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Chelate-mediated changes in soil metal solubility: implications in the uptake and translocation of cadmium by wheat (Triticum aestivum L.) at different growth stages.


Cadmium (Cd) is a non-essential heavy metal pollutant resulting from agricultural, mining, industrial and exhaust gases. It is highly toxic and is quite soluble (Smith, 1994). The quality of soil, nutrient cycling, and agricultural production are affected by the presence of Cd (Adler, 1996; Baker and Brooks, 1989; Faroon et al., 2008; Pence et al., 2000). The Environmental Protection Agency (EPA) has set a limit of 5 parts of Cd per billion in drinking water, and does not allow Cd in pesticides. The Food and Drug Administration (FDA) limits the amount of Cd in food colors to 15 parts per million. The Occupational Safety and Health Administration (OSHA) limits workplace air to 100 [micro]g/[m.sup.3] as Cd fumes and 200 [micro]g/[m.sup.3] as Cd dust. The Department of Health and Human Services (DHHS) has determined that Cd and Cd compounds may reasonably be anticipated to be carcinogens. It is not known whether Cd exposure can affect development in people. However, in animal studies, the offspring of mice exposed to Cd during pregnancy had delayed development. Also, Cd causes kidney damage of mammals, emphysema and acute lung condition (Baker, 1981). From the mammalian toxicity data of elements in injected doses and diets, 1.3 mg/kg Cd is the acute lethal dose (LD50). In human diet, 3 to 330 mg/day is the toxic dose (Hammer and Keller, 2002).

Cognizant of threats that heavy metals pose to the environment, as well as to human and animal health, there has been an increasing interest in phytoextraction as a plant-based alternative for cost-effective and environmentally sound method for the clean up of heavy metal-contaminated soils (Baker and Brooks, 1989; Blaylock et al., 1997; Salt et al., 1995; Shen et al., 2002; Watanabe, 1997). In phytoextraction, an efficient plant species must be able to absorb a substantial amount of the toxic metal into its roots and preferentially translocate the metal into the harvestable aboveground biomass for easier harvesting (Adler, 1996). Through a cropping scheme, suitable species can be planted in succession ultimately leading to the reduction of soil metal concentrations to environmentally acceptable levels. In addition to a plant's high biomass yield and tolerance to toxic metal levels, the success of phytoextraction is also dependent upon the availability of the toxic metal in the soil for plant uptake. Also, another requisite for efficient phytoextraction is to increase and maintain Cd concentrations in the soil solution. Chelates have been used to increase the solubility of metal cations in soils (Lasat, 2002).

In previous studies using a modified hydroponics system (Gosh and Rhyne, 1999) and Cd-amended sand (Begonia et al., 2000), wheat (Triticum aestivum L. cv. TAM-109) was identified as a suitable phytoextraction species because of its high biomass yield under elevated metal levels, and its ability to accumulate high amounts of metal into its shoots. Also, wheat can be grown during the colder months of a year-round cropping scheme, thus ensuring ground cover for an otherwise barren, metal-contaminated soil.

The main objective of this study was to further evaluate the effectiveness of T. aestivum as a phytoextraction species. Specifically, this experiment was conducted to: (a) determine which time is suitable for harvest after chelate application at a specific growth stage; (b) determine which chelate or chelate combination was effective in enhancing shoot uptake of Cd by wheat when grown on a Cd-contaminated soil; and (c) determine which growth stage was best for wheat to attain a maximum translocation index [i.e., shoot Cd/total plant Cd].


Solubility Study

Twelve mL of deionized, distilled water or chelate solution [250 mg/L] were added to each 15 ml centrifuge tube containing 2 g of Cd-contaminated soil [i.e., 250 mg Cd/kg dry soil; equilibrated for 7 weeks prior to metal extraction]. Soil suspensions were agitated in a platform shaker at room temperature for various extraction times. At the end of each designated extraction period, the soil suspensions were centrifuged at 5000 rpm for 30 min. The supernatant was filtered through a Whatman 0.45um filter paper. Cadmium contents of each filtrate were quantified using inductively coupled plasma-optical emission spectrometry [ICP-OES; Perkin Elmer Optima 3300 DV]. For this specific study, experimental units were arranged in a completely randomized design (CRD) with three replications.

