Journal of Environmental Management 146 (2014) 94e99

Contents lists available at ScienceDirect

Journal of Environmental Management journal homepage: www.elsevier.com/locate/jenvman

Different behaviours in phytoremediation capacity of two heavy metal tolerant poplar clones in relation to iron and other trace elements Daniela Baldantoni, Angela Cicatelli, Alessandro Bellino, Stefano Castiglione*  degli Studi di Salerno, Via Giovanni Paolo II 132, 84084 Fisciano (SA), Italy Dipartimento di Chimica e Biologia, Universita

a r t i c l e i n f o

a b s t r a c t

Article history: Received 1 February 2014 Received in revised form 23 July 2014 Accepted 30 July 2014 Available online

Plant biodiversity and intra-population genetic variability have not yet been properly exploited in the framework of phytoremediation and soil reclamation. For this reason, iron and other metal accumulation capacity of two Cu and Zn tolerant poplar clones, namely AL22 (Populus alba L.) and N12 (Populus nigra L.), was investigated in a pot experiment. Cuttings of the two clones were planted in iron rich soil collected from an urban-industrial area. Concentrations of Cd, Cu, Fe, Pb and Zn were analysed in leaves (at different times), as well as in stems and in roots (at the end of the experiment), both in control plants and in plants grown on a soil whose Fe availability was artificially enhanced. Results showed that Cd and Zn were preferentially accumulated in leaves, whereas Cu, Fe and Pb were mainly accumulated in roots. The main differences in metal accumulation between clones were related to Cd (about tenfold higher concentrations in N12) and Cu (higher concentrations in AL22). Once soil Fe availability was enhanced, the uptake and accumulation of all metals declined, with the exception of Fe at the first sampling time in AL22 leaves. The different behaviour of the two poplar clones suggests that a thoughtful choice should be made for their use in relation to soil heavy metal remediation. © 2014 Elsevier Ltd. All rights reserved.

Keywords: Phytoremediation Heavy metals Iron Populus alba L. (AL22) Populus nigra L. (N12)

1. Introduction Iron is one of the most abundant elements on Earth and it is essential to all organisms, being involved in crucial processes like electron transport in photosynthesis and respiration, and blood oxygen exchange in vertebrates. On a global scale, it plays a key role in producing the Earth magnetic field, which protects the biosphere from geomagnetic storms and streams of charged particles ejected from the sun surface (Birkeland, 1916), that are extremely dangerous to all living beings. Even the evolution of the human society has been tightly related to iron use since the early stages of human civilization, and it still heavily relies on iron industry. The huge scale of iron processing, amounting to several millions of tons in many countries worldwide, determines both local and broad scale contamination issues to comply with. Iron, indeed, can enter the food chains and affect human beings through the biomagnification process (Wong, 2003). High ingested doses of Fe can cause serious health problems including DNA, cellular and tissue damages, oncogene activations, hemorrhagic necrosis, sloughing of the stomach mucosa, diabetes, atherosclerosis, and hormonal and

* Corresponding author. E-mail address: [email protected] (S. Castiglione). http://dx.doi.org/10.1016/j.jenvman.2014.07.045 0301-4797/© 2014 Elsevier Ltd. All rights reserved.

immune system abnormalities (Gurzau et al., 2003). The problems related to environmental contamination, however, are not limited to iron. The environmental pollution caused by heavy metals (HMs) in general has been accelerated dramatically over the last decades, since emerging countries, which recently appeared on the global market, have increased their own mining and metallurgical industries. This resulted in a significant increase of polluted sites, both due to the metallurgical deposits and to solid, liquid and gaseous industrial wastes (Wong, 2003). In this context, the reduction of environmental contaminations and human health risks are primary challenges, and appropriate reclamation techniques are needed. Among these, a green technology, known as phytoremediation, underwent a remarkable development and gained broad consensus as an environmentally friendly alternative to the commonly used chemical and physical methods. Phytoremediation involves the use of plants for the reclamation of air, soil and water contaminated by organic and inorganic pollutants (Pilon-Smits, 2005). Phytoremediation is a general term including phyto-extraction, -stabilization, -degradation, -stimulation, -volatilization and rhizo-filtration. In particular, phytoextraction and phytostabilization refer to the preferential accumulation of pollutants in epigeous organs or in roots, respectively (Pilon-Smits, 2005). Phytoremediation has increased its importance during the last decade (Pilon-Smits, 2005; Golubev, 2011), becoming the

