soil remediation and plants || phytoremediation of pb-contaminated soils using synthetic chelates

397Soil Remediation and Plants. http://dx.doi.org/10.1016/B978-0-12-799937-1.00014-0Copyright © 2015 Elsevier Inc. All rights reserved.

Phytoremediation of Pb-Contaminated Soils Using Synthetic Chelates

Saifullah,* Muhammad Shahid,† Muhammad Zia-Ur-Rehman,* Muhammad Sabir*,‡ and Hamaad Raza Ahmad**Institute of Soil and Environmental Sciences, University of Agriculture, Faisalabad, Pakistan, †Department of Environmental Sciences, COMSATS Institute of Information Technology, Vehari, Pakistan, ‡School of Plant Biology, University of Western Australia, Crawley, WA, Australia

INTRODUCTION

Rapid industrial development, urbanization, population explosion, lack of pol-lution control measures, and intensive agricultural activities have resulted in an enormous increase in soil contamination with heavy metals (Sarwar et al., 2010). Heavy metals are the chemicals that cannot be degraded biologically or chemically and upon release into the environment could pose a serious threat to environmental sustainability. Most commonly occurring heavy metals in soils due to anthropogenic activities include: arsenic (As), lead (Pb), nickel (Ni), cadmium (Cd), copper (Cu), cobalt (Co), zinc (Zn) and mercury (Hg). Among many heavy metals, Pb can impose serious risks to ecosystem health because of its potential toxicity to living organisms, and persistence in the environment. It is one of the most common heavy metal contaminants in soils because of its widespread use in industries. The Pb in soils may arise from various anthropo-genic activities including mining, smelting of metals, lead–acid batteries, bul-lets, gasoline, phosphate fertilizers and pesticides. Presence of Pb in soils at high levels can lead to impaired crop productivity, nutrient status and quality of agricultural products. It is therefore imperative to clean up the Pb-contaminated soils in order to produce pollution-safe food from such soils (Saifullah et al., 2009a; Shahid et al., 2013a).

With increasing demands for uncontaminated soils to produce safe food, a large number of techniques are being used worldwide to clean up contaminated soils. Conventional engineering-based methods used for the remediation of pol-luted soil are highly expensive and destroy the soil fertility, structure and could

Chapter 14

398 Soil Remediation and Plants

even permanently change soil texture. Moreover, these techniques are feasible only for small but heavily polluted sites under commercial use. Plants are known as solar driven pumps which extract water and nutrients from soils along with other non-essential elements. The ability of plants to extract and accumulate non-essential elements into their harvestable parts (phytoextraction) has been successfully exploited to remediate polluted soils. Plant-based remediation methods have many advantages compared to other conventional engineer-ing / chemical-based technologies. Plants are solar driven pumps that generally remove the toxic metals from soil without any ill effects on soil health (Mench et al., 2009), and this technique requires relatively lesser inputs and expertise.

Heavy metal phytoextraction can be natural or chemically enhanced / assisted (Saifullah et al., 2009a). Natural phytoextraction relies on plant species with the ability to extract and accumulate high levels of heavy metals in harvestable biomass (Shahid et al., 2012a). Such plants, also known as metal hyperaccu-mulators, should show: (1) fast growth, high tolerance to metals and high bio-mass, and (2) high metal accumulation in harvestable biomass. However, most Pb-hyperaccumulator plant species have generally slow growth rates with low biomass production (McGrath and Zhao, 2003) and are able to take up specifi-cally one or a few metals. One of the most important factors behind successful heavy metal remediation of polluted soils is the phytoavailable portion of a metal in the soil solution phase (Evangelou et al., 2007). Although the natural levels of Pb in Earth’s crust may be high, a major fraction of soil Pb is found in the non-available form due to strong binding with different soil organic and inorganic compartments (Saifullah et al., 2009a; Shahid et al., 2012b). The tis-sue concentration of plants growing in Pb-contaminated soils is generally below 50 mg g−1 Pb. Moreover, a major fraction of root-absorbed Pb does not transport to above-ground harvestable parts of plants. Retention of Pb by soil and root adsorption is greater than Zn, Ni and Cd (Sheoran and Sheoran, 2006), and that could be the possible reason for fewer Pb-hyperaccumulating plants. Natural hyperaccumulator plants lack the ability to extract high amounts of soil bound Pb. These traits associated with natural hyperaccumulators limits the effective-ness of natural phytoextraction in the case of Pb-contaminated soils because of limited availability of Pb for plant uptake.

