Heavy metal phytoextraction—natural and EDTA-assisted remediation of contaminated calcareous soils by sorghum and oat

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The abilities of sorghum (Sorghum bicolor L.) and oat (Avena sativa L.) to take up heavy metals from soils amended with ethylenediaminetetraacetic acid (EDTA) were assessed under greenhouse conditions. Both plants were grown in two soils contaminated

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  Heavy metal phytoextraction  —  natural and EDTA-assistedremediation of contaminated calcareous soils by sorghumand oat Muhammad Mahmood-ul-Hassan  & Vishandas Suthar  &  Rizwan Ahmad  &  Munazza Yousra Received: 5 June 2017 /Accepted: 12 October 2017 # Springer International Publishing AG 2017 Abstract  The abilities of sorghum ( Sorghum bicolor  L.) and oat (  Avena sativa  L.) to take up heavy metalsfrom soils amended with ethylenediaminetetraacetic ac-id (EDTA) were assessed under greenhouse conditions.Both plants were grown in two soils contaminated withheavy metals(Gujranwala  —  silty loamand Pacca  —  clayloam). The soils were treated with 0, 0.625, 1.25, and2.5 mM EDTA kg − 1 soil applied at both 45 and 60 daysafter sowing (DAS); the experiment was terminated at 75 DAS. Addition of EDTA significantly increasedconcentrations of Cd, Cr, and Pb in roots and shoots,and bio-concentration factors and phytoextraction rateswere also increased. Post-harvest soil analysis showedthat soluble fractions of metals were also increasedsignificantly. The increase in Cd was  ≈  3-fold and Pbwas  ≈  15-fold at the highest addition of EDTA inGujranwala soil; in the Pacca soil, the increase wasless. Similarly, other phytoremediation factors, such asmetal translocation, bio-concentration factor, and phytoextraction, efficiency were also maximum whensoils were treated with 2.5 mM EDTA kg − 1 soil. Thestudy demonstrated thatsorghum was better than oat for  phytoremediation. Keywords  Alkalinecalcareoussoil.Heavymetals.Phytoremediation.Oat  . sorghum Introduction Release of heavy metals and metalloids through emis-sion or discharges (effluent and solid) from anthropo-genic activities, such as use of automobiles, agriculturalchemicals, and untreated municipal/industrial effluent/ solid, is badly affecting the environment and causingsoil contamination. Application of untreated municipal/ industrialdischargestoarablelandisacommonpracticein most African and Asian countries including Pakistan.Continuous application of these metal-enriched dis-charges (Hussain et al. 2006; Mahmood-ul-Hassanet al. 2012) and strong affinities of the metals withorganic matter, iron oxides, clay minerals, carbonates,and phosphates increases the concentration of metals insurface soil (Han et al. 2001). The metals are not bio-logically or chemically degradable like organic contam-inants and remain in soil for a long period. Solubilityand availability of metals in soil are basically controlled by sorption and desorption process between metal con-centrations in soil solution and soil constituents. How-ever, upon overloading, the soil liberates adsorbedmetals to soil solution which can be either leached toshallow groundwater or taken up by plants. Although,several trace metals like copper, iron, manganese, nick-el, zinc, and molybdenumare essential for plant growth,high concentrations of these trace element in soil solu-tion may become hazardous and can pose risks and Environ Monit Assess  (2017) 189:591 https://doi.org/10.1007/s10661-017-6302-yM. Mahmood-ul-Hassan ( * ) :  V. Suthar   :  R. Ahmad  : M. YousraLand Resources Research Institute, National AgriculturalResearch Centre, Islamabad 45500, Pakistane-mail: mmh@comsats.net.pk V. Suthar Central Cotton Research