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Can ligand addition to soil enhance Cd phytoextraction? A mechanistic model study

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An Erratum to this article was published on 31 January 2015

Abstract

Phytoextraction is a potential method for cleaning Cd-polluted soils. Ligand addition to soil is expected to enhance Cd phytoextraction. However, experimental results show that this addition has contradictory effects on plant Cd uptake. A mechanistic model simulating the reaction kinetics (adsorption on solid phase, complexation in solution), transport (convection, diffusion) and root absorption (symplastic, apoplastic) of Cd and its complexes in soil was developed. This was used to calculate plant Cd uptake with and without ligand addition in a great number of combinations of soil, ligand and plant characteristics, varying the parameters within defined domains. Ligand addition generally strongly reduced hydrated Cd (Cd2+) concentration in soil solution through Cd complexation. Dissociation of Cd complex (\( \mathrm{CdL} \)) could not compensate for this reduction, which greatly lowered Cd2+ symplastic uptake by roots. The apoplastic uptake of \( \mathrm{CdL} \) was not sufficient to compensate for the decrease in symplastic uptake. This explained why in the majority of the cases, ligand addition resulted in the reduction of the simulated Cd phytoextraction. A few results showed an enhanced phytoextraction in very particular conditions (strong plant transpiration with high apoplastic Cd uptake capacity), but this enhancement was very limited, making chelant-enhanced phytoextraction poorly efficient for Cd.

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References

  • Adhikari T, Rattan RK (2000) Modelling zinc uptake by rice crop using a Barber-Cushman approach. Plant Soil 227:235–242

    Article  CAS  Google Scholar 

  • Alloway BJ (2013) Trace metals and metalloids in soils and their bioavailability. In: Alloway BJ (ed) Heavy metals in soils. Environmental pollution, vol 22, 3rd edn. Springer, Netherlands. doi:10.1007/978-94-007-4470-7

    Chapter  Google Scholar 

  • Barber SA (1962) A diffusion and mass-flow concept of soil nutrient availability. Soil Sci 93:39–49

    Article  CAS  Google Scholar 

  • Barber SA (1995) Soil nutrient bioavailability: a mechanistic approach. Wiley, New York

  • Blaylock MJ et al (1997) Enhanced accumulation of Pb in Indian mustard by soil-applied chelating agents. Environ Sci Technol 31:860–865

    Article  Google Scholar 

  • Carr JD, Swartzfager DG (1975) Kinetics of the ligand exchange and dissociation reactions of calcium-aminocarboxylate complexes. J Am Chem Soc 97:315–321

    Article  CAS  Google Scholar 

  • Chaturvedi PK, Seth CS, Misra V (2006) Sorption kinetics and leachability of heavy metal from the contaminated soil amended with immobilizing agent (humus soil and hydroxyapatite). Chemosphere 64:1109–1114

    Article  CAS  Google Scholar 

  • Chen W, Chang AC, Wu L, Page AL (2006) Modeling dynamic sorption of cadmium in cropland soils. Vadose Zone J 5:1216–1221. doi:10.2136/vzj2006.0037

    Article  CAS  Google Scholar 

  • Ciesielski H, Sterckeman T (1997) A comparison between three methods for the determination of cation exchange capacity and exchangeable cations in soils. Agronomie 17:9–16

    Article  Google Scholar 

  • Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719. doi:10.1016/j.biochi.2006.07.003

    Article  CAS  Google Scholar 

  • Clemens S, Aarts MGM, Thomine S, Verbruggen N (2013) Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci 18:92–99

    Article  CAS  Google Scholar 

  • Collins RN, Merrington G, McLaughlin MJ, Knudsen C (2002) Uptake of intact zinc-ethylenediaminetetraacetic acid from soil is dependent on plant species and complex concentration. Environ Toxicol Chem 21:1940–1945

    CAS  Google Scholar 

  • Collins C, Fryer M, Grosso A (2006) Plant uptake of non-ionic organic chemicals. Environ Sci Technol 40:45–52. doi:10.1021/es0508166

    Article  CAS  Google Scholar 

  • Cornu JY, Denaix L, Schneider A, Pellerin S (2007) Temporal evolution of redox processes and free Cd dynamics in a metal-contaminated soil after rewetting. Chemosphere 70:306–314

    Article  CAS  Google Scholar 

  • Custos J-M (2012) Modélisation de processus rhizosphériques : prélèvement de cadmium en présence de ligand organique et modification du pH par les racines. doctorat, Université de Lorraine

  • Custos J-M, Moyne C, Treillon T, Sterckeman T (2014) Contribution of Cd-EDTA complexes to cadmium uptake by maize: a modelling approach. Plant Soil 374:497–512. doi:10.1007/s11104-013-1906-7

