Abstract
Plants of the urban environment are exposed to a wide range of pollutants, including heavy metals. This research studies in situ the eco-physiological and antioxidant responses of holm oak (Q. ilex) leaves to Pb and Cd to assess the mechanisms of metal tolerance in this species, widely used as biomonitor. Leaves of plants grown at parks and roadsides were analyzed for photosynthetic activity, Pb and Cd concentration in tissues and cell-free extracts, thiol groups, D1 and Rubisco protein content, ascorbic acid (AsA) amount, and catalase (CAT) activity. The main results evidenced that Cd concentration was higher in leaves collected at the park out from the downtown; whereas Pb was most abundant in leaves sampled at the roadside nearby the highway. Pb in cell-free extracts was higher in park than in roadside leaves. Although Cd in the leaf tissues was twofold lower than Pb, it was more abundant than Pb in cellular extracts deprived of all particulate matter. Leaves responded to different concentration of Cd and Pb modulating some eco-physiological and biochemical traits, roadside leaves showed reduced leaf lamina, higher content of photosynthetic pigments, hydrogen peroxide, and AsA, as well as higher CAT activity compared to park leaves. In the roadside leaves, a stress condition for photosynthetic apparatus can be hypothesized on the basis of the decline of photochemical activity, the increase of NPQ, and the reduction of Rubisco and D1 protein content. The elevated presence of thiol groups in these leaves suggests a possible role of Pb and Cd in activation of antioxidant responses.
Similar content being viewed by others
References
Alfani, A., Baldantoni, D., Maisto, G., Bartoli, G., & Virzo De Santo, A. (2000). Temporal and spatial variation in C, N, S and trace element contents in the leaves of Quercus ilex within the urban area of Naples. Environmental Pollution, 109, 119–129.
Alfani, A., Maisto, G., Prati, M. V., & Baldantoni, D. (2001). Leaves of Quercus ilex L. as biomonitors of PAHs in the air of Naples (Italy). Atmospheric Environment, 35, 3553–3559.
Alfani, A., De Nicola, F., Maisto, G., & Prati, M. V. (2005). Long-term PAH accumulation after bud break in Quercus ilex L. leaves in a polluted environment. Atmospheric Environment, 39, 307–314.
Allen, R. (1995). Dissection of oxidative stress tolerance using transgenic plants. Plant Physiology, 107, 1049–1054.
Arena, C., De Maio, A., De Nicola, F., Santorufo, L., Vitale, L., & Maisto, G. (2014). Assessment of eco-physiological performance of Quercus ilex L. leaves in urban area by an integrated approach. Water Air & Soil Pollution, 225, 1–12.
Barber, D. J. W., & Thomas, J. K. (1978). Reactions of radicals with lecithin bilayers. Radiation Research, 74, 51–65.
Bargagli, R. (1995). The elemental composition of vegetation and the possible incidence of soil contamination of samples. Science of the Total Environment, 176, 121–128.
Bargagli, R. (1998). Trace elements in terrestrial plants. Berlin: Springer-Verlag.
Bilger, W., & Björkman, O. (1990). Role of the xanthophyll cycle in photoprotection elucidated by measurements of light induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis L. Photosynthesis Research, 25, 173–185.
Castro-Díez, P., Villar-Salvador, P., Pérez-Rontomé, C., Maestro-Martínez, M., & Montserrat-Martí, G. (1997). Leaf morphology and leaf chemical composition in three Quercus (Fagaceae) species along a rainfall gradient in NE Spain. Trees, 11, 127–134.
Cobbett, C., & Goldsbrough, P. (2002). Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annual Review of Plant Biology, 53, 159–182.
Cornelissen, J. H. C., Lavorel, S., Garnier, E., Dıaz, S., Buchmann, N., Gurvich, D. E., Reich, P. B., Steege, H., Morgan, H. D., Van der Heijden, M. G. A., Pausas, J. G., & Poorter, H. (2003). Handbook of protocols for standardised and easy measurements of plant functional traits worldwide. Australian Journal of Botany, 51, 335–380.