In the second phytoextraction approach, chemicals especially natural or syn-thetic chelants are used to increase the availability, uptake by roots and trans-location from roots to shoots to concentrate the metal in harvestable biomass (Saifullah et al., 2009a; Shahid et al., 2014). This technology is particularly use-ful in phytoremediation of metals having a very low solubility and availability like Pb. During the past two decades, several synthetic chelants have been exper-imented with to enhance Pb uptake by plants from contaminated growth media. These include: EDTA (ethylenediaminetetraacetic acid), NTA (nitrilotriacetate), EDDS (ethylenediaminedisuccinic acid), EGTA [ethyleneglycol-bis-tetraacetic acid], EDDHA [etylenediamine-di (o-hydroxyphenylacetic acid)] and CDTA (trans-1, 2-diaminocyclohexane-N, -tetraacetic acid) (Meers et al., 2008).

399Chapter | 14 Phytoremediation of Pb-Contaminated Soils

The synthetic chelants applied to soil form mobile and thermodynamically sta-ble soluble complexes within pore water (Saifullah et al., 2008, 2010a; Shahid et al., 2012b). Synthetic chelants show very high affinity for Pb present in soil solution as well as that adsorbed on to soil particles. This metal-chelator forma-tion helps release Pb from soil solids into the soil solution. From soil solution, metal–chelator complex moves to roots through diffusion and / or mass flow processes and are taken up along the apoplastic pathway (Tanton and Crowdy, 1971). This complex is then entered into stele through a leaky / underdeveloped Casparian strip. From stele, metals are translocated to above-ground harvestable parts via xylem. Therefore, chelating agents applied to soil not only enhance the Pb solubilization in the soil but also increase the uptake and its translocation from roots to shoots (Tandy et al., 2006).

During the recent past a large number of studies have reported success stories about chelating-agent-assisted Pb phytoextraction. However, many of the scientists have advocated avoiding application of chelating agents for plant-based remediation of heavy metals including Pb due to a number of risks associated with this technology (Saifullah et al., 2009b). The potential risks associated with this technology include: (1) enhanced mobility and thus leach-ing of heavy metals and other essential macro- and micronutrients from soils; (2) ground water pollution due to lixiviation of heavy metals and chelating agents; (3) toxicity of mobilized metals and chelating agents to soil flora and fauna; (4) high cost of synthetic coolants; (5) adverse effects over soil condi-tions due to high amounts of amendments (Saifullah et al., 2009).

THE PROBLEM OF PB

Pb pollution is considered a serious threat to ecosystem health and has been reported since a thousand years ago (Pourrut et al., 2011). The average Pb con-tent in Earth’s crust is estimated as 15 mg kg−1 soil. Lead is released into the environment through many natural and anthropogenic sources. The amount of Pb released through anthropogenic activities is much higher than sourced from natural processes (Pain, 1995). Upon release into the soil environment, Pb forms thermodynamically stable complexes and precipitates of low solubility. The very long half-life (740–5900 years) of metallic Pb in soil indicates that the solubility of metallic lead is very low (Rooney et al., 1999). Translocation of Pb from roots to shoots is generally very low due to its strong binding at root surfaces and cell walls (Jarvis and Leung, 2002; Pourrut et al., 2013).

