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Protective effect of Mn(III)–desferrioxamine B upon oxidative stress caused by ozone and acid rain in the Brazilian soybean cultivar Glycine max “Sambaiba”

Abstract

This study aimed to investigate the effects of the Mn complex (Mn(III)–desferrioxamine B (MnDFB)) on oxidative stress in the Brazilian soybean cultivar Glycine max “Sambaiba” following exposure to ozone and acid rain. We determined the suitable dose of MnDFB to apply to G. max seedlings using a dose–response curve. The highest superoxide dismutase (SOD) activity and Mn content in leaves were found upon the application of 8 μM MnDFB. Thus, G. max seedlings pretreated with 8 μM MnDFB were individually exposed to ozone and acid rain simulated. Pretreatment with MnDFB reduced lipid peroxidation upon ozone exposure and increased SOD activity in leaves; it did not alter the metal content in any part of the plant. Conversely, following acid rain exposure, neither the metal content in leaves nor SOD enzyme activity were directly affected by MnDFB, unlike pH. Our findings demonstrated that exogenous MnDFB application before ozone exposure may modulate the MnSOD, Cu/ZnSOD, and FeSOD activities to combat the ROS excess in the cell. Here, we demonstrated that the applied dose of MnDFB enhances antioxidative defenses in soybean following exposure to acid rain and especially to ozone.

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References

  • Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341

    Article  CAS  Google Scholar 

  • Azevedo RA, Alas RM, Smith RJ, Lea PJ (1998) Response of antioxidant enzymes to transfer from elevated carbon dioxide to air and ozone fumigation, in the leaves and roots of wild-type and a catalase-deficient mutant of barley. Physiol Plant 104:280–292

    Article  CAS  Google Scholar 

  • Baier M, Kandlbinder A, Golldack D, Dietz KJ (2005) Oxidative stress and ozone: perception, signaling and response. Plant Cell Environ 28:1012–1020

    Article  CAS  Google Scholar 

  • Benite AMCB, Machado SP (2002) Sideróforos: uma resposta dos microorganismos. Quim Nova 25:1155–1164

    Article  CAS  Google Scholar 

  • Boukhalfa H, Crumbliss AL (2002) Chemical aspects of siderophore mediated iron transport. BioMetals 15:325–339

    Article  CAS  Google Scholar 

  • Bradford MM (1976) Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Bulbovas P, Souza SR, Esposito JBN, Moraes RM, Alves ES, Domingos M, Azevedo RA (2014) Assessment of the ozone tolerance of two soybean cultivars (Glycine max cv. Sambaíba and Tracajá) cultivated in Amazonian areas. Environ Sci Pollut Res. doi:10.1007/s11356-014-2934-4

    Google Scholar 

  • Castagna A, Ranieri A (2009) Detoxification and repair process of ozone injury: from O3 uptake to gene expression adjustment. Environ Pollut 157:1461–1469

    Article  CAS  Google Scholar 

  • Chernikova T, Robinson JM, Lee EH, Mulchi CL (2000) Ozone tolerance and antioxidant enzyme activity in soybean cultivars. Photosynth Res 64:15–26

    Article  CAS  Google Scholar 

  • Cia MC, Guimarães ACR, Medici LO, Chabregas SM, Azevedo RA (2012) Antioxidant response to water deficit by drought-tolerant and sensitive sugarcane varieties. Ann Appl Biol 161:313–324

    Article  CAS  Google Scholar 

  • Culotta VC (2001) Superoxide dismutase, oxidative stress, and cell metabolism. Curr Top Cell Regul 36:117–132

    Article  Google Scholar 

  • Dias APL, Dafré M, Rinaldi MCS, Domingos M (2011) How the redox state of tobacco ‘Bel-W3’ is modified in response to ozone and other environmental factors in a sub-tropical area? Environ Pollut 159:458–465

    Article  CAS  Google Scholar 

  • Dolatabadian A, Sanavy SAM, Gholamhoseini M, Joghan AK, Majdi M, Kashkooli AB (2013) The role of calcium in improving photosynthesis and related physiological and biochemical attributes of spring wheat subjected to simulated acid rain. Physiol Mol Biol Plants 19:189–198

    Article  CAS  Google Scholar 

  • Dučić T, Polle A (2005) Transport and detoxification of manganese and copper in plants. Braz J Plant Physiol 17:103–112

    Article  Google Scholar 

  • Faulkner KM, Stevens RD, Fridovich I (1994) Characterization of Mn(III) complexes of linear and cyclic desferrioxamines as mimics of superoxide dismutase activity. Arch Biochem Biophys 310:341–346

    Article  CAS  Google Scholar 

  • Fehr WR, Caviness CE, Burmood DT, Pennington JS (1971) Stage of development descriptions for soybeans, Glycine Max (L.) Merrill. Crop Sci 11:929–931