Cosio, C., Martinoia, E., & Keller, K. (2004). Hyperaccumulation of cadmium and zinc in Thlaspi caerulescens and Arabidopsis halleri at the leaf cellular level. Plant Physiology, 134, 716–772.
Cvetanovska, L., Klincharska-Jovanovska, I., Dimeska, G., Srbinoska, M., & Cvetanovska, A. (2010). Anatomic and physiological disorder after intoxication with heavy metals in tobacco (Nicotiana tabacum L.) second Balkan conference on biology, Plovdiv. Biotechnology & Biotechnological Equipment, 24, 4–9.
Dabrowska, G., Mierek-Adamska, A., & Goc, A. (2013). Characterization of Brassica napus L. metallothionein genes (BMTs) expression in organs and during seed germination. Australian Journal of Crop Science, 7, 1324–1332.
De Nicola, F., Maisto, G., Prati, M. V., & Alfani, A. (2005). Temporal variations in PAH concentrations in Quercus ilex L. (holm oak) leaves in an urban area. Chemosphere, 61, 432–440.
De Nicola, F., Maisto, G., Prati, M. V., & Alfani, A. (2008). Leaf accumulation of trace elements and polycyclic aromatic hydrocarbons (PAHs) in Quercus ilex L. Environmental Pollution, 153, 376–383.
De Nicola, F., Lancellotti, C., Prati, M. V., Maisto, G., & Alfani, A. (2011). Biomonitoring of PAHs by using Quercus ilex leaves: source diagnostic and toxicity assessment. Atmospheric Environment, 45, 1428–1433.
De Nicola, F., Alfani, A., & Maisto, G. (2014). Polycyclic aromatic hydrocarbon contamination in an urban area assessed by Q. ilex leaves and soil. Environmental Science and Pollution Research, 21, 7616–7623.
De Nicola, F., Baldantoni, D., Maisto, G., & Alfani, A. (2017). Heavy metal and polycyclic aromatic hydrocarbon concentrations in Quercus ilex L. leaves fit an a priori subdivision in site typologies based on human management. Environmental Science and Pollution Research, 24(13), 11911–11918.
Demmig-Adams, B., Gilmore, A., & Adams, W. W. (1996). In vivo functions of carotenoids in higher plants. Federation of American Societies for Experimental Biology Journal, 10, 403–412.
Dey, S. K., Dey, J., Patra, S., & Pothal, D. (2007). Changes in the antioxidative enzyme activities and lipid peroxidation in wheat seedlings exposed to cadmium and lead stress. Brazilian Journal of Plant Physiology, 19, 53–60.
Durand, T. C., Sergeant, K., Planchon, S., Carpin, S., Label, P., Morabito, D., Hausman, J. F., & Renaut, J. (2010). Acute metal stress in Populus tremula x P. alba (717-1B4 genotype): leaf and cambial proteome changes induced by cadmium 2+. Proteomics, 10, 349–368.
Ellman, G. L. (1959). Tissue sulfydryl groups. Archives of Biochemistry and Biophysics, 82, 70–77.
Emamverdian, A., Ding, Y., Mokhberdora, F., & Xie, Y. (2015). Heavy metal stress and some mechanisms of plant defence response. The Scientific World Journal, 2015, 1–18. https://doi.org/10.1155/2015/756120.
Ercal, N., Gurer-Orhan, H., & Aykin-Burns, N. (2001). Toxic metals and oxidative stress part I: mechanisms involved in metal induced oxidative damage. Current Topics in Medicinal Chemistry, 1, 529–539.
Genty, B., Briantais, J. M., & Baker, N. R. (1989). The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta, 990, 87–92.
Gonçalves, J. F., Becker, A. G., Cargnelutti, D., Tabaldi, A. L., Pereira, L. B., Battisti, V., Spanevello, R. M., Morsch, V. M., Nicoloso, F. T., & Schetinger, M. R. C. (2007). Cadmium toxicity causes oxidative stress and induces response of the antioxidant system in cucumber seedlings. Brazilian Journal of Plant Physiology, 19, 223–232.