Institute, Sakrand, Pakistan  hazards to humans and the ecosystem (Schwab et al.2005). Crops grown in these contaminated soils canaccumulate metals to levels which can be a health hazardto animals and humans causing carcinogenic, cardiovas-cular, and gastrointestinal diseases (Sharma et al. 2014).Oncesoils are contaminatedwithheavymetals,itisa persistent problem and needs special management andremediation practices for safe and sustainable crop pro-duction. Several techniques are used for the remediationof metal-contaminated soil and can be categorized asisolation, stabilization, oxidation, physical separationand phytoextraction. Among these, immobilization and phytoextraction are the main approaches used in soilremediation. In the immobilization technique, contami-nated materials are amended with inorganic and organic binding agents to reduce the bioavailability to livingorganisms mainly by stabilization or precipitation of hydroxides within the solid matrix. In fact, the contam-inants remain in the soil matrix and subsequently sub-strates can release the stabilized or precipitated contam-inants to soil solution. Phytoextraction involves theextraction of heavy metals from contaminated soils by plant roots and then translocation to shoots; it is consid-ered a cost-effective and environmentally safe remedia-tion technique.Phytoextraction involves translocation and accumu-lation of large amount of metals from soil into the below- and above ground-plant parts (Song et al.2005; Mahmood 2010; Zhuang et al. 2007). This tech- nique helps to remove metals from a contaminated soilto a safe level for crop production. The metal-enriched,harvested plant parts can safely be processed by micro- bial (composting and anaerobic digestion) physical (in-cineration and dumping), and chemical means (gasifi-cation and production of pure oil) (Ghosh and Singh2005; Ginneken et al. 2007). Early phytoextraction re- search was mainly focused on hyper-accumulators.However, they were generally element specific, slowgrowing with low biomass and took up only smallamounts of metals (Cunningham et al. 1995).Alternatively, fast-growing and high-yielding plant species were involved in phytoextraction processesand their low metal uptake ability was addressed byincreasing metal solubility and bioavailability by theapplication of suitable chemicals to contaminated soils(Komárek et al. 2007a; Melo et al. 2008; Tandy et al. 2006). In this process, synthetic chelating agents aremixed with soil, (e.g., EDTA (ethylenediaminetriaceticacid), DTPA (diethylenetriaminepentaacetic acid),EDDS (ethylenediamine-disuccinic acid), EDDHA(ethylenediamine-di (o-hydroxyphenylacetic acid),HEDTA (hydroxyethylendiaminetriacetic acid)) to sol-ubilize soil-bonded metals. The increased solubility of the heavy metals increased root metal uptake(Evangelou et al. 2007; Jean et al. 2008) and facilitated root to shoot translocation (Blaylock et al. 1997; Huanget al. 1997; Song et al. 2005). Among these, EDTA is considered the most effective in solubilizing different forms of metals in soil (Kos and Le š ten 2003; Nascimento and Xing 2006).In this study, the natural and EDTA-assisted Cd, Cr,and Pb phytoextraction capacity of native high biomass plants (oat and sorghum) was assessed and compared. Materials and methods Cadmium, chromium, and lead removal capacity of sorghum and oat was assessed by growing on contam-inated soils amended with ethylenediaminetetraaceticacid (EDTA). Bulk surface samples of two contaminat-ed soils, Gujranwala (fine-loamy, mixed, hyperthermicUdic Haplustalf) and Pacca (fine, mixed, hyperthermicUstolic Camborthid) were collected from arable sitesunder untreated municipal/industrial wastewater irriga-tion. A detailed description of both sites