D. Baldantoni et al. / Journal of Environmental Management 146 (2014) 94e99

leading technology for soil and water reclamation in developed countries. It has several advantages, such as cost effectiveness, beneficial environmental impact, good acceptance from public opinion and politicians. However, this technique has also some drawbacks, mainly related to the long time needed to obtain an effective cleaning of the polluted areas, as compared to traditional engineering technologies, that are much faster but also extremely expensive for the municipalities and the environment (Mulligan et al., 2001). Phytoremediation, and phytoextraction in particular, can be achieved through hyperaccumulator plants, which have the capability to take up large quantities of HMs and to translocate them to the epigeous parts (Baker et al., 1994a; Wong, 2003), as in the case of Thlaspi caerulescens (Baker et al., 1994b) and Sedum alfredii (Yang et al., 2004). Hyperaccumulators, however, have strong limitations, due to the slow plant growth and the small biomass they produce, which limit their capacity to effectively reclaim contaminated soils. In the last ten years, to overcome these limitations, scientists have focused their attention on high biomass producing plants, such as maize, sunflower, rice, etc. (Baldantoni et al., 2011b; Komarek et al., 2007; Murakami and Ae, 2009), and on highly productive trees such as willow and poplar (Cicatelli et al., 2010; Tognetti et al., 2013). Poplar, in particular, has several interesting features that make it a good candidate for phytoremediation purposes. It is a fast growing tree with a deep and wide root system, it has a marked adaptability to different soils and climates and a unique capability to vegetative reproduction, which makes its propagation easy. Moreover, it has a very good tolerance to different contaminants, both organics and inorganics; can be pre-inoculated with Arbuscular mycorrhizal fungi (Baldantoni et al., 2011a; Lingua et al., 2008), and has high genetic biodiversity at both the species and the population level (Castiglione et al., 2009). Its capability to be used in short rotation coppices, in addition, allows its use in biomass production. Plant genetic biodiversity has a great potential for phytoremediation. Nehnevajova et al. (2005) demonstrated that different cultivars of sunflower have different HM tolerances, and some of them show pronounced phytoextractive and HM accumulating capacities. However, this potential was not properly exploited yet in the case of poplar and Salicaceae in general. Many papers in the scientific literature, indeed, focus their attention on a limited numbers of clones, or compare one or few clones of the same species with one or few belonging to different species (Pietrini et al., 2010; Migeon et al., 2012). Thus there has not been a clear evaluation of the phytoremediation capacities associated to the high genetic biodiversity present in the different poplar populations and species (Castiglione et al., 2009; Pietrini et al., 2010; Migeon et al., 2012). In this context, the purposes of the present research were to: i) compare the capacity of two poplar clones, namely AL22 (Populus alba L.) and N12 (Populus nigra L.), previously selected for their high tolerance to HMs, to phytostabilize or phytoextract, Cd, Cu, Fe, Pb and Zn from an artificially Fe polluted soil; ii) evaluate the influence of high concentrations of soil available Fe, supplied as iron sulphate, on uptake and bioaccumulation of the analysed metals in roots, stems and leaves of the two poplar clones.

2. Materials and methods 2.1. Experimental setting and analyses Six cuttings for each metal tolerant (Castiglione et al., 2009) P. alba (AL22) and P. nigra (N12) clones were planted (March 2007) in

95

pots filled with soil collected at a depth of 0e20 cm from an urbanindustrial area (40 420 4000 N; 14 460 4900 E) close to the town of Salerno (Italy). Pot filling soil was characterised at the beginning of the experiment (t0) for pH in distilled water (electrometric method on soil solution at a ratio of 1.0:2.5 w:w ¼ soil:water; HI 4212, Hanna, Italy), organic matter content (loss on ignition at 550  C for 4 h; Controller B 170, Nabertherm, Germany) and total and available concentrations of Cd, Cu, Fe, Pb and Zn (see for details Baldantoni et al., 2011a, b). Iron sulphate, Fe2(SO4)3, was added to the soil of three pots for each clone (T ¼ Treated plants) three times at weekly intervals, starting one month before the first leaf sampling (June 2007), reaching a final concentration of 450 mg g1 d.w. The plants grown in the untreated pots were kept as controls (C ¼ Control plants). Poplar leaves were collected after four (July 2007), five (August 2007), seven (October 2007) and sixteen (July 2008) months from cutting plantation. At the end of the experimental period (July 2008), stems and roots, as well as soils, were collected from all the pots. All the matrices were analysed for Cd, Cu, Fe, Pb and Zn concentrations. Metal total concentrations in leaves were determined on pulverised (liquid nitrogen) and dried (75  C, up to constant weight) samples, in stems and roots on ashes obtained from loss on ignition (550  C for 4 h; Controller B 170, Nabertherm, Germany), and in soil granulometric fractions ( leaves > stems (Shi et al., 2011). The Fe treatment, which did not affect the plant growth and health (data not shown), raised the leaf/root TFs in both clones for

