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Predicting zinc bioavailability to wheat improves by integrating pH dependent nonlinear root surface adsorption

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An Erratum to this article was published on 05 November 2014

Abstract

Aim

Our aim was to improve the prediction of Zn bioavailability to wheat grown on low-Zn soils. The classical approach that directly relates Zn in a certain soil extract to Zn uptake has been shown to be inadequate in many cases. We tested a stepwise approach where the steps of the uptake process are characterized with, respectively, Zn solid-solution distribution, adsorption of Zn to root surface, Zn uptake into root and Zn translocation to shoot.

Methods

Two pot experiments were done with wheat grown on nine low-Zn soils varying widely in pH, clay and organic matter content. Soluble Zn concentrations in two soil extracts (DTPA and CaCl2) were measured. Free Zn ion concentrations in CaCl2 soil extracts were determined with the Donnan Membrane Technique. These Zn concentrations were then related to plant Zn uptake following both the direct and the stepwise approach.

Results

In the direct approach, Zn in the DTPA extract was a better predictor for shoot Zn uptake than Zn in the CaCl2 extract. In the stepwise approach, the relationship between Zn in CaCl2 extracts and the root surface adsorbed Zn was pH-dependent and nonlinear. Root surface adsorbed Zn was linearly related to root Zn uptake, and the latter was linearly related to the shoot Zn uptake. The stepwise approach improved the Zn uptake prediction compared to the direct approach and was also validated for different wheat cultivars.

Conclusions

The adsorption of Zn on the root surface is pH dependent and nonlinear with respect to the soil Zn concentration, and a useful proxy for bioavailable Zn over a wide range of soils.

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Abbreviations

ICP-MS:

Inductively coupled plasma mass spectroscopy

ICP-AES:

Inductively coupled plasma atomic emission spectroscopy

DTPA:

Diethylenetriamine penta-acetic acid

DMT:

Donnan membrane technique

UPW:

Ultrapure water

References

  • Arnold T, Kirk GJD, Wissuwa M, Frei M, Zhao FJ, Mason TFD, Weiss DJ (2010) Evidence for the mechanisms of zinc uptake by rice using isotope fractionation. Plant Cell Environ 33:370–381

    Article  PubMed  CAS  Google Scholar 

  • Broadley M, Brown P, Cakmak I, Rengel Z, Zhao F, Petra M (2012) Function of nutrients: Micronutrients. In: Marschner P (ed) Marschner’s mineral nutrition of higher plants, 3rd edn. Academic Press, San Diego 191–248

  • Brown PL, Markich SJ (2000) Evaluation of the free ion activity model of metal-organism interaction: extension of the conceptual model. Aquat Toxicol 51:177–194

    Article  PubMed  CAS  Google Scholar 

  • Catlett KM, Heil DM, Lindsay WL, Ebinger MH (2002) Soil chemical properties controlling zinc2+ activity in 18 Colorado soils. Soil Sci Soc Am J 66:1182–1189

    Article  CAS  Google Scholar 

  • Chairidchai P, Ritchie GSP (1990) Zinc adsorption by a lateritic soil in the presence of organic ligands. Soil Sci Soc Am J 54:1242–1248

    Article  CAS  Google Scholar 

  • Chaney RL (1988) Plants can utilize iron form Fe-N, N′-di-(2-hydroxybenzoyl)-ethylenediamine-N, N′-diacetic acid, a ferric chelate with 106 greater formation constant than Fe-EDDHA. J Plant Nutr 11:1033–1050

    Article  CAS  Google Scholar 

  • Chito D, Weng L, Galceran J, Companys E, Puy J, Van Riemsdijk WH, Van Leeuwen HP (2012) Determination of free Zn2+ concentration in synthetic and natural samples with AGNES (Absence of Gradients and Nernstian Equilibrium Stripping) and DMT (Donnan Membrane Technique). Sci Total Environ 421–422:238–244

    Article  PubMed  Google Scholar 

  • Degryse F, Smolders E, Zhang H, Davison W (2009) Predicting availability of mineral elements to plants with the DGT technique: a review of experimental data and interpretation by modelling. Environ Chem 6:198–218

    Article  CAS  Google Scholar 

  • Duffner A, Hoffland E, Temminghoff EM (2012) Bioavailability of zinc and phosphorus in calcareous soils as affected by citrate exudation. Plant Soil 361:165–175

    Article  CAS  Google Scholar 

  • Feng MH, Shan XQ, Zhang SZ, Wen B (2005) Comparison of a rhizosphere-based method with other one-step extraction methods for assessing the bioavailability of soil metals to wheat. Chemosphere 59:939–949

    Article  PubMed  CAS  Google Scholar 

  • Fried M, Shapiro RE (1961) Soil-plant relationships in ion uptake. Ann Rev Plant Physio 12:91–112

    Article  CAS  Google Scholar 

  • Gramlich A (2013) The influence of organic ligands on zinc availability to wheat. ETH Zürich, Zürich

