Skip to main content

Advertisement

Log in

A simple model for estimating Ni availability and leaf Ni accumulation for the Ni-hyperaccumulator Leptoplax emarginata

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

Abstract

Aims

The aim of the present study was to predict kinetics of both Ni concentration in soil solution and leaf Ni mass for the Ni-hyperaccumulator Leptoplax emarginata cultivated on a fertilized and Ni-contaminated sandy topsoil.

Methods

The 0-D (independent of space) one-site rate-limited desorption model proposed by Ingwersen et al. (J Environ Qual 35:2055–2065, 2006) was modified. The plant sink term of the model was approximated by the biophysical equation which assumes that the leaf nickel mass is equal to the triple product of the Intact Plant Transpiration Stream Concentration Factor for Ni IPTSCFNi (xylem:solution Ni concentration ratio), Ni concentration in solution and the volume of transpired water. The model input variables were the constant mean IPTSCFNi value, determined from independent leaf Ni accumulation kinetics, and the exponential law fitting the transpiration rate kinetics. Using the best calibration, the model was validated and a sensitivity analysis was carried out thereafter. Models were formulated as sets of ordinary differential equation systems which were solved using the fourth-order Runge–Kutta method.

Results

The best model calibration was the joint parameter optimization: the two parameters of the Freundlich Ni adsorption isotherm and of the Ni desorption rate coefficient are obtained using the kinetics of Ni concentrations in the soil solutions for the reference unplanted Ni-contaminated topsoils. The model was validated reasonably well for both Ni concentration in soil solution and leaf Ni mass.

Conclusions

The joint parameter optimization of the two parameters of the Freundlich nickel sorption isotherm and of the Ni desorption rate was successful whereas the Freundlich batch Ni sorption isotherm dramatically overestimated Ni sorption. This joint approach is therefore recommended for any plant metal uptake model. The 0-D one-site rate-limited desorption model linked to a biophysical coupled Ni and water uptake model reasonably validated the kinetics of both Ni concentration in solution and leaf Ni mass. This promising simplified model for predicting both metal concentration in solution and leaf metal mass for metal needs further validations in culture chambers and further improvements in order to use it in the field as a one-dimensional model, taking into account soil moisture dynamics.

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
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adhikari T, Rattan RK (2000) Modelling zinc uptake by rice crop using a Barber-Cushman approach. Plant Soil 227:235–242

    Article  CAS  Google Scholar 

  • Altfelder S, Streck T, Maraqa MA, Voice TC (2001) Nonequilibrium sorption of dimethylphtalate—compatibility of batch and column techniques. Soil Sci Soc Am J 65:102–111

    Article  CAS  Google Scholar 

  • Anderson CWN, Brooks RR, Chiarucci A, LaCoste CJ, Leblanc M, Robinson BH, Simcocke R, Stewart RB (1999) Phytomining for nickel, thallium and gold. J Geochem Explor 67:407–415

    Article  CAS  Google Scholar 

  • Bajracharya K, Tran YT, Barry DA (1996) Cadmium adsorption at different pore water velocities. Geoderma 73:197–216

    Article  CAS  Google Scholar 

  • Barber SA (1995) Soil nutrient bioavailability: a mechanistic approach. John Wiley, New-York, 414 p

    Google Scholar 

  • Barber SA, Cushman JH (1981) Nitrogen uptake model for agronomic crops. In: Iskandar JK (ed) Modeling waste water renovation-land treatment. J.Wiley Inter-Science, New York, pp 382–409

    Google Scholar 

  • Barnes EM, Young JH (1994) Sensitivity analysis of the soil inputs for the growth model PEANUT. Trans ASAE 37:1691–1694

    Article  Google Scholar 

  • Barrow NJ (1998) Effects of time and temperature on the sorption of cadmium, zinc, cobalt, and nickel by a soil. Aust J Soil Res 36:941–950

    Article  CAS  Google Scholar 

  • Bartoli F, Coinchelin D, Robin C, Echevarria G (2012) Impact of active transport and transpiration on nickel and cadmium accumulation in the leaves of the Ni-hyperaccumulator Leptoplax emarginata: a biophysical approach. Plant Soil 350:99–115

    Article  CAS  Google Scholar 

  • Behrendt H, Brüggemann R, Morgenstern M (1995) Numerical and analytical model of pesticide root uptake model comparison and sensitivities. Chemosphere 30:1905–1920

    Article  CAS  Google Scholar 

  • Blossfeld S, Perriguey J, Sterckeman T, Morel J-L, Lösch R (2010) Rhizosphere pH dynamics in trace-metal-contaminated soils, monitored with planar pH optodes. Plant Soil 330:173–184