    Article  CAS  Google Scholar 

  • Degryse F, Smolders E, Merckx R (2006) Labile Cd complexes increase Cd availability to plants. Environ Sci Technol 40:830–836

    Article  CAS  Google Scholar 

  • Degryse F, Smolders E, Parker DR (2009) Partitioning of metals (Cd, Co, Cu, Ni, Pb, Zn) in soils: concepts, methodologies, prediction and applications—a review. Eur J Soil Sci 60:590–612

    Article  CAS  Google Scholar 

  • Degryse F, Shahbazi A, Verheyen L, Smolders E (2012) Diffusion limitations in root uptake of cadmium and zinc, but not nickel, and resulting bias in the Michaelis constant. Plant Physiol 160:1097–1109

    Article  CAS  Google Scholar 

  • do Nascimento CWA (2006) Organic acids effects on desorption of heavy metals from a contaminated soil. Sci Agr 63:276–280

    Google Scholar 

  • Ebbs SD, Kochian LV (1998) Phytoextraction of zinc by oat (Avena sativa), barley (Hordeum vulgare), and Indian mustard (Brassica juncea). Environ Sci Technol 32:802–806

    Article  CAS  Google Scholar 

  • Enstone DE, Peterson CA, Ma F (2003) Root endodermis and exodermis: structure, function, and responses to the environment. J Plant Growth Regul 21:335–351

    Article  Google Scholar 

  • Ernstberger H, Davison W, Zhang H, Tye A, Young S (2002) Measurement and dynamic modeling of trace metal mobilization in soils using DGT and DIFS. Environ Sci Technol 36:349–354. doi:10.1021/es010917d

    Article  CAS  Google Scholar 

  • Evangelou MWH, Ebel M, Schaeffer A (2006) Evaluation of the effect of small organic acids on phytoextraction of Cu and Pb from soil with tobacco Nicotiana tabacum. Chemosphere 63:996–1004. doi:10.1016/j.chemosphere.2005.08.042

    Article  CAS  Google Scholar 

  • Hart JJ, Welch RM, Norvell WA, Kochian LV (2002) Transport interactions between cadmium and zinc in roots of bread and durum wheat seedlings. Physiol Plantarum 116:73–78

    Article  CAS  Google Scholar 

  • Hart JJ, Welch RM, Norvell WA, Kochian LV (2006) Characterization of cadmium uptake, translocation and storage in near-isogenic lines of durum wheat that differ in grain cadmium concentration. New Phytol 172:261–271

    Article  CAS  Google Scholar 

  • Huang JW, Cunningham SD (1996) Lead phytoextraction: species variation in lead uptake and translocation. New Phytol 134:75–84

    Article  CAS  Google Scholar 

  • Huang JW, Chen J, Berti WR, Cunningham SD (1997) Phytoremediation of lead-contaminated soils: role of synthetic chelates in lead phytoextraction. Environ Sci Technol 31:800–805

    Article  CAS  Google Scholar 

  • Jiang XJ, Luo YM, Zhao QG, Baker AJM, Christie P, Wong MH (2003) Soil Cd availability to Indian mustard and environmental risk following EDTA addition to Cd-contaminated soil. Chemosphere 50:813–818

    Article  CAS  Google Scholar 

  • Kayser A, Wenger K, Keller A, Attinger W, Felix HR, Gupta SK, Schulin R (2000) Enhancement of phytoextraction of Zn, Cd, and Cu from calcareous soil: the use of NTA and sulfur amendments. Environ Sci Technol 34:1778–1783

    Article  CAS  Google Scholar 

  • Koopmans GF, Römkens PFAM, Fokkema MJ, Song J, Luo YM, Japenga J, Zhao FJ (2008) Feasibility of phytoextraction to remediate cadmium and zinc contaminated soils. Environ Pollut 156:905–914

    Article  CAS  Google Scholar 

  • Kulli B, Balmer M, Krebs R, Lothenbach B, Geiger G, Schulin R (1999) The influence of nitrilotriacetate on heavy metal uptake of lettuce and ryegrass. J Environ Qual 28:1699–1705. doi:10.2134/jeq1999.00472425002800060002x

    Article  CAS  Google Scholar 

  • Lide DR (2004) CRC handbook of chemistry and physics: a ready-reference book of chemical and physical data. CRC Press

  • Lombi E, Zhao FJ, Dunham AR, McGrath SP (2001) Phytoremediation of heavy metal-contaminated soils: natural hyperaccumulation versus chemically enhanced phytorextraction. J Environ Qual 30:1919–1926

    Article  CAS  Google Scholar 

  • Lux A, Vaculik M, Martinka M, Liskova D, Kulkarni MG, Stirk WA, Van Staden J (2011) Cadmium induces hypodermal periderm formation in the roots of the monocotyledonous medicinal plant Merwilla plumbea. Ann Bot 107:285–292. doi:10.1093/aob/mcq240

