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Hydrogen peroxide mediated tolerance to copper stress in the presence of 28-homobrassinolide in Vigna radiata

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Abstract

Hydrogen peroxide (H2O2) in minute quantity serves as a signalling molecule. However, the role of H2O2 in combination with brassinosteroids (stress regulators) in plants under toxic levels of copper, is poorly understood. With an aim to explore and elaborate their role in plants subjected to abiotic stress, the surface sterilized seeds of mung bean (Vigna radiata) were sown in earthen pots filled with soil and manure enriched with different levels of Cu2+ (50 or 100 mg kg−1 of soil) and allowed to grow under natural environmental conditions. At 15 and 20 days stage, the plants were sprayed with H2O2 (2.5 mM) and/or 28-homobrassinolide (HBL, 10−5 mM), respectively. At 45 days stage, the analysis of the plants revealed that the presence of copper in the soil caused a significant decrease in growth characteristics, activity of carbonic anhydrase and nitrate reductase, relative water content, chlorophyll content and the rate of photosynthesis whereas, the activity of antioxidant enzymes (catalase, peroxidase and superoxide dismutase) and the proline accumulation in leaves increased in Cu stressed plants. However, the exogenously applied HBL and/or H2O2, in the absence of Cu-stress strongly favoured the growth, photosynthetic parameters and also improved the activity of antioxidant enzymes and the proline content. Furthermore, the combined application of HBL and H2O2 to the foliage of the stressed plants neutralized the toxic impact of all copper regimes. Therefore, we are of the opinion that these chemicals somehow maintained the homeostasis of the metal in the plants that exhibit healthy growth.

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Abbreviations

ANOVA:

Analysis of variance

BRs:

Brassinosteroids

CA:

Carbonic anhydrase

CAT:

Catalase

DAS:

Day after sowing

HBL:

28-Homobrassinolide

H2O2 :

Hydrogen peroxide

IRGA:

Infra red gas analyser

C i :

Internal CO2 concentration

LSD:

Least significance difference

P N :

Net photosynthetic rate

NR:

Nitrate reductase

POX:

Peroxidase

ROS:

Reactive oxygen species

RuBisCO:

Ribulose 1,5-bisphosphate carboxylase

g s :

Stomatal conductance

SOD:

Superoxide dismutase

SPAD:

Soil plant analysis development

References

  • Alaoui-Sosse B, Genet P, Vinit-Dunand F, Toussaint ML, Epron D, Badot PM (2004) Effect of copper on growth in cucumber plants (Cucumis sativus) and its relationships with carbohydrate accumulation and changes in ion contents. Plant Sci 166:1213–1218

    Article  CAS  Google Scholar 

  • Ali MB, Hahn EJ, Paek KY (2005) Effects of temperature on oxidative stress defense systems, lipid peroxidation and lipoxygenase activity in Phalaenopsis. Plant Physiol Biochem 43:213–223

    Article  PubMed  CAS  Google Scholar 

  • Allen DJ, McKee IF, Farage PK, Baker NR (1997) Analysis of the limitation to CO2 assimilation on exposure of leaves of two Brassica napus cultivars to UV-B. Plant Cell Environ 20:633–640

    Article  CAS  Google Scholar 

  • Amjad H, Shafqat F, Nayyer I, Rubina A (2004) Influence of exogenous application of hydrogen peroxide on root and seedling growth on wheat (Triticum aestivum L.). Int J Agric Biol 6(2):366–369

    Google Scholar 

  • Andre CM, Larondelle Y, Evers D (2010) Dietary antioxidants and oxidative stress from a human and plant perspective: a review. Curr Nutr Food Sci 6:2–12

    Article  CAS  Google Scholar 

  • Ashfaque F, Khan MIR, Khan NA (2014) Exogenously applied H2O2 promotes proline accumulation, water relations, photosynthetic efficiency and growth of wheat (Triticum aestivum L.) under salt stress. Annu Res Rev Biol 4:105–120