    Article  Google Scholar 

  • Ferreira RR, Fornazier RF, Vitória AP, Lea PJ, Azevedo RA (2002) Changes in antioxidant enzyme activities in soybean under cadmium stress. J Plant Nutr 25:327–342

    Article  CAS  Google Scholar 

  • Foyer CH, Noctor G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071

    Article  CAS  Google Scholar 

  • Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18

    Article  CAS  Google Scholar 

  • Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155:93–100

    Article  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  Google Scholar 

  • González-Fernández I, Calvo E, Gerosa G, Bermejo V, Marzuoli R, Calatayud V, Alonso R (2014) Setting ozone critical levels for protecting horticultural Mediterranean crops: case study of tomato. Environ Pollut 185:178–187

    Article  Google Scholar 

  • Gratão PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal-stressed plants a little easier. Funct Plant Biol 32:481–494

    Article  Google Scholar 

  • Hahn SM, Krishna CM, Samuni A, Mitchell JB, Russo A (1991) Mn(III)-Desferrioxamine superoxide dismutase-mimic: alternatives modes of action. Arch Biochem Biophys 288:215–219

    Article  CAS  Google Scholar 

  • Halliwell B, Gutteridge JMC (2007) Free radicals in biology and medicine. Oxford University Press, New York

    Google Scholar 

  • Hannam RJ, Ohki K (1988) Detection of manganese deficiency and toxicity in plants. In: Graham RD (ed) Manganese in soils and plants. The Netherlands, Dordrecht, pp 344–348

    Google Scholar 

  • Haydon MJ, Cobbett CS (2007) Transporters of ligants for essential metal ions in plants. New Phytol 174:499–506

    Article  CAS  Google Scholar 

  • Hodges M, DeLong JM, Forney CF, Prange RK (1998) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611

    Article  Google Scholar 

  • Inubushi K, Cheng W, Aonuma S, Hoque MM, Kobayashi K, Miura S, Kim HY, Okadas M (2003) Effects of free-air CO2 enrichment (FACE) on CH4 emission from a rice paddy field. Glob Chang Biol 9:1458–1464

    Article  Google Scholar 

  • Izaguirre-Mayoral ML, Sinclair TR (2005) Soybean genotypic difference in growth, nutrient accumulation and ultrastructure in response to manganese and iron supply in solution culture. Ann Bot 96:149–158

    Article  CAS  Google Scholar 

  • Keaney M, Matthussens F, Sharpe M, Vanfleteren J, Gems D (2004) Superoxide dismutase mimetics elevate superoxide dismutase activity in vivo but do not retard ageing in the nematode Caenorhabditis elegans. Free Radical Biol Med 37:239–250

    Article  CAS  Google Scholar 

  • Kwon SY, Jeong YJ, Lee HS, Kim JS, Cho KY, Allen RD, Kwak SS (2002) Enhanced tolerances of transgenic tobacco plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against methyl viologen-mediated oxidative stress. Plant Cell Environ 25:873–882

    Article  Google Scholar 

  • Lavras-Junior J, Reis RA, Rossi ML, Cabral CP, Nogueira NL, Malavolta E (2010) Changes in the ultrastructure of soybean cultivars in response to manganese supply in solution culture. Sci Agric 67:287–294

    Google Scholar 

  • Lee SH, Ahsan N, Lee KW, Kim DH, Lee DG, Kwak SS, Kwon SY, Kim TH, Lee BH (2007) Simultaneous overexpression of both CuZn superoxide dismutase and ascorbate peroxidase in transgenic tall fescue plants confers increased tolerance to a wide range abiotic stresses. J Plant Physiol 164:1626–1638

    Article  CAS  Google Scholar 

  • Lei Y, Korpelainen H, Li C (2007) Physiological and biochemical responses to high Mn concentrations in two contrasting Populus cathayana populations. Chemosphere 68:686–694

    Article  CAS  Google Scholar 

  • LeVier K, Day DA, Guerinot ML (1996) Iron uptake by symbiosomes from soybean root nodules. Plant Physiol 111:693–900

    Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 17:405–410

    Article  Google Scholar 

  • Nawahda A (2014) Effect of Ozone on the relative yield of rice crop in Japan evaluated based on monitored concentrations. Water Air Soil Pollut 225:1797–1802

    Article  Google Scholar 

  • Pitcher LH, Zilinskas BA (1996) Overexpression of copper/zinc superoxide in the cytosol of transgenic tobacco confers partial resistance to ozone-induced foliar necrosis. Plant Physiol 110:583–588

    CAS  Google Scholar 

  • Pleijel H (2011) Reduced ozone by air filtration consistely improved grain yield in wheat. Environ Pollut 159:897–902