and soils wasgiven by Suthar et al. 2014. The soil samples were driedunder shade, ground, and passed through a 2-mm stain-less steel sieve. A small fraction of   ≈  200 g, obtainedfrom the bulk ground samples ( ≤  2 mm), was further groundto ≤ 200 μ  mforchemicalanalysis.Boththesoilswere alkaline calcareous; Pacca soil had higher claycontent but lower organic matter content than Gujran-wala soil (Suthar et al. 2013).Pot experimentsSorghum( Sorghumbicolor  L.)andoat(  Avenasativa L.)were selected for this study due to their widespreadcultivation in Pakistan, high biomass production, fast growth, and tolerance of heavy metals. Plants weregrown in polyethylene-lined earthen pots filled with7 kg of each soil (Mahmood-ul-Hassan et al. 2012).The experiments were conducted under greenhouseconditions with natural photoperiod. A basal dose of nitrogen at 150 mg kg − 1 dry soil in three splits, phos- phorus at 70 mg kg − 1 , and potassium at 50 mg kg − 1 wasapplied. Soil moisture, i.e.,  ≈  60% of the field capacity,  591 Page 2 of 10 Environ Monit Assess  (2017) 189:591  was maintained during the experiment. EDTA at 0,0.625, 1.25, and 2.50 mM kg − 1 soil was applied twice,i.e., 45 and 60 days after sowing (DAS) in three repli-cates. The experiments were terminated at 75 DAS.Plant roots and shoots were dried at 70 °C in a convec-tion oven and weighed. The dried plant shoots and rootswere crushed in a stainless steel mill and Cd, Cr, and Pbconcentrations measured. Soil samples collected after harvesting of plants were analyzed for 0.01 M CaCl 2 extractable Cd, Cr, and Pb concentrations (Sparks et al.1996).Phytoextraction efficiency of the plantsBio-concentration factor (BCF)  —  a measure of naturaland EDTA-assisted phytoextraction efficiency of thetested plant species was calculated using followingequation ((Zhuang et al. 2007):  BCf    ¼  C   p C   s Where  Cp  is the concentration of metals in plant tissues( μ  g g − 1 ) and  Cs  is the total soil metal concentration( μ  g g − 1 ).The following equation was used to calculate thePhytoextraction rate (PR %; Komárek et al. 2007b;Zhuang et al. 2007):  PR  % ð Þ ¼  T   pmu T   smc   : 100Where  T   pmu  is the total metal uptake by plants {metaluptake by shoots + roots ( μ  g)}, and  T   smc  is the total soilmetal content ( μ  g).Soil and plant analysisPhysico-chemical properties of the soils were measuredusing standard procedures (Dane and Topp 2002;Sparks et al. 1996). Total metal concentrations in plantstissue were measured after wet digestion (nitric acid and perchloric acid). Bio-available metal concentrations insoil samples were measured by extracting with DTPAsolution. Metal concentrationsindigestand soilextractswere analyzed using a graphite furnace atomic absorp-tion spectrometer (Perkin Elmer AAnalyst 800).Statistical analysisAnalysis of variance (ANOVA) of the data was calcu-lated using Minitab and the means compared for signif-icance at 5% probability level. Results and discussion Initial soil characteristicsPropertiesofthePacca andGujranwalasoilsusedinthisstudy are reported elsewhere (Suthar et al. 2014). Bothsoils were non-saline, alkaline calcareous with organicmatter concentrations of 1.23 and 1.36%; CEC 11.6 and10.3 cmol/kg and textural classes clay loam and silt loam, respectively. Although the total concentrationsof Cd, Cr, Pb, and Ni were higher than the recommend-ed permissible limits (Ewers 1991) in both soils, theGujranwala soil had higher total metal concentrationsthan that of the Pacca soil. Total metal concentrationsgenerally control the metal concentrations in soil solu-tion and thus the possibility of metal uptake by plants(Samsøe-Petersen et al. 2002).In both the soils, the predominant fraction of Cr andPb was associated