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Long-term impact of sublethal atrazine perturbs the redox homeostasis in pea (Pisum sativum L.) plants

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Abstract

Atrazine frequently contaminates soil, groundwater, rivers, and ponds. It is well know that acute doses (1–5 mM) of atrazine induce massive generation of singlet oxygen by blocking photosystem II. The sublethal concentrations of this herbicide, similar to those found in the environment, also reduce growth and disrupt photosynthesis in a long-term aspect, but exact mechanisms remain much uncertain. In this study the effects of environmentally relevant atrazine levels, ranging from 0.1 to 10 μM, on pea plants were characterized for up to 20 days. The plants exposed to continuous influence of atrazine exhibited perturbed redox homeostasis with increases of the lipid peroxides, the total and oxidized glutathione pools and elevated guaiacol peroxidase and glutathione-S-transferase activities. In contrast, the long-term atrazine impact did not affect superoxide dismutase activity whereas the catalase was inhibited. The perturbations of the redox status and the recruitment of the antioxidant machinery imply that the sublethal atrazine concentrations alter the poise between production and scavenging of reactive oxygen species. Taken together these results show that the long-term impact of sublethal atrazine has hallmarks of oxidative stress most probably triggered by generation of singlet oxygen.

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References

  • Aebi M (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  PubMed  CAS  Google Scholar 

  • Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24:1337–1344

    Article  CAS  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase. Improved assay and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  PubMed  CAS  Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein using the principle of protein-due binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Braun AL, Hawkins LS (1991) Presence of bromacil, diuron, and simazine in surface water runoff from agricultural fields and non-crop in Tulare County. In: Environmental Monitoring and Pesticide Management Branch, USA: California Department of Pesticide Regulation, Sacramento, 1020 N Street, Room 161, 95814, CA PM 91–1

  • Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–310

    Article  PubMed  CAS  Google Scholar 

  • Burnside OC, Fenster CR, Wicks GA (1971) Soil persistence of repeated annual applications of atrazine. Weed Sci 19(3):290–293

    CAS  Google Scholar 

  • Cadet J, Douki T, Ravanat JL (2010) Oxidatively generated base damage to cellular DNA. Free Radic Biol Med 49:9–21

    Article  PubMed  CAS  Google Scholar 

  • Carter AD (2000) Herbicide movement in soils: principles, pathways and processes. Weed Res 40:113–122

    Article  CAS  Google Scholar 

  • Cobb A (1992) Herbicides and plant physiology. Charman & Hall, London

    Google Scholar 

  • Cox C (2001) Atrazine: environmental contamination and ecological effects. J Pest Reform 21(3):12–20

    Google Scholar 

  • Dat JF, Lopez-Delgado H, Foyer C, Scott IM (1998) Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol 116:1351–1357

    Article  PubMed  CAS  Google Scholar 

  • Davies MJ (2004) Reactive species formed on proteins exposed to singlet oxygen. Photochem Photobiol Sci 3:17–25

    Article  PubMed  CAS  Google Scholar 

  • De la Torre W, Burkey K (1992) Physiological effects on sublethal atrazine on barley chloroplast thylakoid membranes. Photosynth Res 32:1–10

    Article  Google Scholar 

  • Dias I, Costa M (1983) Effect of low salt concentration on nitrate reductase and peroxidase of sugar beet leaves. J Exp Bot 34:197–202

    Article  Google Scholar 

  • Edwards R, Dixon DP (2005) Plant glutathione transferases. Methods Enzymol 401:169–186

    Article  PubMed  CAS  Google Scholar 

  • Filkowski J, Yeoman A, Kovalchuk O, Kovalchuk I (2004) Systemic plant signal triggers genome instability. Plant J 38:1–11

    Article  PubMed  CAS  Google Scholar 

  • Fischer BB, Krieger-Liszkay A, Hideg E, Snyrychová I, Wiesendanger M, Eggen RI (2007) Role of singlet oxygen in chloroplast to nucleus retrograde signaling in Chlamydomonas reinhardtii. FEBS Lett 581:5555–5560

