Diffusion limitation of zinc fluxes into wheat roots, PLM and DGT devices in the presence of organic ligands
A. Gramlich A D , S. Tandy A , E. Frossard B , J. Eikenberg C and R. Schulin A
+ Author Affiliations
- Author Affiliations
A Institute of Terrestrial Ecosystems, ETH Zurich, Universitätstraße 16, CH-8092 Zürich, Switzerland.
B Institute for Plant, Animal and Agroecosystems Sciences, ETH Zurich, Eschikon 33, CH-8315 Lindau, Switzerland.
C Radioanalytics Group, Paul Scherrer Institute, CH-5232 Villigen PSI, Switzerland.
D Corresponding author. Email: anja.gramlich@env.ethz.ch
Environmental Chemistry 11(1) 41-50 https://doi.org/10.1071/EN13106
Submitted: 7 June 2013 Accepted: 30 October 2013 Published: 13 February 2014
Environmental context. Zinc is an essential micronutrient for plants and many arid areas of the world have zinc-deficient soils. The bioavailability of Zn to plants is influenced by diffusion limitations and complex lability in the soil solution. To identify the relative importance of these two factors, we investigated the influence of diffusion layer thickness on Zn uptake by wheat and by two bio-mimetic devices in the presence of ethylenediaminetetraacetic acid and two natural ligands found in soil.
Abstract. Organic ligands can increase metal mobility in soils. The extent to which this can contribute to plant metal uptake depends among others, on complex lability and diffusion limitations in solute transfer from the soil solution to root uptake sites. We investigated the influence of diffusion layer thickness on zinc uptake by wheat seedlings in the presence of ethylenediaminetetraacetic acid (EDTA), citrate and histidine with similar free Zn by measuring 65Zn uptake from stirred, non-stirred and agar-containing solutions. Analogous experiments were performed using permeation liquid membranes (PLM) and ‘diffusive gradients in thin films’ (DGT) probes as bio-mimetic devices. In treatments with low EDTA concentrations (~2 µM) or ligand-free Zn solution, increasing diffusion layer thickness reduced Zn fluxes into roots to a similar extent as into PLM and DGT probes, indicating reduced uptake attributable to diffusion limitation. In the citrate treatments root Zn influx was similar to EDTA treatments under stirred conditions, but increasing diffusion layer thickness did not affect Zn uptake. This suggests complex dissociation compensated for reduced Zn2+ diffusion and that the entire complexes were not taken up. The Zn root influxes in the histidine treatments were found to be on average by a factor of 2.5 higher than in the citrate treatments and they also showed no decrease in non-stirred and agar treatments. Dissociation kinetics inferred from PLM measurements explained a large part, although not all, of the increased Zn uptake by the plants in the presence of histidine. The difference may be a result of the uptake of neutral or positive Zn–histidine complexes. The results of this study confirm that labile complexes can contribute to Zn uptake by wheat either through diffusion limitation and complex dissociation or through uptake of entire complexes, depending on the nature of the ligands.
Additional keywords: citrate, diffusive gradients in thin films, EDTA, ethylenediaminetetraacetic acid, histidine, permeation liquid membranes, Zn-bioavailability.
References
[1] I. Cakmak, Enrichment of cereal grains with zinc: agronomic or genetic biofortification? Plant Soil 2008, 302, 1.| Enrichment of cereal grains with zinc: agronomic or genetic biofortification?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXltVKn&md5=27be8ffa8cd92ee7f20ab68e76c43a87CAS |
[2] P. Wang, D. M. Zhou, X. S. Luo, L. Z. Li, 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 2009, 316, 177.
| Effects of Zn-complexes on zinc uptake by wheat (Triticum aestivum) roots: a comprehensive consideration of physical, chemical and biological processes on biouptake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFOksb0%3D&md5=3fa4c254762261ff3d70885450238803CAS |
[3] 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.
| Metal complexes increase uptake of Zn and Cu by plants: implications for uptake and deficiency studies in chelator-buffered solutions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1WnsrrJ&md5=2ab1bee8951b5045e7b800cde62b21c2CAS |
[4] F. Panfili, A. Schneider, A. Vives, F. Perrot, P. Hubert, S. Pellerin, Cadmium uptake by durum wheat in presence of citrate. Plant Soil 2009, 316, 299.