Plant Culture and Experimental Design

Seven weeks before planting, three concentrations [e.g., 0, 250, 500 mg Cd/kg dry soil] of Cd in the form of cadmium nitrate were mixed and equilibrated with the soil [2:1; v: v mixture of silt loam soil (pH 6.9) and peat]. Unless otherwise specified, five wheat [T. aestivum L. cv TAM 109] seeds were sown in each 656 mL D40 Deepot tube [Stuewe and Sons, Inc., Corvallis, OR] containing 550 g of dry soil mixture. Emerged seedlings were thinned out to a desired population density of 2 plants per tube at 5 days after planting. Plants were irrigated every 2-3 days depending on the evaporative demand, with a modified, full strength nutrient solution (Triplett et al., 1980; Begonia, 1997) which contained the following nutrients in mM: N[H.sub.4]N[O.sub.3], 5: [K.sub.2]S[O.sub.4], 1.25; Ca[Cl.sub.2] x 2[H.sub.2]O, 2.0; MgS[O.sub.4] x 7[H.sub.2]O, 0.5; [K.sub.2]HP[O.sub.4], 0.15; CaS[O.sub.4] x 2[H.sub.2]O, 6.0; the following in [micro]M: [H.sub.3]B[O.sub.3], 2.3; MnS[O.sub.4] x [H.sub.2]O, 0.46; ZnS[O.sub.4] x 7[H.sub.2]O, 0.6; CuS[O.sub.4] x 5[H.sub.2]O, 0.15; NaMo[O.sub.4] x 2[H.sub.2]0, 0.10; Co[Cl.sub.2] x 6[H.sub.2]O, 10.0; and 20 mg/L Fe sequestrene. The volume of applied nutrient solution ensured that soil moisture content was maintained at field capacity. Each concentration [e.g., 0, 250, 500 mg/kg dry soil] of ethylenebis (oxyethylenenitrilo) tetraacetic acid (EGTA) was applied to a designated treatment as a 20-mL aqueous solution 5 days before harvest. Also, aqueous solutions [e.g., 0, 250, 500 mg/kg dry soil] of acetic acid (HAc) were applied either alone or in combination with EGTA 5 days before harvest. A 9-oz plastic cup was placed beneath each tube to prevent cross contamination among treatments. Any symptoms of metal toxicity exhibited by plants were visually noted during the experimental period.

Plants were maintained inside a naturally-lit greenhouse with a 31[degrees]C/20[degrees]C day/night temperatures. The photosysnthetically active radiation (PAR, 400-700 nm) measured at the canopy level was no less than 1400 [micro]mol photons [m-.sup.2] [sec.sup.-1] as measured with a LI-COR 6200 portable photosynthesis system (LI-COR, Inc., Lincoln, NE). Plants were harvested at 5 days after chelate application for each designated harvest period (e.g., 6, 8, and 10 weeks after emergence). During harvest, shoots and roots were separated, and roots were washed with distilled water to remove any adhering debris, then oven-dried at 70[degrees]C for at least 48 hours. Dried samples were weighed to obtain biomass, and ground using a Wiley mill equipped with 425 [micro]m (40-mesh) screen.

Cadmium contents of ground, dry plant tissues were extracted using nitric acid-hydrogen peroxide procedures (Edgell, 1989). Cadmium concentrations were quantified using ICP-OES as described above. Treatments were arranged in a completely randomized design (CRD) with 4 replications. Data were analyzed using Statistical Analysis System [SAS], Version 9. Treatment separations were done using Fisher's Protected Least Significant Difference [LSD] test.


Cadmium Solubility of a Seven-Week Old Contaminated Soil After Application of Chelates

Among the chelates tested, EGTA was the most effective in solubilizing soil-bound Cd [Fig 1]. Cd concentration in soil solution increased with extraction time, reaching maximum value at 5 days then slightly declined at 6 and 7 days after chelate amendment. Soil Cd could be solubilized by EGTA in a short time and maintained at a high level afterward. The effectivity of EGTA in solubilizing Cd from the soil may be related to the high binding capacity of EGTA for Cd as shown from previous studies (Stanhope et al., 2000). The concentration of EGTA-extractable Cd in soil decreased with increasing extraction time from day 5 to day 7. Also, HAc-extractable Cd began to decline 3 days after chelate amendment. These results indicate that these chelates are more rapidly degraded than EDTA.