with the residual fraction while Cdwasotherwise(Fig.1).Thenon-residualpoolwasmain-lycomprisedofCaCO 3 andorganic fractionsandwasinline with the earlier results reported by Younas andAfzal (1999) and Kos et al. (2003). The Pacca soil had higher carbonate-bonded Cd than the Gujranwala soilmost probably because of its higher CaCO 3  content (Table 1); a similar positive correlation between CaCO 3 contents and carbonated forms of Cd has also beenreported by Ramos et al. (1994) and Li et al. (2001). Lead was present predominantly in the residual form,while the ratio of different non-residual forms of Pb wascomparableandsimilartoCd.Ahighlycarbonatedformof Pb in soils having high CaCO 3 content was alsoreported by Li and Thornton (2001) and strong bondingof Pb with soil organic matter by Kabata-Pendias andPendias (1992).Dry matter yieldShoot growth and development of both plants werenormal, but after application of EDTA at 45 and 60DAS, effects of heavy metal stress on the plant shootswere obvious. A reduction in shoot growth of both crop Environ Monit Assess  (2017) 189:591 Page 3 of 10  591   plants was observed with increasing levels of EDTA(Table 2) and chlorosis and necrosis symptoms wereobvious at 2.5 EDTA kg − 1 soil. The signs of stress,i.e., dying of plant tissues, were visible even after theapplication of the first dose of EDTA, and after thesecond dose, nearly all plants were partially dried in both the soils. Similarly, Suthar et al. (2014) also ob-served significant reduction (50  –  60%) in maize andsesbania shoot biomass when grown in heavy metal-contaminated soils amended with 5.0 mM EDTA kg − 1 soil. Toxicity of high metal concentrations (Table 3)could be one reason for growth retardation but another could be the presence of free chelate in the soil (Jeanet al. 2008; Nascimento and Xing 2006; Sun et al. 2009). Hernandez-Allica et al. (2003) reported a decrease in transpiration, stomatal conductance and photosynthesis rates in artichokes ( Cynara cardunculus L.) when grown in EDTA-treated (1.0 mM L − 1 ) Pb-contaminated soils.A significant (  p  < 0.05) reduction in root biomassof sorghum was observed in both soils (Table 2) whentreated with EDTA. This reduction was more in theGujranwala soil (up 52%) than the Pacca soil (up33%) at 2.5 mM EDTA kg − 1 soil. The large reductionin the Gujranwala soil was probably due to the highindigenous total metal concentration and subsequent extractable metal concentrations. The high concentra-tions could inhibit plant root growth by reducing the 0102030405060708090100Cd Cr Pb Cd Cr PblioSaccaPlioSalawnar  juG    M  e   t  a   l   P  e  r  c  e  n   t  a  g  e Water soluble Exchangeable Carbonate Oxide Organic Residual Fig. 1  Different fractions of Cd,Cr, and Pb (%) in Gujranwala andPacca soils Table 1  Physico-chemical characteristic and total heavy metalcontents in studied soilsParameter Pacca( Typic Camborthid  )Gujranwala( Udic Haplustalf   ) pH (1:2) 7.86 ± 0.05 7.56 ± 0.06EC (dSm − 1 ) 1.25 ± 0.03 0.44 ± 0.02O.M. (%) 1.23 ± 0.03 1.36 ± 0.05CaCO 3  (%) 11.00 ± 1.00 1.50 ± 0.60CEC (mq/100 g soil) 11.55 ± 1.20 10.29 ± 0.90Particle size distribution (%)Textural Clay loam Silty loamTotal heavy metal contents (mg kg − 1 )Lead 126 ± 7.46 270 ± 11.31Cadmium 6.81 ± 0.39 7.81 ± 1.21Chromium 137.3 ± 5.12 331.8 ± 8.67 Nickel 104.2 ± 4.65 148.5 ± 6.78 Table 2  Dry shoot and roots weight (g pot  − 1 ) of sorghum and oat grown on contaminated soils amended with EDTAEDTA rates Shoots Roots(mM kg − 1 ) Sorghum Oat Sorghum Oat Gujranwala soil0 27.34 4.93 15.57 3.980.625 24.30 4.60 10.33 3.961.25 23.48 3.90 8.78 3.272.5 20.78 3.18 7.32 3.12Mean 23.98 4.15 10.50 3.27LSD (  P   < 0.05) 3.39 0.85 2.75 NSPacca soil0 18.33 4.63 8.95 2.640.625 16.60 3.14 9.19 2.701.25 