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Biochemical Adaptations in Zea mays Roots to Short-Term Pb2+ Exposure: ROS Generation and Metabolism

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Abstract

The present study investigated the effect of lead (0, 16, 40 and 80 mg L−1 Pb2+) exposure for 3, 12 and 24 h on root biochemistry in hydroponically grown Zea mays (maize). Pb2+ exposure (80 mg L−1) enhanced malondialdehyde content (239 %–427 %), reactive carbonyl groups (425 %–512 %) and H2O2 (129 %–294 %) accumulation during 3–24 h of treatment, thereby indicating cellular peroxidation and oxidative damage. The quantitative estimations were in accordance with in situ detection of ROS generation (using 2′,7′-dichlorodihydrofluorescein diacetate dye) and H2O2 accumulation. Pb2+ treatment significantly reduced ascorbate and glutathione content during 3–24 h of exposure. On the contrary, levels of non-protein thiols were enhanced by 3–11.8 time over control in response to 16–80 mg L−1 Pb2+ treatment, after 24 h. A dose-dependent induction in ascorbate peroxidase and lipoxygenase enzyme activity was observed in Z. mays roots. The activities of ascorbate-recycling enzymes (dehydroascorbate reductase and monodehydroascorbate reductase) were significantly increased in relation to concentration and duration of Pb2+ treatment. The study concludes that Pb2+-exposure induces ROS-mediated oxidative damage during early period of exposure despite the upregulation of enzymes of ascorbate–glutathione cycle.

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References

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  Google Scholar 

  • Baker CJ, Mock NM (1994) An improved method for monitoring cell death in cell suspension and leaf disc assays using Evans blue. Plant Cell Tissue Organ Cult 39:7–12

    Article  Google Scholar 

  • Biteur N, Aoues A, Kharoubi O, Slimani M (2011) Oxidative stress induction by lead in leaves of radish (Raphanus sativus) seedlings. Not Sci Biol 3(4):93–99

    CAS  Google Scholar 

  • Blokhina OB, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91:179–194

    Article  CAS  Google Scholar 

  • Boscolo PRS, Menossi M, Jorge RA (2003) Aluminum-induced oxidative stress in maize. Phytochemistry 62:181–189

    Article  CAS  Google Scholar 

  • Chowhan N, Singh HP, Batish DR, Kaur S, Ahuja N, Kohli RK (2013) β-Pinene inhibited germination and early growth involves membrane peroxidation. Protoplasma 250:691–700

    Article  CAS  Google Scholar 

  • Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77

    Article  CAS  Google Scholar 

  • Ezaki B, Gardner RC, Ezaki Y, Matsumoto H (2000) Expression of aluminum-induced genes in transgenic Arabidopsis plants can ameliorate aluminum stress and/or oxidative stress. Plant Physiol 122:657–665

    Article  CAS  Google Scholar 

  • Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25

    Article  CAS  Google Scholar 

  • Geebelen W, Vangronsveld J, Adriano DC, Van Poucke LC, Clijsters H (2002) Effects of Pb-EDTA and EDTA on oxidative stress reactions and mineral uptake in Phaseolus vulgaris. Physiol Plant 115(3):377–384

    Article  CAS  Google Scholar 

  • Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106(1):207–212

    Article  CAS  Google Scholar 

  • Gupta DK, Nicoloso FT, Schetinger MRC, Rossato LV, Pereira LB, Castro GY, Srivastava S, Tripathi RD (2009) Antioxidant defense mechanism in hydroponically grown Zea mays seedlings under moderate lead stress. J Hazard Mater 172:479–484

    Article  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  CAS  Google Scholar 

  • Hossain MA, Asada K (1984) Purification of dehydroascorbate reductase from spinach and its characterization as a thiol enzyme. Plant Cell Physiol 25:85–92

    CAS  Google Scholar 

  • Hossain MA, Nakano Y, Asada K (1984) Monodehydroascorbate reductase in spinach chloroplasts and its participation in regeneration of ascorbate for scavenging hydrogen peroxide. Plant Cell Physiol 25:385–395

