Predicting availability of mineral elements to plants with the DGT technique: a review of experimental data and interpretation by modelling

Fien Degryse; Erik Smolders; Hao Zhang; William Davison

doi:10.1071/EN09010

REVIEW

Previous Next Contents Vol 6(3)

Predicting availability of mineral elements to plants with the DGT technique: a review of experimental data and interpretation by modelling

Fien Degryse ^A ^C , Erik Smolders ^A , Hao Zhang ^B and William Davison ^B

+ Author Affiliations

- Author Affiliations

^A Division of Soil and Water Management, K.U.Leuven, Kasteelpark Arenberg 20, 3001 Heverlee, Belgium.

^B Department of Environmental Science, Lancaster University, Lancaster, LA1 4YQ, UK.

^C Corresponding author. Email: fien.degryse@ees.kuleuven.be

Environmental Chemistry 6(3) 198-218 https://doi.org/10.1071/EN09010
Submitted: 23 January 2009 Accepted: 24 April 2009 Published: 18 June 2009

Environmental context. Total concentrations of mineral elements in soil bear little relation to their availability for plants. The DGT (diffusive gradients in thin-films) technique has been found to be a good predictor of trace metal uptake and P deficiency, though not consistently in all studies for all elements. This review examines the fundamental basis for the relation between DGT fluxes and plant uptake and assesses under which conditions this relation may break down.

Abstract. In the DGT technique, elements are accumulated on a binding gel after their diffusive transport through a hydrogel. In this paper, we explore in more detail why – and under which conditions – DGT correlates with plant uptake. The theoretical considerations are illustrated with experimental results for metal uptake and toxicity, and for phosphorus deficiency. Strong correlations between DGT and plant uptake are predicted if the diffusive transport of the element from soil to the plant roots is rate-limiting for its uptake. If uptake is not limited by diffusive transport, DGT-fluxes and plant uptake may still correlate provided that plant uptake is not saturated. However, competitive cations may affect the plant uptake under these conditions, whereas they have no effect on the DGT flux. Moreover, labile complexes are not expected to contribute to the plant uptake if diffusion is not limiting, but they are measured with DGT. Therefore, if plant uptake is not limited by diffusion, interpretation of the observed correlation in terms of the labile species measured by DGT is inappropriate.

Additional keywords: bioavailability, deficiency, DGT, metals, phosphorus, plants, soils.

Acknowledgements

F. Degryse thanks the Fund for Scientific Research (FWO-Vlaanderen) for a postdoctoral fellowship.

References

[1] A. L. Nolan , E. Lombi , M. J. McLaughlin , Metal bioaccumulation and toxicity in soils - Why bother with speciation? Aust. J. Chem. 2003 , 56, 77.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[2] W. L. Lindsay , W. A. Norvell , Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Sci. Soc. Am. J. 1978 , 42, 421.
        | CAS |

[3] A. L. Nolan , H. Zhang , M. J. McLaughlin , Prediction of zinc, cadmium, lead and copper bioavailability to wheat in contaminated soils using chemical speciation, diffusive gradients in thin films, extraction, and isotope dilution techniques. J. Environ. Qual. 2005 , 34, 496.
        | CAS | PubMed |

[4] E. Lombi , R. E. Hamon , S. P. McGrath , M. J. McLaughlin , Lability of Cd, Cu, and Zn in polluted soils treated with lime, beringite, and red mud and identification of a non-labile colloidal fraction of metals using isotopic techniques. Environ. Sci. Technol. 2003 , 37, 979.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[5] E. Meers , R. Samson , F. M. G. Tack , A. Ruttens , M. Vandegehuchte , J. Vangronsveld , M. G. Verloo , Phytoavailability assessment of heavy metals in soils by single extractions and accumulation by Phaseolus vulgaris. Environ. Exp. Bot. 2007 , 60, 385.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[6] N. W. Menzies , M. J. Donn , P. M. Kopittke , Evaluation of extractants for estimation of the phytoavailable trace metals in soils. Environ. Pollut. 2007 , 145, 121.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[7] J. D. Colwell , The estimation of phosphorus fertilizer requirements of wheat in southern New South Wales by soil analysis. Aust. J. Exp. Agric. 1963 , 3, 190.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[8] R. H. Bray , L. H. Kurtz , Determination of total, organic, and available forms of phosphorus in soils. Soil Sci. 1945 , 59, 39.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[9] M. J. McLaughlin , P. A. Lancaster , P. G. Sale , N. C. Uren , K. I. Peverill , Comparison of cation/anion exchange resin methods for multi-element testing of acidic soils. Plant Soil 1994 , 32, 229.
        | CAS |

[10] S. Saggar , M. J. Hedley , R. E. White , A simplified resin membrane technique for extracting phosphorus from soils. Fert. Res. 1990 , 24, 173.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[11] Barber S. A. , Cushman J. H. , Nitrogen uptake model for agronomic crops, in Modeling waste water renovation-land treatment (Ed. I. K. Iskandar) 1981, pp. 382–409 (Wiley-Interscience: New York).