    Google Scholar 

  • Gramlich A, Tandy S, Slaveykova VI, Duffner A, Schulin R (2012) The use of permeation liquid membranes for free zinc measurements in aqueous solution. Environ Chem 9:429–437

    Article  CAS  Google Scholar 

  • Houba VJG, Novozamsky I, Lexmond TM, Van der Lee JJ (1990) Applicability of 0.01 M CaCl2 as a single extraction solution for the assessment of the nutrient status of soils and other diagnostic purposes. Commun Soil Sci Plant Anal 21:2281–2290

    Article  CAS  Google Scholar 

  • Kalis EJJ, Temminghoff EJM, Visser A, Van Riemsdijk WH (2007) Metal uptake by Lolium perenne in contaminated soils using a four-step approach. Environ Toxicol Chem 26:335–345

    Article  PubMed  CAS  Google Scholar 

  • Kalis EJJ, Weng L, Dousma F, Temminghoff EJM, Van Riemsdijk WH (2006) Measuring free metal ion concentrations in situ in natural waters using the Donnan Membrane Technique. Environ Sci Technol 40:955–961

    Article  PubMed  CAS  Google Scholar 

  • Keizer MG, Van Riemsdijk WH (1995) ECOSAT, a computer program for the calculation of chemical speciation and transport in soil–water systems. Wageningen University, Wageningen

    Google Scholar 

  • Kinniburgh DG, Van Riemsdijk WH, Koopal LK, Borkovec M, Benedetti MF, Avena MJ (1999) Ion binding to natural organic matter: competition, heterogeneity, stoichiometry and thermodynamic consistency. Colloids Surf, A Physicochem Eng Asp 151:147–166

    Article  CAS  Google Scholar 

  • Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Sci Soc Am J 42:421–428

    Article  CAS  Google Scholar 

  • McLaughlin MJ, Zarcinas BA, Stevens DP, Cook N (2000) Soil testing for heavy metals. Commun Soil Sci Plant Anal 31:1661–1700

    Article  CAS  Google Scholar 

  • Meers E, Samson R, Tack FMG, Ruttens A, Vandegehuchte M, Vangronsveld J, Verloo MG (2007) Phytoavailability assessment of heavy metals in soils by single extractions and accumulation by Phaseolus vulgaris. Environ Exp Bot 60:385–396

    Article  CAS  Google Scholar 

  • Menzies NW, Donn MJ, Kopittke PM (2007) Evaluation of extractants for estimation of the phytoavailable trace metals in soils. Environ Pollut 145:121–130

    Article  PubMed  CAS  Google Scholar 

  • Novozamsky I, Van Eck R, Houba VJG, Van der Lee JJ (1996) Solubilization of plant tissue with nitric acid-hydrofluoric acid-hydrogen peroxide in a closed-system microwave digestor. Commun Soil Sci Plant Anal 27:867–875

    Article  CAS  Google Scholar 

  • O’Connor GA (1988) Use and misuse of the DTPA soil test. J Environ Qual 17:715–718

    Article  Google Scholar 

  • Papanicolaou EP, Nobeli C (1977) A contribution to the study of ZnCl+ adsorption by soils. Z Pflanzenernaehr Bodenk 140:543–548

    Article  CAS  Google Scholar 

  • Parker DR, Pedler JF (1997) Reevaluating the free-ion activity model of trace metal availability to higher plants. Plant Soil 196:223–228

    Article  CAS  Google Scholar 

  • Plette ACC, Benedetti MF, Van Riemsdijk WH (1996) Competitive binding of protons, calcium, cadmium, and zinc to isolated cell walls of a gram-positive soil bacterium. Environ Sci Technol 30:1902–1910

    Article  CAS  Google Scholar 

  • Plette ACC, Nederlof MM, Temminghoff EJM, Van Riemsdijk WH (1999) Bioavailability of heavy metals in terrestrial and aquatic systems: a quantitative approach. Environ Toxicol Chem 18:1882–1890

    Article  CAS  Google Scholar 

  • Pueyo M, López-Sánchez JF, Rauret G (2004) Assessment of CaCl2, NaNO3 and NH4NO3 extraction procedures for the study of Cd, Cu, Pb and Zn extractability in contaminated soils. Anal Chim Acta 504:217–226

    Article  CAS  Google Scholar 

  • Redjala T, Sterckeman T, Morel JL (2009) Cadmium uptake by roots: contribution of apoplast and of high- and low-affinity membrane transport systems. Environ Exp Bot 67:235–242

    Article  CAS  Google Scholar 

  • Redjala T, Sterckeman T, Skiker S, Echevarria G (2010) Contribution of apoplast and symplast to short term nickel uptake by maize and Leptoplax emarginata roots. Environ Exp Bot 68:99–106

    Article  CAS  Google Scholar 

  • Rengel Z, Wheal MS (1997) Herbicide chlorsulfuron decreases growth of fine roots and micronutrient uptake in wheat genotypes. J Exp Bot 48:927–934

