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Published in J. Environ. Qual. 33:1779-1785 (2004).
© ASA, CSSA, SSSA
677 S. Segoe Rd., Madison, WI 53711 USA

TECHNICAL REPORTS

Plant and Environment Interactions

Clonal Differences in Mercury Tolerance, Accumulation, and Distribution in Willow

Yaodong Wang* and Maria Greger

Department of Botany, Stockholm University, SE-106 91 Stockholm, Sweden

* Corresponding author (yaodong.wang{at}botan.su.se).

Received for publication November 19, 2003.

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
This study was performed to investigate mercury (Hg) tolerance, accumulation, and translocation within the genus Salix for the potential use of this plant to remediate Hg-contaminated sites. Six clones of willow (Salix spp.) were tested on tolerance to Hg by treating plants grown in solution culture with 0 to 15 µM HgCl2. Results showed that willow had a large variation in its sensitivity to Hg. However, the accumulation and translocation of Hg to shoots was similar in the eight tested willow clones as shown by cold vapor atomic absorption spectrometry analysis when plants were treated with 0.5 µM HgCl2 in a nutrient solution. The majority of total Hg accumulated was localized to the roots, whereas only 0.45 to 0.62% of the total Hg accumulated via roots was translocated to the shoots. Thus, the root system is the main tissue of willow that accumulates Hg and the majority of the Hg in the root system (80%) was bound in the cell wall.

Abbreviations: EC50, the HgCl2 concentration where growth was reduced by 50% • TT95b, toxicity threshold indicating the HgCl2 concentration where growth was reduced by 5% • UTmax, maximum unit toxicity


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
MERCURY POLLUTION is a global environmental problem (Schroeder and Munthe, 1998; Boening, 2002). Mercury pollution of soil is believed to contribute to health risks, phytotoxicity to plants, and long-term effects on soil fertility. Many industrial activities, including the mining of gold, silver, and Hg itself, have caused Hg contamination of terrestrial and aquatic ecosystems. Numerous Hg-contaminated sites exist in the world and new techniques for remediation are urgently needed. One technique for remediating metal-contaminated soil in situ is phytoextraction, which is considered as an environmental friendly method and has been studied for many heavy metals (Salt et al., 1998; Lasat, 2002). In phytoextraction, metal-tolerant plants with high metal accumulation and high biomass production are used. High biomass producing willow clones are examples of high-metal-tolerant and high-metal-accumulating plants, which can be used in phytoextraction of heavy metals such as cadmium and zinc (Greger and Landberg, 1999). Whether willow is sufficiently Hg tolerant and accumulates large amounts of Hg is, however, a question.

Mercury accumulation in plants has been studied in several plant species. Pea (Pisum sativum L.) and spearmint (Mentha spicata L.) absorbed Hg from solution, and roots accumulated much greater amounts of Hg than shoots (Beauford et al., 1977). Similar results were found in Norway spruce [Picea abies (L.) H. Karst.] (Godbold and Hütterman, 1988). Mercury accumulation has also been observed in mushrooms and aquatic plants (Coquery and Welbourn, 1994; Kalac and Svoboda, 2000). However, to our knowledge, no detailed study on Hg accumulation in willow has been presented in the literature.

Mercury is considered to be one of the most toxic metals to plants. Mercuric cations (Hg2+) have high affinities for sulfur. Because almost all proteins contain sulfhydryl groups (-SH) or disulfide bridges (-S-S-), mercurials can disturb almost any function in which proteins are involved (Clarkson, 1972). Many physiological and biochemical reactions (e.g., light and dark reactions in the photosynthesis, mineral nutrient uptake, and transpiration) are affected by Hg (Godbold and Hütterman, 1988; Godbold, 1994; Patra and Sharma, 2000). Plants can generally sequester toxic ions in complexes at the cytoplasm to defend against their phytotoxicity. Glutathione (GSH)-related phytochelatins (Rajesh et al., 1996; Zenk, 1996) are the most dominant molecules found so far to sequester the metal ions. Suhadra et al. (1993) found that, compared with normal seedlings, those from Hg-treated seeds exhibited a larger amount of nonprotein SH, indicating the possible involvement of phytochelatins in the Hg-reduced adaptive response. Expression of genes merA and merB, originating from bacteria, can also detoxify Hg in transgenic plants, which convert hazardous methyl-Hg and Hg2+ to the less toxic volatile elemental Hg (Hg0) that is released to the air (Rugh et al., 1996; Bizily et al., 1999, 2000). Although quite a few reports have involved Hg toxicity, tolerance, and uptake of plants, the systematic study in view of its potential application in plant phytoextraction is far from sufficient.