| Cadmium uptake by durum wheat in presence of citrate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFOks70%3D&md5=8961b24154691787d851300e1f48d0bbCAS |
[5] S. P. Stacey, M. J. Mclaughlin, I. Cakmak, G. M. Hetitiarachchi, K. G. Scheckel, M. Karkkainen, Root uptake of lipophilic zinc–rhamnolipid complexes. J. Agric. Food Chem. 2008, 56, 2112.
| Root uptake of lipophilic zinc–rhamnolipid complexes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXisFWkt74%3D&md5=b7cf034895786ea6c38976da615f93f4CAS | 18303840PubMed |
[6] P. F. Bell, M. J. Mclaughlin, G. Cozens, D. P. Stevens, G. Owens, H. South, Plant uptake of 14C-EDTA, 14C-Citrate, and 14C-Histidine from chelator-buffered and conventional hydroponic solutions. Plant Soil 2003, 253, 311.
| Plant uptake of 14C-EDTA, 14C-Citrate, and 14C-Histidine from chelator-buffered and conventional hydroponic solutions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlsFKru7c%3D&md5=6d1ed1052c3560c7bbfd9cd522376cdeCAS |
[7] N. von Wiren, H. Marschner, V. Römheld, Roots of iron-efficient maize also absorb phytosiderophore-chelated zinc. Plant Physiol. 1996, 111, 1119.
| 1:CAS:528:DyaK28XltVGgt7k%3D&md5=6b488d3f655812300305965104cfd0b5CAS | 12226351PubMed |
[8] F. Degryse, A. Shahbazi, L. Verheyen, E. Smolders, Diffusion limitations in root uptake of cadmium and zinc, but not nickel, and resulting bias in the Michaelis constant. Plant Physiol. 2012, 160, 1097.
| Diffusion limitations in root uptake of cadmium and zinc, but not nickel, and resulting bias in the Michaelis constant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFaktr7M&md5=ef43a3dc4de3a88407da18013d0bd94dCAS | 22864584PubMed |
[9] J. Luo, H. Zhang, F. J. Zhao, W. Davison, Distinguishing diffusional and plant control of Cd and Ni uptake by hyperaccumulator and nonhyperaccumulator plants. Environ. Sci. Technol. 2010, 44, 6636.
| Distinguishing diffusional and plant control of Cd and Ni uptake by hyperaccumulator and nonhyperaccumulator plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXps1Wht7s%3D&md5=f9a1d47d8eee55c473405168993b070dCAS | 20681510PubMed |
[10] M. J. Haydon, C. S. Cobbett, Transporters of ligands for essential metal ions in plants. New Phytol. 2007, 174, 499.
| Transporters of ligands for essential metal ions in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsFOktL0%3D&md5=107c82aaf766b12b82f77bc74a3296e6CAS | 17447906PubMed |
[11] P. J. White, M. R. Broadley, Biofortification of crops with seven mineral elements often lacking in human diets – iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytol. 2009, 182, 49.
| Biofortification of crops with seven mineral elements often lacking in human diets – iron, zinc, copper, calcium, magnesium, selenium and iodine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXksVKhtbw%3D&md5=3537142b40d8f44313dfa2eb85e747ddCAS | 19192191PubMed |
[12] A. Gramlich, S. Tandy, E. Frossard, J. Eikgenberg, R. Schulin, Availability of zinc and the ligands citrate and histidine to wheat – does uptake of entire complexes play a role? J. Agric. Food Chem. 2013, 61, 10 409.
| Availability of zinc and the ligands citrate and histidine to wheat – does uptake of entire complexes play a role?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFGhu7%2FI&md5=3dc86e0d52189e9dc93caac8e0867f1aCAS |
[13] J. J. Hart, W. A. Norvell, R. M. Welch, L. A. Sullivan, L. V. Kochian, Characterization of zinc uptake, binding, and translocation in intact seedlings of bread and durum wheat cultivars. Plant Physiol. 1998, 118, 219.
| Characterization of zinc uptake, binding, and translocation in intact seedlings of bread and durum wheat cultivars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmtV2mu78%3D&md5=2411dc9f25b8233dc00a8d5df2a429aaCAS | 9733541PubMed |
[14] G. Hacisalihoglu, J. J. Hart, L. V. Kochian, High- and low-affinity zinc transport systems and their possible role in zinc efficiency in bread wheat. Plant Physiol. 2001, 125, 456.