Hall, J. L. (2002). Cellular mechanisms for heavy metal detoxification and tolerance. Journal of Experimental Botany, 53, 1–11.
Hossain, Z., & Komatsu, S. (2013). Contribution of proteomic studies towards understanding plant heavy metal stress response. Frontiers Plant Science, 3, 1–12.
Hossain, M. A., Piyatida, P., Teixeira da Silva, J. A., & Fujita, M. (2012). Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. Journal of Botany, 2012, 1–37. https://doi.org/10.1155/2012/872875.
Jarvis, S. C., Joser, L. H. P., & Hopper, M. D. (1976). Cd uptake from solution by plants and its transport from roots to shoots. Plant and Soil, 44, 179–191.
Kieffer, P., Dommes, J., Hoffmann, L., Hausman, J. F., & Renaut, J. (2008). Quantitative changes in protein expression of cadmium-exposed poplar plants. Proteomics, 8, 2514–2530.
Kieffer, P., Planchon, S., Oufir, M., Ziebel, J., Dommes, J., Hoffmann, L., Hausman, J. F., & Renaut, J. (2009). Combining proteomics and metabolite analyses to unravel cadmium stress-response in poplar leaves. Journal of Proteome Research, 8, 400–417.
Krall, J. P., & Edwards, G. E. (1992). Relationship between photosystem II activity and CO2 fixation in leaves. Plant Physiology, 86, 180–187.
Kumar-Nanda, P. B. A., Dushenkov, V., Motto, H., & Raskin, I. (1995). Phytoextraction: the use of plants to remove heavy metals from soils. Environmental Science Technology, 29, 1232–1238.
Kupper, H., Kupper, F., & Spiller, M. (1998). In situ detection of heavy metal substituted chlorophylls in water plants. Photosynthesis Research, 58, 123–133.
Kupper, H., Setlik, I., Spiller, M., Kupper, F. C., & Prasil, O. (2002). Heavy metal-induced inhibition of photosynthesis: targets of in vivo heavy metal chlorophyll formation. Journal of Phycology, 38, 429–441.
Lichtenthaler, H. K. (1987). Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Method Enzymology, 148, 350–382.
Maisto, G., Alfani, A., Baldantoni, D., De Marco, A., & Virzo De Santo, A. (2004a). Trace metals in the soil and in Q. ilex L. leaves at anthropic and remote sites of the Campania region of Italy. Geoderma, 122, 269–279.
Maisto, G., De Nicola, F., Prati, M. V., & Alfani, A. (2004b). Leaf and soil PAH accumulation in an urban area of the Mediterranean region (Naples-Italy). Fresenius Environmental Bulletin, 13, 1263–1268.
Maisto, G., De Nicola, F., Iovieno, P., Prati, M. V., & Alfani, A. (2006). PAHs and trace elements in volcanic urban and natural soils. Geoderma, 136, 20–27.
Maisto, G., Santorufo, L., & Arena, C. (2013). Heavy metal accumulation in leaves affects physiological performance and litter quality of Quercus ilex L. Journal of Plant Nutrition and Soil Science, 176, 776–784.
Monaci, F., Mori, F., Lanciotti, E., Grechi, D., & Bargagli, R. (2000). Biominitoring of airborne metals in urban environments: new tracers of vehicle emission, in place of lead. Environmental Pollution, 107, 321–327.
Monni, S., Uhlig, C., Hansen, E., & Magel, E. (2001). Ecophysiological responses of Empetrum nigrum to heavy metals pollution. Environmental Pollution, 112, 121–129.
Patsikka, E., Kairavuo, M., Sersen, F., Aro, E. M., & Tyystjarvi, E. (2002). Excess copper predisposes photosystem II to photoinhibition in vivo by outcompeting iron and causing decrease in leaf chlorophyll. Plant Physiology, 129, 1359–1367.