    Article  Google Scholar 

  • Bajguz A (2000) Effect of brassinosteroids on nucleic acid and protein content in cultured cells of Chlorella vulgaris. Plant Physiol Biochem 38:209–215

    Article  CAS  Google Scholar 

  • Bajguz A, Hayat S (2009) Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiol Biochem 47:1–8

    Article  PubMed  CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare IW (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Beauchamp CO, Fridovich I (1971) Superoxide dismutase: improved assays and assays applicable to acrylamide gels. Ann Biochem 44:276–287

    Article  CAS  Google Scholar 

  • Bernel M, Ronel M, Ortega JM, Picorel R, Yruela I (2004) Copper effect on cytochrome b555 of photosystem II under photo inhibitory conditions. Physiol Plant 120:686–694

    Article  Google Scholar 

  • Boswell C, Sharma NC, Sahi SV (2002) Copper tolerance and accumulation potential of Chalamydomonas reinhardtii. Bull Environ Contam Toxicol 69:546–553

    Article  PubMed  CAS  Google Scholar 

  • Bright J, Desikan R, Hancock JT, Weir IS, Neill SJ (2006) ABA- induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J 45:113–122

    Article  PubMed  CAS  Google Scholar 

  • Campbell HW (1999) Nitrate reductase structure, function and regulation. Bridging the gap between biochemistry and physiology. Ann Rev Plant Physiol Plant Mol Biol 50:277–303

    Article  CAS  Google Scholar 

  • Cao S, Xu Q, Cao Y, Qian K, An K, Zhu Y, Binzeng H, Zhao H, Kuai B (2005) Loss-of-function mutations in DET2 gene lead to an enhanced resistance to oxidative stress in Arabidopsis. Plant Physiol 123:57–66

    Article  CAS  Google Scholar 

  • Carol RJ, Dolan L (2006) The role of reactive oxygen species in cell growth: lessons from root hairs. J Exp Bot 57:1829–1834

    Article  PubMed  CAS  Google Scholar 

  • Catterou M, Dubois F, Schaller H, Aubanella L, Vilcol B, Sangwan-Norrel BS, Sangwan RS (2001) Brassinosteroids microtubules and cell elongation in Arabidopsis thaliana. II. Effects of brassinosteroids on microtubules and cell elongation in the bull mutant. Planta 212:673–683

    Article  PubMed  CAS  Google Scholar 

  • Chance B, Maehly AC (1955) Assay of catalase and peroxidases. Methods Enzymol 2:764–775

    Article  Google Scholar 

  • Chen LM, Lin CC, Kao CH (2000) Copper toxicity in rice seedlings: changes in antioxidative enzyme activities, H2O2 level and cell wall peroxidase activity in roots. Bot Bull Acad Sci 41:99–103

    CAS  Google Scholar 

  • Chen XY, Ding X, Xu S, Wang R, Shen WB (2009) Endogenous hydrogen peroxide plays a positive role in the upregulation of hemeoxygenase and acclimation to oxidative stress in wheat seedling leaves. J Integr Plant Biol 51(10):951–960

    Article  PubMed  CAS  Google Scholar 

  • Clouse SD (2011) Brassinosteroid signal transduction: from receptor kinase activation to transcriptional networks regulating plant development. Plant Cell 23:1219–1230

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Deng XP, Cheng YJ, Wu XB, Kwak SS, Chen W, Eneji AE (2012) Exogenous hydrogen peroxide positively influences root growth and exogenous hydrogen peroxide positively influences root growth and metabolism in leaves of sweet potato seedlings. Aust J Crop Sci 6(11):1572–1578

    CAS  Google Scholar 

  • Devi SR, Prasad MNV (2005) Antioxidant capacity of Brassica juncea plants exposed to elevated levels of copper. Russ J Plant Physiol 52:205–208

    Article  CAS  Google Scholar 

  • Dunand C, Crevecoeur M, Penel C (2007) Distribution of superoxide and hydrogen peroxide in Arabidopsis root and their influence on root development: possible interaction with peroxidases. New Phytol 174:332–341

