Skip to main content
Log in

Evaluating mechanisms for plant-ion (Ca2+, Cu2+, Cd2+ or Ni2+) interactions and their effectiveness on rhizotoxicity

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

Abstract

Electrical properties of plant cell membranes (CMs) provide a new avenue for exploring the mechanisms of plant-ion interactions and the biotic effects of ions. The modulating effect of Ca2+ on rhizotoxicity of metallic ions was studied to evaluate the mechanisms of plant-ion interaction in terms of the electrical potential at the CM exterior surface CMSe o0 ). Adding Ca2+ to root bathing media (BM) reduced the negativity of ψ o0 at the CMSe. This reduction caused decreases in the activities of toxic metal ions at the CMSe and hence alleviated the toxicity (denoted as Mechanism I). Calcium is an essential element for growth and adding Ca2+ could also restore metal-displaced Ca2+ at the CMSe and alleviated Ca2+ deficiency (Mechanism II). The reduced surface negativity increased the surface-to-surface transmembrane potential difference (E m,surf), thus increasing the electrical driving force for transport of toxic metallic ions across the CM (Mechanism III). The Mechanism III would increase toxicity, but did not offset the alleviation by Mechanisms I and II. Regression analysis of relative root elongation in appropriate nonlinear equations incorporating the effects of above mechanisms provided evidence that under the current experimental conditions, Mechanism I is the most important mechanism for plant-ion interactions. In addition, the intracellular concentration of metals in root was a better predictor of toxicity than the free metal ion activity in the BM and could be predicted with an electrostatic uptake model developed previously. Based on the intracellular concentration and the EUM, the toxicity threshold (EC50, activities producing 50% growth inhibition) could be predicted generally within a factor of 2 of the observed values, indicting its potential utility in risk assessment of toxic metals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

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

Abbreviations

CMSe :

cell membrane exterior surface

BM:

bathing medium

EUM:

electrostatic uptake model

BLM:

biotic ligand model

G-C-S model:

Gouy-Chapman-Stern model

RRL:

relative root length

T :

toxicant intensity

ψ o0 :

cell membrane surface electrical potential

E m,surf :

the electrical potential difference from membrane surface to membrane surface

E m :

transmembrane electrical potential difference between the cell interior and bathing medium

σ0 :

membrane surface charge densities

{I Z}b :

the activity of ion I Z in the bathing medium

{I Z} o0 :

the activity of ion I Z at the cell membrane exterior surface

References

  • Antunes PMC, Berkelaar EJ, Boyle D, Hale BA, Hendershot W, Voigt A (2006) The biotic ligand model for plants and metals: technical challenges for field application. Environ Toxicol Chem 25:875–882

    Article  CAS  PubMed  Google Scholar 

  • De Schamphelaere KAC, Koene JM, Heijerick DG, Janssen CR (2008) Reduction of growth and haemolymph Ca levels in the freshwater snail Lymnaea stagnalis chronically exposed to cobalt. Ecotox Environ Safe 71:65–70

    Article  Google Scholar 

  • Di Toro DM, Allen HE, Bergman HL, Meyer JS, Paquin PR, Santore RC (2001) Biotic ligand model of the acute toxicity of metals. 1. Technical basis. Environ Toxicol Chem 20:2383–2396

    Article  PubMed  Google Scholar 

  • Gibrat R, Grouzis JP, Rigaud J, Grignon C (1985) Electrostatic characteristics of corn root plasmalemma: Effect on the Mg2+-ATPase activity. Biochim Biophys Acta-Biomembr 816:349–357

    Article  CAS  Google Scholar 

  • Haanstra L, Doelman P, Voshaar JHO (1985) The use of sigmoidal dose response curves in soil ecotoxicological research. Plant Soil 84:293–297

    Article  CAS  Google Scholar 

  • Kinraide TB (1994) Use of a Gouy-Chapman-Stern model for membrane-surface electrical potential to interpret some features of mineral rhizotoxicity. Plant Physiol 106:1583–1592

    CAS  PubMed  Google Scholar 

  • Kinraide TB (1998) Three mechanisms for the calcium alleviation of mineral toxicities. Plant Physiol 118:513–520

    Article  CAS  PubMed  Google Scholar 

  • Kinraide TB (1999) Interactions among Ca2+, Na+ and K+ in salinity toxicity: Quantitative resolution of multiple toxic and ameliorative effects. J Exp Bot 50:1495–1505

    Article  CAS  Google Scholar 

  • Kinraide TB (2001) Ion fluxes considered in terms of membrane-surface electrical potentials. Aust J Plant Physiol 18:605–616

    Google Scholar 

  • Kinraide TB (2003) The controlling influence of cell-surface electrical potential on the uptake and toxicity of selenate (SeO42-). Physiol Plant 117:64–71

    Google Scholar 

  • Kinraide TB (2006) Plasma membrane surface potential (PM) as a determinant of ion bioavailability: a critical analysis of new and published toxicological studies and a simplified method for the computation of plant PM. Environ Toxicol Chem 25:3188–3198

    Article  CAS  PubMed  Google Scholar 

  • Kinraide TB, Yermiyahu U (2007) A scale of metal ion binding strengths correlating with ionic charge, Pauling electronegativity, toxicity, and other physiological effects. J Inorg Biochem 101:1201–1213

