Journal of Experimental Botany, Vol. 53, No. 368, pp. 447-453,
March 1, 2002
© 2002 Oxford University Press
Original Papers |
Influence of prior Cd2+ exposure on the uptake of Cd2+ and other elements in the phytochelatin-deficient mutant, cad1-3, of Arabidopsis thaliana
1 Plant Physiology, Lund University, Box 117, S-221 00 Lund, Sweden
2 Department of Crop Science, Swedish University of Agricultural Sciences, Box 44, S-230 53 Alnarp, Sweden
Received 30 May 2001; Accepted 28 September 2001
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Abstract |
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In order to test the potential effect of prior exposure to different Cd concentrations on Cd uptake and accumulation, plants of Arabidopsis thaliana, including a phytochelatin-deficient mutant, cad1-3, and the wild type, were compared. For Cd uptake experiments, plants were grown for 1 week in nutrient solution containing different Cd concentrations (0, 0.05, 0.1, 0.25, 0.5, and 1.0 µM Cd(NO3)2). Thereafter they were subjected to 0.5 µM Cd labelled with 109Cd for 2 h. Uptake experiments with 109Cd showed that the phytochelatin-deficient mutant cad1-3, accumulated less Cd than the wild type. Both a lower proportion and lower total amount of absorbed Cd were translocated to the shoot in cad1-3 plants compared to wild-type plants. Cadmium exposure also influenced the amounts of nutrients found, whereby after exposure to high Cd concentrations (0.5, 1.0 µM) during growth, cad1-3 roots contained less Fe, K, Mg, P, and S compared to roots of the wild type. In cad1-3 these elements decreased with increasing Cd concentration. The total Cd content in roots and shoots increased significantly with increasing Cd concentration during growth, although the increase was much less in cad1-3 plants. In time-dependent experiments of Cd uptake carried out between 15 and 120 min on plants not previously exposed to Cd, no significant difference in Cd accumulation between the mutant and wild type were found, although a smaller amount of Cd was translocated to the shoot in cad1-3 plants. The possibility that the differences in Cd accumulation in mutant and wild-type lines may be due to the cytosolic Cd regulation, which is inhibited by the complexation of Cd by phytochelatins, is discussed.
Key words: Arabidopsis thaliana, cad1-3, cadmium.
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Introduction |
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The contamination of Swedish soils with cadmium has decreased during the last decades due to restrictions in the industrial use of Cd, and of Cd-contaminated fertilizers and sewage sludge. However, the content of Cd in the soil still increases by a few tenths of a per cent each year (Hellstrand and Landner, 1998
). According to Järup et al., Cd intake from food may be a potential health risk to humans (Järup et al., 1998). Since a large proportion of the Cd taken up via diet comes from plants, it is important to understand the processes governing the uptake and translocation of Cd in plants.
In most plant species Cd is accumulated in the roots, although the allocation to the shoot may vary considerably between different species. For example, in sugarbeet 10–20% was transported to the shoot (Greger and Lindberg, 1986), while in soybean only 2% of the accumulated Cd reached the leaves (Cataldo et al., 1981). According to Salt et al., the movement of Cd from root to shoot occurs via the xylem (Salt et al., 1995). It has also been suggested that Cd complexed by phytochelatin (PC) could enhance Cd translocation from root to shoot (Guo and Marschner, 1995).
Hart et al. showed a concentration-dependent Cd2+ uptake in wheat with a linear part representing cell wall binding of Cd2+, and a saturable part that represented carrier-mediated Cd2+ influx across the cell plasma membrane (Hart et al., 1998). The saturable nature of Cd uptake has also been found in soybean, lupin and maize (Cataldo et al., 1983; Mullins and Sommers, 1986; Costa and Morel, 1993). Cataldo et al. showed that Zn inhibits Cd uptake (Cataldo et al., 1983) and therefore it has been suggested that Cd enters the cell via a Zn transport system.