    Google Scholar 

  • Boekhold AE, Van der Zee SEATM (1992) A scaled sorption model validated at the column scale to predict cadmium contents in a spatially variable field soil. Soil Sci 154:105–112

    Article  CAS  Google Scholar 

  • Brusseau ML, Zachara JM (1993) Transport of Co2+ in a physically and chemically heterogeneous porous medium. Environ Sci Technol 27:1937–1939

    Article  CAS  Google Scholar 

  • Burken JG, Schnoor JL (1997) Uptake and metabolism of atrazine by poplar trees. Environ Sci Technol 31:1399–1406

    Article  CAS  Google Scholar 

  • Cacuci DG, Ionescu-Bujor M (2004) A comparative review of sensitivity and uncertainty analysis of large-scale systems. II: statistical methods. Nucl Sci Eng 147:204–217

    CAS  Google Scholar 

  • Cecchi L, Gabbrielli R, Arnetoli M, Gonnelli C, Hasko A, Selvi F (2010) Evolutionary lineages of nickel hyperaccumulation and systematics in European Alysseae (Brassicaceae): evidence from nrDNA sequence data. Ann Bot 106:751–767

    Article  CAS  PubMed  Google Scholar 

  • Chaney RL, Angle JS, Broadhurst CL, Peters CA, Tapppero RV, Sparks DL (2007) Improved understanding of hyperaccumulation yields commercial phytoextraction and phytomining technologies. J Environ Qual 36:1429–1443

    Article  CAS  PubMed  Google Scholar 

  • Chardot V, Massoura ST, Echevarria G (2005) Phytoextraction potential of the nickel hyperaccumulators Leptoplax emarginata and Bornmuellera tymphaea. Int J Phytoremediat 7:323–335

    Google Scholar 

  • Claassen N, Steingrobe B (1999) Mechanistic simulation models for a better understanding of nutrient uptake from soil. In: Rengel Z (ed) Mineral nutrition of crops: fundamental mechanisms and implications. Food Products Press, New York, pp 327–367

    Google Scholar 

  • Coinchelin D, Bartoli F, Robin C, Echevarria G (2012) Ecophysiology of nickel phytoaccumulation: a simplified biophysical approach. J Exp Bot 63:5815–5827

    Article  CAS  PubMed  Google Scholar 

  • Dalton FN, Raats PAAC, Gardner WR (1975) Simultaneous uptake of water and solutes by plant roots. Agron J 67:334–339

    Article  CAS  Google Scholar 

  • Degryse F, Smolders E, Parker DR (2009) Partioning of metals (Cd, Co, Cu, Ni, Pb, Zn) in soils: concepts, methodologies, prediction and applications—a review. Eur J Soil Sci 60:590–612

    Article  CAS  Google Scholar 

  • Echevarria G, Morel JL, Fardeau JC, Leclerc-Cessac E (1998) Assessment of phytoavailability of nickel in soils. J Environ Qual 27:1064–1070

    Google Scholar 

  • Ferreira VA, Weesies GA, Yoder DC, Foster GR, Renard KG (1995) The site and condition specific nature of sensitivity analysis. J Soil Water Conserv 50:493–497

    Google Scholar 

  • Filius A, Streck T, Richter J (1998) Cadmium sorption and desorption in limed topsoils as influenced by pH: isotherms and simulated leaching. J Environ Qual 27:12–18

    Article  CAS  Google Scholar 

  • Ginocchio R, Rodriguez PH, Badilla-Ohlbaum R, Allen HE, Lagos G (2002) Effect of soil copper content and pH on copper uptake of selected vegetables grown under controlled conditions. Environ Toxicol Chem 21:1736–1744

    Article  CAS  PubMed  Google Scholar 

  • Goktas RK, Aral MM (2011) Integrated dynamic modelling of contaminant fate and transport within a soil-plant system. Vadose Zone J 10:1130–1150

    Article  Google Scholar 

  • Grolimund D, Borkovec M, Federer P, Sticher H (1995) Measurement of sorption isotherms with flow-through reactors. Environ Sci Technol 29:2317–2321

    Article  CAS  PubMed  Google Scholar 

  • Hamby DM (1994) A review of techniques for parameter sensitivity analysis of environmental models. Environ Monit Assess 32:135–154

    Article  CAS  PubMed  Google Scholar 

  • Helton JC (1993) Uncertainty and sensitivity analysis techniques for use in performance assessment for radioactive waste disposal. Reliab Eng Syst Saf 42:327–367

    Article  Google Scholar 

  • Hopmans JW, Bristow KL (2002) Current capabilities and future needs of root water and nutrient uptake modelling. Adv Agron 77:103–183