CHELATING AGENTS

Chelating agents are macromolecular compounds with the ability to form sev-eral coordinate bonds to a single metal ion. A chelating agent therefore has the ability to form a complex with metal. The complex form of metal behaves dif-ferently in a water–soil–plant system than in its free state. Complex formation


can free the metals bound to soil components / cation exchange sites or it can decrease the adsorption / precipitation of metals present in soil solution. After its removal from cation exchange sites, metal is available for plant uptake in the immediate vicinity of the roots. There are a number of factors that affect the efficiency of chelating agents in the mobility of metals in soil–plant systems. Among others stability constant (Ks) of the metal-chelating agent’s is the most important. Among many of the chelating agents, EDTA has a very strong affin-ity for Pb due to its higher value of logK and thus forms complex with highly stable over a wide range of pH (Martell et al., 2001).

Ethylene Diamine Tetraacetic Acid (EDTA)

EDTA is a highly stable molecule, and has high industrial and household uses. In agriculture, EDTA is used to increase the uptake of essential nutrients. EDTA is capable of changing metal speciation and thereby its mobility and bioavail-ability (Nowack et al., 2006; Shahid et al., 2011). In the late twentieth century, EDTA was proposed as a chelating substance for metal phytoextraction. EDTA is one of the most widely used chelating agents for remediation of contaminated soils especially those with metals having low bioavailability (Saifullah et al., 2009b; Shahid et al., 2014). A large number of studies confirmed EDTA as one of the most efficient synthetic chelating agents to increase Pb mobilization in a soil–plant system (Blaylock et al., 1997; Huang et al., 1997; Saifullah et al., 2009a; Bareen and Tahira, 2011; Shahid et al., 2011).

Effect of EDTA on Pb Solubilization in SoilLead is a toxic pollutant that can be found in several different forms in soils. These forms include: Pb as the free ion in the pore water, Pb complexed with different inorganic and organic ligands, Pb adsorbed to soil mineral and organic fractions or precipitated as different compounds. Among all these, Pb as the free ion in soil solution is the most bioavilable from soil (Saifullah et al., 2009a). Like all other elements, Pb bound to cation exchange sites is in direct equilib-rium with that found in soil solution. That is why Pb present at exchange sites is also considered a bioavailable fraction. Lead associated with other soil com-ponents like organic matter, oxide and silicate clay minerals, or precipitated as the carbonate, sulphate, or phosphate is the least available form. Complexation with EDTA in soil solution results in decreasing the concentration of free Pb in soil solution, thus releasing more Pb from exchange sites. This shift in equilib-rium enhances the release of Pb from other solid-phase fractions of soil such as organic or sulphide substances (Ramos-Miras et al., 2011). EDTA is capable of extracting Pb from all non-silicate-bound phases in the soil.

A number of factors can affect the efficiency of EDTA in enhancing sol-ubilization of Pb. These factors are: (1) soil physical (texture, structure) and chemical (pH, redox potential, cation exchange capacity, soil buffering capacity, calcareousness, soil organic matter content) properties; (2) concentration of Pb


and EDTA; (3) time and mode of EDTA application; (4) presence of competing cations; (5) Pb species and their distribution among soil fractions; (6) adsorp-tion of free and complexed Pb on to charged soil particles; and (6) the formation constant of metal–ligand complexes (Saifullah et al., 2008, 2009a, b, 2010a, b). Upon the addition of EDTA to Pb-contaminated soils, 600- and 217-fold increases in Pb concentration in soil solution have been reported by Wu et al. (2003) and Nascimento (2006), respectively, in separate studies. Although a large number of studies have confirmed the linear relationship between EDTA concentration and Pb solubility (Hong and Jiang, 2005; Kim et al., 2003), other factors like metal species, concentration in the soil, soil properties, as well as the amount of EDTA applied, also play their specific role in affecting the efficacy of EDTA to solubilize soil-bound Pb.