Fig. 2. Mean concentrations ± standard errors of Cd, Cu, Fe, Pb and Zn in leaves, stems and roots of treated (T) and control (C) P. alba AL22 and P. nigra N12 clones. The asterisks indicate significant (*: P  0.05, **: P  0.01, ***: P  0.001) differences between the treatments.

Table 1 Translocation Factors (TFs) of Cd, Cu, Fe, Pb and Zn in AL22 and N12 poplar clones calculated as Cl/Cr, Cs/Cr and Cl/Cs, where Cl is the metal concentrations in leaves, Cs in stems and Cr in roots of the control (C) and treated (T) plants. AL22

Cd

light on Cu and Zn uptake, compartmentalization and translocation through the use of several “Omics” approaches (Lingua et al., 2012; Cicatelli et al., 2012, 2014). However, little is known about the capabilities of poplar to phytoremediate Fe polluted soils, the available information being published by our research group (Baldantoni et al., 2011a) and by Giachetti and Sebastiani (2006). The problem regarding the phytoremediation of Fe is related to its limited bioavailability (Kabata-Pendias and Mukherjee, 2007). Even in our own experiments, despite the high soil Fe total concentration, its bioavailable fraction was only a thousandth part of the total. To overcome this limitation, and to understand the potentialities for HM phytoremediation with the two poplar clones in the

Cu

Fe

Pb

Zn

Cl/Cr Cs/Cr Cl/Cs Cl/Cr Cs/Cr Cl/Cs Cl/Cr Cs/Cr Cl/Cs Cl/Cr Cs/Cr Cl/Cs Cl/Cr Cs/Cr Cl/Cs

N12

C

T

C

T

1.759 0.887 1.984 0.323 0.247 1.307 0.051 0.012 4.328 0.001 0.001 0.001 4.542 0.810 5.609

2.301 0.890 2.584 0.436 0.285 1.534 0.077 0.014 5.670 0.011 0.001 0.001 5.148 0.942 5.463

3.015 0.522 5.773 0.230 0.210 1.097 0.020 0.004 4.688 0.051 0.014 3.737 1.931 0.395 4.889

3.256 0.954 3.412 0.430 0.451 0.955 0.072 0.001 53.206 0.160 0.079 2.015 6.624 1.412 4.691

98

D. Baldantoni et al. / Journal of Environmental Management 146 (2014) 94e99

Table 2 Total and available metal concentration (mg g1 d.w.) in the soil at the end of the study period for each poplar clone (AL22 and N12) and for each treatment (C and T). Total concentration AL22

C T C T

N12

Cd

Cu

Fe

Pb

Zn

0.13 0.14 0.45 0.43

106.38 113.14 73.87 66.34

36520 37430 36330 36580

98.75 93.40 75.52 73.99

149.00 144.00 140.00 136.00

Available concentration AL22

C T C T

N12

Cd

Cu

Fe

Pb

Zn

0.001 0.001 0.018 0.018

11.59 10.67 23.31 20.93

19.30 17.40 24.30 29.60

5.46 5.08 8.65 8.29

6.48 4.65 6.54 6.62

Table 3 Metal Bioavailability Factors (MBFs) in the pot soil.

AL22 N12

C T C T

Cd

Cu

Fe

Pb

Zn

0.33 0.50 4.05 4.24

10.90 9.43 31.56 31.56

0.05 0.05 0.07 0.08

5.53 5.44 11.45 11.21

4.35 3.22 4.67 4.88

Table 4 Heavy metal (Cd, Cu, Fe, Pb, Zn) Bio-Accumulation Factors (BAFs) in AL22 and N12 poplar clones, calculated as Cl/Csoil, Cs/Csoil and Cr/Csoil, where Cl is the metal concentration in leaves, Cs in stems, Cr in roots of the control (C) and treated (T) plants and Csoil is the metal concentration in the soil at the end of the experiment, for each clone and for each treatment. AL22

