Advertisement

Environmental Science and Pollution Research

, Volume 22, Issue 15, pp 11349–11359 | Cite as

24-Epibrassinolide mitigates the adverse effects of manganese induced toxicity through improved antioxidant system and photosynthetic attributes in Brassica juncea

  • Qazi Fariduddin
  • Mumtaz Ahmed
  • Bilal A. Mir
  • Mohammad Yusuf
  • Tanveer A. Khan
Research Article

Abstract

The objective of this study was to establish relationship between manganese-induced toxicity and antioxidant system response in Brassica juncea plants and also to investigate whether brassinosteroids activate antioxidant system to confer tolerance to the plants affected with manganese induced oxidative stress. Brassica juncea plants were administered with 3, 6, or 9 mM manganese at 10-day stage for 3 days. At 31-day stage, the seedlings were sprayed with deionized water (control) or 10−8 M of 24-epibrassinolide, and plants were harvested at 45-day stage to assess growth, leaf gas-exchange traits, and biochemical parameters. The manganese treatments diminished growth along with photosynthetic attributes and carbonic anhydrase activity in the concentration-dependent manner, whereas it enhanced lipid peroxidation, electrolyte leakage, accumulation of H2O2 as well as proline, and various antioxidant enzymes in the leaves of Brassica juncea which were more pronounced at higher concentrations of manganese. However, the follow-up application of 24-epibrassinolide to the manganese stressed plants improved growth, water relations, and photosynthesis and further enhanced the various antioxidant enzymes viz. catalase, peroxidase, and superoxide dismutase and content of proline. The elevated level of antioxidant enzymes as well as proline could have conferred tolerance to the manganese-stressed plants resulting in improved growth and photosynthetic attributes.

Keywords

Manganese toxicity Brassinosteroids Photosynthesis Lipid peroxidation Antioxidant enzymes 

