Skip to main content
Log in

On the contribution of cadmium – citrate complexes to cadmium uptake by durum wheat

  • Research Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Purpose

To determine if the increase in Cd uptake by durum wheat in the presence of Cd-citrate is due to dissociation or to the transpiration-driven apoplastic uptake of the complex.

Methods

A mechanistic model of Cd uptake in hydroponics was developed, formalising the transport of Cd, citrate and their complex, including the dissociation of the latter and its uptake through apoplastic pathway. Model outputs were compared to Cd and citrate uptake by durum wheat exposed to 35 and 117 nM Cd2+ in aqueous solution, in absence and presence of citrate.

Results

A quasi-doubling (+ 94%) of the Cd uptake was measured when the exposure solution was theoretically 80 nM Cd-citrate in addition to the 35 nM Cd2+, when compared to the exposure to 35 nM Cd2+ alone. The model precisely predicted the Cd uptake with Cd2+ at the two exposure levels (35 and 117 nM Cd2+) without ligand. In the presence of citrate, the modelling showed that Cd-citrate dissociation could increase the Cd uptake by 18.1%. Including the uptake of Cd-citrate through apoplastic uptake increased the simulated uptake by only 19.6%. The [Cd2+] measured here was twice that calculated using VisualMINTEQ (35 nM). Using the measured values of Cd speciation enabled an accurate prediction of the metal uptake.

Conclusions

In the presence of citrate, durum wheat principally absorbs free hydrated Cd ions. The dissociation of the Cd-citrate complexes makes a minor contribution to the Cd2+ uptake flux, while their apoplastic uptake can be regarded as practically negligible.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Data availability

Experimental data are given in the article.

Code availability

MATLAB® scripts are available on demand.

References

  • Barber SA (1995) Soil nutrient bioavailability. A mechanistic approach. John Wiley & Sons, New York

    Google Scholar 

  • Berkelaar EJ, Hale BA (2003a) Accumulation of cadmium by durum wheat roots: Bases for citrate-mediated exceptions to the free ion model. Environ Toxicol Chem 22:1155–1161

    Article  CAS  PubMed  Google Scholar 

  • Berkelaar EJ, Hale BA (2003b) Cadmium accumulation by durum wheat roots in ligand-buffered hydroponic culture: uptake of Cd–ligand complexes or enhanced diffusion? Can J Botany 81:755–763. https://doi.org/10.1139/b03-061

    Article  CAS  Google Scholar 

  • Blaylock MJ, Salt DE, Dushenkov S, Zakharova O, Gussman C, Kapulnik Y, Ensley BD, Raskin I (1997) Enhanced accumulation of Pb in Indian mustard by soil-applied chelating agents. Environ Sci Technol 31:860–865

    Article  Google Scholar 

  • Campi E, Ostacoli G, Meirone M, Saini G (1964) Stability of the complexes of tricarballylic and citric acids with bivalent metal ions in aqueous solution. J Inorg Nucl Chem 26:553–564. https://doi.org/10.1016/0022-1902(64)80288-8

    Article  CAS  Google Scholar 

  • Capone S, De Robertis A, De Stefano C, Sammartano S (1986) Formation and stability of zinc(II) and cadmium(II) citrate complexes in aqueous solution at various temperatures. Talanta 33:763–767. https://doi.org/10.1016/0039-9140(86)80184-9

    Article  CAS  PubMed  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 

  • Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475–486

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  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  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Custos J-M, Moyne C, Sterckeman T (2020) How root nutrient uptake affects rhizosphere pH: A modelling study. Geoderma 369:114314. https://doi.org/10.1016/j.geoderma.2020.114314

    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  PubMed  Google Scholar 

  • Errécalde O, Campbell PGC (2000) Cadmium and zinc bioavailability to Selenastrum capricornutum (Chlorophyceae): accidental metal uptake and toxicity in the presence of citrate. J Phycol 36:473–483. https://doi.org/10.1046/j.1529-8817.2000.99103.x

    Article  PubMed  Google Scholar 

  • Fotovat A, Naidu R (1997) Ion exchange resin and MINTEQA2 speciation of Zn and Cu in alkaline sodic and acidic soil extracts. Soil Res 35:711–726. https://doi.org/10.1071/S96079

    Article  CAS  Google Scholar 

  • Gustafsson JP (2011) Visual MINTEQ 3.0 user guide. KTH, Department of Land and Water Recources, Stockholm, Sweden

  • Han F, Shan X, Zhang S, Wen B, Owens G (2006) Enhanced cadmium accumulation in maize roots - the impact of organic acids. Plant Soil 289:355–368

    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 

  • Holm PE, Christensen TH, Tjell JC, McGrath SP (1995) Speciation of cadmium and zinc with application to soil solutions. J Environ Qual 24:183–190. https://doi.org/10.2134/jeq1995.00472425002400010025x

    Article  CAS  Google Scholar 

  • Jackson AP, Timmerman MP, Bagshaw CR, Ashley CC (1987) The kinetics of calcium binding to fura-2 and indo-1. FEBS Lett 216:35–39. https://doi.org/10.1016/0014-5793(87)80752-4