Possible mechanisms of Cd tolerance in plants involve association with the cell wall, phytochelatin-mediated sequestration in the vacuole together with organic acids and complexation with reduced glutathione in the cytosol (Vögeli-Lange and Wagner, 1996, and references therein). In the presence of heavy metals, phytochelatin synthase is activated, followed by synthesis of PCs from reduced glutathione (Grill et al., 1989). The PCs bind to cadmium in the cytosol and form a complex, which is then transported into the vacuole where it is accumulated in association with organic acids (Vögeli-Lange and Wagner, 1990) or as a high molecular weight PC-Cd complex (Rauser, 1995).
The cad1-3 mutant has wild-type levels of glutathione but is deficient in PC synthase activity, with the level of PC synthase activity being less than 1% of that in the wild type (Howden et al., 1995).
In the present study cad1-3 and the wild type are compared with regard to Cd uptake (0.5 µM Cd labelled with 109Cd) and translocation in order to determine the effect of prior exposure to Cd and the influence of complexation with PCs on the Cd uptake pattern in Arabidopsis thaliana. Growth differences after 2 weeks were also measured.
An uptake experiment was carried out on plant material grown in different Cd concentrations for 1 week, and a time-dependent uptake study was conducted on another set of plants not previously exposed to Cd in order to establish the extent of immediate plant response. In addition, an aim was to determine whether the concentration of other key elements would be affected. In Brassica napus, Cd has been shown to alter the plant concentration of several nutrients (Larsson et al., 1998) and thus these nutrients were also analysed in the present study in order to determine whether the presence or absence of PCs would interfere with any Cd effect on nutrient accumulation.
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Materials and methods |
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Plant material and growth conditions
Two strains of Arabidopsis thaliana L. were used, in this study, the wild type and the cad1-3 mutant (Howden et al., 1995
), both of ecotype Columbia. Seeds were germinated in sandy soil and watered with distilled water. After 3 weeks plants were transferred to black containers with 250 ml of continuously aerated nutrient solution. All experiments were carried out with three plants per container taken together as one sample except for the growth experiment (1 plant per container). The nutrient solution (pH 5.5) consisted of macronutrients (mM): 5.0 KNO3, 2.25 Ca(NO3)2, 0.5 MgSO4, 0.5 KH2PO4, 0.5 Na2HPO4, 0.625 NH4Cl; and micronutrients (µM): 20.0 Fe-EDTA, 5.0 MnSO4, 4.0 ZnSO4, 30.0 H3BO3, 0.75 CuCl2, and 0.5 Na2MoO4. The study was carried out in a climate chamber where the plants received 400 µmol m-2 s-1 photosynthetically active radiation (PAR, 400–700 nm), during a 12 h photoperiod, day/night temperature of 20/18 °C and relative humidity of 70%.
Cadmium uptake in plants after growth in different Cd concentrations
Seventy-two plants of each type were grown for 1 week in nutrient solution containing different amounts of Cd(NO3)2: 0, 0.05, 0.1, 0.25, 0.5, and 1.0 µM. During this period the Cd concentration in the solutions did not decrease by more than 12%. After treatment an uptake experiment with 109Cd was performed. Four containers per Cd concentration were used. During the uptake experiment plants were placed in 250 ml aerated uptake solution for 2 h. The uptake solution consisted of nutrient solution lacking Fe-EDTA, to avoid complexation of Cd, but with the addition of 0.5 µM 109Cd labelled Cd(NO3)2 (1.1 MBq l-1). After the 2 h uptake period, plants were transferred to a washing solution consisting of 250 ml aerated nutrient solution without Fe-EDTA but containing 10 times the original Ca(NO3)2. The desorption period continued for 20 min after which the plants were divided into roots and shoots and blotted between filter paper. The plant material was first air-dried for 1 d and then dried at 70 °C for 2 d. The experiment was carried out twice.
Time-dependent Cd uptake
Plants were grown for 1 week in nutrient solution without Cd. Thereafter an uptake experiment was performed as described above, with the exception that the uptake time was varied between 15 and 120 min. This experiment was also carried out twice.
Plant growth at different Cd concentrations
One plant per container was grown in aerated nutrient solution containing 0, 0.5 or 1.0 µM Cd(NO3)2. Each plant was weighed every second day and the experiment was continued for 10 d. Before weighing, the nutrient solution was allowed to run off and then plants were mounted suspended in a holder on a balance. Both the wild type and the mutant were represented by six plants per treatment.
