Abstract
Purpose
Rhizosphere processes are known to modify uptake of elements from soil, but limited information is available for hyperaccumulators. We investigated labile Ni fractions and their kinetics of replenishment in the rhizospheres of the Ni-hyperaccumulator Odontarrhena serpyliffolia, the Ni-excluder Holcus lanatus and in bulk soils collected at the same serpentine outcrop.
Methods
Labile Ni fractions in rhizosphere and bulk soil were evaluated using conventional extractions and also by the Diffusive Gradients in Thin Films (DGT) technique. DGT data were used to predict the kinetics of Ni resupply using DIFS modelling. Chemical imaging of Ni distribution along roots using DGT coupled with laser-ablation was conducted.
Results
Labile Ni forms were higher in both rhizosphere than in bulk soils, together with an increase in dissolved organic C, cation exchange capacity and the Ca/Mg ratio. Ni fractionation indicated a shift towards less stable Ni fractions in the rhizosphere, particularly in the hyperaccumulator.
DIFS modelling showed that the rhizosphere of the excluder was able to sustain the initially lower soluble Ni concentration through replenishment from the solid phase, while Ni resupply in the rhizosphere of the hyperaccumulator was not sufficient to maintain the initially high concentrations of soluble Ni. However, the amount of DGT-labile Ni was higher in the rhizosphere of the hyperaccumulator compared to the excluder in all deployment times.
Conclusion
Our data suggest that compounds derived from root activity, in particular DOC, are important controls of Ni availability to plants growing on serpentine soil.
Similar content being viewed by others
References
Abou-Shanab R, Angle J, Chaney R (2006) Bacterial inoculants affecting nickel uptake by Alyssum murale from low, moderate and high Ni soils. Soil Biol Biochem 38:2882–2889
Adriano DC (2001) Trace elements in terrestrial environments: biogeochemistry, bioavailability, and risks of metals. Springer New York
Álvarez-López V, Prieto-Fernández Á, Becerra-Castro C, Monterroso C, Kidd PS (2015) Rhizobacterial communities associated with the flora of three serpentine outcrops of the Iberian Peninsula. Plant Soil: 1–20
Antić-Mladenović S, Rinklebe J, Frohne T, Stärk H-J, Wennrich R, Tomić Z, Ličina V (2011) Impact of controlled redox conditions on nickel in a serpentine soil. J Soils Sediments 11:406–415
Awad F, Römheld V (2000) Mobilization of heavy metals from contaminated calcareous soils by plant born, microbial and synthetic chelators and their uptake by wheat plants. J Plant Nutr 23:1847–1855
Bani A, Echevarria G, Sulçe S, Morel JL (2015) Improving the agronomy of Alyssum murale for extensive phytomining: a five-year field study. Int J Phytorem 17:117–127
Becerra-Castro C, Kidd P, Kuffner M, Prieto-Fernández A, Hann S, Monterroso C, Sessitsch A, Wenzel W, Puschenreiter M (2013) Bacterially induced weathering of ultramafic rock and its implications for phytoextraction. Appl Environ Microbiol 79:5094–5103
Boudreau BP (1997) Diagenetic models and their implementation vol 55. Springer Verlag, Berlin, Germany
Brooks RR, Chambers MF, Nicks LJ, Robinson BH (1998) Phytomining. Trends Plant Sci 3:359–362
Cabello-Conejo MI (2015) Nickel hyperaccumulating plants: strategies to improve phytoextraction and a characterisation of Alyssum endemic to the Iberian Peninsula. PhD Thesis, Universidade de Santiago de Compostela (Spain)
Cabello-Conejo MI, Becerra-Castro C, Prieto-Fernández Á, Monterroso C, Saavedra-Ferro A, Mench M, Kidd PS (2014) Rhizobacterial inoculants can improve nickel phytoextraction by the hyperaccumulator Alyssum pintodasilvae. Plant Soil 379:35–50
Carballeira A, Devesa C, Retuerto R, Santillán E, Ucieda F (1983) Bioclimatología de Galicia. Fundación Pedro Barrié de la Maza, Conde de Fenosa, A Coruña
Cattani I, Capri E, Boccelli R, Del Re AAM (2009) Assessment of arsenic availability to roots in contaminated Tuscany soils by a diffusion gradient in thin films (DGT) method and uptake by Pteris vittata and Agrostis capillaris. Eur J Soil Sci 60:539–548
Chaney RL, Angle JS, Broadhurst CL, Peters CA, Tappero RV, Sparks DL (2007) Improved understanding of hyperaccumulation yields commercial phytoextraction and phytomining technologies. J Environ Qual 36:1429–1443