Cd

Cu

Fe

Pb

Zn

Cl/Csoil Cs/Csoil Cr/Csoil Cl/Csoil Cs/Csoil Cr/Csoil Cl/Csoil Cs/Csoil Cr/Csoil Cl/Csoil Cs/Csoil Cr/Csoil Cl/Csoil Cs/Csoil Cr/Csoil

N12

C

T

C

T

2.09 1.05 1.19 0.14 0.11 0.44 0.006 0.001 0.125 0.001 0.001 0.112 2.64 0.47 0.58

1.90 0.74 0.83 0.13 0.09 0.30 0.006 0.001 0.072 0.001 0.001 0.064 2.08 0.38 0.40

3.61 0.63 1.20 0.12 0.11 0.54 0.002 0.001 0.079 0.005 0.001 0.108 2.98 0.61 1.54

2.80 0.82 0.86 0.16 0.16 0.36 0.004 0.001 0.058 0.011 0.006 0.071 3.26 0.69 0.49

contamination. In these cases, methods to reduce Fe availability, such as oxidation or precipitation, could enhance the uptake of other metals by the two poplar clones. The different behaviour in relation to leaf Fe concentration of AL22 and N12 suggests different mechanisms of Fe absorption, transport and accumulation (Baldantoni et al., 2011a). The decrease in leaf Fe concentration along the time in AL22 clone, in particular, was similar to that observed for Cu in another P. alba clone (AL35), selected by our research team (Castiglione et al., 2009). We supposed in that case that the metal was moved and re-translocated to the roots (Lingua et al., 2014), where a high concentration of Cu was observed, and this could be the case for Fe in AL22 clone. Heavy metal total concentrations in the soil were comparable between the two clones and between the treatments, whereas HM available fractions were generally higher in the soil where the N12 plants grew. This was particularly evident for Cu and Pb, and especially for Cd, which showed MBF values about ten-fold higher in the soils planted with N12 cuttings, independently from Fe addition. This could be due to root exudates produced by this specific poplar clone, which may increase the bioavailable fraction of many HMs and enhance the metal uptake of some of them. 5. Conclusions Our research highlights that the two poplar clones (P. alba AL22 and P. nigra N12), previously selected for high tolerance to Cu and Zn, show a remarkable capacity to absorb and accumulate HMs. Both clones are suitable for phytostabilization of Cu, Fe and Pb, and for phytoextraction of Cd and Zn. The N12 clone is particularly suitable for Cd remediation. High Fe bioavailability reduces HM accumulations, suggesting the usefulness of soil pretreatments to reduce Fe bioavailability and enhance phytoremediation of multi metal polluted soils. Acknowledgements This work was supported by funds from the Italian Ministry for Education, University and Research (PRIN 2005_2005055337), the Italian Ministry of Environment, Land and Sea Protection (“Research and development in biotechnology applied to the protection of the environment” in collaboration with the People's Republic of China), and the University of Salerno (Fondo d’Ateneo per la Ricerca di Base, FARB 2006-07, project ORSA065479). We also acknowledge Prof. Elizabeth Illingworth for the English revision, and for the careful reading and correction of the text. References

all analysed HMs. Concerning this, the T plants showed lower root concentrations for all the analysed metals, but this was not coupled with a higher metal accumulation in the epigeous parts. The only improvement in metal accumulation due to Fe treatment was found for Fe in the leaves of AL22 clone during the first vegetative season, although the accumulation was time dependent, and the concentration decreased along the time. These observations suggest that a high Fe availability could reduce the uptake and accumulation of the analysed metals (with the exception of Fe in an early stage in AL22 clone) that resulted in lower root metal concentrations and thus higher leaf/root TFs (that cannot be thus considered indicative of higher translocation to the leaves). This finding could be of interest to enhance phytoremediation in the case of multi-metal polluted soils with high Fe availability. Although such condition is rarely an issue in phytoremediation, this could be the case for particular sites and certain types of