    Article  Google Scholar 

  • Hough RL, Young SD, Crout NMJ (2003) Modelling of Cd, Cu, Ni, Pb and Zn uptake by winter wheat and forage maize from a sewage disposal farm. Soil Use Manag 19:19–27

    Article  Google Scholar 

  • Hough RL, Tye AM, Crout NMJ, McGrath SP, Zhang H, Young SD (2005) Evaluating a ‘Free Ion Activity Model’ applied to metal uptake by Lolium perenne L. grown incontaminated soils. Plant Soil 270:1–12

    Article  CAS  Google Scholar 

  • Ingwersen J, Streck T (2005) A regional-scale study on the crop uptake of cadmium from sandy soils: measurement and modeling. J Environ Qual 34:1026–1035

    Article  CAS  PubMed  Google Scholar 

  • Ingwersen J, Bücherl B, Neumann G, Streck T (2006) Cadmium leaching from micro-lysimeters planted with the hyperaccumulator Thlaspi caerulescens: experimental findings and modeling. J Environ Qual 35:2055–2065

    Article  CAS  PubMed  Google Scholar 

  • Ionescu-Bujor M, Cacuci DG (2004) A comparative review of sensitivity and uncertainty analysis of large-scale systems. I: deterministic methods. Nucl Sci Eng 147:189–203

    CAS  Google Scholar 

  • Johnson GR, Gupta K, Putz DK, Hu Q, Brusseau ML (2003) The effects of local-scale physical heterogeneity and nonlinear, rate-limited sorption/desorption on contaminant transport in porous media. J Contam Hydrol 64:35–58

    Article  CAS  PubMed  Google Scholar 

  • Kalis EJJ, Temminghoff EJM, Weng L, van Riemsdijk WH (2006) Effects of humic acid and competing cations on metal uptake by Lolium perenne. Environ Toxicol Chem 25:702–711

    Article  CAS  PubMed  Google Scholar 

  • Kemanian AR, Stöckle CO, Huggins DR (2005) Transpiration-use efficiency of barley. Agric For Meteorol 130:1–11

    Article  Google Scholar 

  • Koopmans GF, Römkens PFAM, Song J, Temminghohh EJM, Japenga J (2007) Predicting the phytoextration duration to remediate heavy metals contaminated soils. Water Air Soil Pollut 181:355–371

    Article  CAS  Google Scholar 

  • Krämer U (2005) Phytoremediation: novel approaches to cleaning up polluted soils. Curr Opin Biotechnol 16:133–141

    Article  PubMed  Google Scholar 

  • Krämer U (2010) Metal hyperaccumulation in plants. Annu Rev Plant Biol 61:517–534

    Article  PubMed  Google Scholar 

  • Larbi A, Morales F, Abadia A, Gogorcena Y, Lucena JJ, Abadia J (2002) Effects of Cd and Pb in sugar beet plants grown in nutrient solution: induced Fe deficiency and growth inhibition. Funct Plant Biol 29:1453–1464

    Article  CAS  Google Scholar 

  • Lehto NJ, Davison W, Zhang H, Wlodek T (2006) Analysis of micro-nutrient behaviour in the rhizosphere using a DGT parameterized dynamic plant uptake model. Plant Soil 282:227–238

    Article  CAS  Google Scholar 

  • Li Y-M, Chaney RL, Brewer E, Roseberg RJ, Angle JS, Baker AJM, Reeves RD, Nelkin J (2003) Development of a technology for commercial phytoextraction of nickel: economic and technical considerations. Plant Soil 249:107–115

    Article  CAS  Google Scholar 

  • Liang H-M, Lin T-H, Chiou J-M, Yeh K-C (2009) Model evaluation of the phytoextraction potential of heavy métal hyperaccumulators and non-hyperaccumulators. Environ Pollut 157:1945–1952

    Article  CAS  PubMed  Google Scholar 

  • Liao L, Selim HM (2010) Transport of nickel in different soils: column experiments and kinetic modeling. Soil Sci Soc Am J 74:1946–1955

    Article  CAS  Google Scholar 

  • Limousin G, Gaudet J-P, Charlet L, Szenknect S, Barthes V, Krimissa M (2007) Sorption isotherms: a review on physical bases, modeling and measurement. Appl Geochem 22:249–275

    Article  CAS  Google Scholar 

  • Luo YM, Christie P, Baker AJM (2000) Soil solution Zn and pH dynamics in nonrhizosphere soil and in the rhizosphere of Thlaspi caerulescens grown in a Zn/Cdcontaminated soil. Chemophere 41:161–164