[12] T. Adhikari , R. K. Rattan , Modelling zinc uptake by rice crop using a Barber-Cushman approach. Plant Soil 2000 , 227, 235.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[13] U. S. Sadana , N. Claassen , Manganese dynamics in the rhizosphere and Mn uptake by different crops evaluated by a mechanistic model. Plant Soil 2000 , 218, 233.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[14] T. Sterckeman , J. Perriguey , M. Cael , C. Schwartz , J. L. Morel , 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 2004 , 262, 289.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[15] H. Zhang , F.-J. Zhao , B. Sun , W. Davison , S. P. McGrath , A new method to measure effective soil solution concentration predicts copper availability to plants. Environ. Sci. Technol. 2001 , 35, 2602.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[16] J. Song , F. J. Zhao , Y. M. Luo , S. P. McGrath , H. Zhang , Copper uptake by Elsholtzia splendens and Silene vulgaris and assessment of copper phytoavailability in contaminated soils. Environ. Pollut. 2004 , 128, 307.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[17] H. Zhang , E. Lombi , E. Smolders , S. McGrath , Kinetics of Zn release in soils and prediction of Zn concentration in plants using diffusive gradients in thin films. Environ. Sci. Technol. 2004 , 38, 3608.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[18] M. Koster , L. Reijnders , N. R. van Oost , W. G. J. M. Peijnenburg , Comparison of the method of diffusive gels in thin films with conventional extraction techniques for evaluating zinc accumulation in plants and isopods. Environ. Pollut. 2005 , 133, 103.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[19] N. Lehto , W. Davison , H. Zhang , W. Tych , Theoretical comparison of how soil processes affect uptake of metals by Diffusive Gradients in Thin-films and plants. J. Environ. Qual. 2006 , 35, 1903.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[20] N. Lehto , W. Davison , H. Zhang , W. Tych , Analysis of micro-nutrient behaviour in the rhizosphere using a DGT parameterised dynamic plant uptake model. Plant Soil 2006 , 282, 227.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[21] S. D. Young , H. Zhang , A. M. Tye , A. Maxted , C. Thums , I. Thornton , Characterizing the availability of metals in contaminated soils. I. The solid phase: sequential extraction and isotopic dilution. Soil Use Manage. 2006 , 21, 450.
        | Crossref | GoogleScholarGoogle Scholar |

[22] R. E. Hamon , D. R. Parker , E. Lombi , Advances in isotopic dilution techniques in trace element research: a review of methodologies, benefits, and limitations. Adv. Agron. 2008 , 99, 289.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[23] G. Kirchhof , Measurement of root length and thickness using a hand-held computer scanner. Field Crops Res. 1992 , 29, 79.
        | Crossref | GoogleScholarGoogle Scholar |

[24] M. M. Lasat , A. J. M. Baker , L. V. Kochkian , Physiological characterization of root Zn²⁺ absorption and translocation to shoots in Zn hyperaccumulator and nonaccumulator species of Thlaspi. Plant Physiol. 1996 , 112, 1715.
        | CAS | PubMed |

[25] E. Lombi , F. J. Zhao , S. P. McGrath , S. D. Young , G. A. Sacchi , Physiological evidence for a high-affinity cadmium transporter highly expressed in a Thlaspi caerulescens ecotype. New Phytol. 2001 , 149, 53.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[26] F. Degryse , E. Smolders , D. R. Parker , Metal complexes increase uptake of Zn and Cu by plants: implications for uptake and deficiency studies in chelator-buffered solutions. Plant Soil 2006 , 289, 171.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[27] Campbell P. G. C. , Interactions between trace metals and aquatic organisms: a critique of the free-ion activity model, in Metal Speciation and Bioavailability in Aquatic Systems (Eds A. Tessier, D. R. Turner) 1995, pp. 45–102 (Wiley: Chichester, UK).