    Article  CAS  Google Scholar 

  • Sadiq M (1991) Solubility and speciation of zinc in calcareous soils. Water Air Soil Pollut 57–58:411–421

    Article  Google Scholar 

  • Santa María GE, Cogliatti DH (1988) Bidirectional Zn-fluxes and compartmentation in wheat seedling roots. J Plant Physiol 132:312–315

    Article  Google Scholar 

  • Sillanpää M, Vlek PLG (1985) Micronutrients and the agroecology of tropical and Mediterranean regions. Fert Res 7:151–167

    Article  Google Scholar 

  • Sommer AL, Lipman CB (1926) Evidence on the indispensable nature of zinc and boron for higher green plants. Plant Physiol 1:231–249

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tandy S, Mundus S, Yngvesson J, de Bang TC, Lombi E, Schjoerring JK, Husted S (2011) The use of DGT for prediction of plant available copper, zinc and phosphorus in agricultural soils. Plant Soil 346:1–14

    Article  Google Scholar 

  • Temminghoff EJ, Van der Zee SEATM, Keizer MG (1994) The influence of pH on the desorption and speciation of copper in a sandy soil. Soil Sci 158:398–408

    Article  CAS  Google Scholar 

  • Temminghoff EJM, Plette ACC, Van Eck R, Van Riemsdijk WH (2000) Determination of the chemical speciation of trace metals in aqueous systems by the Wageningen Donnan Membrane Technique. Anal Chim Acta 417:149–157

    Article  CAS  Google Scholar 

  • Van Leeuwen HP, Town RM, Buffle J, Cleven RFMJ, Davison W, Puy J, Van Riemsdijk WH, Sigg L (2005) Dynamic speciation analysis and bioavailability of metals in aquatic systems. Environ Sci Technol 39:8545–8556

    Article  PubMed  Google Scholar 

  • Von Wirén N, Marschner H, Römheld V (1996) Roots of iron-efficient maize also absorb phytosiderophore-chelated zinc. Plant Physiol 111:1119–1125

    Google Scholar 

  • Walinga I, Kithome M, Novozamsky I, Houba VJG, Van der Lee JJ (1992) Spectrophotometric determination of organic carbon in soil. Commun Soil Sci Plant Anal 23:1935–1944

    Article  CAS  Google Scholar 

  • Weng L, Alonso Vega F, Van Riemsdijk WH (2011) Strategies in the application of the Donnan membrane technique. Environ Chem 8:466–474

    Article  CAS  Google Scholar 

  • Weng L, Lexmond TM, Wolthoorn A, Temminghoff EJM, Van Riemsdijk WH (2003) Phytotoxicity and bioavailability of nickel: chemical speciation and bioaccumulation. Environ Toxicol Chem 22:2180–2187

    Article  PubMed  CAS  Google Scholar 

  • Weng L, Temminghoff EJM, Lofts S, Tipping E, Van Riemsdijk WH (2002) Complexation with dissolved organic matter and solubility control of heavy metals in a sandy soil. Environ Sci Technol 36:4804–4810

    Article  PubMed  CAS  Google Scholar 

  • Weng L, Temminghoff EJM, Van Riemsdijk WH (2001) Determination of the free ion concentration of trace metals in soil solution using a soil column Donnan membrane technique. Eur J Soil Sci 52:629–637

    Article  CAS  Google Scholar 

  • White PJ (2012) Ion uptake mechanisms of individual cells and roots: short-distance transport. In: Marschner P (ed) Marschner’s mineral nutrition of higher plants, 3rd edn. Academic Press, San Diego 7–47

  • White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511

    Article  PubMed  CAS  Google Scholar 

  • Wu Y, Hendershot WH (2009) Cation exchange capacity and proton binding properties of pea (pisum sativum l.) roots. Water Air Soil Pollut 200:353–359

    Article  CAS  Google Scholar 

  • Zhang F-S, Römheld V, Marschner H (1991) Diurnal rhythm of release of phytosiderophores and uptake rate of zinc in iron-deficient wheat. Soil Sci Plant Nutri 37:671–678

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors wish to thank Peter Nobels for the ICP-MS analyses, Ismail Cakmak (Sabancı University, Istanbul), Paul Damon and Zed Rengel (University of Western Australia, Perth) and Pascal Weijters (AkzoNobel Micronutrients) for providing the soil samples, Medhin Berhe for assistance with the pot experiment and providing the soils from Ethiopia and Simon Jeffery for language editing. This work was funded (Project number 818.01.015) by the NWO (Netherlands Organization for Scientific Research).

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Correspondence to Andreas Duffner.

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Duffner, A., Hoffland, E., Weng, L. et al. Predicting zinc bioavailability to wheat improves by integrating pH dependent nonlinear root surface adsorption. Plant Soil 373, 919–930 (2013). https://doi.org/10.1007/s11104-013-1845-3

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