    Article  CAS  Google Scholar 

  • McGrath SP, Lombi E, Gray CW, Caille N, Dunham SJ, Zhao FJ (2006) Field evaluation of Cd and Zn phytoextraction potential by the hyperaccumulators Thlaspi caerulescens and Arabidopsis halleri. Environ Pollut 141:115–125

    Article  CAS  Google Scholar 

  • Meers E, Hopgood M, Lesage E, Vervaeke P, Tack FMG, Verloo MG (2004) Enhanced phytoextraction: in search of EDTA alternatives. Int J Phytoremediat 6:95–109

    Article  CAS  Google Scholar 

  • Metselaar K, Jong D, van Lier Q (2011) Scales in single root water uptake models: a review, analysis and synthesis. Eur J Soil Sci 62:657–665

    Article  Google Scholar 

  • Morel FMM, Hering JG (1993) Principles and applications of aquatic chemistry. Wiley, New York

  • Niu L, Shen Z, Luo C, Y-e D, Wang C (2012) Accumulation mechanisms and subcellular distribution of Cu in maize grown on soil treated with [S, S]-ethylenediamine disuccinic acid. Plant Soil 351:237–247

    Article  CAS  Google Scholar 

  • Nowack B, Schulin R, Robinson BH (2006) Critical assessment of chelant-enhanced metal phytoextraction. Environ Sci Technol 40:5225–5232

    Article  CAS  Google Scholar 

  • Panfili F, Schneider A, Vives A, Perrot F, Hubert P, Pellerin S (2009) Cadmium uptake by durum wheat in presence of citrate. Plant Soil 316:299–309

    Article  CAS  Google Scholar 

  • PDE Solutions Inc. (2012) A flexible solution system for partial differential equations. Available at http://www.pdesolutions.com

  • Ponizovsky AA, Metzler DM, Allen HE, Ackerman AJ (2006) The effect of moisture content on the release of organic matter and copper to soil solutions. Geoderma 135:204–215. doi:10.1016/j.geoderma.2005.12.004

    Article  CAS  Google Scholar 

  • Qin F, Shan XQ, Wei B (2004) Effects of low-molecular-weight organic acids and residence time on desorption of Cu, Cd, and Pb from soils. Chemosphere 57:253–263. doi:10.1016/j.chemosphere.2004.06.010

    Article  CAS  Google Scholar 

  • Quartacci MF, Irtelli B, Baker AJM, Navari-Izzo F (2007) The use of NTA and EDDS for enhanced phytoextraction of metals from a multiply contaminated soil by Brassica carinata. Chemosphere 68:1920–1928. doi:10.1016/j.chemosphere.2007.02.058

    Article  CAS  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Roose T, Fowler AC, Darrah PR (2001) A mathematical model of plant nutrient uptake. J Math Biol 42:347–360. doi:10.1007/s002850000075

    Article  CAS  Google Scholar 

  • Saltelli A, Tarantola S, Campolongo F, Ratto M (2004) Sensitivity analysis in practice: a guide to assessing scientific models. Wiley, Chichester

  • Sarkar D (2008) Lattice: multivariate data visualization with R. Springer, New York

    Book  Google Scholar 

  • Sarkar D, Andrews F (2013) latticeExtra: extra graphical utilities based on lattice. Available at http://CRAN.R-project.org/package=latticeExtra

  • Sarret G, Vangronsveld J, Manceau A, Musso M, D’Haen J, Menthonnex J-J, Hazemann J-L (2001) Accumulation forms of Zn and Pb in Phaseolus vulgaris in the presence and absence of EDTA. Environ Sci Tech 35:2854–2859

    Article  CAS  Google Scholar 

  • Schaider L, Parker D, Sedlak D (2006) Uptake of EDTA-complexed Pb, Cd and Fe by solution- and sand-cultured Brassica juncea. Plant Soil 286:377–391

    Article  CAS  Google Scholar 

  • Schneider A, Nguyen C (2011) Use of an exchange method to estimate the association and dissociation rate constants of cadmium complexes formed with low-molecular-weight organic acids commonly exuded by plant roots. J Environ Qual 40:1857–1862. doi:10.2134/jeq2010.0529

    Article  CAS  Google Scholar 

  • Schneider A, Nguyen C, Denaix L (2009) Estimation of the association and dissociation rate constants of Cd complexes with various aminopolycarboxylic acids by an exchange method. Environ Chem 6:334–340

    Article  CAS  Google Scholar 

  • Schwartz C, Echevarria G, Morel JL (2003) Phytoextraction of cadmium with Thlaspi caerulescens. Plant Soil 249:27–35