Notes

Acknowledgments

Financial assistance rendered by Council of Science and Technology, U.P. Lucknow, India in the form of Research Project [Project No. CST/D-615] is gratefully acknowledged by Qazi Fariduddin.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abou M, Symconidis L, Hatzistavrou E, Yupsanis T (2002) Nucleolytic activities and appearance of a new DNase in relation to nickel and manganese accumulation in Alyssum murale. J Plant Physiol 159:1087–1095CrossRefGoogle Scholar
  2. Alam M, Hayat S, Ali B, Ahmad A (2007) Effect of 28-homobrassinolide treatment on nickel toxicity in Brassica juncea. Photosynthetica 45:139–142CrossRefGoogle Scholar
  3. Ali B, Hasan SA, Hayat S, Yadav S, Fariduddin Q, Ahmad A (2008) A role of brassinosteroids in the amelioration of aluminium stress through antioxidants system in mungbean (Vigna radiata L. Wilczek). Environ Exp Bot 62:153–159CrossRefGoogle Scholar
  4. Alscher R, Donahue J, Cramer CL (1997) Reactive oxygen species and antioxidants: relationships in green cells. Physiol Plant 100:224–233CrossRefGoogle Scholar
  5. Anuradha S, Rao SSR (2007) The effect of brassinosteroids on radish (Raphanus sativus L.) seedlings growing under cadmium stress. Plant Soil Environ 53:465–472Google Scholar
  6. Bachman GR, Miller WB (1995) Iron chelate inducible iron/manganese toxicity in zonal geranium. J Plant Nutr 18:1917–1929CrossRefGoogle Scholar
  7. Barcelo J, Poschenreider C (1990) Plant water relations as affected by heavy metal stress: a review. J Plant Nutr 13:1–37CrossRefGoogle Scholar
  8. Bates LS, Waldeen RP, Teare ID (1973) Rapid determination of free proline water stress studies. Plant Soil 39:205–207CrossRefGoogle Scholar
  9. Beauchamp CO, Fridovich I (1971) Superoxide dismutase: improved assays and assays applicable to acrylamide gels. Ann Biochem 44:276–287CrossRefGoogle Scholar
  10. Bolwell GP (1999) Role of active oxygen species and NO in plant defence responses. Curr Opin Plant Biol 2:287–294CrossRefGoogle Scholar
  11. Boojar MMA, Goodarzi F (2008) Comparative evaluation of oxidative stress status and manganese availability in plants growing on manganese mine. Ecotoxicol Environ Saf 71:692–699CrossRefGoogle Scholar
  12. Buchanan BB, Gruissem W, Jones RL (2000) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville MDGoogle Scholar
  13. Campbell HW (1999) Nitrate reductase structure, function and regulation bridging the gap between biochemistry and physiology. Annu Rev Plant Physiol Plant Mol Biol 50:277–303CrossRefGoogle Scholar
  14. Catterou M (2001) Arabidopsis thaliana I. Molecular, cellular and physiological characterization of the Arabidopsis bull-1 mutant, defective in the 7-sterol-C5- desaturation step, leading to brassinosteroid biosynthesis. In: Dubois F, Schaller H, Aubanelle L, Vilcot B, Sangwan-Norrel B, Sangawan R (eds) Brassinosteroids, microtubules and cell elongation in Arabidopsis thaliana. Planta 212:659-672Google Scholar
  15. Chance B, Maehly AC (1956) Assay of catalase and peroxidases. Methods Enzymol 2:764–775CrossRefGoogle Scholar
  16. Chen CT, Chen TH, Lo KF, Chiu CY (2004) Effects of proline on copper transport in rice seedlings under excess copper stress. Plant Sci 166:103–111CrossRefGoogle Scholar
  17. Cho UH, Park JO (2000) Mercury-induced oxidative stress in tomato seedlings. Plant Sci 156:1–9CrossRefGoogle Scholar
  18. Choudhary SP, Kanwar M, Bhardwaj R, Yu JQ, Tran LSP (2012) Chromium stress mitigation by polyamine-brassinosteroid application involves phytohormonal and physiological strategies in Raphanus sativus L. PLoS ONE 7:e33210CrossRefGoogle Scholar
  19. Clouse SD, Sasse JM (1998) Brasisnosteroids: essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Biol 49:427–451CrossRefGoogle Scholar
  20. Demirevska K, Simova SL, Stoyanova Z, Holzer R, Feller U (2004) Biochemical changes in barley plants after excessive supply of copper and manganese. Environ Exp Bot 52:253–266CrossRefGoogle Scholar
  21. Dwivedi RS, Randhawa NS (1974) Evolution of a rapid test for the hidden hunger of zinc in plants. Plant Soil 40:445–451CrossRefGoogle Scholar
  22. Fariduddin Q, Yusuf M, Hayat S, Ahmad A (2009) Effect of 28 homobrassinolide on antioxidant capacity and photosynthesis in Brassica juncea plants exposed to copper. Environ Exp Bot 66:418–424CrossRefGoogle Scholar