15.94 2.90 7.83 2.252.5 15.29 2.74 5.96 2.03Mean 16.54 3.36 7.98 2.41LSD (  P   < 0.05) 1.77 1.87 2.11 0.22  591 Page 4 of 10 Environ Monit Assess  (2017) 189:591  viscosity and elasticity of cell walls (Feng et al. 2004).Further, high Pb absorption by the roots due to ele-vated concentrations in the soil may also retard root growth (Heidari et al. 2005). Wu et al. (2004) related dying of Indian mustard leaves after the addition of EDTA into the soil with phytotoxicity of EDTAmetals.Metal concentrations in plant tissuesSignificant increases in soil solution metal concentra-tions with the addition of EDTA (Suthar et al. 2013) bydesorbing from the soil and forming ligands (Komárek et al. 2007a; Komárek et al. 2007b) also resulted in significant (  p  < 0.05) increases of Cd, Cr, and Pb con-centrations in plant shoots (Fig. 2a). EDTA at 2.5 mM kg − 1 soil gave the highest increase in Pb con-centrations (sorghum  —  95% and oat   —  140% inthe Guj-ranwala soil and 138%  —  sorghum and 118%  —  oat inthe Pacca soil). Increases in Cd and Cr concentrations insorghum shoots were similar   ≈  60 and  ≈  43% in Guj-ranwala and Pacca soils, respectively. However, in oat,the increases in Cd and Cr concentrations were different in the two soils; most probably, this was due to thereduction in biomass with increased soil solution metalconcentrations as a result of increasing rates of EDTA(as confirmed earlier). Komárek et al. (2007a) describedthat the addition of chelating agents enhancedtranspiration in stressed environments which ultimatelyresulted in the death of plants. Metal concentrationswere significantly higher in the roots of both crops thanin the shoots. The difference between root and shoot metal concentrations was greater in Pacca soil thanGujranwalasoil(Fig.2 b).Nowacketal.(2006)reported that amendment of soil with chelates not only enhancedthe bio-available fraction, but also improved the metaluptake process depending upon metal and plant speciesand amount of chelate. Likewise, significant increase in bothsoilbioavailabilityPbandinshootconcentrationof Indian mustard with addition of EDTA to soil was alsoobserved by Wu et al. (2004). Pb and Cr concentrationswere  ≈  15 times higher than Cd in roots whereas thedifference between Pb and Cd concentration in shootswas smaller, i.e., Pb was  ≈  3 times higher than Cd. Thisis most likely attributable to the Cr and Pb complexesformed with EDTA and are generally dominated inmany soil as ligands (Sommers and Lindsay 1979).The ability of EDTA to enhance Pb bioavailability morethan Cd has also been observed by Kos et al. (2003) andTuran and Esringü (2007). According to Turan andEsringü (2007), internal restriction in the translocationof Pband Cd from roots to shoots can resultin high root concentrations. Another reason could be the ability of  plant roots to produce secretions as organic acids that form ligands and thereby enhance absorption by roots(Pereira et al. 2007). Table 3  Extractable metal concentrations (mg kg − 1 ) in soils after harvesting sorghum and oat EDTA rates Cd Cr Pb(mM kg − 1 ) Sorghum Oat Sorghum Oat Sorghum Oat Gujranwala0 0.212 0.197 0.355 0.217 2.181 1.8250.625 0.564 0.398 0.357 0.272 20.777 17.9031.25 0.684 0.453 0.505 0.376 33.287 29.0092.5 0.638 0.545 0.592 0.531 32.506 35.981Mean 0.524 0.398 0.452 0.349 22.188 21.179LSD (  P   < 0.05) 0.135 0.083 0.086 0.067 5.673 4.752Pacca0 0.204 0.222 0.132 0.092 1.812 1.4720.625 0.326 0.298 0.149 0.130 6.259 2.9861.25 0.355 0.291 0.147 0.155 8.970 7.1082.5 0.402 0.402 0.173 0.161 9.093 7.800Mean 0.322 0.303 0.150 0.134 6.534 4.842LSD (  P   < 0.05) 0.105 0.076 0.025 0.031 2.784 1.958Environ Monit Assess  (2017) 189:591 Page 5 of 10  591
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