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Cadmium and nickel uptake by tomato and spinach seedlings: plant or transport control?

Fien Degryse A B C and Erik Smolders A
+ Author Affiliations
- Author Affiliations

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

B Present address: School of Food, Agriculture and Wine, University of Adelaide, PMB1, Glen Osmond, SA 5064, Australia.

C Corresponding author. Email: fien.degryse@adelaide.edu.au

Environmental Chemistry 9(1) 48-54 https://doi.org/10.1071/EN11060
Submitted: 2 May 2011  Accepted: 16 August 2011   Published: 23 November 2011

Environmental context. Uptake of metal ions by plants is often predicted with equilibrium models, which assume that the rate limiting step is trans-membrane uptake of the metal in the roots rather than the transport of the metal ion towards the site of uptake. Evidence is given that uptake of cadmium by plants is under strong transport control at environmentally relevant concentrations, whereas nickel uptake borders between transport and plant control. This explains the lack of ion competition effects for Cd uptake, whereas both proton and Mg ions were found to compete with Ni uptake.

Abstract. Equilibrium models for metal uptake by biota assume that the uptake is rate limited by the internalisation of the metal across the cell membrane (plant control). However, evidence has been found that Cd uptake by plants is controlled by the diffusive transport of the free ion to the root at low Cd2+ activities. In this study, the uptake of Cd and Ni by tomato and spinach in nutrient solution was compared to assess whether Ni uptake is under plant or transport control. The diffusive gradient in thin films (DGT) technique was used to measure the maximal diffusive flux. In unbuffered solutions, the uptake flux of Ni was approximately three-fold smaller than that of Cd at free ion concentrations below 1 µM. Stirring the solution increased the uptake of Cd, but not that of Ni at low free ion concentration. The presence of DGT-labile complexes increased the uptake of Cd, but not that of Ni, except at high pH (pH 7). Increasing the solution pH increased Cd uptake only when solution Cd2+ activities were strongly buffered. Overall, the results indicated that the Cd uptake was strongly diffusion limited and that uptake is likely to be under transport control in natural environments. Uptake of nickel, on the other hand, appears to be at the border between plant and transport control. This finding has practical applications, e.g. competition effects at the root have little effect on Cd uptake and chelator-assisted phytoextraction is expected to have less effect for Ni than for Cd.

Additional keywords: DGT, diffusion, metals, plants.


References

[1]  F. M. M. Morel, Principles of Aquatic Chemistry 1983 (Wiley: New York).

[2]  R. C. Playle, Modelling metal interactions at fish gills. Sci. Total Environ. 1998, 219, 147.
Modelling metal interactions at fish gills.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlslWltrs%3D&md5=daa3120abfc5bb8f8cad4266f1e6a3e3CAS |

[3]  M. J. McLaughlin, E. Smolders, R. Merckx, A. Maes, 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.) 1997, pp. 113–118 (Kluwer Academic: Dordrecht, the Netherlands).

[4]  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.
Free metal activity and total metal concentrations as indices of micronutrient availability to barley (Hordeum vulgare (L.) ‘Klages’).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXhsVaiurw%3D&md5=02d30a97da8e277c79cf0a990cb83806CAS |

[5]  F. Degryse, E. Smolders, R. Merckx, Labile Cd complexes increase Cd availability to plants. Environ. Sci. Technol. 2006, 40, 830.
Labile Cd complexes increase Cd availability to plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlarsrfK&md5=d73463cd9a6d8a542cc113c08df5f71aCAS |

[6]  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=2b11871c95988474526b80331e92cf1eCAS |

[7]  S. Jansen, R. Blust, H. P. Van Leeuwen, Metal speciation dynamics and bioavailability: ZnII and CdII uptake by mussel (Mytilus edulis) and carp (Cyprinus carpio). Environ. Sci. Technol. 2002, 36, 2164.
Metal speciation dynamics and bioavailability: ZnII and CdII uptake by mussel (Mytilus edulis) and carp (Cyprinus carpio).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitVOjtrc%3D&md5=72caefc3f259dbd35b06d2c09f2ce8f6CAS |

[8]  H. Zhang, W. Davison, Performance characteristics of diffusion gradients in thin films for the in situ measurement of trace metals in aqeous solution. Anal. Chem. 1995, 67, 3391.
Performance characteristics of diffusion gradients in thin films for the in situ measurement of trace metals in aqeous solution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnslKgtrc%3D&md5=87242e0da4eca5a0b457f07f56562955CAS |

[9]  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=fe7661ab2593a6d3a4565e2fb4bb6acfCAS |

[10]  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=0d661215d1d68f99b4a96b09f7313876CAS |

[11]  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=0651bcd5f4aab1ac186750a1bba5903bCAS |

[12]  M. Puschenreiter, A. Schnepf, I. M. Millan, W. J. Fitz, O. Horak, J. Klepp, T. Schrefl, E. Lombi, W. W. Wenzel, Changes of Ni biogeochemistry in the rhizosphere of the hyperaccumulator Thlaspi goesingense. Plant Soil 2005, 271, 205.
Changes of Ni biogeochemistry in the rhizosphere of the hyperaccumulator Thlaspi goesingense.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXks1Ojt7k%3D&md5=6b23a686e6f712be3666ff9ae331ce8aCAS |