109Cd and nutrient analysis
The dried root and shoot samples were wet-combusted in 10 ml HNO3 (65%) in a microwave oven. The contents of Ca, Cd, Cu, Fe, K, Mg, Mn, P, S, and Zn were determined by inductively coupled plasma emission (ICP-AES, JY 238 ULTRACE, Paris, France). Radioactivity was measured by liquid scintillation spectrometry. Uptake rates and nutrient concentration were expressed on the basis of root and shoot dry weight.
Statistics
The means of the different results were compared by one-way ANOVA and the Student–Newman–Keuls test (SNK-test) was used as a post-test. The post-test was used only if P<0.05. The statistical package used was Instat from GraphPad Software, San Diego, CA. The results shown in the figures and the table represent one of the experiments, although similar results were obtained for all replicates.
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Results |
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Cadmium uptake in plants after growth in different Cd concentrations
The cad1-3 plants grown in 1.0 µM Cd prior to the uptake experiment with 0.5 µM Cd, showed a large and significant (P<0.05) decrease in Cd uptake compared to the wild type (Fig. 1A
). The Cd uptake in the wild type increased with increasing Cd in the growth solutions, although saturation was reached at 0.25 µM in one of the replications (not shown in Fig. 1A). The significant difference between the two strains at the highest concentration was valid for both replicates. The cad1-3 mutant showed a saturated Cd uptake at lower Cd concentrations for all replications and a significantly decreased uptake when 1.0 µM Cd was present in the growth solution. Cadmium translocation to the shoots of cad1-3 was lower than to the shoots of the wild type when the plants were grown in 0.5 and 1.0 µM Cd (P<0.01; Fig. 1B). The proportion of Cd translocated to the shoot in wild-type plants expressed as a percentage of the total Cd uptake showed little change with increasing Cd concentration (Fig. 1C). In contrast, in the concentration interval 0.25–1.0 µM, the phytochelatin mutant, cad1-3, translocated less of the absorbed Cd to the shoot than the wild type (Fig. 1C). As shown in Fig. 1D the Cd uptake rate in cad1-3 was inhibited at a root tissue Cd concentration above c. 0.2 µmol g-1 DW, although the much higher Cd concentrations reached in wild-type roots did not inhibit Cd uptake rate.
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) and wild-type (
) Arabidopsis thaliana grown for 1 week in nutrient solution containing 0, 0.05, 0.1, 0.25, 0.5, and 1.0 µM Cd(NO3)2 and then exposed to 0.5 µM Cd labelled with 109Cd for 2 h. The Cd concentration was 0.5 µM in the uptake experiment. (A) Total Cd uptake in root and shoot measured at the different Cd concentrations given during growth, (B) Cd translocation to shoot, (C) amount of Cd translocated to the shoot as a % of the total amount of Cd taken up, and (D) total Cd uptake as a function of the Cd concentration in the roots (see Table 1The Cd content in the root and shoot of cad1-3 grown at 1.0 µM Cd was significantly lower (P<0.001) than that of the wild type (1.0 µM; Table 1
). In the shoot, even 0.5 µM Cd during growth resulted in a significant decrease (P<0.001). The content of Cd in both roots and shoots of the wild type increased significantly with exposure to increasing Cd concentrations. The phytochelatin mutant, cad1-3, showed the same increasing pattern as the wild type, although this was less marked. The Cd content in cad1-3 plants was, at least at higher Cd concentrations (0.25, 0.5, 1.0 µM), less dependent on the Cd concentration that they were exposed to during growth.
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Exposure to different Cd concentrations during growth also influenced the content of nutrients measured after plants were exposed to 0.5 µM uptake solution for 2 h. The cad1-3 plants contained less S in roots (Table 1
) and shoots (data not shown) compared to the wild-type plants. The concentration of Fe, K, Mg, P, and S in roots was significantly lower (P<0.01) in cad1-3 plants exposed to 1.0 µM Cd compared to the wild-type plants. The cad1-3 plants showed a decreasing trend in the content of Fe, K, Mg, P, and S, and at higher Cd exposure (1.0 µM) the decrease was significant. The wild type did not show a particular trend in the content of the above-mentioned elements.