| High- and low-affinity zinc transport systems and their possible role in zinc efficiency in bread wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjslyls7Y%3D&md5=b6a93958483064f4c8202a58e8359f19CAS | 11154353PubMed |
[15] K. Vercauteren, R. Blust, Bioavailability of dissolved zinc to the common mussel Mytilus edulis in complexing environments. Mar. Ecol. Prog. Ser. 1996, 137, 123.
| Bioavailability of dissolved zinc to the common mussel Mytilus edulis in complexing environments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XlsVSnu7c%3D&md5=1008b4a982c98c9dd071d72830e16ed0CAS |
[16] H. P. van Leeuwen, Metal speciation dynamics and bioavailability: Inert and labile complexes. Environ. Sci. Technol. 1999, 33, 3743.
| Metal speciation dynamics and bioavailability: Inert and labile complexes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlvV2jtLc%3D&md5=01ba596cdb30a5d9cfe36b128bff313cCAS |
[17] A. L. Nolan, H. Zhang, M. J. Mclaughlin, Prediction of zinc, cadmium, lead, and copper availability to wheat in contaminated soils using chemical speciation, diffusive gradients in thin films, extraction, and isotopic dilution techniques. J. Environ. Qual. 2005, 34, 496.
| Prediction of zinc, cadmium, lead, and copper availability to wheat in contaminated soils using chemical speciation, diffusive gradients in thin films, extraction, and isotopic dilution techniques.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXislOlt7k%3D&md5=9bc9af38a7305afc565f526799d99660CAS | 15758102PubMed |
[18] F. Degryse, E. Smolders, D. R. Parker, An agar gel technique demonstrates diffusion limitations to cadmium uptake by higher plants. Environ. Chem. 2006, 3, 419.
| An agar gel technique demonstrates diffusion limitations to cadmium uptake by higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlWnur7P&md5=eb10b7e8ea83523a9cf93ec67258e2adCAS |
[19] H. Zhang, W. Davison, Direct in situ measurements of labile inorganic and organically bound metal species in synthetic solutions and natural waters using diffusive gradients in thin films. Anal. Chem. 2000, 72, 4447.
| Direct in situ measurements of labile inorganic and organically bound metal species in synthetic solutions and natural waters using diffusive gradients in thin films.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXls1Oku70%3D&md5=19d8be12ffc8f144ae87bb282d8200d2CAS | 11008782PubMed |
[20] S. Scally, W. Davison, H. Zhang, Diffusion coefficients of metals and metal complexes in hydrogels used in diffusive gradients in thin films. Anal. Chim. Acta 2006, 558, 222.
| Diffusion coefficients of metals and metal complexes in hydrogels used in diffusive gradients in thin films.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotFygtw%3D%3D&md5=d4fec5b95bb959613edea7d541b63742CAS |
[21] F. Degryse, E. Smolders, H. Zhang, W. Davison, Predicting availability of mineral elements to plants with the DGT technique: a review of experimental data and interpretation by modelling. Environ. Chem. 2009, 6, 198.
| Predicting availability of mineral elements to plants with the DGT technique: a review of experimental data and interpretation by modelling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1CjurfI&md5=cafd8c0632f34b93501644322053cd5cCAS |
[22] H. P. van Leeuwen, R. M. Town, J. Buffle, R. F. M. Cleven, W. Davison, J. Puy, W. H. Van Riemsdijk, L. Sigg, Dynamic speciation analysis and bioavailability of metals in aquatic systems. Environ. Sci. Technol. 2005, 39, 8545.
| Dynamic speciation analysis and bioavailability of metals in aquatic systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVOis73M&md5=784d2d8f64142e8b9e859ade0577a2a7CAS | 16323747PubMed |
[23] N. Parthasarathy, M. Pelletier, J. Buffle, Transport of lipophilic ligands through permeation liquid membrane in relation to natural water analysis. J. Membr. Sci. 2008, 309, 182.
| Transport of lipophilic ligands through permeation liquid membrane in relation to natural water analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitVan&md5=bc651bdd77f28995430a6e3632d88e59CAS |
[24] A. Gramlich, S. Tandy, V. I. Slaveykova, A. Duffner, R. Schulin, The use of permeation liquid membranes for free zinc measurements in aqueous solution. Environ. Chem. 2012, 9, 429.
| The use of permeation liquid membranes for free zinc measurements in aqueous solution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslSmtrrJ&md5=58493c35db9c4e0ba6d87bfb331750edCAS |
[25] V. I. Slaveykova, N. Parthasarathy, J. Buffle, K. J. Wilkinson, Permeation liquid membrane as a tool for monitoring bioavailable Pb in natural waters. Sci. Total Environ. 2004, 328, 55.