    Google Scholar 

  • Manzoni S, Molini A, Porporato A (2011) Stochastic modeling of contaminated soil phytoremediation. Proc R Soc Lond A. doi:10.1098/rspa.2011.0209

    Google Scholar 

  • Marino S, Hogue IB, Ray CJ, Kirschner DE (2008) A methodology for performing global uncertainty and sensitivity analysis in systems biology. J Theor Biol 254:178–196

    Article  PubMed Central  PubMed  Google Scholar 

  • Maxted AP, Black CR, West HM, Crout NMJ, McGrath SP, Young SD (2007) Phytoextraction of cadmium and zinc from arable soils amended with sewage sludge using Thlaspi caerulescens: development of a predictive model. Environ Pollut 150:363–372

    Article  CAS  PubMed  Google Scholar 

  • McBride MB (2002) Cadmium uptake by crops estimated from soil total Cd and pH. Soil Sci 167:62–67

    Article  CAS  Google Scholar 

  • McGrath SP, Zhao FJ, Lombi E (2002) Phytoremediation of metals, metalloids and radionuclides. Adv Agron 75:1–56

    Article  CAS  Google Scholar 

  • Mehra O, Jackson ML (1960) Iron-oxide removal from soils and clays by a dithionite-citrate system buffered with sodium bicarbonate. Clay Clay Miner 7:317–327

    Google Scholar 

  • Monsant AC, Tang C, Baker AJM (2008) The effect of nitrogen form on rhizosphere soil pH and zinc phytoextraction by Thlaspi caerulescens. Chemosphere 73:635–642

    Google Scholar 

  • Morel FMM (1983) Principles of aquatic chemistry. John Wiley, New York, 446 p

    Google Scholar 

  • Mullins GL, Sommers LE, Barber SA (1986) Modeling the plant uptake of cadmium and zinc from soils treated with sewage sludge. Soil Sci Am J 50:1245–1250

    Article  CAS  Google Scholar 

  • Nick LJ, Chambers MF (1995) Farming for metals? Min Environ Manag 3:15–18

    Google Scholar 

  • Paquin PR, Gorsuch JW, Apte S, Batley GE, Bowles KC, Campbell PGC, Delos CG, Di Toro DM, Dwyer RL, Galvez F, Gensemer RW, Goss GG, Hogstrand C, Janssen CR, McGeer JC, Naddy RB, Playle RC, Santore RC, Schneider U, Stubblefield WA, Wood CM, Wu KB (2002) The biotic ligand model: a historical overview. Comp Biochem Physiol C Toxicol Pharmacol 133:3–35

    Article  PubMed  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 

  • Peer WA, Mahmoudian M, Freeman, Lahner B, Richards EL, Reeves RD, Murphy AS, Salt DE (2006) Assessment of plants from the Brassicaceae family as genetic models for the study of nickel and zinc hyperaccumulation. New Phytol 172:248–260

  • Peijnenburg W, Baerselman R, de Groot A, Jager T, Leenders D, Posthuma L, Van Veen R (2000) Quantification of metal bioavailability for lettuce (Lactuca sativa L.) in field soils. Arch Environ Contam Toxicol 39:420–430

    Article  CAS  PubMed  Google Scholar 

  • Puschenreiter M, Schnepf A, Millan IM, Fitz WJ, Horak O, Klepp J, Schreff T, Lombi E, Wenzel WW (2005) Changes of Ni biogeochemistry in the rhizosphere of the hyperaccumulator Thlaspi goesingense. Plant Soil 271:205–218

    Article  CAS  Google Scholar 

  • Redjala T, Sterckeman T, Skikker 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

    Google Scholar 

  • Reeves RD, Brooks RR, Press JR (1980) Nickel accumulation by species of Peltaria Jacq. (Cruciferae). Taxonomy 29:629–633

    Article  Google Scholar 

  • Richards LA (1931) Capillary conduction of liquids through porous mediums. Physics 1:318–333

    Article  Google Scholar 

  • Robinson B, Fernandez J-E, Madejon P, Maranon T, Murillo JM, Green S, Clothier B (2003) Phytoextraction and assessment of biogeochemical and economic viability. Plant Soil 249:117–125

    Article  CAS  Google Scholar 

  • Robinson BH, Schulin R, Nowack B, Roulier S, Menon M, Clothier B, Green S, Mills T (2006) Phytoremediation for the management of metal flux in contaminated sites. For Snow Landsc Res 80:221–234

    Google Scholar 

  • Roose T, Fowler AC (2004) A mathematical model for water and nutrient uptake by roots. J Theor Biol 228:173–184