Chardot V, Massoura ST, Echevarria G, Reeves RD, Morel JL (2005) Phytoextraction potential of the nickel hyperaccumulators Leptoplax emarginata and Bornmuellera tymphaea. Int J Phytoremediation 7:323–335. https://doi.org/10.1080/16226510500327186
Chardot-Jacques V, Calvaruso C, Simon B, Turpault MP, Echevarria G, Morel JL (2013) Chrysotile dissolution in the rhizosphere of the nickel hyperaccumulator Leptoplax emarginata. Environ Sci Technol 47:2612–2620. https://doi.org/10.1021/es301229m
Davison W, Zhang H (1994) In situ speciation measurements of trace components in natural waters using thin-film gels. Nature 367:546–548
Davison W, Lin C, Gao Y, Zhang H (2015) Effect of gel interactions with dissolved organic matter on DGT measurements of trace metals. Aquat Geochemistry 21:281–293. https://doi.org/10.1007/s10498-014-9244-9
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
EC (2000) Natura:2000 https://ec.europa.eu/environment/nature/natura2000/index_en.htm
Echevarria G, Massoura ST, Sterckeman T, Becquer T, Schwartz C, Morel JL (2006) Assessment and control of the bioavailability of nickel in soils. Environ Toxicol Chem 25:643–651
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
Ernstberger H, Zhang H, Tye A, Young S, Davison W (2005) Desorption kinetics of cd, Zn, and Ni measured in soils by DGT. Environ Sci Technol 39:1591–1597
Estrade N, Cloquet C, Echevarria G, Sterckeman T, Deng T, Tang YT, Morel JL (2015) Weathering and vegetation controls on nickel isotope fractionation in surface ultramafic environments (Albania). Earth Planet Sci Lett 423:24–35. https://doi.org/10.1016/j.epsl.2015.04.018
Everhart JL, McNear D Jr, Peltier E, van der Lelie D, Chaney RL, Sparks DL (2006) Assessing nickel bioavailability in smelter-contaminated soils. Sci Total Environ 367:732–744
Fitz WJ, Wenzel WW, Zhang H, Nurmi J, Štipek K, Fischerova Z, Schweiger P, Köllensperger G, Ma LQ, Stingeder G (2003) Rhizosphere characteristics of the arsenic hyperaccumulator Pteris vittata L. and monitoring of phytoremoval efficiency. Environ Sci Technol 37:5008–5014
Hammer D, Keller C, McLaughlin MJ, Hamon RE (2006) Fixation of metals in soil constituents and potential remobilization by hyperaccumulating and non-hyperaccumulating plants: results from an isotopic dilution study. Environ Pollut 143:407–415
Harper MP, Davison W, Zhang H, Tych W (1998) Kinetics of metal exchange between solids and solutions in sediments and soils interpreted from DGT measured fluxes. Geochim Cosmochim Acta 62:2757–2770
Harper MP, Davison W, Tych W (2000) DIFS—a modelling and simulation tool for DGT induced trace metal remobilisation in sediments and soils. Environ Model Softw 15:55–66
Hinsinger P, Gobran GR, Gregory PJ, Wenzel WW (2005) Rhizosphere geometry and heterogeneity arising from root-mediated physical and chemical processes. New Phytol 168:293–303
Hoefer C, Santner J, Puschenreiter M, Wenzel WW (2015) Localized metal solubilization in the rhizosphere of Salix smithiana upon sulfur application. Environ Sci Technol 49:4522–4529
Hutchinson JJ, Young SD, McGrath SP, West HM, Black CR, Baker AJM (2000) Determining uptake of ‘non-labile’ soil cadmium by Thlaspi caerulescens using isotopic dilution techniques. New Phytol 146:453–460
IUSS W (2015) World Reference Base for soil resources 2014, update 2015 international soil classification system for naming soils and creating legends for soil maps. FAO, Rome
Jannasch HW, Honeyman BD, Balistrieri LS, James WM (1988) Kinetics of trace element uptake by marine particles. Geochim Cosmochim Acta 52:567–577
Jones DL, Willett VB (2006) Experimental evaluation of methods to quantify dissolved organic nitrogen (DON) and dissolved organic carbon (DOC) in soil. Soil Biol Biochem 38:991–999
Kong T, Steffens D (1989) Bedeutung der Kalium-Verarmung in der Rhizosphäre und derTonminerale für die Freisetzung von nichtaustauschbrem Kalium und dessen Bestimmungmit CHl. Z Pflanzenernähr Bodenk 152:337–343
Kreuzeder A, Santner J, Prohaska T, Wenzel WW (2013) Gel for simultaneous chemical imaging of anionic and cationic solutes using diffusive gradients in thin films. Anal Chem 85:12028–12036