    Article  PubMed  CAS  Google Scholar 

  • Dwivedi RS, Randhawa NS (1974) Evaluation of rapid test for hidden hunger of zinc in plants. Plant Soil 40:445–451

    Article  CAS  Google Scholar 

  • Fariduddin Q, Yusuf M, Hayat Q, Ahmad A (2009) Effects of 28-homobrassinolide on antioxidant capacity and photosynthesis in Brassica juncea plants exposed to different levels of copper. Environ Exp Bot 66:418–424

    Article  CAS  Google Scholar 

  • Fariduddin Q, Shaista C, Yusuf M, Hayat S, Ahmad A (2011) 28-Homobrassinolide improves growth and photosynthesis in Cucumis sativus L. through enhanced antioxidant system in the presence of chilling stress. Photosynthetica 49(1):55–64

    Article  CAS  Google Scholar 

  • Fariduddin Q, Radwan RAEK, Mir BA, Yusuf M, Ahmad A (2013) 24-Epibrassinolide regulates photosynthesis, antioxidant enzyme activities and proline content of Cucumis sativus under salt and/or copper stress. Environ Monit Assess 185:7845–7856

    Article  PubMed  CAS  Google Scholar 

  • Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signalling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. BioEssays 28:1091–1101

    Article  PubMed  CAS  Google Scholar 

  • Gomez KA, Gomez AA (1984) Statistical procedures for agricultural research, 2nd edn. John Wiley and Sons, New York

    Google Scholar 

  • Gudesblat GE, Russinova E (2011) Plants grow on brassinosteroids. Curr Opin Plant Biol 14:530–537

    Article  PubMed  CAS  Google Scholar 

  • Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11

    Article  PubMed  CAS  Google Scholar 

  • Halliwell B, Gutteridge JMC (1984) Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem J 219:1–14

    PubMed  CAS  PubMed Central  Google Scholar 

  • Hamilton WE, Heckathorn SA (2001) Mitochondrial adaptations to NaCl complex I is protected by anti-oxidants and small heat shock proteins, whereas complex II is protected by proline and betanine. Plant Physiol 126:1266–1274

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hasan SA, Hayat S, Ali B, Ahmad A (2008) 28-Homobrassinolide protect chickpea (Cicer arietinum) from cadmium toxicity by stimulating antioxidant. Environ Pollut 151:60–66

    Article  PubMed  CAS  Google Scholar 

  • Haung K, Vitorello V (1996) Aluminium co-ordination to calmodulin: thermodynamic and kinetic aspects. Coord Chem Rev 149:113–124

    Article  Google Scholar 

  • Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signal Behav 7:1456–1466

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hernandez LE, Carpena-Ruiz R, Garate A (1996) Alteration mineral nutrition of pea seedlings exposed to cadmium. J Plant Nutr 19:1581–1598

    Article  CAS  Google Scholar 

  • Holmstrom KO, Somersalo S, Mandal A, Palva ET, Welin B (2000) Improved tolerance to salinity and low temperature in transgenic tobacco producing glycine betaine. J Exp Bot 51:177–185

    Article  PubMed  CAS  Google Scholar 

  • Hopkins WJ (1995) Physiology of plants under stress. In: Introduction to Plant Physiology. John Wiley & Sons Inc., New York, p 438

  • Huang CH, Kuo WY, Jinn TL (2012) Models for the mechanism for activating copper-zinc superoxide dismutase in the absence of the CCS Cu chaperone in Arabidopsis. Plant Signal Behav 7:428–430

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Jaworski EG (1971) Nitrate reductase assay in intact plant tissue. Biochem Biophys Res Commun 43:1274–1279

    Article  PubMed  CAS  Google Scholar 

  • Jayakumar K, Abdul Jaleel C, Vijayarengan P (2009) Effect of different concentrations of cobalt on pigment contents of soybean. Bot Res Int 2:153–156

    CAS  Google Scholar 

  • John R, Ahmad P, Gadgil K, Sharma S (2009) Heavy metal toxicity: effect on plant growth, biochemical parameters and metal accumulation by Brassica juncea L. Int J Plant Prod 3:65–76