An, Y., 2004. Soil ecotoxicity assessment using cadmium sensitive plants. Environ. Pollut. 127, 21e26. Baker, A.J.M., McGrath, S.P., Sidoli, C.M.D., Reeves, R.D., 1994a. The possibility of in situ heavy metal decontamination of polluted soils using crops of metalaccumulating plants. Resour. Conser. Recycl. 11, 41e49. Baker, A.J.M., Reeves, R.D., Hajar, A.S.M., 1994b. Heavy-Metal accumulation and tolerance in british populations of the metallophyte Thlaspi-Caerulescens J-andC-Presl (Brassicaceae). New. Phytol. 127, 61e68. Baldantoni, D., Bellino, A., Cicatelli, A., Castiglione, S., 2011a. Artificial mycorrhization does not influence the effects of iron availability on Fe, Zn, Cu, Pb and Cd accumulation in leaves of a heavy metal tolerant white poplar clone. Plant Biosyst. 145, 236e240. Baldantoni, D., Cicatelli, A., Castiglione, S., 2011b. Genetic biodiversity of maize and sunflower commercial cultivars and their phytoextraction capability of a multimetal artificially polluted soil. In: Golubev, I.A. (Ed.), Handbook of Phytoremediation Nova Science Publishers Inc. Hauppauge, NY, pp. 631e650. Baldantoni, D., Ligrone, R., Alfani, A., 2009. Macro- and trace-element concentrations in leaves and roots of Phragmites australis in a volcanic lake in Southern Italy. J. Geochem. Explor. 101, 166e174. Birkeland, K., 1916. Are the Solar Corpuscular Rays that Penetrate the Earth's Atmosphere Negative or Positive Rays?. Videnskapsselskapets Skrifter, I Mat e Naturv. Klasse 1.

D. Baldantoni et al. / Journal of Environmental Management 146 (2014) 94e99 Castiglione, S., Todeschini, V., Franchin, C., Torrigiani, P., Gastaldi, D., Cicatelli, A., Rinaudo, C., Berta, G., Biondi, S., Lingua, G., 2009. Clonal differences in survival capacity, copper and zinc accumulation, and correlation with leaf polyamine levels in poplar: a large-scale field trial on heavily polluted soil. Environ. Pollut. 157, 2108e2117. Cicatelli, A., Lingua, G., Todeschini, V., Biondi, S., Torrigiani, P., Castiglione, S., 2010. Arbuscular mycorrhizal fungi restore normal growth in a white poplar clone grown on heavy metal-contaminated soil, and this is associated with upregulation of foliar metallothionein and polyamine biosynthetic gene expression. Ann. Bot. 106, 791e802. Cicatelli, A., Lingua, G., Todeschini, V., Biondi, S., Torrigiani, P., Castiglione, S., 2012. Arbuscular mycorrhizal fungi modulate the leaf transcriptome of a Populus alba L. clone grown on a zinc and copper-contaminated soil. Environ. Exp. Bot. 75, 25e35. Cicatelli, A., Todeschini, V., Lingua, G., Biondi, S., Torrigiani, P., Castiglione, S., 2014. Epigenetic control of heavy metal stress response in mycorrhizal versus nonmycorrhizal poplar plants. Environ. Sci. Pollut. Res. Int. 21, 1723e1737. Dos Santos Utmazian, M.N., Wenzel, W.W., 2007. Cadmium and zinc accumulation in willow and poplar species grown on polluted soils. J. Plant. Nutr. Soil. Sci. 170, 265e272. Giachetti, G., Sebastiani, L., 2006. Metal accumulation in poplar plant grown with industrial wastes. Chemosphere 64, 446e454. Golubev, I.A., 2011. Handbook of Phytoremediation. Nova Science Publishers, Inc., Hauppauge e NY. Gross, J., Ligges, U., 2012. Nortest: Tests for Normality. R package version 1.0-2. Gurzau, E.S., Neagu, C., Gurzau, A.E., 2003. Essential metals - case study on iron. Ecotoxicol. Environ. Saf. 56, 190e200. Hu, Y., Nan, Z., Su, J., Wang, N., 2013. Heavy metal accumulation by poplar in calcareous soil with various degrees of multi-metal contamination: implications for phytoextraction and phytostabilization. Environ. Sci. Pollut. Res. 20, 7194e7203. Kabata-Pendias, A., Mukherjee, A.B., 2007. Trace Elements from Soil to Human. Springer, Berlin, Heidelberg, New York. Kabata-Pendias, A., Pendias, H., 2001. Trace Elements in Soils and Plants, third ed. CRC Press. Komarek, M., Tlustos, P., Szakova, J., Chrastny, V., Ettler, V., 2007. The use of maize and poplar in chelant-enhanced phytoextraction of lead from contaminated agricultural soils. Chemosphere 67, 640e651. Lindsay, W.L., Norvell, W.A., 1978. Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil. Sci. Soc. Am. J. 42, 421e428. Lingua, G., Bona, E., Todeschini, V., Cattaneo, C., Marsano, F., Berta, G., Cavaletto, M., 2012. Effects of heavy metals and Arbuscular mycorrhiza on the leaf proteome of a selected poplar clone: a time course analysis. PLoS ONE 7, e38662. Lingua, G., Franchin, C., Todeschini, V., Castiglione, S., Biondi, S., Burlando, B., Parravicini, V., Torrigiani, P., Berta, G., 2008. Arbuscular mycorrhizal fungi differentially affect the response to high zinc concentrations of two registered poplar clones. Environ. Pollut. 153, 137e147. Lingua, G., Todeschini, V., Grimaldi, M., Baldantoni, D., Proto, A., Cicatelli, A., Biondi, S., Torrigiani, P., Castiglione, S., 2014. Polyaspartate, a biodegradable