    Article  CAS  PubMed  Google Scholar 

  • Lattanzio FA, Bartschat DK (1991) The effect of pH on rate constants, ion selectivity and thermodynamic properties of fluorescent calcium and magnesium indicators. Biochem Bioph Res Co 177:184–191. https://doi.org/10.1016/0006-291X(91)91966-G

    Article  CAS  Google Scholar 

  • Lebourg A, Sterckeman T, Ciesielski H, Proix N (1998) Trace metal speciation in three unbuffered salt solutions used to assess their bioavailability in soil. J Environ Qual 27:584–590

    Article  CAS  Google Scholar 

  • Li NC, Lindenbaum A, White JM (1959) Some metal complexes of citric and tricarballylic acids. J Inorg Nucl Chem 12:122–128. https://doi.org/10.1016/0022-1902(59)80101-9

    Article  CAS  Google Scholar 

  • Lide DR (ed) (2010) CRC Handbook of Chemistry and Physics, 90th Edition (Internet Version 2010). CRC Press/Taylor and Francis, Boca Raton, FL., p 2758

    Google Scholar 

  • Lin Z, Schneider A, Nguyen C, Sterckeman T (2015) Can ligand addition to soil enhance Cd phytoextraction? A mechanistic model study (vol 21, pg 12811, 2014). Environ Sci Pollut R 22:5587–5588. https://doi.org/10.1007/s11356-015-4128-0

    Article  Google Scholar 

  • Lovy L, Latt D, Sterckeman T (2013) Cadmium uptake and partitioning in the hyperaccumulator Noccaea caerulescens exposed to constant Cd concentrations throughout complete growth cycles. Plant Soil 362:345–354

    Article  CAS  Google Scholar 

  • Lux A, Martinka M, Vaculik M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37. https://doi.org/10.1093/jxb/erq281

    Article  CAS  PubMed  Google Scholar 

  • Meites L (1951) Polarographic studies of metal complexes. V. The cadmium (II), zinc (II) and iron (III) citrates. J Am Chem Soc 73:3727–3731

    Article  CAS  Google Scholar 

  • Naraghi M (1997) T-jump study of calcium binding kinetics of calcium chelators. Cell Calcium 22:255–268. https://doi.org/10.1016/S0143-4160(97)90064-6

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  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 

  • Redjala T, Zelko I, Sterckeman T, Legué V, Lux A (2011) Relationship between root structure and root cadmium uptake in maize. Environ Exp Bot 71:241–248

    Article  CAS  Google Scholar 

  • 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 Technol 35:2854–2859

    Article  CAS  PubMed  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. https://doi.org/10.2134/jeq2010.0529

    Article  CAS  PubMed  Google Scholar 

  • Scoppa P (1975) Cadmium-isocitrate complex: Its stability as a function of ionic strength. Zeitschrift Für Naturforschung C 30:555–561. https://doi.org/10.1515/znc-1975-9-1001

    Article  CAS  Google Scholar 

  • Smith RM, Martell AE, Motekaitis RJ (2004) NIST critically selected stability constants of metal complexes database. NIST Standard Reference Database 46. 8.0 for Windows edn. National Institute of Standards and Technology, Gaithersburg, MD, USA

  • Sterckeman T, Moyne C (2021) Could root excreted iron ligands contribute to cadmium and zinc uptake by the hyperaccumulator Noccaea caerulescens? Plant Soil 467:129–153

    Article  CAS  Google Scholar 

  • Sterckeman T, Thomine S (2020) Mechanisms of cadmium accumulation in plants. Crit Rev Plant Sci 39:322–359

    Article  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, Oxford

    Book  Google Scholar 

  • Treumann WB, Ferris LM (1958) The determination of a thermodynamic stability constant for the cadmium citrate (CdCit-) complex ion at 25° by an EMF method. J Am Chem Soc 80:5050–5052

    Article  CAS  Google Scholar 

  • Tsai HH, Schmidt W (2017) Mobilization of iron by plant-borne coumarins. Trends Plant Sci 22:538–548. https://doi.org/10.1016/j.tplants.2017.03.008

    Article  CAS  PubMed  Google Scholar 

  • Wang P, Zhou D, Luo X, Li L (2009) Effects of Zn-complexes on zinc uptake by wheat (Triticum aestivum) roots: a comprehensive consideration of physical, chemical and biological processes on biouptake. Plant Soil 316:177–192

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The author thanks Dr Christian Moyne for his help in coding with MATLAB, and Dr Pierre Leglize both for his careful reading of the manuscript and for his advice.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Thibault Sterckeman.

Ethics declarations

Conflict of interest

The author declares that he has no conflict of interest.

Additional information

Responsible Editor: Miroslav Nikolic.

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sterckeman, T. On the contribution of cadmium – citrate complexes to cadmium uptake by durum wheat. Plant Soil 487, 455–465 (2023). https://doi.org/10.1007/s11104-023-05943-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-023-05943-6

Keywords

Navigation