Effect of EDTA on Pb Uptake by PlantsEDTA application greatly increases Pb mobility in soil and plants. The first and most important mechanism behind EDTA-enhanced uptake is the increased mobility of Pb in the soil–plant system with applied EDTA. The literature reports two different theories of EDTA-enhanced Pb uptake by plants. The first theory believes in the free metal ion concept, which states that EDTA–Pb com-plexes cannot be taken up by plants. According to this theory, the EDTA makes a complex with Pb and facilitates the Pb movement to the root surface where it is broken down into its components. Pb is absorbed by the roots and EDTA remains in soil for further metal complexation. With the advancement in ana-lytical techniques and availability of equipments to study the metal speciation and behaviour within a plant body, recently, many scientists (Sarret et al., 2001; Vassil et al., 1998; Cooper et al., 1999; Epstein et al., 1999) were able to find Pb as a Pb–EDTA complex within the plant body. The size and polarity of the Pb–EDTA complex does not permit it to enter directly through cell membranes or the symplastic pathway. However, from soil solution Pb–EDTA complex may be taken up along the apoplastic pathway and is then entered into stele through a leaky / underdeveloped Casparian strip. From stele it is translocated to above-ground harvestable parts via xylem under the force of plant transpiration (Tan-ton and Crowdy, 1971).

Effect of EDTA on Pb Translocation to Shoot TissuesLead is a unique element which shows very limited movement both outside (soil) and inside the plants. Most of the Pb absorbed by plants is retained by roots with very limited translocation to above-ground plant parts. The limited translocation of Pb from roots to shoots could be attributed to many factors including: (1) high affinity of free ionic Pb to plasma membrane (Jiang and Liu, 2010); (2) its pre-cipitation at the surface of roots as insoluble salts (Pourrut et al., 2011); (3) hin-drance offered by the Casparian strip (Mingorance et al., 2012); (4) precipitation in intercellular space (Meyers et al., 2008); or (5) accumulation in the vacuoles


(Kopittke et al., 2007). However, Pb chelation by EDTA results in the formation of a complex that behaves differently in the soil–plant system. Chelated lead is less retained by plant roots and is rapidly translocated to shoot tissues (Crist et al., 2004; Zhivotovsky et al., 2011). The translocation of Pb–EDTA com-plex across the root cortex into the xylem may occur via the symplastic or the apoplastic pathway and varies with plant type and the concentration of EDTA (Saifullah et al., 2009a; Shahid et al., 2012b). A number of studies reported several-fold enhanced translocation of Pb from roots to aerial parts by EDTA (Epstein et al., 1999; López et al., 2005; Barrutia et al., 2010). Blaylock et al. (1997) reported about 1000–10,000 times greater Pb accumulation by Brassica juncea (L.) Czern with the application of EDTA compared to untreated controls. In another study, Jarvis and Leung (2001) using transmission electron micros-copy found free ionic Pb species in root tissue plants while Pb complexed with chelating agents was mainly found in the shoots of Chamaectisus palmensis. Likewise, other studies (Huang et al., 1997; Vassil et al., 1998) also confirmed the transportation of Pb as Pb–EDTA complex in B. Juncea.

Although concentration of EDTA considerably affects the Pb uptake, both time and method of application also play significant roles in the effectiveness of EDTA-enhanced Pb accumulation. Greman et al. (2001) reported about 105 times higher concentration of Pb in the shoots of Brassica rapa grown in con-taminated soil and treated with a single dose addition of 10 mmol EDTA kg−1, while the Pb concentration in root was 1.7 times lower compared to control treatments. Application of EDTA in many small doses shows more effectiveness compared to the single-dose application method. Saifullah et al. (2009b) found that the split application of EDTA significantly enhanced the shoot Pb contents of Triticum aestivum L. compared to single-dose application.

Plant species do respond differently to EDTA-enhanced uptake of heavy met-als including Pb. Shen et al. (2002) reported that cabbage mung bean and wheat crops accumulated Pb differently when exposed to EDTA at 3.0 mmol EDTA kg−1 of soil. Although all the plants showed increased concentration of Pb in shoots and roots, cabbage plants accumulated higher Pb than other plant species. It has been reported by Saifullah et al., (2010c) that crop cultivars also differed significantly in accumulating EDTA-mobilized Pb. The authors investigated the effects of EDTA on lead accumulation by two spring wheat varieties (Auqab-2000 and Inqalab-91). The results indicated that the addition of EDTA to the soil significantly increased Pb solubility and Inqalab-91 was superior in toler-ance to Pb than Auqab-2000.