    CAS  Google Scholar 

  • Khripach VA, Zhabinskii VN, Khripach NB (2003) New practical aspects of brassinosteroids and results of their 10 year agricultural use in Russia and Belarus. In: Hayat S, Ahmad A (eds) Brassinosteroid: bioactivity and crop productivity. Kluwer Academic Publ, Dordrecht, pp 189–230

    Chapter  Google Scholar 

  • Mai Y, Lin S, Zeng X, Ran R (1989) Effect of brassinolide on nitrate reductase activity in rice seedlings. Plant Physiol Commun 2:50–52

    Google Scholar 

  • Maksymiec W, Krupa Z (2007) Effects of methyl jasmonate and excess copper on root and leaf growth. Biol Plant 51:322–326

    Article  CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, London

    Google Scholar 

  • Matysik J, Alai Bhalu B, Mohanty P (2002) Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Curr Sci 82:525–532

    CAS  Google Scholar 

  • Meharg AA (1993) Integrated tolerance mechanism, constitutive and adaptive plant responses to elevated metal concentrations in the environment. Plant Cell Environ 17:989–993

    Article  Google Scholar 

  • Morillon R, Catterou M, Sangwan RS, Sangwan BS, Lassalles JP (2001) Brassinolide may control aquaporin activities in Arabidopsis thaliana. Planta 212:199–204

    Article  PubMed  CAS  Google Scholar 

  • Moskova I, Todorova D, Alexieva V, Ivanov S, Sergiev I (2009) Effect of exogenous hydrogen peroxide on enzymatic and non-enzymatic antioxidants in leaves of young pea plants treated with paraquat. Plant Growth Regul 57:193–202

    Article  CAS  Google Scholar 

  • Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421

    Article  PubMed  CAS  Google Scholar 

  • Murphy TM, Sung WW, Lin CH (2002) H2O2 treatment induces glutathione accumulation and chilling tolerance in mung bean. Funct Plant Biol 29:1081–1087

    Article  Google Scholar 

  • 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. J Plant 33:887–898

    Article  CAS  Google Scholar 

  • Obata H, Inoue N, Umebayashi M (1996) Effect of cadmium on plasma membrane ATPase from plant roots differing in tolerance to cadmium. Soil Sci Plant Nutr 42:361–366

    Article  CAS  Google Scholar 

  • Ogweno JO, Song XS, Shi K, Hu WH, Mao WH, Zhou YH, Yu JQ, Nogues S (2008) Brassinosteroids alleviate heat-Induced inhibition of photosynthesis by increasing carboxylation efficiency and enhancing antioxidant systems in Lycopersicon esculentum. J Plant Growth Regul 27:49–54

    Article  CAS  Google Scholar 

  • Quan LJ, Zhang B, Shi WW, Li HY (2008) Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network. J Integ Plant Biol 50:2–18

    Article  CAS  Google Scholar 

  • Rozentsvet OA, Viktor NN, Natalia FS (2012) The effect of copper ions on the lipid composition of subcellular membranes in Hydrilla verticillata Chemosphere 89:108–113

    CAS  Google Scholar 

  • Raven JA, Evans MCW, Korb RE (1999) The role of trace metals in photosynthetic electron transport in O2-evolving organisms. Photosynth Res 60:11–149

    Article  Google Scholar 

  • Ren D, Yang H, Zhang S (2002) Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis. J BiolChem 277:559–565

    CAS  Google Scholar 

  • Sakurai A, Yokota T, Clouse SD (1999) Brassinosteroids steroidal plant hormones. Springer, Tokyo

    Google Scholar 

  • Sharma P, Bhardwaj R (2007) Effects of 24-epibrassinolide on growth and metal uptake in Brassica juncea L. under copper metal stress. Acta Physiol Plant 29:259–263

    Article  CAS  Google Scholar 

  • Sharma P, Sardana V, Banga SS (2013) Salt tolerance of Indian mustard (Brassica juncea) at germination and early seedling growth. Environ Exp Biol 11:39–46

