Abstract
The effect of heavy metal deposition onto soil from a copper smelter on lipid peroxidation and antioxidant enzyme activity in the fine roots of two poplars (Populus nigra L. and Populus deltoides Bartr. ex Marsch) was analyzed. The subjects were mature trees growing in real environments. In both analyzed species, heavy metals stimulated the overproduction of free radicals in fine roots (measured as malondialdehyde level), which was directly proportional to advancing senescence. In young fine roots, heavy metals caused a decrease in guaiacol peroxidase activity and presumably disturbed the lignification process. Catalase was highly sensitive to the presence of heavy metals in the soil. In contrast, ascorbate peroxidase and glutathione reductase activities were unaffected by heavy metals. In the case of superoxide dismutase, a clear increase in enzyme activity was observed only in P. nigra under drought conditions, whereas it was inhibited in polluted stands.
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References
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126
Alloway BJ (1995) Heavy metals in soils, 2nd edn. Blackie Academic & Profesional, Glasgow
Bacelar EA, Santos DL, Moutinho-Pereira JM, Lopes JI, Gonçalves BC, Ferreira TC et al (2007) Physiological behaviour, oxidative damage and antioxidative protection of olive trees grown under different irrigation regimes. Plant Soil 292:1–12
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287
Bernardi R, Nali C, Ginestri P, Pugliesi C, Lorenzini G, Durante M (2004) Antioxidant enzyme isoforms on gels in two poplar clones differing in sensitivity after exposure to ozone. Biol Plant 48:41–48
Chaoui A, El Ferjani E (2005) Effects of cadmium and copper on antioxidant capacities, lignification and auxin degradation in leaves of pea (Pisum sativum L.) seedlings. C R Biol 328:23–31
Chen YX, He YF, Luo YM, Yu YL, Lin Q, Wong MH (2003) Physiological mechanism of plant roots exposed to cadmium. Chemosphere 50:789–793
Edwards EA, Enard C, Creissen GP, Mullineaux PM (1994) Synthesis and properties of glutathione reductase in stressed peas. Planta 192:137–143
Eklund M, Håkansson K (1996) Distribution of cadmium, copper and zinc emitted from a Swedish copperworks, 1750–1900. J Geochem Explor 58:291–299
Gaudinski JB, Trumbore SE, Davidson EA, Cook AC, Markewitz D, Richter DD (2001) The age of fine root carbon in three forests of the eastern United States measured by radiocarbon. Oecologia 129:420–429
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
Hu N, Li Z, Huang P, Tao C (2006) Distribution and mobility of metals in agricultural near a copper smelter in South China. Environ Geochem Health 28:19–26
Janssens IA, Sampson DA, Curiel-Yuste J, Carrara A, Ceulemans R (2002) The carbon cost of fine root turnover in Scots pine forest. For Ecol Manag 168:231–240
Karpińska B, Karlsson M, Schinkel H, Streller S, Süss K-H, Melzer M et al (2001) A novel superoxide dismutase with a high isoelectric point in higher plants. Expression, regulation, and protein localization. Plant Physiol 126:1668–1677
Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170
Laureysens I, De Temmerman L, Hastir T, Van Gysel M, Ceulemans R (2005) Clonal variation in heavy metal accumulation and biomass production in a poplar coppice culture. II. Vertical distribution and phytoextraction potential. Environ Pollut 133:541–551
Lehmann C, Rebele F (2004) Evaluation of heavy metal tolerance in Calamagrostis epigejos and Elymus repens revealed copper tolerance in a copper smelter population of C. epigejos. Environ Exp Bot 51:199–213
Lin C-C, Chen L-M, Liu Z-H (2005) Rapid effect of copper on lignin biosynthesis in soybean roots. Plant Sci 168:855–861
Lorenc-Plucińska G, Stobrawa K (2005) Acclimation of poplar trees to heavy metals in polluted habitats: I. Carbohydrate metabolism in fine roots of Populus deltoides. Acta Soc Bot Pol 74:11–16