    Article  CAS  Google Scholar 

  • Ravet K, Pilon M (2013) Copper and iron homeostasis in plants: the challenges of oxidative stress. Antioxid Redox Signal 19:919–932

    Article  CAS  Google Scholar 

  • Reddi AR, Jensen LT, Naranuntarat A, Rosenfeld L, Leung E, Shah R, Culotta VC (2009) The overlapping roles of manganese and Cu/Zn SOD in oxidative stress protection. Free Radic Biol Med 46:154–162

    Article  CAS  Google Scholar 

  • Reddy AR, Chaitanya KV, Jutur PP, Sumithra K (2004) Diferencial antioxidative responses to water stress among five mulberry (Morus alba L.) cultivars. Environ Exp Bot 52:33–42

    Article  CAS  Google Scholar 

  • Rodhe H, Dentener F, Schulz M (2002) The global distribution of acidifying wet. Environ Sci Technol 1536:4382–4388

    Article  Google Scholar 

  • Shi Q, Bao Z, Zhu Z, He Y, Qian Q, Yu J (2005) Silicon-mediated alleviation of Mn toxicity in Cucumis sativus in relation to activities of superoxide dismutase and ascorbate peroxidase. Phytochemistry 66:1551–1559

    Article  CAS  Google Scholar 

  • Silva LC, Azevedo AA, Silva EAM, Oliva MA (2005) Effects of simulated acid rain on the growth of five Brazilian tree species and anatomy of the most sensitive species (Joannesia princeps). Aust J Bot 53:79–796

    Google Scholar 

  • Souza SR, Pagliuso JD (2009) Design and assembly of an experimental laboratory for the study of atmosphere-plant interactions in the system of fumigation chambers. Environ Monit Assess 158:243–249

    Article  CAS  Google Scholar 

  • Souza SR, Blande JD, Holopainen J (2013) Pre-exposure to nitric oxide modulates the effect of ozone on oxidative defenses and volatile in lima bean. Environ Pollut 179:111–119

    Article  CAS  Google Scholar 

  • Srivastava S, Dubey RS (2011) Manganese-excess induces oxidative stress, lowers the pool of antioxidants and elevates activities of key antioxidative enzymes in rice seedlings. Plant Growth Regul 64:1–16

    Article  CAS  Google Scholar 

  • Sun Z, Wang L, Zhou Q, Huang X (2013) Effects and mechanisms of the combined pollution of lanthanum and acid rain on the root phenotype of soybean seedlings. Chemosphere 93:344–352

    Article  CAS  Google Scholar 

  • Tsang WT, Bowler C, Herouart D, Van Camp W, Villarroel R, Genetello C, Van Montagu M, Inze D (1991) Differential regulation of superoxide dismutases in plants exposed to environmental stress. Plant Cell 3:783–792

    Article  CAS  Google Scholar 

  • Van Camp W, Willekens H, Bowler C, Van Montagu M, Inzé D, Reupold P, Sandermann H, Langebarels C (1994) Elevated levels of superoxide dismutase protect transgenic plants against ozone dmage. Biotechnology 12:165–187

    Article  Google Scholar 

  • Van Dingenen R, Dentener FJ, Raes F, Krol MC, Emberson L, Cofala J (2009) The global impact of ozone on agricultural crop yields under current and future air quality legislation. Atmos Environ 43:604–618

    Article  Google Scholar 

  • Whitfield BCP, Davison AW, Ashenden TW (1998) The effects of nutrient limitation on the response of Plantago major to ozone. New Phytol 140:219–230

    Article  CAS  Google Scholar 

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Acknowledgments

The authors acknowledge financial support from CAPES/PNADB, FAPESP (02/04751-6; 12/11663-8) and CNPq (Brazilian funding agencies) and Embrapa Soja for donating soybean seed. We express our gratitude to Dr. Salete Aparecida Gaziola for her assistance with analytical work and Mr. Thiago Andrade for technical assistance with the synthesis of MnDFB. S.R Souza and R.A. Azevedo are grateful to CNPq for research fellowships.

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Correspondence to Silvia Ribeiro de Souza.

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Esposito, J.B.N., Esposito, B.P., Azevedo, R.A. et al. Protective effect of Mn(III)–desferrioxamine B upon oxidative stress caused by ozone and acid rain in the Brazilian soybean cultivar Glycine max “Sambaiba”. Environ Sci Pollut Res 22, 5315–5324 (2015). https://doi.org/10.1007/s11356-014-3951-z

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  • DOI: https://doi.org/10.1007/s11356-014-3951-z

Keywords

  • Soybean
  • Abiotic stress
  • Air pollution
  • Antioxidant enzymes
  • Manganese complex
  • Exogenous chemicals