Skip to main content

Hyperaccumulation of nickel by Alyssum corsicum is related to solubility of Ni mineral species

Abstract

Aims

Past studies have demonstrated that hyperaccumulators absorb Ni from the same labile pools in soil as normal plant species. This study investigated whether the Ni hyperaccumulator plant Alyssum corsicum possesses distinct extraction mechanisms for different Ni species present in soils. Different Ni species have different solubilities and potential bioavailabilities to roots.

Methods

Uptake of Ni in shoots of A. corsicum was analyzed after four weeks of plant growth in nutrient solution with 17 different Ni compounds or soils.

Results

The results indicate that Ni uptake is related to Ni solubility and plant transpiration rate. The most soluble compounds had the highest Ni uptake, with the exception of Ni3(PO4)2, Ni phyllosilicate, Ni-acid birnessite which showed a low solubility but a relatively high plant uptake and transpiration rate. In serpentine soils and insoluble NiO plant transpiration rate was high but uptake was very low and statistically comparable to the control.

Conclusions

It appears that Ni uptake is driven by convection, which depends on the initial concentration of Ni in solution and the plant transpiration rate.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. Abou-Shanab RA, Angle JS, Delorme TA, Chaney RL, Van Berkum P, Moawad H, Ghanem K, Ghozlan HA (2003) Rhizobacterial effects on nickel extraction from soil and uptake by Alyssum murale. New Phytol 158:219–224

    Article  CAS  Google Scholar 

  2. Allison JD, Brown DS, Novo-Gradac KJ (1991) MINTEQA2/PRODEFA2, a geochemical assessment model for environmental systems. U.S. Environmental Protection Agency

  3. Arai Y (2008) Spectroscopic evidence for Ni(II) surface speciation at the iron oxyhydroxides - Water interface. Environ Sci Technol 42:1151–1156

    PubMed  Article  CAS  Google Scholar 

  4. Bani A, Echevarria G, Sulce S, Morel JL, Mullai A (2007) In-situ phytoextraction of Ni by a native population of Alyssum murale on an ultramafic site (Albania). Plant Soil 293:79–89

    Article  CAS  Google Scholar 

  5. Bernal MP, McGrath SP, Miller AJ, Baker AJM (1994) Comparison of the chemical changes in the rhizosphere of the nickel hyperaccumulator Alyssum murale with the non-accumulator Raphanus sativus. Plant Soil 164:251–259

    Article  CAS  Google Scholar 

  6. Brooks RR (1987) Serpentine and its vegetation. A multidisciplinary approach. Dioscorides, Portland

    Google Scholar 

  7. 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 36:1429–1433

    PubMed  Article  CAS  Google Scholar 

  8. Decarreau A, Bonnin D, Badauttrauth D, Couty R, Kaiser P (1987) Synthesis and crystallogenesis of ferric smectite by evolution of the Si-Fe coprecipitates in oxidizing conditions. Clay Miner 22:207–223

    Article  CAS  Google Scholar 

  9. Depege C, ElMetoui FZ, Forano C, deRoy A, Dupuis J, Besse JP (1996) Polymerization of silicates in layered double hydroxides. Chem Mater 8:952–960

    Article  CAS  Google Scholar 

  10. Fellet G, Centofanti T, Chaney RL, Green CE (2009) NiO(s) (bunsenite) is not available to Alyssum species. Plant Soil 319:219–223

    Article  CAS  Google Scholar 

  11. Feng XH, Zhai LM, Tan WF, Liu F, He JZ (2007) Adsorption and redox reactions of heavy metals on synthesized Mn oxide minerals. Environ Pollut 147:366–373

    PubMed  Article  CAS  Google Scholar 

  12. Ford RG, Scheinost AC, Scheckel KG, Sparks DL (1999) The link between clay mineral weathering and the stabilization of Ni surface precipitates. Environ Sci Technol 33:3140–3144