The aim of this paper was to determine whether willow is tolerant to Hg, and if it accumulates and translocates large quantities of Hg to the shoots. This could clarify the potential use of willow to remediate Hg-contaminated soils. The hypotheses were as follows. First, willow clones may differ in their sensitivity to Hg, because willow has been shown to have a large variation among clones in their sensitivity to many other heavy metals (Landberg and Greger, 1996; Greger and Landberg, 1999; Greger et al., 2001). Second, willow clones may also vary in accumulation and translocation of Hg, because there is a distinct variation in accumulation and translocation of other heavy metals among different clones (Greger and Landberg, 1999; Greger et al., 2001). It was assumed that willow clones with high tolerance, accumulation, and translocation of Hg to the shoots could be selected for future phytoextraction studies.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Plant Growth Condition
Selected clones of willow included Orm, Tora, 88-31-7, 88-19-3, 88-11-4, 78183, and 78118 (from Salix viminalis L.) and Björn (from S. viminalis x Salix schwerinii E. L. Wolf.). Woody cuttings from 1-yr-old shoots with high or low capacities in accumulation, tolerance, and translocation of Zn, Cd, and Cu (Greger and Landberg, 1999) were cultivated in a climate chamber. Cuttings were mounted six by six in polystyrene plates, rooted, and cultivated in 1-L pots containing 100 µM Ca(NO3)2 solution. Plants were illuminated 16 h per day with a photon flux density of 250 to 300 µmol m–2 s–1 of halogen lamps (Osram Powerstar HOI-R; Hanf, Oldenburg, Germany). The temperature was 23°C in light and 19°C in dark and the relative humidity was 70%. The cultivation conditions of climate chamber described above remained the same in all experiments.

Mercury Sensitivity
Two-week-old cuttings of six willow clones were treated in 1 L of 100 µM Ca(NO3)2 solution with 0, 0.5, 1.5, 3, 5, and 15 µM of HgCl2 for 2 wk, respectively. The stored nutrients in the cutting can support willow growth for 4 wk with only 100 µM Ca(NO3)2 addition (shown in pre-tests). Therefore, to avoid Hg complex formation with other ions, only Ca(NO3)2 was added in the Hg toxicity tests. To study the variation in Hg tolerance among clones, the six cuttings in one pot were considered as one replicate, and three replicates were conducted for each treatment.

Mercury Accumulation and Translocation
Three-week-old cuttings of eight willow clones were transferred to a nutrient solution that contains (in µM) the following: 163 KNO3, 51 KH2PO4, 36 MgSO4, 182 Mg(NO3)2, 0.42 MgCl2, 1.6 FeSO4, 1.6 K2EDTA, 205 Ca(NO3)2, 0.93 MnSO4, 2.4 H3BO3, 0.064 CuCl2, 0.064 ZnCl2, 0.013 Na2MoO4, and 0.093 Na2SiO4. The initial pH of the solution was 5.3, and pH was not adjusted during the experiments. The solution was changed once a week and plants were grown in this solution for 3 wk. Thereafter, to evaluate differences in Hg accumulation and translocation among clones, plants were transferred into a plant chamber system (described below), where roots were sealed in 550 mL of nutrient solution with one addition of 0.5 µM HgCl2. Plants were grown for 3 d in the plant chamber.

Two willow clones with low and high Hg-tolerant properties, respectively, were further used to study their susceptibilities to Hg and accumulation of Hg in nutrient solution with additions of 0.5, 1, and 2 µM HgCl2, respectively. Because most of the Hg added in solution was found to be accumulated by plants within two days of cultivation, or evaporated from the surface of solution, long-term effects of Hg on plant accumulation and translocation were investigated with these two clones by changing 550 mL of nutrient solution with 1 µM HgCl2 addition every second day for 10 d. All experiments were performed with three replicates for each Hg treatment and a control without Hg.