    Google Scholar 

  • Su GX, Zhang WH, Liu YL (2006) Involvement of hydrogen peroxide generated by polyamine oxidative degradation in the development of lateral roots in soybean. J Integr Plant Biol 48:426–432

    Article  CAS  Google Scholar 

  • Swarna K, Bhanumathi G, Vijaya BRT, Murthy SDS (2012) Copper stress induced alterations in the primary photosynthetic processes of maize leaves. Int J Plant Ani Environ Sci 2:121–124

    CAS  Google Scholar 

  • Thounaojam TC, Panda P, Mazumdar P, Kumar D, Sharma GD, Sahoo L (2012) Excess copper induced oxidative stress and response of antioxidants in rice. Plant Physiol Biochem 53:33–39

    Article  PubMed  CAS  Google Scholar 

  • Torres MA, Jones JDG, Dangl JL (2006) Reactive oxygen species signalling in response to pathogens. Plant Physiol 141:373–378

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Van Breusegem F, Dat JF (2006) Reactive oxygen species in plant cell death. Plant Physiol 141:384–390

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Li JL, Wang JZ, Li ZK (2010) Exogenous H2O2 improves the chilling tolerance of manila grass and mascaren grass by activating the antioxidative system. Plant Growth Regul 61(2):195–204

    Article  CAS  Google Scholar 

  • Xia XJ, Wang YJ, Zhou YH, Tao Y, Mao WH, Shi K, Asami T, Chen ZX, Yu JQ (2009) Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiol 150:801–814

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Xiao Z, Dong FC, Gao JF, Song CP (2001) Hydrogen peroxide induced changes in intracellular pH of guard cells precede stomatal closure. Cell Res 11:37–43

    Article  Google Scholar 

  • Yang CJ, Zhang C, Lu YN, Jin JQ, Wang XL (2011) The mechanisms of brassinosteroids action: from signal transduction to plant development. Mol Plant 4:588–600

    Article  PubMed  CAS  Google Scholar 

  • Yruela I (2005) Copper in plants. Braz J Plant Physiol 17:145–156

    Article  CAS  Google Scholar 

  • Yruela I (2009) Copper in plants: acquisition, transport and interactions. Funct Plant Biol 36:409–430

    Article  CAS  Google Scholar 

  • Yu M, Hu CX, Wang YH (2002) Molybdenum efficiency in winter wheat cultivars as related to molybdenum uptake and distribution. Plant Soil 245:287–293

    Article  CAS  Google Scholar 

  • Yu JQ, Huang LF, Hu WH, Zhou YH, Mao WH, Ye SF, Nogues S (2004) A role of brassinosteroids in the regulation of photosynthesis in Cucumissativus. J Exp Bot 55:1135–1143

    Article  PubMed  CAS  Google Scholar 

  • Yu CW, Murphy TM, Lin CH (2003) Hydrogen peroxide-induced chilling tolerance in mung beans mediated through ABA-independent glutathione accumulation. Funct Plant Biol 30:955–963

    Article  CAS  Google Scholar 

  • Yusuf M, Fariduddin Q, Ahmad A (2011) 28-Homobrassinolide mitigates boron induced toxicity through enhanced antioxidant system in Vigna radiata plants. Chemosphere 85:1574–1584

    Article  PubMed  CAS  Google Scholar 

  • 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 57:143–153

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

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

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  1. Plant Physiology and Biochemistry Section, Department of Botany, Aligarh Muslim University, Aligarh, 202002, India

    Qazi Fariduddin, Tanveer A. Khan & M. Yusuf

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  1. Qazi Fariduddin
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  2. Tanveer A. Khan
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Correspondence to Qazi Fariduddin.

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Communicated by H. Li.

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Fariduddin, Q., Khan, T.A. & Yusuf, M. Hydrogen peroxide mediated tolerance to copper stress in the presence of 28-homobrassinolide in Vigna radiata . Acta Physiol Plant 36, 2767–2778 (2014). https://doi.org/10.1007/s11738-014-1647-0

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