Kreuzeder A, Santner J, Zhang H, Prohaska T, Wenzel WW (2015) Uncertainty evaluation of the diffusive gradients in thin films technique. Environ Sci Technol 49:1594–1602
Kukier U, Peters CA, Chaney RL, Angle JS, Roseberg RJ (2004) The effect of pH on metal accumulation in two Alyssum species. J Environ Qual 33:2090–2102. https://doi.org/10.2134/jeq2004.2090
Lehto NJ, Davison W, Zhang H, Tych W (2006a) Analysis of micro-nutrient behaviour in the rhizosphere using a DGT parameterised dynamic plant uptake model. Plant Soil 282:227–238
Lehto NJ, Davison W, Zhang H, Tych W (2006b) An evaluation of DGT performance using a dynamic numerical model. Environ Sci Technol 40:6368–6376
Lehto NJ, Sochaczewski L, Davison W, Tych W, Zhang H (2008) Quantitative assessment of soil parameter (KD and TC) estimation using DGT measurements and the 2D DIFS model. Chemosphere 71:795–801
Marschner H (1995) Mineral nutrition of higher plants. Academic press, New York, NY
Marschner P, Crowley D, Rengel Z (2011) Rhizosphere interactions between microorganisms and plants govern iron and phosphorus acquisition along the root axis - model and research methods. Soil Biol Biochem 43:883–894
Massoura ST, Echevarria G, Leclerc-Cessac E, Morel JL (2004) Response of excluder, indicator, and hyperaccumulator plants to nickel availability in soils. Aust J Soil Res 42:933–938
McLaren RG, Clucas LM, Speir TW, van Schaik AP (2007) Distribution and movement of nutrients and metals in a Pinus radiata forest soil following applications of biosolids. Environ Pollut 147:32–40
McLaughlin MJ, Andrew SJ, Smart MK, Smolders E (1998) Effects of sulfate on cadmium uptake by Swiss chard: I. effects of complexation and calcium competition in nutrient solutions. Plant Soil 202:211–216
Menezes-Blackburn D, Sun J, Lehto NJ, Zhang H, Stutter M, Giles CD, Darch T, George TS, Shand C, Lumsdon D, Blackwell M, Wearing C, Cooper P, Wendler R, Brown L, al-Kasbi M, Haygarth PM (2019) Simultaneous quantification of soil phosphorus labile pool and desorption kinetics using DGTs and 3D-DIFS. Environ Sci Technol 53:6718–6728. https://doi.org/10.1021/acs.est.9b00320
Muhammad I, Puschenreiter M, Wenzel WW (2012) Cadmium and Zn availability as affected by pH manipulation and its assessment by soil extraction, DGT and indicator plants. Sci Total Environ 416:490–500
Neumann G, Römheld V (2007) The release of root exudates as affected by the plant physiological status. In: Pinton R, Varanini Z, Nannipieri P (eds) The Rhizosphere: biochemistry and organic substances at the soil-plant interface. Marcel Dekker, New York, pp 23–72
Olsen SR, Cole CV, Watanabe FS (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. Circular / United States Department of Agriculture;no. 939. USDA, Washington
Puschenreiter M, Wieczorek S, Horak O, Wenzel WW (2003) Chemical changes in the rhizosphere of metal hyperaccumulator and excluder Thlaspi species. J Plant Nutr Soil Sci 166:579–584
Puschenreiter M, Wittstock F, Friesl-Hanl W, Wenzel WW (2013) Predictability of the Zn and cd phytoextraction efficiency of a Salix smithiana clone by DGT and conventional bioavailability assays. Plant Soil 369:531–541
Puschenreiter M, Gruber B, Wenzel WW, Schindlegger Y, Hann S, Spangl B, Schenkeveld WDC, Kraemer SM, Oburger E (2017) Phytosiderophore-induced mobilization and uptake of cd, cu, Fe, Ni, Pb and Zn by wheat plants grown on metal-enriched soils. Environ Exp Bot 138:67–76. https://doi.org/10.1016/j.envexpbot.2017.03.011
Salt DE, Kato N, Krämer U, Smith R, Raskin I (2000) The role of root exudates in nickel hyperaccumulation and tolerance in accumulator and non-accumulator. In: Terry N, Bañuelos G (eds) Phytoremediation of contaminated soil and water. Lewis Publishers, Boca Raton, London, NY, Washington D.C, p 189
Santner J, Larsen M, Kreuzeder A, Glud RN (2015) Two decades of chemical imaging of solutes in sediments and soils – a review. Anal Chim Acta 878:9–42
Sarkar, A. N., Jenkins, D. A. and Wyn Jones, R. G. (1979). Modification to mechanical and mineralogical composition of soil within the rhizosphere. In The soil-root Interface (J. L. Harley and R. Scott- Russell, eds.), pp. 125–136. Academic Press, London and Orlando