    Article  CAS  Google Scholar 

  13. Genin P, Delahayevidal A, Portemer F, Tekaiaelhsissen K, Figlarz M (1991) Preparation and characterization of alpha-type nickel hydroxides obtained by chemical precipitation – Study of the anionic species. Eur J Solid State Inorg Chem 28:505–518

    CAS  Google Scholar 

  14. Gustafsson JP (2004) Visual MINTEQ v 2.30. Swedish Royal Institute of Technology (KTH)

  15. 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

    PubMed  Article  CAS  Google Scholar 

  16. Institute S (1989) SAS procedures guide, Version 6, 3rd edn. SAS Institute, Cary

    Google Scholar 

  17. 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

    PubMed  Article  CAS  Google Scholar 

  18. Li YM, Chaney RL, Brewer EP, Angle JS, Nelkin J (2003) Phytoextraction of nickel and cobalt by hyperaccumulator Alyssum species grown on nickel-contaminated soils. Environ Sci Technol 37:1463–1468

    Article  CAS  Google Scholar 

  19. Ma Y, Rajkumar M, Freitas H (2009) Improvement of plant growth and nickel uptake by nickel resistant-plant-growth promoting bacteria. J Hazard Mater 166:1154–1161

    PubMed  Article  CAS  Google Scholar 

  20. 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

    Article  CAS  Google Scholar 

  21. Massoura ST, Echevarria G, Becquer T, Ghanbaja J, Leclerc-Cessac E, Morel J-L (2006) Control of nickel availability by nickel bearing minerals in natural and anthropogenic soils. Geoderma 136:28–37

    Article  CAS  Google Scholar 

  22. McGrath SP, Shen ZG, Zhao FJ (1997) Heavy metal uptake and chemical changes in the rhizosphere of Thlaspi caerulescens and Thlaspi ochroleucum grown in contaminated soils. Plant Soil 188:153–159

    Article  CAS  Google Scholar 

  23. McKenzie RM (1971) Synthesis of birnessite, cryptomelane, and some other oxides and hydroxides of manganese. Mineral Mag 38:493–502

    Article  CAS  Google Scholar 

  24. McNear DH Jr, Chaney RL, Sparks DL (2007) The effects of soil type and chemical treatment on nickel speciation in refinery enriched soils: A multi-technique investigation. Geochimica et Cosmochimica Acta 71:2190–2208

    Article  CAS  Google Scholar 

  25. Milner MJ, Kochian LV (2008) Investigating heavy-metal hyperaccumulation using Thlaspi caerulescens as a model system. Ann Bot 102:3–13

    PubMed  Article  CAS  Google Scholar 

  26. Moradi AB, Conesa HM, Robinson BH, Lehmann E, Kaestner A, Schulin R (2009) Root responses to soil Ni heterogeneity in a hyperaccumulator and a non-accumulator species. Environ Pollut 157:2189–2196

    PubMed  Article  CAS  Google Scholar 

  27. Moradi AB, Oswald SE, Nordmeyer-Massner JA, Pruessmann KP, Robinson BH, Schulin R (2010) Analysis of nickel concentration profiles around the roots of the hyperaccumulator plant Berkheya coddii using MRI and numerical simulations. Plant Soil 328:291–302

    Article  CAS  Google Scholar 

  28. Nolan AL, Ma Y, Lombi E, McLaughlin MJ (2009) Speciation and isotopic exchangeability of nickel in soil solution. J Environ Qual 38:485–492

    PubMed  Article  CAS  Google Scholar 

  29. Parker DR, Chaney RL, Norvell WA (1995) Chemical equilibrium models: applications to plant nutrition research. Chemical equilibrium models: applications to plant nutrition research. In: Loeppert RH, Schwab AP, Goldberg S (eds) Chemical equilibrium and reaction models. Soil Science Society of America Special Publ. No. 42. Soil Sci. Soc. Am./Am. Soc. Agron., Madison, WI, pp 163–200

