Abstract
The current study evaluated the toxicity of three heavy metals to aerial roots of the Chinese banyan (Ficus microcarpa), which is a tree species native to China. In a laboratory experiment, segments of aerial roots cut from trees were treated with 0, 25, 50, 100, and 200 μM of lead, cadmium, or copper (Cu). The contents of these heavy metals in cells increased and root cell viability decreased with increases in treatment concentration. High levels of reactive oxygen species accumulated in the aerial root sections after heavy metal treatment. Both biochemical assay and histochemical localization showed that O2 •−, which is a precursor of H2O2 accumulated in root sections and that the amount accumulated was positively related to heavy metal concentration, especially for Cu-treated samples. Histochemical staining with diaminobenzidine (DAB) and a fluorometric scopoletin oxidation assay indicated that the amount of H2O2 accumulated was positively related to heavy metal concentration in the treatments; the scopoletin fluorescence assay was more sensitive and efficient than DAB staining for detection and quantification of H2O2. The results indicate that aerial roots are sensitive to heavy metal-induced oxidative damage and that aerial roots have the potential to be used as indicators of heavy metal pollution in urban areas.
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Alaoui-Sossé 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 change in ion contents. Plant Sci 166:1213–1218
Aust SD, Marehouse LA, Thomas CE (1985) Role of metals in oxygen radical reactions. J Free Radic Biol Med 1:3–25
Benavides MP, Gallego SM, Tomaro ML (2005) Cadmium toxicity in plants. Braz J Plant Physiol 17:21–34
Danesino C (2009) Environmental indicators for heavy metals pollution: soils and higher plants. Sci Acta 3:23–26
Ďurčeková K, Huttová J, Mistrík I, Ollé M, Tamás L (2007) Cadmium induces premature xylogenesis in barley roots. Plant Soil 290:61–68
Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JDG, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446
Garnier L, Simon-Plas F, Thuleau P, Agnel JP, Blein JP, Ranjeva R, Montillet JL (2006) Cadmium affects tobacco cells by a series of three waves of reactive oxygen species that contribute to cytotoxicity. Plant Cell Environ 29:1956–1969
Guan LL, Wen DZ (2011) More nitrogen partition in structural proteins and decreased photosynthetic nitrogen-use efficiency of Pinus massoniana under in situ polluted stress. J Plant Res 124:663–673
Halliwel B (2006) Reactive specie and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322
Islam E, Liu D, Li T, Yang X, Jin X, Mahmood Q, Tian S, Li J (2008) Effect of Pb toxicity on leaf growth, physiology and ultrastructure. J Hazard Mater 154:914–926
Kappus H (1985) Overview of enzyme systems involved in bioreduction of drugs and redox-cycling. Biochem Pharmacol 35:1–6
Khatun S, Ali MB, Hahn EJ, Paek KY (2008) Copper toxicity in Withania somnifera: growth and antioxidant enzymes responses of in vitro grown plants. Environ Exp Bot 64:279–285
Kong GH, Lu YD, Liu SZ, Zhang QM, Hu XC, Xue KN, Chu GW (2003) Injury symptoms of 38 woody species exposed to air pollutants. J Trop Subtrop Bot 11:319–328
Lin ZF, Liu N, Lin GZ, Peng CL (2009) In situ localisation of superoxide generated in leaves of Alocasia macrorrhiza (L.) Schott under various stresses. J Plant Biol 52:340–347
Liu D, Jiang W, Wang W, Zhao F, Lu C (1994) Effects of lead on root growth, cell division, and nucleolus of Allium cepa. Environ Pollut 131:453–459
Liu N, Lin ZF, Lin GZ, Song LY, Chen SW, Mo H, Peng CL (2010) Lead and cadmium induced alterations of cellular functions in leaves of Alocasia macrorrhiza L. Schott. Ecotoxicol Environ Safe 73:1238–1245
MacFarlane GR (2003) Chlorophyll a fluorescence as a potential biomarker of zinc stress in the grey mangrove, Avicennia marina. Bull Environ Contam Toxicol 70:90–96
Madejón P, Ramírez-Benítez JE, Corrales I, Barceló J, Poschenrieder C (2009) Copper-induced oxidative damage and enhanced antioxidant defense in the root apex of maize cultivars differing in Cu tolerance. Environ Exp Bot 67:415–420