    CAS  Google Scholar 

  • Huang H, Gupta DK, Tian S, Yang X, Li T (2012) Lead tolerance and physiological adaptation mechanism in roots of accumulating and non-accumulating ecotypes of Sedum alfredii. Environ Sci Pollut Res 19:1640–1651

    Article  CAS  Google Scholar 

  • Kaur G, Singh HP, Batish DR, Kohli RK (2012) A time-course assessment of changes in reactive oxygen species generation and antioxidant defense in hydroponically grown wheat in response to lead ions (Pb2+). Protoplasma 249:1091–1100

    Article  CAS  Google Scholar 

  • Kaur G, Singh HP, Batish DR, Kohli RK (2014) Pb-inhibited mitotic activity in onion roots involves DNA damage and disruption of oxidative metabolism. Ecotoxicology 23:1292–1304

    Article  CAS  Google Scholar 

  • Komárek M, Tlustos P, Száková J, Chrastný V, Ettler V (2007) The use of maize and poplar in chelant-enhanced phytoextraction of lead from contaminated agricultural soils. Chemosphere 67:640–651

    Article  Google Scholar 

  • Krzesłowska M, Lenartowska M, Samardakiewicz S, Bilski H, Wόzny A (2010) Lead deposited in the cell wall of Funaria hygrometrica protonemata is not stable—a remobilization can occur. Environ Pollut 158(1):325–338

    Article  Google Scholar 

  • Kumar A, Prasad MNV, Achary VMM, Panda BB (2013) Elucidation of lead-induced oxidative stress in Talinum triangulare roots by analysis of antioxidant responses and DNA damage at cellular level. Environ Sci Pollut Res 20:4551–4561

    Article  CAS  Google Scholar 

  • Law MY, Charles SA, Halliwell B (1983) Glutathione and ascorbic acid in spinach (Spinacia oleracea) chloroplasts. The effect of hydrogen peroxide and of Paraquat. Biochem J 210(3):899–903

    CAS  Google Scholar 

  • Levine RL, Williams JA, Stadtman ER, Shacter E (1994) Carbonyl assay for determination of oxidatively modified proteins. Methods Enzymol 233:346–357

    Article  CAS  Google Scholar 

  • Logani MK, Davies RE (1980) Lipid oxidation: biologic effects and antioxidants—a review. Lipids 15:485–495

    Article  CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein estimation with Folin–phenol reagent. J Biol Chem 193:265–278

    CAS  Google Scholar 

  • Maestri E, Marmiroli M, Visioli G, Marmiroli N (2010) Metal tolerance and hyperaccumulation: costs and trade-offs between traits and environment. Environ Exp Bot 68(1):1–13

    Article  CAS  Google Scholar 

  • Małecka A, Piechalak A, Tomaszewska B (2009) Reactive oxygen species production and antioxidative defense system in pea root tissues treated with lead ions: the whole roots level. Acta Physiol Plant 31:1053–1063

    Article  Google Scholar 

  • Malecka A, Piechalak A, Mensinger A, Hanc A, Baralkiewicz D, Tomaszewska B (2012) Antioxidative defense system in Pisum sativum rooots exposed to heavy metals (Pb, Cu, Cd, Zn). Pol J Environ Stud 21:1721–1730  

    CAS  Google Scholar 

  • Møller IM, Kristensen BK (2004) Protein oxidation in plant mitochondria as a stress indicator. Photochem Photobiol Sci 3(8):730–735

    Article  Google Scholar 

  • Nadgórska-Socha A, Kandziora-Ciupa M, Ciepał R, Walasek K (2011) Effects of Zn, Cd, Pb on physiological response of Silene vulgaris plants from selected populations. Pol J Environ Stud 20:599–604

    Google Scholar 

  • Nakano Y, Asada K (1987) Purification of ascorbate peroxidase in spinach chloroplasts; its inactivation in ascorbate-depleted medium and reactivation by monodehydroascorbate radical. Plant Cell Physiol 28:131–140