  23. Fariduddin Q, Radwan RAEK, Mir BA, Yusuf M, Ahmad A (2013b) 24-Epibrassinolide regulates photosynthesis, antioxidant enzyme activities and proline content of Cucumis sativus under salt and/or copper stress. Environ Monit Assess 185:7845–7856CrossRefGoogle Scholar
  24. Fariduddin Q, Yusuf M, Ahmad I, Ahmad A (2014) Brassinosteroids and their role in response of plants to abiotic stresses. Biol Plant 58:9–17CrossRefGoogle Scholar
  25. Fecht-Christoffer MM, Maier P, Horst WJ (2003) Apoplastic peroxidises and ascorbate are involved in manganese toxicity and tolerance of Vigna unguiculata. Physiol Plant 117:237–244CrossRefGoogle Scholar
  26. Fuhrs H, Hartwig M, Buitrago L, Heintz D, Van Dorsselar A, Braun H, Horst W (2008) Early manganese toxicity response in Vigna radiata L. - a proteomic and transcriptomic study. Proteomics 8:149–159CrossRefGoogle Scholar
  27. Haag-Kerwer A, Schafer H, Heiss S, Walter C, Rausch T (1999) Cadmium exposure in Brassica juncea causes a decline in transpiration rate and leaf expansion without effect on photosynthesis. J Exp Bot 50:1827–1835CrossRefGoogle Scholar
  28. Halliwell B, Gutteridge J (1999) Free radicals in biology and medicine, 3rd edn. Oxford University Press, Oxford, p 936Google Scholar
  29. Hauck M, Paul A, Mulack C, Fritz E, Runge M (2002) Effects of manganese on the viability of vegetative diaspore of the epiphytic lichens Hypogymnia physodes. Environ Exp Bot 47:127–142CrossRefGoogle Scholar
  30. Hauck M, Paul A, Gross S, Raubuch M (2003) Manganese toxicity in epiphytic lichens: chlorophyll degradation and interaction with iron and phosphorus. Environ Exp Bot 49:81–191CrossRefGoogle Scholar
  31. Hayat S, Ali B, Hasan SA, Ahmad A (2007) Brassinosteroid enhanced the level of antioxidants under cadmiums tress in Brassica juncea. Environ Exp Bot 60:33–41CrossRefGoogle Scholar
  32. Hayat S, Yadav S, Wani AS, Irfan M, Ahmad A (2011) Comparative effect of 28-homobrassinolide and 24-epibrassinolide on the growth, carbonic anhydrase activity and photosynthetic efficiency of Lycopersicon esculentum. Photosynthetica 49:397–404CrossRefGoogle Scholar
  33. Hernandez LE, Carpena-Ruiz R, Garate A (1996) Alternation mineral nutrition of pea seedlings exposed to cadmium. J Plant Nutr 19:1581–1598CrossRefGoogle Scholar
  34. Hodges MD, De Long JM, Forney CF, Prange RK (1999) Improving the thiobutric acid reactive substances assay for lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611CrossRefGoogle Scholar
  35. Jain M, Mathur G, Koul S, Sarin NB (2001) Ameliorative effect of proline on the salt stress induced lipid peroxidation in cell lines of groundnut (Arachis hypogea L.). Plant Cell Rep 20:463–468CrossRefGoogle Scholar
  36. Kering MK (2008) Manganese nutrition and photosynthesis in NAD-malic enzymes C4 plants. Ph.D. Dissertation, University of MissouriGoogle Scholar
  37. Kim HJ, Bracey MH, Barlett SG (1994) Nucleotide sequence of a gene encoding carbonic anhydrase in Arabidopsis thaliana. Plant Physiol 105:449–450CrossRefGoogle Scholar
  38. Lei Y, Chen K, Tian X, Korpelainen H, Li C (2007) Effects of Mn toxicity on morphological and physiological changes in two Populus cathayama population originating from different habitats. Trees 21:569–580CrossRefGoogle Scholar
  39. Li Q, Chen LS, Jiang HX, Tang N, Yang LT, Lin ZH, Li Y, Yang GH (2010) Effects of manganese-excess on CO2 assimilation, ribulose-1,5-bisphosphate carboxylase/oxygenase, carbohydrates and photosynthetic electron transport of leaves, and antioxidant systems of leaves and roots in Citrus grandis seedlings. BMC Plant Biol 10:42CrossRefGoogle Scholar
  40. Lidon FC, Teixeira MG (2000a) Rice tolerance to excess Mn: implications in the chloroplast lamellae and synthesis of a novel Mn protein. Plant Physiol Biochem 38:969–978CrossRefGoogle Scholar
  41. Lidon FC, Teixeira MG (2000b) Oxyradicals production and control in the chloroplast of Mn treated rice. Plant Sci 152:7–15CrossRefGoogle Scholar
  42. Lidon FC, Barreiro M, Ramalho J (2004) Manganese accumulation in rice: implications for photosynthetic functioning. J Plant Physiol 161:1235–1244CrossRefGoogle Scholar
  43. Maheshwari R, Dubey RS (2009) Nickel induced oxidative stress and role of antioxidant defence in rice seedlings. Plant Growth Regul 59:37–49CrossRefGoogle Scholar
  44. Matysik J, Alia A, Bhalu B, Mohanty P (2002) Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Curr Sci 82:525–532Google Scholar
  45. Meharg AA (1993) The role of the plasmalemma in metal tolerance in angiosperms. Physiol Plant 88:191–198CrossRefGoogle Scholar