Mazhoudi S, Chaoui A, Ghorbal MH, Ferjani EE (1997) Response of antioxidant enzymes to excess copper in tomato (Lycopersicon esculentum, Mill.). Plant Sci 127:129–137
Ministry of Environmental Protection of People’s Republic of China (2011) 2010 Report on the state of the environment of China
Monferrán MV, Sánchez Agudo JA, Pignata ML, Wunderlin DA (2009) Copper-induced response of physiological parameters and antioxidant enzymes in the aquatic macropyte Potamogeton pusillus. Environ Pollut 157:2570–2576
Olmos E, Martínez-Solano JR, Piqueras A, Hellín E (2003) Early steps in the oxidative burst induced by cadmium in cultured tobacco cells (BY-2 line). J Exp Bot 54:291–301
Onder S, Dursun S (2006) Air borne heavy metal pollution of Cedrus libani (A. Rich.) in the city centre of Konya (Turkey). Atmos Environ 40:1122–1133
Passardi F, Penel C, Dunand C (2004) Performing the paradoxical: how plant peroxidasas modify the cell wall. Trends Plant Sci 9:534–540
Prasad MNV (1998) Metal-biomolecule complexes in plants: occurrence, functions, and applications. Met Biomol 26:25–28
Ren H, Cai XA, Li CH, Ye YS (2010) Atlas on tool species of vegetation recovery in South China. Huazhong University of Science & Technology Press, Wuhan
Robson AD, Reuter DJ (1981) Diagnosis of copper deficiency and toxicity. In: Loneragan JF, Robson AD, Graham RD (eds) Copper in soils and plants. Academic Press, London, pp 287–312
Rossato LV, Nicoloso FT, Farias JG, Cargnelluti D, Tabaldi LA, Antes FG, Dressler VL, Morsch VM, Schetinger MRC (2012) Effects of lead on the growth, lead accumulation and physiological responses of Pluchea sagittalis. Ecotoxicology 21:111–123
Sagi M, Fluhr R (2006) Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol 141:336–340
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
Sanita di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130
Schopfer P, Plachy C, Frahry G (2001) Release of reactive oxygen intermediates (superoxide radicals, hydrogen peroxide, and hydroxyl radicals) and peroxidase in germinating radish seeds controlled by light, gibberellin and abscisic acid. Plant Physiol 125:1591–1602
Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 372:1351–1365
Srivastava S, Mishra S, Tripathi RD, Dwivedi S, Gupta DK (2006) Copperinduced oxidative stress and responses of antioxidants and phytochelatins in Hydrilla verticillata (L. f.). Royle Aquat Toxicol 80:405–415
Sun FF, Wen DZ, Kuang YW, Li J, Zhang JG (2009) Concentrations of sulphur and heavy metals in needles and rooting soils of masson pine (Pinus massoniana L.) tree growing along an urban-rural gradient in Guangzhou, China. Environ Monit Assess 154:263–274
Van Assche F, Cliisters H (1990) Effects of metals on enzyme activity in plants. Plant Cell Environ 13:195–206
Weast RC (1984) CRC handbook of chemistry and physics, 64th edn. CRC Press, Boca Raton
Wierzbicka M, Obidzinska J (1998) The effect of lead on seed imbibition and germination in different plant species. Plant Sci 137:155–171
Yang XF, Guo XQ (2001) Fe(II)-EDTA chelate-induced aromatic hydroxylation of terephthalate as a new method for the evaluation of hydroxyl radical—scavenging ability. Analyst 126:928–932
Zhang J, Kirkham MB (1996) Enzymatic responses of the ascorbate-glutathione cycle to drought in sorghum and sunflower plants. Plant Sci 113:139–147
Acknowledgments
This research is supported by the Knowledge Innovation Program of the Chinese Academy of Sciences, Grant No. KSCX2-EW-J-28. The authors are grateful to Huanfang Liu and Yong Liu for preparations of aerial root paraffin sections. We also appreciate the English editing work by Bruce Jaffee and suggestions by the two anonymous reviewers on the early version of this manuscript.
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Liu, N., Lin, Z. & Mo, H. Metal (Pb, Cd, and Cu)-induced reactive oxygen species accumulations in aerial root cells of the Chinese banyan (Ficus microcarpa). Ecotoxicology 21, 2004–2011 (2012). https://doi.org/10.1007/s10646-012-0935-y
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DOI: https://doi.org/10.1007/s10646-012-0935-y