Risks Associated with EDTA-Assisted Pb PhytoextractionAlthough EDTA has been the most efficient synthetic chelating agent for assisted phytoremediation of Pb, many concerns have been raised about the use of EDTA in remediation technology (Alkorta et al., 2004; Evangelou et al., 2008; Saifullah et al., 2009a). In spite of many efforts to decrease the adverse


effects of EDTA-assisted Pb phytoextraction (changing mode, time and rate of application), its large-scale use is still controversial. EDTA is not an ideal can-didate for Pb phytoextraction for the following reasons:

1. Soil-applied EDTA can adversely impact soil enzymatic and microbial activities.

2. At high concentrations EDTA can negatively affect soil fungi and plants. 3. Pb–EDTA is a highly soluble complex and thus can easily leach to ground-

water. 4. EDTA and Pb–EDTA complexes are not easily biodegradable and may per-

sist in soil for several months. 5. The complex is not ideal in terms of plant uptake and translocation. 6. EDTA salt can destroy the physical and chemical properties of soil. 7. EDTA can enhance the stimulation of Pb as well as other elements leaching

into groundwater. 8. Competition of major cations like Ca and Fe with Pb for EDTA can lower

the efficiency the EDTA to solubilize Pb. 9. High costs associated with EDTA-assisted Pb phytoextraction. 10. At higher rates, soil-applied EDTA can result in eutrophication because of

excessive release of nitrogen from EDTA. 11. EDTA can affect soil nutrients status due to unspecific co-mobilization of

macro- and micronutrients.

Ethylene Diamine Disuccinic Acid

Ethylenediamine disuccinic acid (EDDS), C10H16N2O8, is an isomer of EDTA that is produced either artificially or naturally by various microorganisms (Takahashi et al., 1999; Ullmann et al., 2013). EDDS was first separated from the filtrate of Amycolatopsis orientalis filtrate (Nishikiori et al., 1984; Alkorta et al., 2004). EDDS posses two chiral centres, and therefore four isomers: two enantiomers (–S,S and –R,R) and two mesoisomers (–S,R and –R,S) (Ullmann et al., 2013). The –R,R isomer of EDDS is non-biodegradable, whereas the –R,S, and –S,R are partially degradable; therefore, the SS-isomer is commonly used in remediation studies (Schowanek et al., 1997; Fabbricino et al., 2013). Recently EDDS has appeared as a potential substitute to EDTA in heavy metals remediation studies (Kos and Leštan, 2003; Meers et al., 2005; Quartacci et al., 2007; Wang et al., 2012; Chang et al., 2013; Lan et al., 2013). It has the ability to improve solubilization / mobilization and the accumulation of heavy metals such as Cd, Pb, Cu, Ni, Hg and Zn by different plant varieties. It is highly bio-degradable and more than 90% of [S,S]-EDDS is reported to mineralize within four to eight weeks of its application (Schowanek et al., 1997; Meers et al., 2005; Yang et al., 2013). In some reports it has been shown to be more efficient for both ex situ washing and phytoextraction treatments than EDTA or NTA (Wang et al., 2007; Xu and Thomson, 2007).