[28] V. I. Slaveykova , K. J. Wilkinson , Predicting the bioavailability of metals and metal complexes: critical review of the biotic ligand model. Environ. Chem. 2005 , 2, 9.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[29] V. Zitko , W. V. Carson , W. G. Carson , Prediction of incipient lethal levels of copper to juvenile Atlantic salmon in the presence of humic acid by cupric electrode. Bull. Environ. Contam. Toxicol. 1973 , 10, 265.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[30] W. G. Sunda , J. A. M. Lewis , Effect of complexation by natural organic ligands on the toxicity of copper to a unicellular alga, Monochrysis lutheri. Limnol. Oceanogr. 1978 , 23, 870.
        | CAS |

[31] C. Fortin , P. G. C. Campbell , Silver uptake by the green alga Chlamydomonas reinhardtii in relation to chemical speciation: influence of chloride. Environ. Toxicol. Chem. 2000 , 19, 2769.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[32] P. C. DeKock , R. L. Mitchell , Uptake of chelated metals by plants. Soil Sci. 1957 , 84, 55.
        | Crossref | GoogleScholarGoogle Scholar |

[33] V. Römheld , H. Marschner , Effect of Fe stress on utilization of Fe chelates by efficient and inefficient plant-species. J. Plant Nutr. 1981 , 3, 551.
        | Crossref | GoogleScholarGoogle Scholar |

[34] R. T. Checkai , L. L. Hendrickson , R. B. Corey , P. A. Helmke , A method for controlling the activities of free metal, hydrogen and phosphate ions in hydroponic solutions using ion exchange and chelating resins. Plant Soil 1987 , 99, 321.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[35] P. F. Bell , R. L. Chaney , J. S. Angle , Free metal activity and total metal concentrations as indices of micronutrient availability to barley [Hordeum vulgare (L.) ‘Klages’]. Plant Soil 1991 , 130, 51.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[36] McLaughlin M. J. , Smolders E. , Merckx R. , Maes A. , Plant uptake of Cd and Zn in chelator-buffered nutrient solution depends on ligand type, in Plant Nutrition – For Sustainable Food Production and Environment (Eds T. Ando, K. Fujita, T. Mae, H. Matsumoto, S. Mori, J. Sekiya) 1997, pp. 113–118 (Kluwer Academic Publishers: the Netherlands).

[37] E. Smolders , M. J. McLaughlin , Chloride increases cadmium uptake in Swiss Chard in a resin-buffered nutrient solution. Soil Sci. Soc. Am. J. 1996 , 60, 1443.
        | CAS |

[38] E. J. Berkelaar , B. A. Hale , Cadmium accumulation by durum wheat roots in ligand-buffered hydroponic culture: uptake of Cd-ligand complexes or enhanced diffusion? Can. J. Bot. 2003 , 81, 755.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[39] D. R. Parker , J. F. Pedler , Z. A. S. Ahnstrom , M. Resketo , Reevaluating the free-ion activity model of trace metal toxicity toward higher plants: experimental evidence with copper and zinc. Environ. Toxicol. Chem. 2001 , 20, 899.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[40] K. A. C. De Schamphelaere , C. R. Janssen , A biotic ligand model predicting acute copper toxicity for daphnia magna: the effects of calcium, magnesium, sodium, potassium, and pH. Environ. Sci. Technol. 2002 , 36, 48.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[41] D. G. Heijerick , K. A. C. De Schamphelaere , C. R. Janssen , Biotic ligand model development predicting Zn toxicity to the alga Pseudokirchneriella subcapitata: possibilities and limitations. Comp. Biochem. Phys. C 2002 , 133, 207.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[42] S. Thakali , H. E. Allen , D. M. Di Toro , A. A. Ponizovsky , C. P. Rooney , F.-J. Zhao , S. P. McGrath , P. Criel , et al. Terrestrial biotic ligand model. 2. Application to Ni and Cu toxicities to plants, invertebrates, and microbes in soil. Environ. Sci. Technol. 2006 , 40, 7094.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[43] S. Thakali , H. E. Allen , D. M. Di Toro , A. A. Ponizovsky , C. P. Rooney , F.-J. Zhao , S. P. McGrath , A Terrestrial Biotic Ligand Model. 1. Development and application to Cu and Ni toxicities to barley root elongation in soils. Environ. Sci. Technol. 2006 , 40, 7085.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[44] K. Lock , H. Van Eeckhout , K. A. C. De Schamphelaere , P. Criel , C. R. Janssen , Development of a biotic ligand model (BLM) predicting nickel toxicity to barley (Hordeum vulgare). Chemosphere 2007 , 66, 1346.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[45] K. Lock , K. A. C. De Schamphelaere , S. Becaus , P. Criel , H. Van Eeckhout , C. R. Janssen , Development and validation of a terrestrial biotic ligand model predicting the effect of cobalt on root growth of barley (Hordeum vulgare). Environ. Pollut. 2007 , 147, 626.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[46] R. L. Hough , A. M. Tye , N. M. J. Crout , S. P. McGrath , H. Zhang , S. D. Young , Evaluating a ‘Free Ion Activity Model’ applied to metal uptake by Lolium perenne L. grown in contaminated soils. Plant Soil 2005 , 270, 1.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[47] S. Jansen , R. Blust , H. P. Van Leeuwen , Metal speciation dynamics and bioavailability: Zn(II) and Cd(II) uptake by mussel (Mytilus edulis) and carp (Cyprinus carpio). Environ. Sci. Technol. 2002 , 36, 2164.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[48] P. H. Nye , P. B. Tinker , The concept of a root demand coefficient. J. Appl. Ecol. 1969 , 6, 293.
        | Crossref | GoogleScholarGoogle Scholar |

