causes enhanced root growth, drought tolerance, and leaf mineral enrichment in Arabidopsis and tobacco. Plant Cell, 22, 3905–3920.PubMedPubMedCentralCrossRefGoogle Scholar
  128. Wu, C. Y., Trieu, A., Radhakrishnan, P., Kwok, S. F., Harris, S., Zhang, K., Wang, J. L., Wan, J. M., Zhai, H. Q., Takatsuto, S., Matsumoto, S., Fujioka, S., Feldmann, K. A., & Pennell, R. I. (2008). Brassinosteroids regulate grain filling in rice. Plant Cell, 20, 2130–2145.PubMedPubMedCentralCrossRefGoogle Scholar
  129. Xi, Z., Wang, Z., Fang, Y., Hu, Z., Hu, Y., Deng, M., & Zhang, Z. (2013). Effects of 24- epibrassinolide on antioxidation defense and osmoregulation systems of young grapevines (V. vinifera L.) under chilling stress. Plant Growth Regulation, 71, 57–65.CrossRefGoogle Scholar
  130. Xia, X. J., Huang, L. F., Zhou, Y. H., Mao, W. H., Shi, K., Wu, J. X., Asami, T., Chen, Z., & Yu, J. Q. (2009). Brassinosteroids promote photosynthesis and growth by enhancing activation of Rubisco and expression of photosynthetic genes in Cucumis sativus. Planta, 230, 1185–1196.PubMedCrossRefGoogle Scholar
  131. Xia, X. J., Zhou, Y. H., Ding, J., Shi, K., Asami, T., Chen, Z., & Yu, J. Q. (2011). Induction of systemic stress tolerance by brassinosteroid in Cucumis sativus. The New Phytologist, 191, 706–720.PubMedCrossRefGoogle Scholar
  132. Xu, W., Bak, S., Decker, A., Paquette, S. M., Feyereisen, R., & Galbraith, D. W. (2002). Microarray-based analysis of gene expression in very large gene families: The cytochrome P450 gene super family of Arabidopsis thaliana. Gene, 272, 61–74.CrossRefGoogle Scholar
  133. Yan, J., Guan, L., Sun, Y., Zhu, Y., Liu, L., Lu, R., Jiang, M., Tan, M., & Zhang, A. (2015). Calcium and ZmCCaMK are involved in brassinosteroid-induced antioxidant defense in maize leaves. Plant & Cell Physiology, 56, 883–896.CrossRefGoogle Scholar
  134. Yu, J. Q., Zhou, Y. H., Huang, L. F., & Allen, D. J. (2002). Chill induced inhibition of photosynthesis: Genotype variation within Cucumis sativus. Plant & Cell Physiology, 43, 1182–1188.CrossRefGoogle Scholar
  135. Yuan, G. F., Jia, C. G., Li, Z., Sun, B., Zhang, L. P., Liu, N., & Wang, Q. M. (2010). Effect of brassinosteroids on drought resistance and abscisic acid concentration in tomato under water stress. Scientia Horticulturae, 126, 103–108.CrossRefGoogle Scholar
  136. Yuan, L. B., Peng, Z. H., Zhi, T. T., Zho, Z., Liu, Y., Zhu, Q., Xiong, X. Y., & Ren, C. M. (2015). Brassinosteroid enhances cytokinin-induced anthocyanin biosynthesis in Arabidopsis seedlings. Biologia Plantarum, 59, 99–105.CrossRefGoogle Scholar
  137. Yuldashev, R., Avalbaev, A., Bezrukova, M., Vysotskaya, L., Khripach, V., & Shakirova, F. (2012). Cytokinin oxidase is involved in the regulation of cytokinin content by 24-epibrassinolide in wheat seedlings. Plant Physiology and Biochemistry, 55, 1–6.PubMedCrossRefGoogle Scholar
  138. Yusuf, M., Fariduddin, Q., Hayat, S., Hasan, S. A., & Ahmad, A. (2011). Protective responses of 28 homobrassinolide in cultivars of Triticum aestivum with different levels of nickel. Archives of Environmental Contamination and Toxicology, 60, 68–76.PubMedCrossRefGoogle Scholar