Effect of EDDS on Pb Solubilization in SoilOwing to less disruptive effects on the environment, EDDS is gaining atten-tion as an amendment to enhance Pb phytoextraction (Yan et al., 2010; Suzuki et al., 2013). EDDS is capable of metal ions complexation. Like EDTA, EDDS can form complexes with Pb and other metals through its oxygen atom of carboxylate groups or nitrogen item of imine groups. Cao et al. (2013) reported up to 99.8% desorption of Pb by EDDS (10 mM) in soil. Mohtadi et al. (2013) observed that 95% of Pb was in the chelated form in a solution containing 1 μM Pb and 3.1 μM EDDS. Presence of EDDS is reported to enhance several times the solubilization / mobilization of Pb and other heavy metals (Fässler et al., 2010; Lozano et al., 2011; Fabbricino et al., 2013; Hseu et al., 2013; Prieto et al., 2013; Ullmann et al., 2013). The abil-ity of EDDS to desorb / solubilize metals including Pb is dependent on many factors including amount of EDDS, concentration of Pb and its distribution among different soil fractions, ratio of EDDS to Pb (stoichiometric effects), soil pH and soil organic matter content (Begum et al., 2012, 2013; Fab-bricino et al., 2013). It has been reported to desorb Pb from soil solids very rapidly and making stable Pb–EDDS complex in soil solution (Yan et al., 2010; Cao et al., 2013; Suzuki et al., 2013; Chang et al., 2013; Yang et al., 2013). Generally EDDS-induced extraction of Pb and other metals is a quite fast process. The process of metal extraction by EDDS is greater and faster for metal fractions bound to the carbonate and exchangeable phases (Yip et al., 2009; Ardwidsson et al., 2010). Once EDDS–Pb complex is formed, it prevents the re-adsorption of metals on to solid phases, thus increasing the solubility of Pb in soil. However, the degradation of EDDS in soil results in Pb release to soil, and subsequent re-adsorption or re-precipitation in the soil (Yan et al., 2010; Lo et al., 2011; Yang et al., 2013). It is reported that EDDS-induced solubilization / mobilization of Pb in soil first increases and then gradually decreases with time due to the degradation of EDDS (Wang et al., 2009; Yang et al., 2013).

Effect of EDDS on Pb Accumulation by PlantsLike many other chelating agents, EDDS has the ability to enhance the Pb uptake by plant roots and translocation towards plant shoots. Several previous studies have reported the use of EDDS in chelant assisted phytoextraction of Pb and other metals in polluted soil (Kulli et al., 1999; Kayser et al., 2000; Kos and Leštan, 2003; Quartacci et al., 2007; Wang et al., 2009; Mohtadi et al., 2013; Fabbricino et al., 2013). Metal–EDDS complexes are more mobile inside the plants than free metal ions including Pb (Prieto et al., 2013). The mechanism of EDDS-induced Pb uptake is still unidentifiable. The absorption pathway varies with concentration of EDDS. At low concentrations, diffusion across the root apoplastic spaces into root xylem is considered as the main absorption mecha-nism. However, free EDDS at high concentrations, whether in hydroponics or in soil, can result in destruction of physiological barriers in roots through removal


of Fe2+, Ca2+ and other cations from the plasma membrane (Gunawardana et al., 2010; Niu et al., 2011). Mohtadi et al. (2013) reported increased Pb uptake and translocation in hydroponically grown Matthiola flavida only at higher levels of EDDS and Pb application. Tandy et al. (2006) proposed passive uptake mecha-nism for EDDS-induced Pb uptake by Helianthus annuus.

Lead is reported to be sequestered in plant roots for the majority of the plants (Pourrut et al., 2011). Unlike EDTA, EDDS is not always reported to facili-tate root to shoot Pb translocation (Mohtadi et al., 2013). This may be due to weak Pb–EDDS (log K 12.7) complexes compared to Pb–EDTA complexes (log K 18) (Martell et al., 2001). Pb–EDDS complex may dissociate before plant uptake or inside the plant, thus giving rise to free Pb and free EDDS inside plants. Free-EDDS has been detected in shoots and xylem sap of Helianthus annuus (Tandy et al., 2006).

Degradation of EDDSOne of the main advantages of EDDS utilization for soil phytoremediation is certainly its biodegradability (Jones and Williams 2001; Vandevivere et al., 2001; Finžgar et al., 2006; Prieto et al., 2013; Yang et al., 2013). The biodegrad-ability of EDDS depends on its two l-aspartic amino acids, which are the main structural components of EDDS (Ullmann et al., 2013). The EDDS has a range of degradation rates, and the majority of the studies reported its half-life to be from 2 to 9 days in soils (Schowanek et al., 1997; Tandy et al., 2006). Hauser et al. (2005) reported that approximately 18–42% of EDDS in soil was degraded over 7 weeks. According to Meers et al. (2005), EDDS may degrade fully within 54 days. Prieto et al. (2013) showed a significant decrease in metal leaching in the presence of EDDS which was due to the degradation of EDDS. Cao et al. (2007) also reported that solubilization / mobilization of metals decreased to control values within 50 days in the presence of EDDS.