Lorenc-Plucińska G, Szadel A, Kieliszewska-Rokicka B, Stobrawa K, Michalak A, Pluciński A (2005) Acclimation of poplar trees to heavy metals in polluted habitats: II. Alcoholic fermentation in fine roots of Populus nigra and P. deltoides. Poster presented at XVII International Botanical Congress, Vienna, Austria
Mancini A, Buschini A, Restivo FM, Rossi C, Poli P (2006) Oxidative stress as DNA damage in different transgenic tobacco plants. Plant Sci 170:845–852
Mazhoudi S, Chaoui A, Ghorbal MH, El Ferjani E (1997) Response of antioxidant enzymes to excess copper in tomato (Lycopersicon esculentum, Mill.). Plant Sci 127:129–137
McCord IM, Fridovich I (1969) Superoxide dismutase, an enzymic function for erythrocuprein. J Biol Chem 224:6049–6055
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxide in spinach chloroplasts. Plant Cell Physiol 22:867–880
Niewiadomska E, Gaucher-Veilleux C, Chevrier N, Mauffette Y, Dizengremel P (1999) Elevated CO2 does not provide protection against ozone considering the activity of several antioxidant enzymes in the leaves of sugar maple. J Plant Physiol 155:70–77
Reddy AR, Chaitanya KV, Jutur PP, Sumithra K (2004) Differential antioxidative responses to water stress among five mulberry (Morus alba L.) cultivars. Environ Exp Bot 52:33–42
Ros Barceló A, Gómez Ros LV, Ferrer MA, Hernández JA (2006) The apoplastic antioxidant enzymatic system in the wood-forming tissues of trees. Trees 20:145–156
Sakihama Y, Cohen MF, Grace SC, Yamasaki H (2002) Plant phenolic antioxidant and prooxidant activities: phenolics-induced oxidative damage mediated by metals in plants. Toxicology 177:67–80
Schützendübel A, Nikolova P, Rudolf C, Polle A (2002) Cadmium and H2O2-induced oxidative stress in Populus × canescens roots. Plant Physiol Biochem 40:577–584
Scott ML, Shafroth PB, Auble GT (1999) Responses of riparian cottonwoods to alluvial water table declines. Environ Manage 23:347–358
Shah K, Kumar RG, Verma S, Dubey RS (2001) Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Sci 161:1135–1144
Shimizu N, Kobayashi K, Hayashi K (1984) The reaction of superoxide radical with catalase. Mechanism of the inhibition of catalase by superoxide radical. J Biol Chem 259:4414–4418
Ślesak I, Miszalski Z (2003) Superoxide dismutase-like protein from roots of the intermediate C3-CAM plant Mesembryanthemum crystallinum L. in in vitro culture. Plant Sci 164:497–505
Stobrawa K, Lorenc-Plucińska G (2007) Changes in carbohydrate metabolism in fine roots of the native European black poplar (Populus nigra L.) in a heavy-metal-polluted environment. Sci Total Environ 373:157–165
Tewari RK, Kumar P, Sharma PN (2006) Antioxidant responses to enhanced generation of superoxide anion radical and hydrogen peroxide in the copper-stressed mulberry plants. Planta 223:1145–1153
Tuskan GA, DiFazio SP, Jansson S, Bohlmann J, Grigoriev I, Hellsten U et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604
Varga A, Garcinuno-Martinez RM, Zaray G, Fodor F (1999) Investigation of effects of cadmium, lead, nickel and vanadium contamination on the uptake and transport processes in cucumber plants by TXRF spectrometry. Spectrochim Acta B 54:1455–1462
Zimmerlin A, Wojtaszek P, Bolwell GP (1994) Synthesis of dehydrogenation polymers of ferulic acid with high specificity by a purified cell-wall peroxidase from French bean (Phaseolus vulgaris L.). Biochem J 299:747–753
Acknowledgements
This study was partly supported by grant no.3 PO4G 075 25 from the State Committee for Scientific Research, Poland. Research was a part of the doctoral thesis of K. Stobrawa. Thanks are due to Ms. K. Grewling for her excellent technical assistance. We would also like to thank the editor and anonymous reviewers for their comments.
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Stobrawa, K., Lorenc-Plucińska, G. Changes in antioxidant enzyme activity in the fine roots of black poplar (Populus nigra L.) and cottonwood (Populus deltoides Bartr. ex Marsch) in a heavy-metal-polluted environment. Plant Soil 298, 57–68 (2007). https://doi.org/10.1007/s11104-007-9336-z
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DOI: https://doi.org/10.1007/s11104-007-9336-z