[49] J. B. Best , The inference of intracellular enzymatic properties from kinetic data obtained on living cells. 1. Some kinetic considerations regarding an enzyme enclosed by a diffusion barrier. J. Cell. Comp. Physiol. 1955 , 46, 1.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[50] F. Degryse , E. Smolders , R. Merckx , Labile Cd complexes increase Cd availability to plants. Environ. Sci. Technol. 2006 , 40, 830.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[51] J. J. Hart , R. M. Welch , W. A. Norvell , L. V. Kochian , Transport interactions between cadmium and zinc in roots of bread and durum wheat seedlings. Physiol. Plant. 2002 , 116, 73.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[52] C. K. Cohen , T. C. Fox , D. F. Garvin , L. V. Kochian , The role of iron-deficiency stress response in stimulating heavy-metal transport in plants. Plant Physiol. 1998 , 116, 1063.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[53] J. L. Brewster , K. K. S. Bhat , P. H. Nye , Possibility of predicting solute uptake and plant-growth response from independently measured soil and plant characteristics. 5. Growth and phosphorus uptake of rape in soil at a range of phosphorus concentrations and a comparison of results with predictions of a simulation-model. Plant Soil 1976 , 44, 295.
        | CAS | | Crossref |

[54] S. Itoh , S. A. Barber , Phosphorus uptake by six plant species as related to root hairs. Agron. J. 1983 , 75, 457.


[55] J. F. Loneragan , J. F. Ascher , Response of plants to phosphate concentration in solution culture. II. Rate of phosphate absorption and its relation to growth. Soil Sci. 1967 , 103, 311.
        | CAS | | Crossref |

[56] Barber S. A. , Soil Nutrient Availability: a Mechanistic Approach, 2nd edn 1995 (Wiley: New York).

[57] A. L. Nolan , M. J. McLaughlin , S. D. Mason , Chemical speciation of Zn, Cd, Cu and Pb in pore waters of agricultural and contaminated soils using Donnan dialysis. Environ. Sci. Technol. 2003 , 37, 90.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[58] H. P. van Leeuwen , Metal speciation dynamics and bioavailability: inert and labile complexes. Environ. Sci. Technol. 1999 , 33, 3743.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[59] Degryse F. , Smolders E. , Parker D. R. , Partitioning of trace metals (Cd, Co, Cu, Ni, Pb, Zn) in soils: concepts, methodologies, prediction and applications – a review. Eur. J. Soil Sci. 2009, in press.