    Article  PubMed  CAS  Google Scholar 

  • Foyer C, Lopez-Delgado H, Dat JE, Scott IM (1997) Hydrogen peroxide and glutathione-associated mechanisms of acclamatory stress tolerance and signalling. Physiol Plant 100:241–254

    Article  CAS  Google Scholar 

  • Gronwald J, Fuerst E, Eberlein C, Egli M (1987) Effect of herbicide antidote on glutathione content and glutathione-S-transferase activity of sorghum shoots. Pestic Biochem Physiol 29:66–76

    Article  CAS  Google Scholar 

  • Halliwell B, Gutteridge J (2002) Free radicals in biology and medicine, 3rd edn. Oxford University Press, New York

    Google Scholar 

  • Ivanov S, Kerchev P (2007) Separation and quantification of the cellular thiol pool of pea plants treated with heat, salinity and atrazine. Phytochem Anal 18(4):283–290

    Article  PubMed  CAS  Google Scholar 

  • Ivanov S, Alexieva V, Karanov E (2005) Cumulative effect of low and high atrazine concentrations on Arabidopsis thaliana (L.) Heynh plants. Russ J Plant Physiol 52(2):213–219

    Article  CAS  Google Scholar 

  • Jettner RJ, Walker SR, Churchett JD, Blameye FC, Adkins SW, Bell K (1999) Plant sensitivity to atrazine and chlorsulfuron residues in a soil-free system. Weed Res 39:287–295

    Article  CAS  Google Scholar 

  • Kim C, Meskauskiene R, Apel K, Laloi C (2008) No single way to understand singlet oxygen signalling in plants. EMBO Rep 9:435–439

    Article  PubMed  CAS  Google Scholar 

  • Kochevar IE (2004) Singlet oxygen signaling: from intimate to global. Sci STKE. doi:10.1126/stke.2212004pe7

  • Kramarenko GG, Hummel SG, Martin SM, Buettner GR (2006) Ascorbate reacts with singlet oxygen to produce hydrogen peroxide. Photochem Photobiol 82:1634–1637

    PubMed  CAS  Google Scholar 

  • Krieger-Liszkay A, Fufezan C, Trebst A (2008) Singlet oxygen production in photosystem II and related protection mechanisms. Photosynth Res 98:551–564

    Article  PubMed  CAS  Google Scholar 

  • Laloi C, Przybyla D, Apel K (2006) A genetic approach towards elucidating the biological activity of different reactive oxygen species in Arabidopsis thaliana. J Exp Bot 57:1719–1724

    Article  PubMed  CAS  Google Scholar 

  • Lambrev P, Ivanov S, Goltsev V (2003) Effect of prolonged action of sub-herbicide concentration of atrazine on the photosynthetic function of pea plants. Comp Rend Acad Bulg Sci 56(3):59–62

    CAS  Google Scholar 

  • Marrs KA (1996) The functions and regulation of glutathione-S-transferases in plants. Annu Rev Plant Physiol 47:127–158

    Article  CAS  Google Scholar 

  • Miteva L, Ivanov S, Alexieva V, Karanov E (2004) Effect of atrazine on glutathione levels, glutathione S-transferase and glutathione reductase activities in pea and wheat plants. Plant Prot Sci 40(1):16–20

    Google Scholar 

  • Moller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58:459–481

    Article  PubMed  Google Scholar 

  • Noctor G, Gomez L, Vanacker H, Foyer C (2002) Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signaling. J Exp Bot 53(372):1283–1304

    Article  PubMed  CAS  Google Scholar 

  • Pallet KE, Dodge AD (1980) Studies into the action of some photosynthetic inhibitor herbicides. J Exp Bot 31:1051–1058

    Article  Google Scholar 

  • Parvanova D, Ivanov S, Konstantinova T, Karanov E, Atanassov A, Tsvetkov T, Alexieva V, Djilianov D (2004) Transgenic tobacco plants accumulating osmolytes show reduced oxidative damage under freezing stress. Plant Physiol Biochem 42:57–63

    Article  PubMed  CAS  Google Scholar 

  • Ramel F, Sulmon C, Bogard M, Couée I, Gouesbet G (2009) Differential patterns of reactive oxygen species and antioxidative mechanisms during atrazine injury and sucrose-induced tolerance in Arabidopsis thaliana plantlets. BMC Plant Biol 9:28. doi:10.1186/1471-2229-9-28