    Article  CAS  PubMed  Google Scholar 

  • Russel RS (1977) Plant root systems: their function and interaction with the soil. McGraw-Hill, New York

    Google Scholar 

  • Russel RS, Barber DA (1960) The relationship between salt uptake and the absorption of water by intact plants. Annu Rev Plant Physiol 11:127–140

    Article  Google Scholar 

  • Sadana US, Claassen N (2000) Manganese dynamics in the rhizosphere and Mn uptake by different crops evaluated by a mechanistic model. Plant Soil 218:233–238

    Article  CAS  Google Scholar 

  • Saltelli A, Ratto M, Tarantola S, Campolongo F (2005) Sensitivity analysis for chemical models. Chem Rev 105:2811–2827

    Article  CAS  PubMed  Google Scholar 

  • Schoups G, Hopmans JW (2002) Analytical model for vadose zone solute transport with root water and solute uptake. Vadose Zone J 1:158–171

    CAS  Google Scholar 

  • Selim HM, Buchter B, Hinz C, Ma L (1992) Modeling the transport and retention of cadmium in soils: multireaction and multicomponent approaches. Soil Sci Soc Am J 56:1004–1015

    Article  CAS  Google Scholar 

  • Silberbush M, Barber SA (1983) Sensitivity of simulated phosphorus uptake to parameters used by a mechanistic-mathematical model. Plant Soil 74:93–100

    Article  CAS  Google Scholar 

  • Sterckeman T, Perriguey J, Caël M, Schwartz C, Morel J-L (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 

  • Trapp S (2000) Modelling uptake into roots and subsequent translocation of neutral and ionisable organic compounds. Pest Manag Sci 56:767–778

    Article  CAS  Google Scholar 

  • Trapp S (2004) Plant uptake and transport models for neutral and ionic chemicals. Environ Sci Pollut Res 11:33–39

    Article  CAS  Google Scholar 

  • Van der Vliet L, Peterson C, Hale B (2007) Cd accumulation in roots and shoots of durum wheat: the roles of transpiration rate and apoplastic bypass. J Exp Bot 58:2939–2947

    Article  PubMed  Google Scholar 

  • Van Nevel L, Mertens J, Oorts K, Verheyen K (2007) Phytoextraction of metals from soils: how far from practice? Environ Pollut 150:34–40

    Article  PubMed  Google Scholar 

  • Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181:759–776

    Article  CAS  PubMed  Google Scholar 

  • Warren GP, Alloway BJ, Lepp NW, Singh BR, Bochereau FJM, Penny C (2003) Field trials to assess the uptake of arsenic by vegetables from contaminated soils and soil remediation with iron oxides. Sci Total Environ 311:19–33

    Article  CAS  PubMed  Google Scholar 

  • Weltje L, Hollander WD, Wolterbeek HT (2003) Adsorption of metals to membrane filters in view of their speciation in nutrient solution. Environ Toxicol Chem 22:265–271

    Article  CAS  PubMed  Google Scholar 

  • Williams M, Yanai RD (1996) Multi-dimensional sensitivity analysis and ecological implications of a nutrient uptake model. Plant Soil 180:311–324

    Article  CAS  Google Scholar 

  • WRB (World Reference Base for Soil Resources) (2001) In: Driessen P, Deckers J, Spaargaren O, Nachtergaele F (eds) Lecture Notes on the Major Soils of the World. FAO World Soil Resources Reports 94. Food and Agriculture Organization of the United Nations, Rome

Download references

Acknowledgments

We thank Mathilde Royer for her participation in the hyperaccumulator/Ni-contaminated soil experiment, Stéphane Colin for designing the culture pots and our colleagues from TCEM INRA Bordeaux for rendering accessible their experimental site for the topsoil sampling. Trust and financial support from INPL, ADEME and Lorraine Regional Council given to the first author for his PhD grant were greatly appreciated. We thank very much Claude Doussan, UMR EMMAH INRA-Université d’Avignon et Pays de Vaucluse, France, for his very helpful constructive comments on an earlier draft of the paper, and Helen Selliez for improving the English. We finally also thank very much the reviewer for key very helpful comments and criticisms, as well as for careful editorial comments, that have greatly improved the former version of this paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to F. Bartoli.

Additional information

Responsible Editor: Henk Schat.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Coinchelin, D., Stemmelen, D. & Bartoli, F. A simple model for estimating Ni availability and leaf Ni accumulation for the Ni-hyperaccumulator Leptoplax emarginata . Plant Soil 374, 131–147 (2014). https://doi.org/10.1007/s11104-013-1873-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-013-1873-z

Keywords

Navigation