  30. Peltier E, Allada R, Navrotsky A, Sparks DL (2006) Nickel solubility and precipitation in soils: a thermodynamic study. Clays Clay Miner 54:153–164

    Article  CAS  Google Scholar 

  31. 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

    Article  CAS  Google Scholar 

  32. Reeves RD, Brooks RR, Dudley TR (1983) Uptake of nickel by species of Alyssum, Bornmuellera, and other genera of Old World Tribus Alysseae. Taxon 32:184–192

    Article  Google Scholar 

  33. Reeves RD, Baker AJM, Becquer T, Echevarria G, Miranda ZJG (2007) The flora and biogeochemistry of the ultramafic soils of Goiás state, Brazil. Plant Soil 293:107–119

    Article  CAS  Google Scholar 

  34. Scheinost AC, Sparks DL (2000) Formation of layered single- and double-metal hydroxide precipitates at the mineral/water interface: a multiple-scattering XAFS analysis. J Colloid Interface Sci 223:167–178

    PubMed  Article  CAS  Google Scholar 

  35. Schwartz C, Morel JL, Saumier S, Whiting SN, Baker AJM (1999) Root development of the zinc-hyperaccumulator plant Thlaspi caerulescens as affected by metal origin, content and localization in soil. Plant Soil 208:103–115

    Article  CAS  Google Scholar 

  36. Schwertmann U, Cornell RM (2000) Iron oxides in the laboratory: preparation and characterization, 2nd edn. Whiley-VCH, Weinheim

    Google Scholar 

  37. Shallari S, Echevarria G, Schwartz C, Morel JL (2001) Availability of nickel in soils for the hyperaccumulator Alyssum murale Waldst. & Kit. S Afr J Sci 97:568–570

    CAS  Google Scholar 

  38. Smith RM, Martell AE, Motekaitis RJ (2003) NIST critically selected stability constants of metal complexes database. NIST standard reference database 46, version 7.0. NIST, Gaithersburg, MD, USA

  39. Stumm W, Morgan JJ (1981) Aquatic chemistry, 2nd edn. Wiley, New York

    Google Scholar 

  40. Tan HK (2003) Humic matter in soil and the environment: principles and controversies. Marcel Dekker, Inc., New York

    Book  Google Scholar 

  41. Taylor RM (1984) The rapid formation of crystalline double hydroxy salts and other compounds by controlled hydrolysis. Clay Miner 19:591–603

    Article  CAS  Google Scholar 

  42. 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

    PubMed  Article  CAS  Google Scholar 

  43. Whiting SN, Leake JR, Mcgrath SP, Baker AJM (2000) Positive responses to Zn and Cd by roots of the Zn and Cd hyperaccumulator Thlaspi caerulescens. New Phytol 145:199–210

    Article  CAS  Google Scholar 

  44. Zhao FJ, Hamon RE, McLaughlin MJ (2001) Root exudates of the hyperaccumulator Thlaspi caerulescens do not enhance metal mobilization. New Phytol 151:613–620

    Article  CAS  Google Scholar 

  45. Zhou P, Yan H, Gu BH (2005) Competitive complexation of metal ions with humic substances. Chemosphere 58:1327–1337

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Dr. G. Echevarria for providing the garnierite and limonite soils from Brazil and Dr. C. Green for carrying out the ICP analyses.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Tiziana Centofanti.

Additional information

Responsible Editor: Juan Barcelo.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 283 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Centofanti, T., Siebecker, M.G., Chaney, R.L. et al. Hyperaccumulation of nickel by Alyssum corsicum is related to solubility of Ni mineral species. Plant Soil 359, 71–83 (2012). https://doi.org/10.1007/s11104-012-1176-9

Download citation

Keywords

  • Ni minerals
  • Alyssum
  • Hyperaccumulators
  • Ni solubility