Plant Chamber System
The plant chamber was designed to study Hg accumulation and translocation, and to avoid Hg accumulation by leaves from air volatilized from the surface of the solution. The plant chamber consisted of two PVC cylinders, the lower gray one with a volume of 0.59 L and the higher transparent one with 2.6 L (Fig. 1). In the upper part, there were holes for airflow (3.5 mm in diameter) through which a 3- to 4-cm gray PVC tube was mounted. To prevent Hg penetration from nutrient solution in the lower cylinder into the upper cylinder, several precautions were taken. A third part was placed between the two cylinders with airflow through. Between the upper and the middle part as well as the middle part and the lower part of the cylinder a circular rubber sleeve was placed, with a hole of 12 mm in diameter. To be able to get the plant through the rubber sleeve, two stair-shaped cuts were made, 2 cm in each direction. To avoid air penetration from the solution to the system without passing through the plant, the soft sealing material Terostat IX (Teroson; KG Knutsson Handels AB, Sollentuna, Sweden) and silicon glue (Silikon; Casco Nobel AB, Stockholm, Sweden) were put around the stem. Metallic clips were used to keep the two parts of the cylinder together.



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  		Fig. 1. Illustration of the plant chamber, a system to evaluate Hg accumulation and translocation.

 
Air was pumped into the upper cylinder by means of a membrane pump (Type LM 22; ASF Thomas, Wuppertal, Germany). Up to 10 plant cylinders were connected to one pump and airflow was regulated with plastic taps (aquaria taps; Algarde Aquatic Products Enterprise House, Pinxton, UK) and measured with a flow meter. The airflow was 55 L h–1. To avoid Hg contamination in the passing air, a hopcalite trap (200 mg granules of Cu and Mn oxides; ORBO no. 1002; Supelco, Bellefonte, PA) was used to trap the Hg before the airflow passed into the upper cylinder.

Transpiration Measurements
To measure the water transpiration of plants cultivated in cylinders, all cylinders were weighed at the beginning, before and after intermediate change of solutions, and before harvesting the plant. The water loss was calculated for each 24-h period according to the formula:

[1]
where WL is the water loss during 24 h, ws is the shoot dry weight (40°C) at the end of the measurements, and w1 and w2 are the weights of cylinders with plants at the beginning and end of the interval, respectively.

Harvest and Analyses
Plant roots were washed successively with 2x distilled water, 20 mM Na2–ethylenedinitrilic tetraacetic acid (EDTA), and 2x distilled water (4 s in each) (Naraho and Gaur, 1995). Thereafter, plants were divided in shoots, woody cuttings, and roots and dried at 40°C for 3 d. For calculations on a real dry-weight basis, parts of the dried material were further dried at 105°C for 24 h. To measure the Hg fraction bound to the cell wall, the crude cell wall was obtained according to the method used by Zornoza et al. (2002). Roots (100 mg dry wt.) were incubated in 2 mL of absolute ethanol (99%) for 60 min in a water bath (40°C). Afterward, the residue was successively washed with ethanol (three times), chloroform and methanol (2/1, v/v) (once), and acetone (three times), and the Hg content of the dry residues was thereafter analyzed.

Samples analyzed for Hg content were wet-digested in HNO3 and HClO4 (7:3 v/v) for 18 h in a heating program with the highest temperature set to 180°C. As standard reference material, BCR No. 60 with a Hg concentration of 0.34 mg kg–1 was used. Solution samples and plant materials with standard additions were thereafter analyzed with cold vapor atomic absorption spectrophotometry (CVAAS) (SpectrAA-100; Varian, Palo Alto, CA) using 0.3% NaBH4 in 0.5% NaOH as reducing agent and 5 M HCl to convert Hg ions into Hg0. Nitrogen was used as carrying gas. Detection limit for the method used was 5 µg kg–1 of total Hg.