Time-dependent Cd uptake
The uptake period in the experiment above was 2 h and small differences (ns) between cad1-3 and wild-type control plants (no Cd pretreament) occurred during this time. Thus, in plants not previously exposed to Cd, a time-dependent experiment was conducted to determine whether there was a direct differential response between the two strains or if changes would develop during the 2 h exposure to Cd.
Time-dependent Cd accumulation in the roots of cad1-3 and the wild type showed a similar pattern during the 2 h of Cd exposure (Fig. 2A). The time-dependent Cd uptake began with a lag phase (15–30 min) followed by a fast phase, which then levelled off after 45 min.
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In the shoot, Cd accumulation was more or less linear during the time-course of the experiment (15–120 min; Fig. 2B
). At uptake times longer than 45 min, 10% of the total Cd absorbed by the cad1-3 roots was translocated to the shoot, while wild-type roots allocated 15–20% to the shoot (Fig. 2C). Thus the PC-deficient mutant, cad1-3, tended to translocate less Cd to the shoot than the wild type as in the previous experiment, although this was not significant in this case.
Plant growth at different Cd concentrations
The relative growth rate was analysed during a 10 d period in plants growing in nutrient solution containing 0, 0.5 or 1.0 µM Cd (Fig. 3). The relative growth rate of cad1-3 plants was reduced upon exposure to 1.0 µM Cd compared to 0 µM Cd, although there was no significant difference when the increase in total fresh weight for cad1-3 plants grown at 1.0 µM was compared to that of wild-type plants (1.0 µM; Fig. 4).
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) µM Cd(NO3)2 for 10 d. Plants were weighed every second day and the increase in fresh weight was expressed as a % of the prior measurement. Error bars represent SE of the mean, n=6.
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After 10 d exposure to 0.5 or 1.0 µM Cd during the growth experiment, leaves were yellowish and this was most marked in the cad1-3 mutant (data not shown). The root system of cad1-3 plants exposed to 0.5 or 1.0 µM Cd differed from that of wild-type plants exposed to similar conditions in that the cad1-3 roots were darker brown, shorter and thicker than control roots (cad1-3 and wild type (0 µM Cd)). The cad1-3 and wild-type plants responded differently to Cd with regard to their root systems, although they achieved approximately equal root masses.
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Discussion |
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Cadmium among other heavy metals, induces the synthesis of phytochelatins in plants. Tukendorf and Rauser found that maize seedlings exposed to 0.05 µM Cd significantly increased the content of PCs (24 nmol g-1 FM) (Tukendorf and Rauser, 1990
). In Silene vulgaris exposed to 0.5 µM and 5 µM Cd the content of PCs were 5.35 µmol PC g-1 DW and 20.14 µmol PC g-1 DW, respectively (Sneller, 1999). Plants contain low amounts of PC without being exposed to excessive amounts of toxic metals due to the occurrence of the essential metal nutrients Zn, Cu and Fe. According to Grill et al. PCs in a cell culture are synthesized upon exposure to Cd (200 µM) without any observable lag phase (Grill et al., 1987), which may be important to consider when discussing the time-dependent uptake experiment, where the shortest Cd exposure time was 15 min.
The results of Cd accumulation in this study indicate that, at least at higher Cd concentrations in the growth solution (Fig. 1A, B), or higher Cd concentrations in roots (Fig. 1D), the PC-deficient mutant accumulated less Cd than the wild type. This is in accordance with the results of Howden and Cobbett who compared the wild type with another cad1 mutant, CC5, in a Cd uptake study without prior Cd exposure during growth (Howden and Cobbett, 1992). The withdrawal of free Cd ions from the cytosol by the complexation with PCs and eventual transport to the vacuole (Tomsett and Thurman, 1988) or the shoot (Guo and Marschner, 1995), may depress any mechanism regulating the cytosolic Cd concentration. One explanation could be that the PC-complexed Cd is inaccessible for an active efflux (as speculated by Costa and Morel, 1993) and shown for Zn and Cd in E. coli (Rensing et al., 1997). Another possible mechanism is that the cytosolic Cd concentration may regulate any carrier-mediated uptake as is suggested for several macronutrients (Jensén and Pettersson, 1978).