    Article  PubMed  Google Scholar 

  • Rao KV, Sresty TV (2000) Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan L. Millspaugh) in response to Zn and Ni stresses. Plant Sci 157:113–128

    Article  Google Scholar 

  • Rutherford AW, Krieger-Liszkay A (2001) Herbicide-induced oxidative stress in photosystem II. Trends Biochem Sci 26(11):648–653

    Article  PubMed  CAS  Google Scholar 

  • Sandalio LM, Dalurzo HC, Gómez M, Romero-Puertas MC, del Río LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126

    PubMed  CAS  Google Scholar 

  • Shimabukuro RH (1967) Atrazine metabolism and herbicidal selectivity. Plant Physiol 42:1269–1276

    Article  PubMed  CAS  Google Scholar 

  • Shimabukuro RH, Swanson HR, Walsh WC (1970) Glutathione conjugation: atrazine detoxification mechanism in corn. Plant Physiol 46:103–107

    Article  PubMed  CAS  Google Scholar 

  • Tanaka K, Kondo N, Sugahara K (1982) Accumulation of hydrogen peroxide in chloroplast of SO2-fumigated spinach leaves. Plant Cell Physiol 23:999–1007

    CAS  Google Scholar 

  • Tausz M, Ircelj H, Grill D (2004) The glutathione system as a stress marker in plant ecophysiology is a stress-response concept valid? J Exp Bot 55:1955–1962

    Article  PubMed  CAS  Google Scholar 

  • Taylor AW (1995) The volatilization of pesticide residues. In: Roberts TR, Kearney PC (eds) Environmental behaviour of agrochemicals. Willey, Chichester, pp 257–306

    Google Scholar 

  • Van Maanen J, De Vaan M, Veldstra A, Hendrix W (2001) Pesticides and nitrate in groundwater and rainwater in the province of Limburg in the Netherlands. Environ Monit Assess 72(1):95–114

    Article  PubMed  Google Scholar 

  • Vitanov N, Lekova K, Dobreva N (2003) Monitoring river water in the Danube for atrazine contamination. Acta Chromatogr 13:230–242

    CAS  Google Scholar 

  • Willekens H, Inze D, Van Montagu M, Van Camp W (1995) Catalases in plants. Mol Breed 1:207–228

    Article  CAS  Google Scholar 

Download references

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Authors and Affiliations

  1. Centre of Food Biology, PO Box 120, Sofia, 1592, Bulgaria

    Sergei Ivanov

  2. Institute of Plant Physiology and Genetics, Bulgarian Academy of Sciences, Acad. G. Bonchev Str., bl. 21, 1113, Sofia, Bulgaria

    Elena Shopova, Pavel Kerchev, Iskren Sergiev, Lyuba Miteva, Djovani Polizoev & Vera Alexieva

  3. Centre for Plant Sciences, Faculty of Biology, University of Leeds, Leeds, LS2 9JT, UK

    Pavel Kerchev

Authors
  1. Sergei Ivanov
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  2. Elena Shopova
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  3. Pavel Kerchev
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  4. Iskren Sergiev
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  5. Lyuba Miteva
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  6. Djovani Polizoev
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  7. Vera Alexieva
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Correspondence to Sergei Ivanov.

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Handling Editor: Peter Nick

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Fig. 1

Effect of atrazine treatment on the length of aboveground parts of pea plants (in millimeters ± SD) (EPS 552 kb)

Fig. 2

Changes in the percent dry weight of aboveground parts of pea plants (in percent, ± SD) (EPS 615 kb)

Fig. 3

Electrolytes release of aboveground parts of pea plants (in microsiemens, ± SD) (EPS 661 kb)

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Ivanov, S., Shopova, E., Kerchev, P. et al. Long-term impact of sublethal atrazine perturbs the redox homeostasis in pea (Pisum sativum L.) plants. Protoplasma 250, 95–102 (2013). https://doi.org/10.1007/s00709-012-0378-6

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  • DOI: https://doi.org/10.1007/s00709-012-0378-6

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