Sochaczewski Ł, Tych W, Davison B, Zhang H (2007) 2D DGT induced fluxes in sediments and soils (2D DIFS). Environ Model Softw 22:14–23
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 346:167–180
Tao S, Liu W, Chen Y, Xu F, Dawson R, Li B, Cao J, Wang X, Hu J, Fang J (2004) Evaluation of factors influencing root-induced changes of copper fractionation in rhizosphere of a calcareous soil. Environ Pollut 129:5–12
Uren N, Reisenauer H (1988) The role of root exudates in nutrient acquisition. In: Tinker P, Lauchli A (eds) Advances in plant nutrition, vol 3. Praeger, New York, pp 79–114
Valentinuzzi F, Mimmo T, Cesco S, Al Mamun S, Santner J, Hoefer C, Oburger E, Robinson B, Lehto N (2015) The effect of lime on the rhizosphere processes and elemental uptake of white lupin. Environ Exp Bot 118:85–94
van der Ent A, Baker AJM, Reeves RD, Chaney RL, Anderson CWN, Meech JA, Erskine PD, Simonnot M-O, Vaughan J, Morel JL, Echevarria G, Fogliani B, Rongliang Q, Mulligan DR (2015) Agromining: farming for metals in the future? Environ Sci Technol 49:4773–4780
Warnken KW, Zhang H, Davison W (2004) Analysis of polyacrylamide gels for trace metals using diffusive gradients in thin films and laser ablation inductively coupled plasma mass spectrometry. Anal Chem 76:6077–6084. https://doi.org/10.1021/ac0400358
Wenzel WW, Bunkowski M, Puschenreiter M, Horak O (2003) Rhizosphere characteristics of indigenously growing nickel hyperaccumulator and excluder plants on serpentine soil. Environ Pollut 123:131–138
Wenzel WW, Lombi E, Adriano DC (2004) Root and rhizosphere processes in metal hyperaccumulation and phytoremediation technology. In: Prasad MNV (ed) Heavy metal stress in plants. Springer, Berlin Heidelberg, pp 313–344
Zeien H, Brümmer G (1989) Chemische extraktion zur bestimmung von schwermetallbindungsformen in böden. Mitteling Dtsch Bondenkundl Gesellsch 59:505–510
Zelano IO, Cloquet C, van der Ent A, Echevarria G, Gley R, Landrot G, Pollastri S, Fraysse F, Montargès-Pelletier E (2020) Coupling nickel chemical speciation and isotope ratios to decipher nickel dynamics in the Rinorea cf. bengalensis-soil system in Malaysian Borneo. Plant Soil 454:225–243. https://doi.org/10.1007/s11104-020-04541-0
Zhang FS, Treeby M, RÖmheld V, Marschner H (1991) Mobilization of iron by phytosiderophores as affected by other micronutrients. In: Chen Y, Hadar Y (eds) Iron nutrition and interactions in plants: “Proceedings of the Fifth International Symposium on Iron nutRition and Interactions in Plants”, 11–17 June 1989, Jerusalem, Israel, 1989. Springer Netherlands, Dordrecht, pp 205–210
Zhang H, Zhao F-J, Sun B, Davison W, McGrath SP (2001) A new method to measure effective soil solution concentration predicts copper availability to plants. Environ Sci Technol 35:2602–2607
Zhang X, Houzelot V, Bani A, Morel JL, Echevarria G, Simonnot M-O (2014) Selection and combustion of Ni-hyperaccumulators for the phytomining process. Int J Phytorem 16:1058–1072
Acknowledgments
In memory of Petra S. Kidd (1972-2020†). Her dedication, enthusiasm and generosity were an essential contribution to this work. Her passion for the science will always be an inspiration to us. Vanessa Álvarez-López also thanks Christoph Hoefer and Andreas Kreuzeder for their help and company in the laboratory. This research was supported by the Spanish Ministerio de Economía y Competitividad (CTM2012-39904-C02-01) and FEDER, and by the 7th Framework Program of the European Commission (FP7-KBBE-266124, GREENLAND).
Funding
Spanish Ministerio de Economía y Competitividad (CTM2012-39904-C02-01) and FEDER, and the 7th Framework Program of the European Commission (FP7-KBBE-266124, GREENLAND.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflicts of interest/competing interests
Not applicable.
Additional information
Responsible editor: Antony Van der Ent
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
P.S. Kidd Deceased
Rights and permissions
About this article
Cite this article
Álvarez-López, V., Puschenreiter, M., Santner, J. et al. Evidence for nickel mobilisation in rhizosphere soils of Ni hyperaccumulator Odontarrhena serpyllifolia. Plant Soil 464, 89–107 (2021). https://doi.org/10.1007/s11104-021-04944-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-021-04944-7