Another problem associated with chelate-assisted phytoremediation is the possible residual effects of chelate on the following crop (Leštan et al., 2008; Yang et al., 2013), which may affect the successful phytoextraction process of a polluted site (Luo et al., 2005). Because of its rapid biodegradability in natural mediums, very little residual effects of EDDS on the environment has been reported (Evangelou et al., 2007; Quartacci et al., 2007; Lan et al., 2013; Mohtadi et al., 2013; Yang et al., 2013). Luo et al. (2006) reported no signifi-cant residual effects on Pb concentrations in corn plants six months after EDDS application to soil. Komárek et al. (2010) also reported no marked toxic effect on poplar growth 1 year after EDDS application. It has been reported that Pb solu-bilization by EDDS sharply decreases within 30–50 days (Wang et al., 2009). Different factors affect the rate of EDDS degradation in soil which include the applied rate and soil physico-chemical properties (Meers et al., 2008; Lo et al., 2011; Yang et al., 2013). Moderately contaminated soils display almost the same lag phase despite their different textures (Fabbricino et al., 2013). The lag phase increases from 3 to 4 weeks with increasing level of contamination


for soils with the same texture (Meers et al., 2008). The stability constant of the metal–chelate complex has no effect on the degradation of EDDS complexes (Kołodyńska et al., 2013). These findings suggest that EDDS might be a bet-ter substitute of EDTA for the remediation of Pb-polluted soil due to its rapid degradation and limiting potential of metal leaching.

Drawbacks of EDDS-Assisted PhytoremediationAlthough EDDS is highly biodegradable, and is capable of increasing Pb solu-bilization, the threat of Pb leaching to deep soil profiles or groundwater is not fully addressed (Tandy et al., 2006; Leštan et al., 2008; Fedje et al., 2013). Therefore, it is highly necessary to predict the possible consequences of EDDS application on the environment before its real field-scale application. Kos and Leštan (2003) reported that EDDS application caused Pb leaching of 20–25% from 27-cm soil column. Similarly, EDDS-induced metal leaching from a soil column of 60 cm depth was reported by Wang et al. (2012). Likewise, Hauser et al. (2005) and Hu et al. (2007) observed Pb and / or Cu leaching from sur-face to subsurface soil with the use of EDDS as metal solubilizer. Metal leach-ing with EDDS application is suggested by the two possible processes. Firstly, EDDS has shown rapid degradation in soil, that might result in short-term com-plexation and then release of Pb into soil atmosphere (Yan et al., 2010; Lo et al., 2011). Secondly, EDDS-induced metal leaching may occur via its exchange by Fe. Fe–EDDS complex has a high stability constant compared to Pb–EDDS or other metal–EDDS complexes. Therefore, EDDS is generally applied to soil in continuous or multiple additions of EDDS solution (Yan et al., 2010).

Nitrilotriacetic Acid (NTA)

Nitrilotriacetic acid (NTA), C6H9NO6, is a tertiary amino-polycarboxylic acid which has been used widely as a chelating agent in the recent past. NTA forms coordination compounds with metal. NTA can chelate Pb and other metal ions to form soluble complexes. NTA is proposed as an alternative to EDTA, for chelate-assisted phytoextraction of Pb and other heavy metals (Quartacci et al., 2007). NTA has high biodegradability and degrades in soil as fast as oxalate or citric acid (Quartacci et al., 2005; Ruley et al., 2006). NTA has been used as a chelating agent in several metal-remediation studies owing to its posi-tive properties (Quartacci et al., 2006; Ruley et al., 2006; Chang et al., 2013 Reinoso-Maset et al., 2013).