Phytochelatin in roots was assayed by the monobromobimane (mBBr) method (Newton et al., 1981). Samples (200 mg fresh root) were ultramixed (Polytron PT 2000; Kinematica, Littau, Switzerland) for 10 s in 1 mL 0.1 M HCl. The samples were then centrifuged (Biofuge A 1230; Heraeus, Hanau, Germany) at 16000 x g for 5 min at 4°C. The supernatant was filtered with a 0.45-µm Millex HA filter (Millipore, Billerica, MA). Fifty microliters of sample, 35 µL H2O, 10 µL Tris (pH 8), and 5 µL 20 mM mBBr (dissolved in acetonitrile) was mixed in an Eppendorf (Wertheim, Germany) tube and incubated at 37°C for 15 min. The reaction was terminated by adding 900 µL 5% acetic acid. Extracts were thereafter separated by high performance liquid chromatography (HPLC) on a Chromolith column (50 mm; VWR, West Chester, PA) using an acetonitrile gradient. The SH-containing compounds were detected fluorimetrically.

Calculation
Mercury toxicity was measured in terms of dry weight of shoot mass and dry weight of root mass, respectively, of treated plants in relation to the control in all treatments. To analyze the Hg tolerance differences among willow clones, a modified Weibull model according to Taylor et al. (1991) was used to compare dose–response curves. Data were analyzed by using the iterative fitting procedure nonlinear fit of JMP Version 2.0.2 software (SAS Institute, 1991) and the modified Weibull formula (Eq. [2]) according to Taylor et al. (1991) based on works by Rawling and Cure (1985) and Kinraide and Parker (1989):

[2]
where y is the response (yield) of the concentration of Hg in the growth medium (x), a is the absolute minimum growth, b is the unaffected growth, and c and d are the parameters showing the shape of the curve. The toxicity threshold indicating the HgCl2 concentration where growth was reduced by 5% (TT95b), the HgCl2 concentration where growth was reduced by 50% (EC50), and the maximum unit toxicity (UTmax) indicating the point of maximum slope of the dose–response curves were calculated by:

[3]

[4]

[5]

Effective accumulation, translocation, and Hg fraction in the cell wall after Hg treatments were calculated as:

[6]

[7]

[8]

Background concentrations of Hg in plants cultivated without Hg were subtracted from concentrations in treated plants before these calculations.

Statistical Analysis
Student's t test (p = 0.05) and ANOVA ({alpha} = 0.05) were used to statistically test for significant differences. For all statistical analyses Statistica '99 Version 5.5 (StatSoft, 1999) was used.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
The result from the Hg sensitivity study demonstrated that willow clones had a large variation in their sensitivity to Hg. The EC50 value of the six willow clones ranged from 0.28 to 1.55 µM in terms of dry weight of shoot mass and from 0.29 to 1.95 µM in terms of dry weight of root mass (Table 1). Toxicity threshold (TT95b) and maximum unit toxicity (UTmax) also showed large differences among clones. Clone 88-31-7 was the most sensitive according to TT95b, UTmax, and EC50 in both roots and shoots. The clone with highest tolerance, however, depended on which parameter was used. According to TT95b, clone Björn had the highest root tolerance while clone 88-11-4 had the highest shoot tolerance. However, according to UTmax or EC50, 88-11-4 had the highest root tolerance, and Björn had the highest shoot tolerance.


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  		Table 1. Interpretation of the differences in Hg toxicity among six willow clones using the modified Weibull frequency distribution to model dose responses to Hg (n = 3, ±SE).{dagger}

 
The mean value of effective Hg accumulation among eight tested clones ranged from 55.0 to 73.9% after cultivation in 0.5 µM HgCl2 for 3 d (Table 2). Most of the Hg accumulated via roots remained in the roots, and only 0.45 to 0.62% of the Hg accumulated by the plants was translocated to the shoots. There was no significant difference between clones in accumulation and distribution of Hg among the eight studied willow clones.


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  		Table 2. Accumulation and distribution of Hg in eight willow clones cultivated in 550 mL of nutrient solution with 0.5 µM HgCl2 for 3 d (n = 3, ±SE).