  139. Yusuf, M., Fariduddin, Q., & Ahmad, A. (2012). 24-epibrassinolide modulates growth, nodulation, antioxidant system and osmolyte in tolerant and sensitive varieties of Vigna radiata under different levels of nickel: A shotgun approach. Plant Physiology and Biochemistry, 57, 143–153.PubMedCrossRefGoogle Scholar
  140. Yusuf, M., Fariduddin, Q., Ahmad, I., & Ahmad, A. (2014). Brassinosteroid-mediated evaluation of antioxidant system and nitrogen metabolism in two contrasting cultivars of Vigna radiata under different levels of nickel. Physiology and Molecular Biology of Plants, 20, 449–460.PubMedPubMedCentralCrossRefGoogle Scholar
  141. Yusuf, M., Fariduddin, Q., Khan, T. A., & Hayat, S. (2017a). Epibrassinolide reverses the stress generated by combination of excess aluminum and salt in two wheat cultivars through altered proline metabolism and antioxidants. South African Journal of Botany, 112, 391–398.CrossRefGoogle Scholar
  142. Yusuf, M., Khan, T. A., & Fariduddin, Q. (2017b). Brassinosteroids: Physiological roles and its signalling in plants. In M. Sarwat, A. Ahmad, M. Z. Abdin, & M. M. Ibrahim (Eds.), Stress signaling in plants: Genomics and proteomics perspective (Vol. 2, pp. 241–260). Berlin: Springer International Publishing.CrossRefGoogle Scholar
  143. Zhang, S., Hu, J., Zhang, Y., Xie, X. J., & Knapp, A. (2007). Seed priming with brassinolide improves lucerne (Medicago sativa L.) seed germination and seedling growth in relation to physiological changes under salinity stress. Australian Journal of Agricultural Research, 58, 811–815.CrossRefGoogle Scholar
  144. Zhang, M. C., Zhai, Z. X., Tian, X. L., Duan, L. S., & Li, Z. H. (2008). Brassinolide alleviated the adverse effect of water deficits on photosynthesis and the antioxidant of soybean (Glycine max L.). Plant Growth Regulation, 56, 257–264.CrossRefGoogle Scholar
  145. Zhang, J., Li, W., Xiang, T., Liu, Z., Laluk, K., Ding, X., Zou, Y., Gao, M., Zhang, X., Chen, S., Mengiste, T., Zhang, Y., & Zhou, J. M. (2010). Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host & Microbe, 7, 290–301.CrossRefGoogle Scholar
  146. Zhang, Y. P., Zhu, X. H., Ding, H. D., Yang, S. J., & Chen, Y. Y. (2013). Foliar application of 24-epibrassinolide alleviates high-temperature-induced inhibition of photosynthesis in seedlings of two melon cultivars. Photosynthetica, 51, 341–349.CrossRefGoogle Scholar
  147. Zhu, J. Y., Sae-Seaw, J., & Wang, Z. Y. (2013). Brassinosteroid signalling. Development, 140, 1615–1620.PubMedPubMedCentralCrossRefGoogle Scholar
  148. Zurek, D. M., & Clouse, S. D. (1994). Molecular cloning and characterization of a brassinosteroid-regulated gene from elongating soybean epicotyls. Plant Physiology, 104, 161–170.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Mohammad Yusuf
    • 1
    Email author
  • Qazi Fariduddin
    • 2
  • Tanveer Alam Khan
    • 3
  • Mohammad Faizan
    • 2
  • Ahmad Faraz
    • 2
  1. 1.Department of Biology, College of ScienceUnited Arab Emirates UniversityAl AinUAE
  2. 2.Plant Physiology Section, Department of BotanyAligarh Muslim UniversityAligarhIndia
  3. 3.Department of Physiology and Cell BiologyLeibniz Institute for Plant Genetics and Crop Plant ResearchGaterslebenGermany

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