  46. Mora M, Rosas A, Ribera A, Rengel R (2009) Differential tolerance to Mn toxicity in perennial ryegrass genotypes: involvement of antioxidant enzymes and root exudation of carboxylates. Plant Soil 320:79–89CrossRefGoogle Scholar
  47. Moroni J, Scott B, Wratten N (2003) Differential tolerance of high manganese among rapeseed genotypes. Plant Soil 253:507–519CrossRefGoogle Scholar
  48. Obata H, Inone N, Umebayshi M (1996) Effect of cadmium on plasma membrane ATPase from plant root differing in tolerance to cadmium. Soil Sci Plant Nutr 42:361–366CrossRefGoogle Scholar
  49. Patterson BD, MacRae EA, Ferguson IB (1984) Estimation of hydrogen peroxide in plant extracts using titanium (IV). Anal Biochem 139:487–492Google Scholar
  50. Pendias K, Pendias H (1992) Trace elements in soils and plants. CRR Press, USA, p 365Google Scholar
  51. Poschenrieder C, Barcelo J (2004) Water relations in heavy metal stress plants. In: Prasad MNV (ed) Heavy metal stress in plants: from biomolecules to ecosystem. Narosa Publishing House, New Delhi, pp 249–270CrossRefGoogle Scholar
  52. Prasad MNV (1995) Cadmium toxicity and tolerance in vascular plants. Environ Exp Bot 35:525–545CrossRefGoogle Scholar
  53. Ramakrishna B, Rao SSR (2014) Foliar application of brassinosteroids alleviates adverse effects of zinc toxicity in radish (Raphanus sativus L.) plants. Protoplasma. doi: 10.1007/s00709-014-0714-0 Google Scholar
  54. Rengel Z (2000) Uptake and transport of manganese in plants. In: Sigel A, Sigel H (eds) Metals ion in biological systems. Marcel Dekker, New York, pp 58–87Google Scholar
  55. Rosas A, Rengtel Z, Mora M (2007) Manganese supply and pH influence growth, carboxylate exudation and peroxidise activity of ryegrass and white clover. J Plant Nutr 30:253–270CrossRefGoogle Scholar
  56. Sasse JM (2003) Physiological actions of brassinosteroids: an update. J Plant Growth Regul 22:276–288CrossRefGoogle Scholar
  57. Schlichting E, Sparrow LA (1988) Distribution and amelioration of manganese toxic soils. In: Webb MJ, Nable RO, Graham RD, Hanam RJ (eds) Manganese in Soils and Plants. Kluwer Academic Publishers, Dordrecht, pp 277–292. ISBN 90-247-3758-3CrossRefGoogle Scholar
  58. Sharma P, Dubey RS (2007) Involvement of oxidative stress and role of antioxidants defense system in growing rice seedlings exposed to toxic concentration of aluminium. Plant Cell Rep 26:2027–2038CrossRefGoogle Scholar
  59. Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot. doi: 10.1155/2012/217037 Google Scholar
  60. Shi QH, Zhu ZJ, He Y, Qian QQ, Yu JQ (2005) Silicon mediated alleviation of Mn toxicity in Cucumis sativus L; in relation to activities of superoxie dismutase and acerbate peroxidise. Phytochemistry 66:1551–1559CrossRefGoogle Scholar
  61. Shi QH, Zhu ZJ, Xu M, Qian QQ, Yu JQ (2006) Effects of excess manganese toxicity on the antioxidants system in Cucumis sativus L. under two light intensities. Environ Exp Bot 58:197–205CrossRefGoogle Scholar
  62. Srivastava S, Dubey RS (2011) Manganese excess induces oxidative stress, lowers the pool of antioxidants and elevates activities of key antioxidants enzymes in rice seedlings. Plant Growth Regul 64:1–16CrossRefGoogle Scholar
  63. Sullivan CY, Ross WM (1979) Selecting the drought and heat resistance in grain sorghum. In: Mussel H, Staples RC (eds) Stress physiology in crop plants. Wiley, New York, pp 263–281Google Scholar
  64. Wu S (1994) Effect of manganese excess on the soybean plant cultivated under various growth conditions. J Plant Nutr 17:993–1003Google Scholar
  65. Yu JQ, Huang LF, Hu WH, Zhou YH, Mao WH, Ye SF, Nogoes S (2004) A role of brassinosteroids in the regulations of photosynthesis in Cucumis sativus. J Exp Bot 55:1135–1143CrossRefGoogle Scholar
  66. Yusuf M, Fariduddin Q, Hayat S, Hasan SA, Ahmad A (2011) Protective response of 28-homobrassinolide in cultivars of Triticum aestivum with different levels of nickel. Arch Environ Contam Toxicol 60:68–76CrossRefGoogle Scholar
  67. 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 Physiol Biochem 57:143–153CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Qazi Fariduddin
    • 1
  • Mumtaz Ahmed
    • 1
  • Bilal A. Mir
    • 1
  • Mohammad Yusuf
    • 1
  • Tanveer A. Khan
    • 1
  1. 1.Plant Physiology and Biochemistry Section, Department of BotanyAligarh Muslim UniversityAligarhIndia

Personalised recommendations