 
The tolerant clone Björn and the sensitive clone 88-31-7 were selected to study the accumulation and translocation of Hg at different Hg concentrations. Results show that Hg concentrations in both roots and shoots of the two studied clones increased with increasing Hg concentrations (Fig. 2). The translocation of Hg to shoots tended to decrease in the sensitive clone 88-31-7 when Hg concentrations in the solution increased, whereas the tolerant clone Björn did not. Björn had a significantly higher effective Hg accumulation than the sensitive clone 88-31-7 at 2 µM HgCl2 treatment (Table 3).



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  		Fig. 2. Mercury accumulation in the roots and shoots increased in relation to the Hg concentration in solution. Plants were cultivated in 550 mL of nutrient solution with different concentrations of HgCl2 addition for 3 d in the plant chamber system (n = 3, ±SE).

 

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  		Table 3. Mercury accumulation and distribution in Hg-sensitive (88-31-7) and Hg-tolerant (Björn) willow clones cultivated in nutrient solution either for 3 d in 0.5, 1, or 2 µM of HgCl2 added once, or for 10 d in 1 µM HgCl2 added every second day (n = 3, ±SE).

 
When the solutions with 1 µM HgCl2 were changed every second day for 10 d compared with one addition of 1 µM HgCl2 during 3 d, there was no significant difference in translocation in both clones (Table 3). The effective Hg accumulation was significantly reduced in both clones when changing the 1 µM HgCl2 solution every second day for 10 d compared with giving one addition for 3 d. The sensitive clone 88-31-7 had a significantly lower effective Hg accumulation than the tolerant clone Björn after changing 1 µM HgCl2 solutions every second day for 10 d, which was not seen at one addition of 1 µM HgCl2.

To find out if Hg affects the transpiration and thereby the Hg accumulation and Hg translocation to shoots, the influence of Hg on transpiration of water was studied. The sensitive clone 88-31-7 showed a significant decrease of water transpiration when treated with 2 µM HgCl2 during 3 d compared with the control, whereas the tolerant clone Björn was not affected (Table 4). Similarly, the sensitive clone 88-31-7 showed a significant decrease of water transpiration when changing 1 µM HgCl2 solutions every second day for 10 d compared with the controls, whereas the tolerant clone Björn was not significantly affected (Table 5). Moreover, compared with the controls the sensitive clone had a significant decrease of shoot and root dry weight, whereas the tolerant clone was not affected after changing 1 µM HgCl2 solutions every second day for 10 d (Table 5).


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  		Table 4. Effect of water transpiration in Hg-sensitive (88-31-7) and Hg-tolerant (Björn) willow clones cultivated in nutrient solution with different concentrations of HgCl2 for 3 d (n = 3, ±SE).{dagger}

 

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  		Table 5. Effect of water transpiration in Hg-sensitive (88-31-7) and Hg-tolerant (Björn) willow clones cultivated in nutrient solution with 1 µM HgCl2 changed every second day for 10 d (n = 3, ±SE).{dagger}

 
The Hg fraction in cell wall analyses showed that most Hg located in roots were bound to the cell walls in both clones of willow after treatment with 1 µM HgCl2 for 3 d. In the tolerant clone Björn, 80.1 ± 5.4% of the Hg in roots was bound to cell wall, whereas in the case of the sensitive clone 88-31-7, 80.6 ± 6.7% was bound. Thus, there was no significant difference between the sensitive and the tolerant clones with regard to Hg bound to cell walls.

Phytochelatin analysis showed that no phytochelatins were found in either sensitive or tolerant willow clones by taking into account that the detection limit was 2.5 nmol g–1 root fresh wt.. The results were the same between the roots that had been treated with 1 µM HgCl2 for 3 d and the controls without Hg treatment.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
The Hg toxicity study performed in this paper showed up to 30 times difference in sensitivity to Hg among six clones of willow in terms of TT95b, and up to five times in terms of UTmax and EC50 (Table 1). This verified our first hypothesis that various willow clones could have different sensitivity to Hg, because willow clones have a large variation among clones in their sensitivity to many other heavy metals (Landberg and Greger, 1996; Greger and Landberg, 1999; Greger et al., 2001). However, our second hypothesis that willow clones may also vary in accumulation and translocation of Hg could be rejected because there was no difference in accumulation and translocation among the clones. Thus, it seems unlikely that Hg tolerance is related to low accumulation or low translocation of Hg to the shoots, as suggested for other metals by Landberg and Greger (1996).