In a study (Haag-Kerwer et al., 1999) using a hydroponics system, EGTA was the most effective chelator for enhancing Cd accumulation in B. juncea. From one study using a CaCl2-spiked soil containing 32% clay (pH 6.5; 15.32 CEC) and aged for 2, 10, 15, and 20 months, there were higher levels of Cd in the exchangable, and Fe-Mn oxide fractions, and less in the carbonates, organic matter and residual fractions at 2 months than the other three aging times (Su et al., 1999). This suggested that for longer aging times, there is a movement of Cd from exchangeable, Fe-Mn oxides, to carbonates and residual fractions, during the aging process. The longer the residence time of the heavy metal in the soil, the lower is its bioavailability. In addition to determining the best type of suitable chelate, the time of harvest after chelate addition was also determined. For EGTA, the best time was determined to be 5 days after chelate application. The time of harvest after chelate application is important because synthetic chelates are persistent and not biodegradable. The time of harvest could be manipulated to lessen the leaching of the non-biodegradable chelates and / or chelate-metal complexes to the underground water.


Effects of Cadmium and Chelates on Dry Root and Shoot Biomass of Wheat

T. aestivum did not produce high biomass [Figs. 2, 3]. For each growth period, root dry weights were significantly greater (p = 0.037) in wheat that were not exposed to Cd (control treatment) compared to Cd--exposed plants (Fig. 2). Also, for each growth stage, there were no significant differences in root dry weights due to chelate treatments, except those amended with both a combination of EGTA/HAc, which showed significantly lower root biomass compared to the control especially at 10 weeks after emergence. However, root dry weights were correspondingly lower with increasing amounts of spiked Cd. For instance at 6 weeks after emergence, the mean root dry weights of control plants were 0.1195 g/plant. During the same period, the average root dry weights were 0.035 and 0.023 g for plants exposed to 250 mg Cd / Kg and 500 mg Cd / Kg, respectively. Similar trends of decreasing root dry weights with increasing levels of soil-spiked Cd were observed in plants at 8 and 10 weeks after emergence.

Regardless of chelate treatments and growth stage, shoot dry weight reductions were greater as the concentration of soil-applied Cd increased from 250 mg Cd / Kg to 500 mg /Kg. For example at 6 weeks after emergence, shoot dry weights of control plants averaged across chelate treatments was 0.1972 g/plant. For the same growth period, the average shoot dry weights for plants exposed to 250 mg Cd / Kg and 500 mg Cd / Kg were 0.0782 g/plant and 0.0362 g/plant, respectively. Similar trends of greater shoot dry weight reductions with increasing concentrations of soil-applied Cd were observed at 8 and 10 weeks after emergence.

The first requisite in phytoextraction is the production of high plant biomass at the contaminated site. Generally, T. aestivum did not produce high biomass but was able to tolerate elevated levels of Cd/EGTA in the soil [Figs. 2, 3]. Metal phytotoxicity causes stress to the plant, resulting in a reduction in biomass and in some cases eventually death. There is a tendency of cadmium to affect manganese, copper and chlorophyll concentration in leaves at concentration in solution that had no effect on biomass production, thereby affecting photosynthesis (Saygideger, 2000). Also, cadmium has been reported to have an effect on sulfhydryl groups in proteins, inactivating major enzymes and replacing activated cations. Plants respond to heavy metal toxicity in different ways, such as immobilization, exclusion, chelation, compartmentalization of metal ions and expression of stress proteins (Cobbett, 2000). Plants respond to metal toxicity through ligands, which are naturally occurring metal binding ligands known as phytochelatins and metallothioneins. These ligands make the metal less toxic to the plant, but at this stage we are not certain whether the same tolerance mechanism applies to T. aestivum, hence further study is warranted.

Wheat (T. aestivum) was tolerant to high concentrations of cadmium but there were significant reductions in root and shoot biomass among treatments [Figs. 2, 3]. From the results of this study, Cd caused reductions in dry weights of plants when chelates were applied at 6, 8 and 10 weeks after emergence. The severity of cadmium phytotoxicity was most evident from study of dry matter yields, where dry weights were significantly reduced by 2 mg Cd/kg and further depressed by 10 and 50 mg Cd/kg treatments (John and van Laerhoven, 1976). Using Thlaspi caerulescens Brown et al. (1995) observed significant yield reduction (p < 0.01) after 28 days of Cd exposure. Reports from one study (Cooper et al., 1999) indicated that synthetic chelators at high concentrations could also be toxic to plants. When using S. alfredii Liu et al. (2008) found that shoot dry weights of plants grown in 400 mg Pb/ Kg soil and 1200 mg Pb/ Kg soil were decreased significantly along with the increase of EDTA addition as 1, 5, and 10 mM. The results of this study were consistent with the findings of McCarthy et al. (2001) where they reported oxidative stress in pea leaves due to cadmium treatment. The reductions in the plant biomass could also be due to a decline in photosynthetic pigments (Bibi and Hussain, 2005). Ethylenediamine tetraacetic acid is a synthetic chelator that has been shown to substantially lower soil cation exchange capacity (CEC). It has been used since the 1950s to alleviate iron deficiency, and has been used frequently to improve phytoextraction of metal contaminants, such as lead, from soil. Often times, a sudden increase in bioavailable metals resulting in EDTA application is fatal to plants. This can be overcome by growing plants up to a large biomass, then adding EDTA. The metal will become highly bioavailable, and will be taken up in large quantities by the plant for a short time before the plant dies (Salt et al., 1998). In this way, large amounts of metal can be extracted from soil. This strategy is referred to as chelator-assisted phytoextraction (Salt et al., 1998). A similar compound called ethyleneglycol tetraacetic acid (EGTA) has been shown to be very effective at increasing Cd bioavailability.