99

chelant that improves the phytoremediation potential of poplar in a highly metal-contaminated agricultural soil. J. Environ. Manage. 132, 9e15. n, P., Maraonn, T., Murillo, J.M., Robinson, B., 2004. White poplar (Populus Madejo alba) as a biomonitor of trace elements in contaminated riparian forests. Environ. Pollut. 132, 145e155. Marmiroli, M., Imperiale, D., Maestri, E., Marmiroli, N., 2013. The response of Populus spp. to cadmium stress: chemical, morphological and proteomics study. Chemosphere 93, 1333e1344. Migeon, A., Richaud, P., Guinet, F., Blaudez, D., Chalot, M., 2012. Hydroponic screening of poplar for trace element tolerance and accumulation. Int. J. Phytoremed. 14, 350e361. Mulligan, C.N., Yong, R.N., Gibbs, B.F., 2001. An evaluation of technologies for the heavy metal remediation of dredged sediments. J. Hazard. Mater. 85, 145e163. Murakami, M., Ae, N., 2009. Potential for phytoextraction of copper, lead, and zinc by rice (Oryza sativa L.), soybean (Glycine max [L.] Merr.), and maize (Zea mays L. J. Hazard. Mater. 162, 1185e1192. Nehnevajova, E., Herzig, R., Federer, G., Erismann, K.H., Schwitzgubel, J.P., 2005. Screening of sunflower cultivars for metal phytoextraction in a contaminated field prior to mutagenesis. Int. J. Phytoremed. 7, 337e349. Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O'Hara, R.B., Simpson, G.L., Solymos, P., Henry, H., Wagner, S., Wagner, H., 2013. Vegan: Community Ecology Package. R package version 2.0-8. Panda, S.K., Choudhury, S., 2005. Chromium stress in plants. Braz. J. Plant Physiol. 17, 95e102. Pietrini, F., Zacchini, M., Iori, V., Pietrosanti, L., Bianconi, D., Massacci, A., 2010. Screening of poplar clones for cadmium phytoremediation using photosynthesis, biomass and cadmium content analyses. Int. J. Phytoremed. 12, 105e120. Pilon-Smits, E., 2005. Phytoremediation. Annu. Rev. Plant Biol. 56, 15e39. R Core Team, 2., 2013. R Core Team 2013. R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Robinson, B., Mills, T., Petit, D., Fung, L., Green, S., Clothier, B., 2000. Natural and induced cadmium-accumulation in poplar and willow: implications for phytoremediation. Plant Soil. 227, 301e306. Shi, X., Zhang, X., Chen, G., Chen, Y., Wang, L., Shan, X., 2011. Seedling growth and metal accumulation of selected woody species in copper and lead/zinc mine tailings. J. Environ. Sci. 23, 266e274. 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. Int. J. Chem. Engin. 2011, 1e31. Tognetti, R., Cocozza, C., Marchetti, M., 2013. Shaping the multifunctional tree: the use of Salicaceae in environmental restoration. iForest 6, 37e47. Wong, M.H., 2003. Ecological restoration of mine degraded soils, with emphasis on metal contaminated soils. Chemosphere 50, 775e780. Yang, X.E., Long, X.X., Ye, H.B., He, Z.L., Calvert, D.V., Stoffella, P.J., 2004. Cadmium tolerance and hyperaccumulation in a new Zn-hyperaccumulating plant species (Sedum alfredii Hance). Plant Soil. 259, 181e189. Zeileis, A., Torsten, H., 2002. Diagnostic checking in regression relationships. R. News 2, 7e10.

Different behaviours in phytoremediation capacity of two heavy metal tolerant poplar clones in relation to iron and other trace elements.

Plant biodiversity and intra-population genetic variability have not yet been properly exploited in the framework of phytoremediation and soil reclama...
523KB Sizes 4 Downloads 5 Views