Use of NTA for Pb PhytoremediationNTA is a strong potential synthetic chelate for Pb phytoremediation owing to its relatively fast biodegrability and chelating ability. NTA application to soil reduces the adsorption of Pb and other metals on pure minerals and soils (Howard and Shu, 1996). The addition of NTA increased the exchangeable frac-tion of Pb with a simultaneous decrease of Pb bound to organic matter. However,


Pb–NTA complex is highly degradable and the dissociation of this complex can reduce the effect of aqueous complexation on Pb sorption (Nowack and Sigg, 1997). Several studies used NTA for the solubilization / extraction of Pb and other metals from polluted soils (Hseu et al., 2013; Lan etal., 2013). Zhao et al. (2013) reported that application of NTA increased Pb uptake 3.8 times by Festuca arundinacea and at the same resulted in minimal leaching of Pb. Quartacci et al. (2006) also found that application of NTA enhanced metal con-centrations in Indian mustard shoots.

Application of NTA as Pb remediation chelant has the advantage of being non-toxic to plants and soil microorganisms. Zhao et al. (2011) reported that application of NTA has no toxic effect on plant growth of Festuca arundinacea. The low toxicity of NTA to plants is probably because of fast degradation of metal–NTA complex (Evangelou et al., 2007; Quartacci et al., 2007). Compared to EDTA, several other studies also reported reduced toxicity of Pb in the pres-ence of NTA (de Souza Freitas and do Nascimento, 2009). NTA is even reported to have positive effects on plant growth (Duo et al., 2010; Zhao et al., 2011).

COMPARISON OF SYNTHETIC CHELATING AGENTS

Several studies compared synthetic chelates with respect to their efficiency to improve metal uptake by plants (Saifullah et al., 2010a, 2010b). In most cases, the effect of EDTA was many times higher than that of other synthetic chelates (Hadi et al., 2010; Jean-Soro et al., 2012). For example, Meers et al. (2004) observed that EDTA was more effective than NTA and DTPA at increasing Pb uptake by Zea mays. Lesage et al. (2005) reported that EDTA was more effi-cient than citric acid in enhancing heavy metals (Pb, Cd, Cu and Zn) uptake by Helianthus annuus. Ruley et al. (2006) showed that chelates increased Pb accumulation in Sesbania drummondii cultivated on polluted soil in the order EDTA > HEDTA > DTPA > NTA. Huang et al. (1997) reported that the effect of synthetic chelates on Pb uptake by Pisum sativum and Zea mays was: EDTA > HEDTA > DTPA > EGTA > EDDHA. Similarly, Sekhar et al. (2005) revealed that EDTA was the most effective in enhancing Pb accumulation by Hemidesmus indicus. EDDS is reported to desorb more Pb than NTA because of its highest affinity constants with Pb (Meers et al., 2005). Theoretically, the metal remedia-tion efficiency of a chelate depends on the binding constant (log K) of the metal complex. EDTA has higher affinity for Pb than other synthetic chelates and is therefore more efficient for the remediation of Pb-polluted sites.

CONCLUSIONS

Heavy metal contamination has become a serious threat to biological systems. Lead contamination can be decreased to acceptable levels through high bio-mass plants aided with the applied EDTA as an amendment which forms highly soluble and stable metal–EDTA complexes with Pb. A large number of factors


affect the efficiency of EDTA-induced metal phytoremediation. A better under-standing of soil, plant and climatic factors can help improve the effectiveness of chelant-assisted phytoremediation of Pb.

Many concerns have been raised about the adverse impacts of EDTA-assisted phytoextraction. Therefore, it has been advocated to avoid EDTA-assisted phy-toremediation. Recently many biodegradable synthetic chelants such as EDDS and NTA have been employed to assist high biomass crops in removing met-als from contaminated soils. Although chemically assisted phytoextraction has always shown more disruptive effects on the ecosystem than natural phyto-extraction, more research on the role of non-persistent chelants with minimal effects on the environment should be continued under real-field conditions to improve understanding of the mechanisms involved in assisted phytoextraction.

REFERENCES

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soil remediation and plants || phytoremediation of pb-contaminated soils using synthetic chelates

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