    Article  CAS  Google Scholar 

  • Schwertmann U (1991) Solubility and dissolution of iron-oxides. Plant Soil 130:1–25. doi:10.1007/bf00011851

    Article  CAS  Google Scholar 

  • Shen Z-G, Li X-D, Wang C-C, Chen H-M, Chua H (2002) Lead phytoextraction from contaminated soil with high-biomass plant species. J Environ Qual 31:1893–1900. doi:10.2134/jeq2002.1893

    Article  CAS  Google Scholar 

  • Smith RM, Martell AE (2004) NIST Standard Reference Database 46. NIST critically selected stability constants of metal complexes database (version 8.0 for windows). National Institute of Standards & Technology, Standard Reference Data Program. Gaithersburg, MD 20899

  • Souza LA, Piotto FA, Nogueirol RC, Azevedo RA (2013) Use of non-hyperaccumulator plant species for the phytoextraction of heavy metals using chelating agents. Sci Agr 70:290–295

    Article  CAS  Google Scholar 

  • Sterckeman T, Perriguey J, Caël M, Schwartz C, Morel JL (2004) Applying a mechanistic model to cadmium uptake by Zea mays and Thlaspi caerulescens: consequences for the assessment of the soil quantity and capacity factors. Plant Soil 262:289–302

    Article  CAS  Google Scholar 

  • Tinker PB, Nye PH (2000) Solute movement in the rhizosphere. Oxford University Press, New York, Oxford

  • Tsang DCW, Zhang W, Lo IMC (2007) Modeling cadmium transport in soils using sequential extraction, batch, and miscible displacement experiments. Soil Sci Soc Am J 71:674–681

    Article  CAS  Google Scholar 

  • Vassil AD, Kapulnik Y, Raskin I, Salt DE (1998) The role of EDTA in lead transport and accumulation by Indian mustard. Plant Physiol 117:447–453

    Article  CAS  Google Scholar 

  • Verbruggen N, Juraniec M, Baliardini C, Meyer CL (2013) Tolerance to cadmium in plants: the special case of hyperaccumulators. Biometals 26:633–638. doi:10.1007/s10534-013-9659-6

    Article  CAS  Google Scholar 

  • Wallace A, Mueller RT, Alexander GV (1974) Effect of high levels of nitrilotriacetate on metal uptake by plants grown in soil. Agron J 66:707–708. doi:10.2134/agronj1974.00021962006600050030x

    Article  CAS  Google Scholar 

  • Welch RM, Norvell WA (1999) Mechanisms of cadmium uptake, translocation and deposition in plants. In: McLaughlin MJ, Singh BR (eds) Cadmium in soils and plants. Kluwer Academic Publishers, Dordrecht, pp 125–150

    Chapter  Google Scholar 

  • Williams M, Yanai RD (1996) Multi-dimensional sensitivity analysis and ecological implications of a nutrient uptake model. Plant Soil 180:311–324

    Article  CAS  Google Scholar 

  • Wu LH, Luo YM, Christie P, Wong MH (2003) Efects of EDTA and low molecular weight organic acids on soil solution properties of a heavy metal polluted soil. Chemosphere 50:819–822

    Article  CAS  Google Scholar 

  • Wuertz D (2013) fOptions: Basics of Option Valuation, R package version 2160.82. Available at http://CRAN.R-project.org/package=foptions

  • Yin YJ, Impellitteri CA, You SJ, Allen HE (2002) The importance of organic matter distribution and extract soil: solution ratio on the desorption of heavy metals from soils. Sci Total Environ 287:107–119. doi:10.1016/s0048-9697(01)01000-2

    Article  CAS  Google Scholar 

  • You SJ, Yin YJ, Allen HE (1999) Partitioning of organic matter in soils: effects of pH and water/soil ratio. Sci Total Environ 227:155–160. doi:10.1016/s0048-9697(99)00024-8

    Article  CAS  Google Scholar 

  • Zhao FJ, Lombi E, McGrath SP (2003) Assessing the potential for zinc and cadmium phytoremediation with the hyperaccumulator Thlaspi caerulescens. Plant Soil 249:37–43

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by the ANR 2011 CESA 008 01 funding (including Z. Lin grant). We are grateful to Mark Irvine (INRA Bordeaux, UMR ISPA) and Claude Bruchou (INRA PACA, Unité BioSP) for their great assistance with high-performance computer management.

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Correspondence to Thibault Sterckeman.

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Lin, Z., Schneider, A., Nguyen, C. et al. Can ligand addition to soil enhance Cd phytoextraction? A mechanistic model study. Environ Sci Pollut Res 21, 12811–12826 (2014). https://doi.org/10.1007/s11356-014-3218-8

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