[13]  I. A. M. Worms, N. Parthasarathy, K. J. Wilkinson, Ni uptake by a green alga. 1. Validation of equilibrium models for complexation effects. Environ. Sci. Technol. 2007, 41, 4258.
Ni uptake by a green alga. 1. Validation of equilibrium models for complexation effects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlt1OgsLg%3D&md5=093f6fbdd85e6245065708d45d9e92e8CAS |

[14]  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.
In situ measurements of metal complex exchange kinetics in freshwater.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjsV2mur0%3D&md5=74efd69bbb7b902c4175005efc63545dCAS |

[15]  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.
In situ measurements of dissociation kinetics and labilities of metal complexes in solution using DGT.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhsFWjt7s%3D&md5=68c64651fc7a170b604322a23acb22adCAS |

[16]  M. Eigen, R. G. Wilkins, The kinetics and mechanism of formation of metal complexes, in Mechanisms of Inorganic Reactions, Advances in Chemistry Series 49 (Eds J. Kleinberg, R. K. Murmann, R. T. M. Fraser, J. Bauman) 1965, pp. 55–80 (American Chemical Society: Washington, DC).

[17]  R. Uribe, S. Mongin, J. Puy, J. Cecilia, J. Galceran, H. Zhang, W. Davison, Contribution of partially labile complexes to the DGT metal flux. Environ. Sci. Technol. 2011, 45, 5317.
Contribution of partially labile complexes to the DGT metal flux.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmsVWlsLs%3D&md5=0806f7b68503ff4b785e84006817b8a5CAS |

[18]  M. N. Bravin, A. L. Marti, M. Clairotte, P. Hinsinger, Rhizosphere alkalisation – a major driver of copper bioavailability over a broad pH range in an acidic, copper-contaminated soil. Plant Soil 2009, 318, 257.
Rhizosphere alkalisation – a major driver of copper bioavailability over a broad pH range in an acidic, copper-contaminated soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltVWrtL4%3D&md5=50ba7b08dfad287322209be4e300351eCAS |

[19]  P. Hinsinger, A. G. Bengough, D. Vetterlein, I. M. Young, Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant Soil 2009, 321, 117.
Rhizosphere: biophysics, biogeochemistry and ecological relevance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXos1enu78%3D&md5=c0e013b8b355a2aa457005e1505ff9ddCAS |

[20]  E. Berkelaar, B. Hale, The relationship between root morphology and cadmium accumulation in seedlings of two durum wheat cultivars. Can. J. Bot. 2000, 78, 381.
The relationship between root morphology and cadmium accumulation in seedlings of two durum wheat cultivars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktVKnur8%3D&md5=7a1fcc9c88ae558690fb3ad2bf8857f2CAS |

[21]  I. A. M. Worms, K. J. Wilkinson, Ni uptake by a green alga. 2. Validation of equilibrium models for competition effects. Environ. Sci. Technol. 2007, 41, 4264.
Ni uptake by a green alga. 2. Validation of equilibrium models for competition effects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlt1OgsLk%3D&md5=132f18d40339a9404eabdbe264ce55a3CAS |

[22]  F. M. M. Morel, R. J. M. Hudson, N. M. Price, Limitation of productivity by trace-metals in the sea. Limnol. Oceanogr. 1991, 36, 1742.
Limitation of productivity by trace-metals in the sea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XktFeqtrY%3D&md5=e3b0a3e1b504070576b9745c37075f79CAS |

[23]  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=dea1b527d2b88c2d801ffb117ee7c2d0CAS |

[24]  T. Redjala, I. Zelko, T. Sterckeman, V. Legue, A. Lux, Relationship between root structure and root cadmium uptake in maize. Environ. Exp. Bot. 2011, 71, 241.
Relationship between root structure and root cadmium uptake in maize.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhvFWit7k%3D&md5=be7f9ecf7b24c8c65f2bcdb57dc9b069CAS |

[25]  D. R. Parker, R. L. Chaney, W. A. Norvell, Chemical equilibrium models: applications to plant nutrition research., in Chemical Equilibrium and Reaction Models (Eds R. H. Loeppert, A. P. Schwab, S. Goldberg) 1995, Special Publication 42, pp. 163–200 (Soil Science Society of America: Madison, WI).

[26]  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.
A method for controlling the activities of free metal, hydrogen and phosphate ions in hydroponic solutions using ion exchange and chelating resins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXltlegs7g%3D&md5=947bb1959b711f8e65ed26b58e21ad30CAS |

[27]  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.
Chemical speciation of Zn, Cd, Cu and Pb in pore waters of agricultural and contaminated soils using Donnan dialysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovV2ltLs%3D&md5=2734f3b6c5977d460d45447a468c8df6CAS |