    CAS  Google Scholar 

  • Pena LB, Zawoznik MS, Tornado ML, Gallego SM (2008) Heavy metals effects on proteolytic system in sunflower leaves. Chemosphere 72:741–746

    Article  CAS  Google Scholar 

  • Pirslova B, Kuna R, Libantova J, Moravcikova J, Matusikova I (2011) Biochemical and physiological comparison of heavy metal-triggered defense responses in the monocot maize and dicot soybean roots. Mol Biol Rep 38:3437–3446

    Article  Google Scholar 

  • Pourrut B, Shahid M, Dumat C, Winterton P, Pinelli E (2011) Lead uptake, toxicity, and detoxification in plants. Rev Environ Contam Toxicol 213:113–136

    CAS  Google Scholar 

  • Qureshi MI, Abdin MZ, Qadir S, Iqbal M (2007) Lead induced oxidative stress and metabolic alterations in Cassia angustifolia Vahl. Biol Plant 51:121–128

    Article  CAS  Google Scholar 

  • Rucińska-Sobkowiak R, Pukacki PM (2006) Antioxidative defense system in lupin roots exposed to increasing concentrations of lead. Acta Physiol Plant 28:357–364

    Article  Google Scholar 

  • Schützendūbel A, Schwanz P, Teichmann T, Gross K, Langenfeld-Heyser R, Godbold DL, Polle A (2001) Cadmium-induced changes in antioxidative systems, hydrogen peroxide content, and differentiation in Scots pine roots. Plant Physiol 127:887–898

    Article  Google Scholar 

  • Sengar RS, Gautam M, Sengar RS, Garg SK, Sengar K, Chaudhary R (2008) Lead stress effects on physiobiochemical activities of higher plants. Rev Environ Contam Toxicol 196:73–93

    CAS  Google Scholar 

  • Seregin IV, Shpigun LK, Ivanon VB (2004) Distribution and toxic effects of cadmium and lead on maize roots. Russ J Plant Physiol 51:525–533

    Article  CAS  Google Scholar 

  • Seth CS, Remans T, Keunen E, Jozefczak M, Gielen H, Opdenakker K, Weyens N, Vangronsveld J, Cuypers A (2012) Phytoextraction of toxic metals: a central role for glutathione. Plant Cell Environ 35(2):334–346

    Article  CAS  Google Scholar 

  • Sharma P, Dubey RS (2005) Lead toxicity in plants. Braz J Plant Physiol 17(1):35–52

    Article  CAS  Google Scholar 

  • Singh HP, Batish DR, Kaur G, Arora K, Kohli RK (2008) Nitric oxide (as sodium nitroprusside) supplementation ameliorates Cd toxicity in hydroponically grown wheat roots. Environ Exp Bot 63:158–167

    Article  CAS  Google Scholar 

  • Stone JR, Yang S (2006) Hydrogen peroxide: a signaling messenger. Antioxid Redox Signal 8:243–270

    Article  CAS  Google Scholar 

  • Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants, H2O2 accumulation in papillae and hypersensitive response during barley–powdery mildew interaction. Plant J 11:1187–1194

    Article  CAS  Google Scholar 

  • Uzu G, Sobanska S, Sarret G, Munoz M, Dumat C (2010) Foliar lead uptake by lettuce exposed to atmospheric fallouts. Environ Sci Technol 44:1036–1042

    Article  CAS  Google Scholar 

  • Verma S, Dubey RS (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164:645–655

    Article  CAS  Google Scholar 

Download references

Acknowledgment

GK is thankful to University Grants Commission (New Delhi, India) for research fellowship.

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The authors declare that they have no conflict of interest.

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Correspondence to Harminder Pal Singh.

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Kaur, G., Kaur, S., Singh, H.P. et al. Biochemical Adaptations in Zea mays Roots to Short-Term Pb2+ Exposure: ROS Generation and Metabolism. Bull Environ Contam Toxicol 95, 246–253 (2015). https://doi.org/10.1007/s00128-015-1564-y

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  • DOI: https://doi.org/10.1007/s00128-015-1564-y

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