There was a significant difference in Cd uptake between cad1-3 and wild type when grown in 1.0 µM Cd (Fig. 1A), with the Cd uptake rate for cad1-3 being c. 2/3 of that for the wild type. If the only difference between the mutant and the wild type is the PC synthesis then these results suggest that PC occurrence increases Cd uptake. An alternative explanation to the lower Cd uptake in the mutant could be the changed appearance of the root system in the Cd-treated cad1-3 plants. Thus, although approximately the same root masses were achieved in all tested plants, the uptake surface might have been different, favouring Cd uptake in the wild-type plants.
The difference in Cd accumulation between cad1-3 and the wild type was generally more pronounced in the shoot than in the root. A smaller proportion of the absorbed Cd as well as a lower total amount was translocated to the shoot in cad1-3 plants compared to the wild type (Fig. 1B, C). Guo and Marschner suggested that Cd–PC complexes may be a mobile form in the translocation of Cd from roots to shoots (Guo and Marschner, 1995). This offers one explanation for the higher translocation to the shoot of Cd in the wild type compared to the PC-deficient cad1-3 mutant. Another explanation for the lower Cd accumulation in the shoots could be a more efficient retranslocation of Cd in the cad1-3 mutant than in the wild type. However, this is unlikely to be the case here. The amount of 109Cd taken up and transported during the 2 h was extremely low compared to the Cd already present in the shoots. In an experiment with lettuce 109Cd movement between roots and shoots was studied. Cadmium movements were followed during 6 h after interrupted 109Cd exposure. During this period there was no indication of retranslocation of Cd from shoot to root (data not shown).
In the wild type, the Cd concentration increased significantly (Table 1) with increasing Cd concentration in the nutrient solution, but in cad1-3 this increase was much weaker. These results support the conclusions regarding the Cd uptake results discussed earlier. With regard to the nutrient concentrations, cad1-3 plants contained less Fe, K, Mg, P, and S in roots compared to the wild type at higher Cd concentrations. In fact the concentration of these elements decreased in cad1-3 with increasing Cd exposure. This might have been due to a Cd toxicity response of the uptake mechanisms for these elements.
Time-dependent Cd uptake (Fig. 2A), in Arabidopsis roots consisted of a lag phase followed by a fast phase and then a linear phase. Both cad1-3 and wild-type plants showed the same pattern of time-dependent root uptake. The occurrence of an early plateau, or lag phase, probably reflects Cd binding to the root apoplast and a rather low actual influx. In a study of Cd uptake kinetics, Cataldo et al. found that 20–25% of the absorbed Cd was bound in a non-exchangeable way to the root surface (Cataldo et al., 1983). During the linear part, unidirectional Cd influx into the symplast would probably occur, thereafter Cd influx would be suppressed or efflux would begin (Hart et al., 1998). The time-dependent experiment again showed that the cad1-3 mutant translocated less Cd to the shoot than the wild type (Fig. 2B, C).
In the present experiments 120 min of Cd exposure was shown to be too short to detect differences in Cd uptake kinetics, and thus the influence of the presence or absence of PCs was not evident. The lack of those differences may have been due to the insufficient exposure time leading to a too low Cd concentration in the cytosol to trigger any signalling system to the PC-synthase.
In conclusion, it seems that the presence of PC in Arabidopsis thaliana plants increases the total Cd uptake and also the accumulation and translocation of Cd to the shoot. The results indicate that Cd complexation with PC either increases Cd uptake or decreases its sequestration. This may imply that two different mechanisms act to reduce the toxicity of Cd in Arabidopsis: one mechanism that reduces the net uptake of Cd and one that detoxifies Cd by binding to organic compounds. In addition, excess Cd in the cytosol may have a negative impact on the uptake of essential nutrient elements, as indicated by the decreased uptake of nutrients with increasing Cd concentration in the mutant.
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Acknowledgments |
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Seeds of Arabidopsis thaliana, wild type and cad1-3, were kindly provided by CS Cobbett. The authors wish to thank Sven Svensson for careful technical assistance. H Asp is grateful to SJFR for partial funding of the project.
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Notes |
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3 To whom correspondence should be addressed. Fax: +4640465590. E-mail: hakan.asp{at}vv.slu.se
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Abbreviations |
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PC, phytochelatin.
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