Cadmium Concentrations in Dry Roots and Shoots of Wheat

For each growth period, root cadmium concentrations were significantly greater (p = 0.0045) in wheat that were exposed to 500 mg / kg Cd compared to those exposed to 250 mg Cd / Kg (Fig. 4). For instance at 6 weeks after emergence, the mean root cadmium concentrations for plants grown at 250 mg Cd / kg were 901 mg Cd / Kg dry weight. During the same period, the average root cadmium concentrations were 4395 mg Cd/Kg dry weight for plants exposed to 500 mg Cd / Kg. Also, for each growth stage, there were no significant differences in root cadmium concentrations due to chelate treatments except at 10 weeks after emergence. During this specific growth stage, plants exposed to 500 mg Cd/kg with no chelate amendment exhibited the least root Cd concentrations. Similar trends of increasing root cadmium concentrations with increasing levels of soil-spiked Cd were observed in plants at 8 and 10 weeks after emergence.

Generally for each developmental stage, there were no significant differences in shoot cadmium concentrations as a result of chelate treatments (Fig. 5). The only exception to these observations were the significantly greater shoot cadmium concentrations of plants grown in 500 mg Cd / Kg that were amended with EGTA alone especially at 10 weeks after emergence. Shoot cadmium concentrations were greater as the concentration of soil applied Cd increased from 250 mg Cd / Kg to 500 mg /Kg. For example at 6 weeks after emergence, the average shoot cadmium concentration of plants exposed to 250 mg Cd / Kg was 586 mg Cd / Kg dry weight. Similar trends of increasing shoot cadmium concentrations with increasing concentrations of soil-applied Cd were observed at 8 and 10 weeks after emergence.

When chelates were applied at 6, 8 and 10 weeks after emergence, significant increases in cadmium concentrations were remarkable in plants grown at 500 mg Cd / Kg with the addition of chelates. Using four different chelating agents, such as ethylenediamine tetraacetic acid (EDTA), oxyethylenenitrilo tetraacetic acid (EGTA), trans-1, 2diaminicyclohexane-N, N, N', N'-tetraacetic acid (CDTA) and diethylenetriaminepentaacetic acid (DTPA), Van Engelen et al. (2007) found that plants grown in soil without chelators had cadmium concentrations of 131 mg Cd/kg dry weight, as compared to 1283, 1240, 962 and 437 mg Cd/kg dry weight from plants grown in soil with EDTA, EHTA, CDTA, DTPA, respectively. Other chelating agents increased the solubility of Cd in the leachate but not to the extent of EDTA. DTPA increased plant uptake in terms of Cd in dried plant concentration most relative to the solubility of complexed Cd in runoff water. EDTA was also shown to be better at solubilizing Pb and Cd than EDDS (Luo et al., 2005). EDTA was found to be ineffective for Viola baoshanensis or Vetivera zizanoides (Zhuang et al., 2005). They also found that cadmium concentrations in the roots were significantly (p > 0.05) increased by EDTA, while stem concentration decreased significantly from 3.33 mg/g biomass to 1.34 mg/g biomass (p = 0.026). The leaves contained similar levels of cadmium of 0.88 mg/g biomass and 0.66 mg/g biomass with and without EDTA, respectively.

Yang et al. (2005) suggested that major processes involved in hyperaccumulation of trace metals from soil to shoot include a) bioactivation of metals in the rhizosphere through root--microbe interaction, b) enhanced uptake by metal transporters in the plasma membranes, c) detoxification of metals by disrupting the apoplast-like binding to the cell walls and chelation of metals in the cytoplasm with various ligands such as phytochelatins, metallothioneins, metal binding proteins, and d) sequestration of metals into the vacuole by tonoplast-located transporters.