Qian, H., Li, J., Sun, L., Chen, W., Sheng, G. D., Liu, W., & Fu, Z. (2009). Combined effect of copper and cadmium on Chlorella vulgaris growth and photosynthesis-related gene transcription. Aquatic Toxicology, 94, 56–61.
Sergiev, I., Alxieva, V., & Karanov, E. (1997). Effect of spermone, atrazine and combination between them on some endogenous protective systems and stress markers in plants. Comptes rendus de l'Academie bulgare des Sciences, 51, 121–124.
Seyyednejad, S. M., Niknejad, M., & Koochak, H. (2011). A review of some different effects of air pollution on plants. Research Journal of Environmental Sciences, 5, 302–309.
Sharma, P., & Dubey, R. (2005). Lead toxicity in plants. Brazilian Journal of Plant Physiology, 17, 35–52.
Steinnes, E., & Friedland, A. J. (2006). Metal contamination of natural surface soils from long-range atmospheric transport: existing and missing knowledge. Environmental Reviews, 14, 169–186.
Tangahu, B. V., Abdullah, S. R. S., Basri, H., Idris, M., Anuar, N., & Mukhlisin, M. (2011). A review on heavy metals (As, Pb, and Hg) uptake by plants through phytoremediation. International Journal of Chemical Engineering, 2011, 1–31. https://doi.org/10.1155/2011/939161.
Thormalley, P. J., & Vasak, M. (1985). Possible role for metallothionein in protection against radiation-induced oxidative stress. Kinetics and mechanism of its reaction with superoxide and hydroxyl radicals. Biochimica et Biophysica Acta, 827, 36–44.
Tiwari, S., Agrawal, M., & Marshall, F. M. (2006). Evaluation of ambient air pollution impact on carrot plants at a sub urban site using open top chambers. Environmental Monitoring and Assessment, 119, 15–30.
Tripathi, B. N., & Gaur, J. P. (2004). Relationship between copper- and zinc-induced oxidative stress and proline accumulation in Scenedesmus sp. Planta, 219, 397–404.
Tripathi, A. K., & Gautam, M. (2007). Biochemical parameters of plants as indicators of air pollution. Journal of Environmental Biology, 28, 127–132.
Ugolini, F., Tognetti, R., Raschia, A., & Bacci, L. (2013). Quercus ilex L. as bioaccumulator for heavy metals in urban areas: effectiveness of leaf washing with distilled water and considerations on the trees distance from traffic. Urban Forestry & Urban Greening, 12, 576–584.
Verbruggen, N., Hermans, C., & Schat, H. (2009). Molecular mechanisms of metal hyperaccumulation in plants. New Phytologist, 181, 759–776.
Verma, S., & Dubey, R. S. (2003). Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Science, 164, 645–655.
Waalkes, M. (2000). Cadmium carcinogenesis in review. Journal of Inorganic Biochemistry, 79, 241–244.
Wang, Y. S., Pi, L. Y., Chen, X., Chakrabarty, P. K., Jiang, J., Lopez De Leon, A., Liu, G-Z, Li, L., Benny, U., Oard, J., Ronald, P. C. & Songa, W-Y. (2006). Rice XA21 binding protein 3 is a ubiquitin ligase required for full Xa21-mediated disease resistance. The Plant Cell, 18, 3635–3646.
Wong, C. S. C., Li, X., & Thornton, I. (2006). Urban environmental geochemistry of trace metals. Environmental Pollution, 142, 1–16.
Yang, Z., & Chu, C. (2011). Towards understanding plant response to heavy metal stress. In A. Shanker (Ed.), Abiotic stress in plants – Mechanisms and adaptations (pp. 59–78). Shanghai: In Tech.
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
ESM 1
(DOCX 27 kb)
Rights and permissions
About this article
Cite this article
Arena, C., Santorufo, L., Cataletto, P.R. et al. Eco-physiological and Antioxidant Responses of Holm Oak (Quercus ilex L.) Leaves to Cd and Pb. Water Air Soil Pollut 228, 459 (2017). https://doi.org/10.1007/s11270-017-3638-4
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11270-017-3638-4