| Permeation liquid membrane as a tool for monitoring bioavailable Pb in natural waters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltVWjt7g%3D&md5=d0dcf2ae211dfe466fd8df23922c1e53CAS | 15207573PubMed |
[26] S. Bayen, I. Worms, N. Parthasarathy, K. Wilkinson, J. Buffle, Cadmium bioavailability and speciation using the permeation liquid membrane. Anal. Chim. Acta 2006, 575, 267.
| Cadmium bioavailability and speciation using the permeation liquid membrane.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnvVSku7o%3D&md5=c43506c704171eb3f6547351cd12a1dbCAS | 17723601PubMed |
[27] S. Bayen, K. J. Wilkinson, J. Buffle, The permeation liquid membrane as a sensor for free nickel in aqueous samples. Analyst (Lond.) 2007, 132, 262.
| The permeation liquid membrane as a sensor for free nickel in aqueous samples.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXitVOksrk%3D&md5=a01410b6bef1e00da51b9c5a910c93bbCAS |
[28] V. I. Slaveykova, I. B. Karadjova, M. Karadjov, D. L. Tsalev, Trace metal speciation and bioavailability in surface waters of the Black Sea coastal area evaluated by HF-PLM and DGT. Environ. Sci. Technol. 2009, 43, 1798.
| Trace metal speciation and bioavailability in surface waters of the Black Sea coastal area evaluated by HF-PLM and DGT.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvVylurk%3D&md5=7354b21bab99fc5a2bce6e172adc080aCAS | 19368174PubMed |
[29] L. Aristilde, Y. Xu, F. M. M. Morel, Weak organic ligands enhance zinc uptake in marine phytoplankton. Environ. Sci. Technol. 2012, 46, 5438.
| Weak organic ligands enhance zinc uptake in marine phytoplankton.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xltl2ht7c%3D&md5=7368eb9754a3c109609836c5be8ec301CAS | 22494184PubMed |
[30] Y. Xu, D. Shi, L. Aristilde, F. M. M. Morel, The effect of pH on the uptake of zinc and cadmium in marine phytoplankton: possible role of weak complexes. Limnol. Oceanogr. 2012, 57, 293.
| The effect of pH on the uptake of zinc and cadmium in marine phytoplankton: possible role of weak complexes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XivVarsLk%3D&md5=c3a9aef48cac08b4d4e2b2457a8fbbd5CAS |
[31] A. H. Khoshgoftarmanesh, A. Sadrarhami, H. R. Sharifi, D. Afiuni, R. Schulin, Selecting zinc-efficient wheat genotypes with high grain yield using a stress tolerance index. Agron. J. 2009, 101, 1409.
| Selecting zinc-efficient wheat genotypes with high grain yield using a stress tolerance index.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsV2jtLrI&md5=7f20607f76e1f2fa23461b7abe32f0e4CAS |
[32] A. Kandegedara, D. B. Rorabacher, Noncomplexing tertiary amines as “better” buffers covering the range of pH 3–11. Temperature dependence of their acid dissociation constants. Anal. Chem. 1999, 71, 3140.
| Noncomplexing tertiary amines as “better” buffers covering the range of pH 3–11. Temperature dependence of their acid dissociation constants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjvFams7o%3D&md5=7d9b389eade8d690f822a92bfbad391aCAS | 21662904PubMed |
[33] DGT Research Manual DGT for measurement in waters, soils and sediments 2003 (DGT Research Ltd: Quernmore, UK). Available at http://www.dgtresearch.com/WebProducts.aspx?CATID=TEC [Verified 4 December 2013].
[34] A. E. Martell, R. M. Smith, R. J. Motekaitis, NIST critically selected stability constants of metal complexes, NIST Standard Reference Database 46 2001 (US Department of Commerce: Gaithersburg, MD).
[35] M. R. Twiss, O. Errecalde, C. Fortin, P. G. C. Campbell, C. Jumarie, F. Denizeau, E. Berkelaar, B. Hale, K. Van Rees, Coupling the use of computer chemical speciation models and culture techniques in laboratory investigations of trace metal toxicity. Chem. Spec. Bioavail. 2001, 13, 9.
| Coupling the use of computer chemical speciation models and culture techniques in laboratory investigations of trace metal toxicity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXotFGqsb8%3D&md5=55da72c4ea93b5f1bf1dd65be0b0904bCAS |
[36] R Development Core Team, R: a language and environment for statistical computing 2009 (R Institute for Statistical Computing: Vienna, Austria). Available at http://www.R-project.org [Verified 17 December 2012].