[60] K. W. Warnken , W. Davison , H. Zhang , J. Galceran , J. Puy , In situ measurements of metal complex exchange kinetics in freshwater. Environ. Sci. Technol. 2007 , 41, 3179.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[61] W. Davison , H. Zhang , In situ speciation measurements of trace components in natural waters using thin-film gels. Nature 1994 , 367, 546.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[62] K. W. Warnken , H. Zhang , W. Davison , Accuracy of the Diffusive Gradients in Thin-films technique: diffusive boundary layer and effective sampling area considerations. Anal. Chem. 2006 , 78, 3780.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[63] M. H. Tusseau-Vuillemin , R. Gilbin , M. Taillefert , A dynamic numerical model to characterize labile metal complexes collected with diffusion gradient in thin films devices. Environ. Sci. Technol. 2003 , 37, 1645.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[64] S. Scally , W. Davison , H. Zhang , In situ measurements of dissociation kinetics and labilities of metal complexes in solution using DGT. Environ. Sci. Technol. 2003 , 37, 1379.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[65] O. A. Garmo , N. J. Lehto , H. Zhang , W. Davison , O. Royset , E. Steinnes , Dynamic aspects of DGT as demonstrated by experiments with lanthanide complexes of a multidendate ligand. Environ. Sci. Technol. 2006 , 40, 4754.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[66] H. Zhang , W. Davison , B. Knight , S. McGrath , In situ measurements of solution concentrations and fluxes of trace metals in soils using DGT. Environ. Sci. Technol. 1998 , 32, 704.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[67] H. Ernstberger , W. Davison , H. Zhang , A. Tye , S. Young , Measurement and dynamic modeling of trace metal mobilization in soils using DGT and DIFS. Environ. Sci. Technol. 2002 , 36, 349.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[68] M. P. Harper , W. Davison , H. Zhang , W. Tych , Kinetics of metal exchange between solids and solutions in sediments and soils interpreted from DGT measured fluxes. Geochim. Cosmochim. Acta 1998 , 62, 2757.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[69] L. Sochaczewski , W. Tych , W. Davison , H. Zhang , DGT induced fluxes in sediments and soils (2D DIFS). Environ. Model. Softw. 2007 , 22, 14.
        | Crossref | GoogleScholarGoogle Scholar |

[70] H. Ernstberger , H. Zhang , A. Tye , S. Young , W. Davison , Desorption kinetics of Cd, Zn, and Ni measured in soils by DGT. Environ. Sci. Technol. 2005 , 39, 1591.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[71] N. J. Lehto , L. Sochaczewski , W. Davison , W. Tych , H. Zhang , Quantitative assessment of soil parameter (Kd and Tc) estimation using DGT measurements and the 2D DIFS model. Chemosphere 2008 , 71, 795.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[72] H. Zhang , W. Davison , R. Gadi , T. Kobayashi , In situ measurement of dissolved phosphorus in natural waters using DGT. Anal. Chim. Acta 1998 , 370, 29.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[73] N. W. Menzies , B. Kusomo , P. W. Moody , Assessment of P availability in heavily fertilized soils using the diffusive gradient in thin films (DGT) technique. Plant Soil 2005 , 269, 1.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[74] T. M. McBeath , M. J. McLaughlin , R. D. Armstrong , M. Bell , M. D. A. Bolland , M. K. Conyers , R. E. Holloway , S. D. Mason , Predicting the response of wheat (Triticum aestivum L.) to liquid and granular phosphorus fertilisers in Australian soils. Aust. J. Soil Res. 2007 , 45, 448.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[75] S. Mason , R. Hamon , H. Zhang , J. Anderson , Investigating chemical constraints to the measurement of phosphorus in soils using diffusive gradients in thin films (DGT) and resin methods. Talanta 2008 , 74, 779.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[76] B. van Raij , J. A. Quaggio , N. M. da Silva , Extraction of phosphorus, potassium, calcium and magnesium from soils by an ion-exchange resin procedure. Commun. Soil Sci. Plant Anal. 1986 , 17, 547.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[77] R. W. McDowell , L. M. Condron , Chemical nature and potential mobility of phosphorus in fertilized grassland soils. Nutr. Cycl. Agroecosyst. 2000 , 57, 225.
        | Crossref | GoogleScholarGoogle Scholar |

[78] P. S. Hooda , H. Zhang , W. Davison , A. C. Edwards , Measuring bioavailable trace metals by diffusive gradients in thin films (DGT): soil moisture effects on its performance in soils. Eur. J. Soil Sci. 1999 , 50, 285.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[79] A. Jungk , Root hairs and the acquisition of plant nutrients from soil. J. Plant Nutr. Soil Sci. 2001 , 164, 121.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[80] M. A. Piñeros , J. E. Shaff , V. Kochian , Development, characterization, and application of a cadmium-selective microelectrode for the measurement of cadmium fluxes in roots of Thlaspi species and wheat. Plant Physiol. 1998 , 116, 1393.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |

[81] H. Marschner , V. Römheld , W. J. Horst , P. Martin , Root-induced changes in the rhizosphere: importance for the mineral nutrition of plants. J. Plant Nutr. Soil Sc. 1986 , 149, 441.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[82] D. L. Jones , Organic acids in the rhizosphere – a critical review. Plant Soil 1998 , 205, 25.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[83] P. M. C. Antunes , B. A. Hale , The effect of metal diffusion and supply limitations on conditional stability constants determined for durum wheat roots. Plant Soil 2006 , 284, 229.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[84] C. Oporto , E. Smolders , F. Degryse , L. Verheyen , C. Vandecasteele , DGT-measured fluxes explain the chloride-enhanced cadmium uptake by plants at low but not at high Cd supply. Plant Soil 2009 , 318, 127.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[85] M. J. McLaughlin , L. T. Palmer , K. G. Tiller , T. A. Beech , M. K. Smart , Increased soil-salinity causes elevated cadmium concentrations in field-grown potato-tubers. J. Environ. Qual. 1994 , 23, 1013.
        | CAS |

[86] L. V. Kochian , W. J. Lucas , Potassium transport in corn roots. 1. Resolution of kinetics into a saturable and linear component. Plant Physiol. 1982 , 70, 1723.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[87] L. H. Wu , Y. M. Luo , X. R. Xing , P. Christie , EDTA-enhanced phytoremediation of heavy metal contaminated soil with Indian Mustard and associated potential leaching risk. Agric. Ecosyst. Environ. 2004 , 102, 307.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[88] F. Degryse , E. Smolders , I. Oliver , H. Zhang , Relating soil solution Zn concentration to DGT measurements in contaminated soils. Environ. Sci. Technol. 2003 , 37, 3958.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[89] E. Smolders , J. Buekers , I. Oliver , M. J. McLaughlin , Soil properties affecting toxicity of zinc to soil microbial properties in laboratory-spiked and field-contaminated soils. Environ. Toxicol. Chem. 2004 , 23, 2633.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[90] F. J. Zhao , C. P. Rooney , H. Zhang , S. P. McGrath , Comparison of soil solution speciation and Diffusive Gradients in Thin-films measurement as an indicator of copper bioavailability to plants. Environ. Toxicol. Chem. 2006 , 25, 733.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[91] O. Sonmez , G. M. Pierzynski , Assessment of zinc phytoavailability by diffusive gradients in thin films (DGT). Environ. Toxicol. Chem. 2005 , 24, 934.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[92] Smolders E. , Buekers J. , Waegeneers N. , Oliver I. , McLaughlin M. J. , Effects of field and laboratory Zn contamination on soil microbial processes and plant growth. Final Report to the International Lead and Zinc Research Organisation (ILZRO) 2003 (K.U.Leuven/CSIRO: Leuven, Belgium).

[93] Marschner H. , Mineral Nutrition of Higher Plants 1986 (Academic Press Limited: San Diego, CA).

[94] P. Pypers , J. Delrue , J. Diels , E. Smolders , R. Merckx , Phosphorus intensity determines short-term P uptake by pigeon pea (Cajanus cajan L.) grown in soils with differing P buffering capacity. Plant Soil 2006 , 284, 217.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[95] D. Föhse , N. Claassen , A. Jungk , Phosphorus efficiency of plants. 1. External and internal P requirement and P uptake efficiency of different plant-species. Plant Soil 1988 , 110, 101.
        | Crossref |

[96] W. Davison , P. S. Hooda , H. Zhang , A. C. Edwards , DGT measured fluxes as surrogates for uptake of metals by plants. Adv. Environ. Res. 2000 , 3, 550.


[97] Y. Q. He , Y. G. Zhu , S. E. Smith , F. A. Smith , Interactions between soil moisture content and phosphorus supply in spring wheat plants grown in pot culture. J. Plant Nutr. 2002 , 25, 913.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[98] Mason S. , McNeill A. , Diffusive Gradients in Thin-films (DGT) as a technique for accurately predicting phosphorus fertiliser requirements, in Proc. 14th Austr. Agron. Conf., Adelaide, September 2008 (The Regional Institute Ltd: Gosford, Australia).

[99] Bennett W. F. , Nutrient deficiencies and toxicities in crop plants 1993 (APS Press: Saint Paul, MN).