When metals are initially absorbed by the roots, parts of them are trapped in the cell wall, which reduces the amount of metals entering the cytoplasm. Our result showed that the cell wall is the major Hg binding component of plant tissue, similar to what has been reported for pea and spearmint by Beauford et al. (1977). Mercury taken into the cytoplasm of the cells is generally attributable to the sequestration of toxic ions in complexes. Glutathione-related phytochelatins with the general structure ({gamma} Glu-Cys)nGly (n = 2–11) (Rajesh et al., 1996; Zenk, 1996) are the most dominant molecules found so far to sequester metal ions. However, from our results there is no evidence that phytochelatins are responsible for Hg tolerance in willow, because no phytochelatins were detected in either sensitive or tolerant willow clones (data not shown), as has also been found in the case of other heavy metals (Landberg and Greger, 2004). Therefore, other mechanisms must be operative to explain the observed differences in Hg tolerance in willow clones.

Our studies further showed that willow clones efficiently accumulate Hg in hydroponics. The Hg concentrations of roots ranged from 216 to 274 mg Hg kg–1 dry wt. after the plants had been cultivated in 0.5 µM HgCl2 (100 µg Hg L–1) for 3 d. However, the majority of total Hg accumulated was localized to the roots, whereas only 0.45 to 0.62% of the total Hg accumulated via roots was translocated to the shoots (Table 2). Our data were consistent with those reported in previous studies. For example, Godbold and Hütterman (1988) found that the Hg level in roots of Norway spruce exceeded that of the needles by a factor of more than 100 after the roots had been exposed in Hg solution. Beauford et al. (1977) also found much larger amounts of Hg in the roots than in the shoots of pea and spearmint. Such a low translocation of Hg to the shoots is probably due to roots having strong affinities for Hg, whereby most of the Hg in solution is trapped in the roots and mainly bound to the cell walls of root tissues.

Toxicity of Hg may affect the accumulation of Hg. The sensitive clone 88-31-7 had a significantly lower effective Hg accumulation than the tolerant clone Björn after changing 1 µM HgCl2 solutions every second day for 10 d (Table 3). The lower accumulation of clone 88-31-7 had a significant decrease of water transpiration as well as the dry weight of shoots and roots, compared with the controls, whereas this was not found in the clone Björn after 10 d of Hg treatment (Table 5). Thus, it is necessary to choose Hg-tolerant plants in phytoextraction of Hg.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
The present data could be used to predict the tolerance in aged, contaminated soils for possible phytoextraction of Hg. The bioavailability of Hg in such soil is normally low and it may not cause strong toxic effects even to the sensitive willow clone. However, low bioavailability in the contaminated soil results in low efficiency when removing Hg from soils. Methods are needed to increase the bioavailability to further enhance the phytoextraction efficiency. In this case, plants used must be sufficiently tolerant to Hg. In the present study, the tolerant clone Björn showed no effects on growth or water transpiration when tested with changed 1 µM HgCl2 (200 µg Hg L–1) (Table 5). Even though willow is a well-known plant with high biomass production, and widely used in bioenergy production in Sweden, its low translocation of Hg to the shoots leads a low efficiency of Hg removal from contaminated soil if plant shoots alone are harvested. Thus, it is not realistic to use willow to phytoextract Hg. However, its efficiency in accumulating Hg in the roots, with a very low translocation to the shoots, may make willow more feasible for phytostabilization. The plant takes up a large amount of water and has a large root system that traps mobile Hg in the soil, thereby preventing leaking of Hg from contaminated soils. However, further investigations are needed to reveal whether Hg phytostabilization works in practice.


   ACKNOWLEDGMENTS
 
We thank Tommy Landberg for help with analyses of phytochelatins and calculations of Weibull parameters as well as Professor Lena Kautsky and Professor Marianne Pedersén for critical comments on the manuscript. This work was financed by the MISTRA program COLDREM—Soil Remediation in a Cold Climate.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 


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This Issue in Journal of Environmental Quality

JEQ 2004 33: 1589-1599. [Full Text]  




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