[37] M. Häussling, C. A. Jorns, G. Lehmbecker, C. Hechtbuchholz, H. Marschner, Ion and water-uptake in relation to root development in norway spruce (Picea abies (L.) Karst.). J. Plant Physiol. 1988, 133, 486.
| Ion and water-uptake in relation to root development in norway spruce (Picea abies (L.) Karst.).Crossref | GoogleScholarGoogle Scholar |
[38] A. D. Vassil, Y. Kapulnik, I. Raskin, D. E. Salt, The role of EDTA in lead transport and accumulation by Indian mustard. Plant Physiol. 1998, 117, 447.
| The role of EDTA in lead transport and accumulation by Indian mustard.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjvFGks7w%3D&md5=699a3158f631e7d5e7a5803ede597b44CAS | 9625697PubMed |
[39] N. Parthasarathy, M. Pelletier, J. Buffle, Hollow fiber based supported liquid membrane: a novel analytical system for trace metal analysis. Anal. Chim. Acta 1997, 350, 183.
| Hollow fiber based supported liquid membrane: a novel analytical system for trace metal analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlsVWgt70%3D&md5=3ddce79b138fac208b384d5830daab79CAS |
[40] N. Parthasarathy, M. Pelletier, J. Buffle, Permeation liquid membrane for trace metal speciation in natural waters – transport of liposoluble CuII complexes. J. Chromatogr. A 2004, 1025, 33.
| Permeation liquid membrane for trace metal speciation in natural waters – transport of liposoluble CuII complexes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpvVWrtrw%3D&md5=1992381afff275c0acbeeb94c7a45ec8CAS | 14753668PubMed |
[41] J. Buffle, Z. Zhang, K. Startchev, Metal flux and dynamic speciation at (Biol.)interfaces. part 1: critical evaluation and compilation of physicochemical parameters for complexes with simple ligands and fulvic/humic substances. Environ. Sci. Technol. 2007, 41, 7609.
| Metal flux and dynamic speciation at (Biol.)interfaces. part 1: critical evaluation and compilation of physicochemical parameters for complexes with simple ligands and fulvic/humic substances.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1ymtr3E&md5=bb9e478acf30e32ed4514934dc0fe993CAS | 18075065PubMed |
[42] C. Maurel, M. J. Chrispeels, Aquaporins. A molecular entry into plant water relations. Plant Physiol. 2001, 125, 135.
| Aquaporins. A molecular entry into plant water relations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjslymur4%3D&md5=be27252c3467007e51e797185da1e88aCAS | 11154316PubMed |
[43] H. Svennerstam, S. Jamtgard, I. Ahmad, K. Huss-Danell, T. Nasholm, U. Ganeteg, Transporters in Arabidopsis roots mediating uptake of amino acids at naturally occurring concentrations. New Phytol. 2011, 191, 459.
| Transporters in Arabidopsis roots mediating uptake of amino acids at naturally occurring concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFSqtr%2FF&md5=900a2876c8cc9bb436cc160fa0ec8627CAS | 21453345PubMed |
[44] D. L. Jones, Organic acids in the rhizosphere – a critical review. Plant Soil 1998, 205, 25.
| Organic acids in the rhizosphere – a critical review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhtlGjs78%3D&md5=c4c36a5b71f655c2908e55f121734685CAS |
[45] D. L. Jones, D. Shannon, T. Junvee-Fortune, J. F. Farrarc, Plant capture of free amino acids is maximized under high soil amino acid concentrations. Soil Biol. Biochem. 2005, 37, 179.
| Plant capture of free amino acids is maximized under high soil amino acid concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovVKntLc%3D&md5=8591b8d95d05f4411d442f8a46318441CAS |
[46] E. Kalis, E. Temminghoff, L. Weng, W. Van Riemsdijk, Effects of humic acid and competing cations on metal uptake by Lolium perenne. Environ. Toxicol. Chem. 2006, 25, 702.
| Effects of humic acid and competing cations on metal uptake by Lolium perenne.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XitVaju7s%3D&md5=45cf472b4c3218394952ef3e10203956CAS | 16566154PubMed |