Salix viminalis plants exhibited strong stress symptoms at 100 [micro]M, with impaired survival at 200 [micro]M Cd (Cosio et al., 2006). Cadmium was localized mainly in the tips and edges of the younger leaves and at the base of the older leaves indicating that Cd tolerance had been exceeded. Liphadzi and Kirkham (2006) in their investigations of the effects of chelates after successive cropping found that EDTA applied the previous season reduced the growth of subsequent crops. They also found that in soil with or without plants, EDTA mobilized Cd, Fe, Mn, Ni, Pb and Zn, which leached to drainage water. Research was conducted by numerous groups to find a way to make chelator-induced in situ phytoextraction effective and safe in the environment, but the added chelating agents caused unavoidable leaching of chelated metals down the soil profile (Chaney et al., 2007). In several field tests of EDTA in firing range soils in the US, rapid leaching of metal to groundwater proved an unacceptable side effect of chelator-induced phytoextraction. The addition of Zn, Cu, and many other metals to nutrient solutions containing FeEDTA was suggested to cause displacement and precipitation of the Fe and chelation part or all of the added test metal ion (Chaney et al., 2007).

Cadmium bioavailability is promoted by soil acidity, [Cl.sup.-], or SO[4.sup.2-], soil salinity and, in some cases, by large Cd/Zn ratios (Oporto et al., 2007). They reported that [Cl.sup.-] or S[O.sub.4.sup.2-] forms complexes with [Cd.sup.2+] and mobilizes Cd in the soil. A Zn/ Cd ratio less than 100 in soils contaminated by mine wastes and most other sources of Cd and Zn causes Zn hyperaccumulation to reach phytotoxic levels and limit yields of most plant species before much Cd can be accumulated. Unfortunately, most soils that require Cd remediation to protect human health have the Cd contamination associated with a high ratio of Zn to Cd ratio. Therefore, any plant that tolerates Cd must also tolerate high levels of Zn which usually occurs with Cd contamination.


Differences in the accumulation of Cd between plant species or varieties of the same species are also recognized. Cd accumulation in many crops varies significantly among species and cultivars. Many researchers have shown that there are variations in Cd accumulation among cultivars or genotypes in cereals such as wheat, rice, and potato. In leafy vegetables Cd accumulates in the leaves, whereas in cereals, accumulation is greatest in the roots declining towards the top of the plant (Zheng et al., 2008). The decrease that has been observed was attributed to plants absorbing and translocating [Cd.sup.2+] rather than the chelated form. Some combinations of organic chelator caused Cd to precipitate leaving only a small amount that was soluble and available to be transported by the plants (Gerard et al., 2000).



Plants that are regarded as extreme accumulators are classified as hyperaccumulators. Wheat (T. aestivum) is a Cd hyperaccumulator because it bioaccumulated more than 100 mg Cd / kg dry tissue. Chelates may pose environmental risks and possible contamination of groundwater, if allowed to stay for long in a polluted soil (Haag-Kerwer et al., 1999). In this experiment we concluded that: (a) 5 days after chelate application was the most suitable time for harvest of a Cd-laden biomass, (b) EGTA was effective in enhancing shoot uptake of Cd by wheat when grown on a Cd-contaminated soil, and (c) 8 weeks after emergence was the best growth stage for wheat to attain maximum Cd translocation to the shoots.

The results of this study indicated that wheat can be an efficient Cd- accumulating plant even in the absence of chelation. Further investigations are warranted specifically to periodically quantify the amount of soluble Cd at different strata of the soil profile. This study will be extended in future research to plants growing under natural environmental conditions in areas contaminated by cadmium or other heavy metals.


This research was made possible through support provided by the NASA through The University of Mississippi (Subcontract No. 08-08-012 to Jackson State University) under the terms of Agreement No. NNG05GJ72H. This research was also partially supported by the U.S. Department of Education (Title III Program Grant No. P031B040101-07). The opinions expressed herein are those of the authors and do not necessarily reflect the views of NASA or The University of Mississippi. Thanks to Christian Rogers for his technical assistance with metal analyses.


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Jennifer Ntoni, Gloria Miller, Marche Smith, Maria Begonia *, and Gregorio Begonia

Plant Physiology/Microbiology Laboratory, Department of Biology, P.O. Box 18540, College of Science, Engineering and Technology, Jackson State University, 1000 Lynch Street, Jackson, Mississippi 39217, USA

* Corresponding Author:
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Author:Ntoni, Jennifer; Miller, Gloria; Smith, Marche; Begonia, Maria; Begonia, Gregorio
Publication:Journal of the Mississippi Academy of Sciences
Article Type:Report
Geographic Code:1USA
Date:Oct 1, 2011
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