    Article  CAS  PubMed  Google Scholar 

  • Kinraide TB, Ryan PR, Kochian LV (1992) Interactive Effects of Al3+, H+, and other cations on root elongation considered in terms of cell-surface electrical potential. Plant Physiol 99:1461–1468

    Article  CAS  PubMed  Google Scholar 

  • Kinraide TB, Ryan PR, Kochian LV (1993) Al3+-Ca2+ interactions in aluminum rhizotoxicity. II: evaluating the Ca2+-displacement hypothesis. Planta 192:104–110

    Article  Google Scholar 

  • Kinraide TB, Yermiyahu U, Rytwo G (1998) Computation of surface electrical potentials of plant cell membranes. Correspondence to published Zeta potentials from diverse plant sources. Plant Physiol 118:505–512

    Article  CAS  PubMed  Google Scholar 

  • Kinraide TB, Pedler JF, Parker DR (2004) Relative effectiveness of calcium and magnesium in the alleviation of rhizotoxicity in wheat induced by copper, zinc, aluminum, sodium, and low pH. Plant Soil 259:201–208

    Article  CAS  Google Scholar 

  • Peijnenburg WJGM, Posthuma L, Eijsackers HJP, Allen HE (1997) A conceptual framework for implementation of bioavailability of metals for environmental management purposes. Ecotox Environ Safe 37:163–172

    Article  CAS  Google Scholar 

  • Reid RJ, Tester MA, Smith FA (1995) Calcium/aluminium interactions in the cell wall and plasma membrane of chara. Planta 195:362–368

    CAS  Google Scholar 

  • Rooney CP, Zhao FJ, McGrath SP (2007) Phytotoxicity of nickel in a range of European soils: Influence of soil properties, Ni solubility and speciation. Environ Pollut 145:596–605

    Article  CAS  PubMed  Google Scholar 

  • Ryan PR, Kinraide TB, Kochian LV (1993) Al3+-Ca2+ interactions in aluminum rhizotoxicity. I: Inhibition of root growth is not caused by reduction of calcium uptake. Planta 192:98–103

    Article  Google Scholar 

  • Ryan PR, Reid RJ, Smith FA (1997) Direct evaluation of the Ca2+-displacement hypothesis for Al toxicity. Plant Physiol 113:1351–1357

    CAS  PubMed  Google Scholar 

  • Schwab AP (2000) The soil solution. In: Sumner ME (ed) Handbook of soil science. CRC Press, New York

    Google Scholar 

  • Slaveykova VI, Wilkinson KJ (2005) Predicting the bioavailability of metals and metal complexes: Critical review of the biotic ligand model. Environ Chem 2:9–24

    Article  CAS  Google Scholar 

  • Tatulian SA (1999) Surface electrostatics of biological membranes and ion binding. Dekker, New York, pp 871–922

    Google Scholar 

  • Wang P, Zhou DM, Kinraide TB, Luo XS, Li LZ, Li DD, Zhang HL (2008) Cell membrane surface potential (ψ0) plays a dominant role in the phytotoxicity of copper and arsenate. Plant Physiol 148:2134–2143

    Article  CAS  PubMed  Google Scholar 

  • Wang P, Zhou DM, Li LZ, Luo XS (2010) Evaluating the biotic ligand model for toxicity and the alleviation of toxicity in terms of cell membrane surface potential. Environ Toxicol Chem. doi:10.1002/etc.186

    Google Scholar 

  • Weng LP, Wolthoorn A, Lexmond TM, Temminghoff EJM, Van Riemsdijk WH (2004) Understanding the effects of soil characteristics on phytotoxicity and bioavailability of nickel using speciation models. Environ Sci Technol 38:156–162

    Article  CAS  PubMed  Google Scholar 

  • Wu Y (2007) Bioavailability and rhizotoxicity of trace metals to pea: Development of a terrestrial biotic ligand model. In Department of Natural Resource Sciences. Mcgill University, Ottawa, Canada

  • Yermiyahu U, Nir S, Ben-Hayyim G, Kafkafi U, Kinraide TB (1997a) Root elongation in saline solution related to calcium binding to root cell plasma membranes. Plant Soil 191:67–76

    Article  CAS  Google Scholar 

  • Yermiyahu U, Rytwo G, Brauer DK, Kinraide TB (1997b) Binding and electrostatic attraction of lanthanum (La3+) and aluminum (Al3+) to wheat root plasma membranes. J Membr Biol 159:239–252

    Article  CAS  PubMed  Google Scholar 

  • Yermiyahu U, Kinraide TB, Huang PM and Gobran GR (2005) Binding and electrostatic attraction of trace elements to plant root surfaces. In Biogeochemistry of Trace Elements in the Rhizosphere. Elsevier, Amsterdam, pp 365–389

  • Zhang Q, Smith FA, Sekimoto H, Reid RJ (2001) Effect of membrane surface charge on nickel uptake by purified mung bean root protoplasts. Planta 213:788–793

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors are grateful for the help and discussion from Dr. Thomas Kinraide (U.S. Department of Agriculture). This work was supported financially by the National Natural Science Foundation (Grant No. 40871115; 40930739), the Natural Science Foundation of Jiangsu Province (Grant No. BK 2009339) and the Graduate Innovative Program of Graduate School of Chinese Academy of Sciences.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dong-Mei Zhou.

Additional information

Responsible Editor: Robert Reid.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, P., Zhou, DM., Peijnenburg, W.J.G.M. et al. Evaluating mechanisms for plant-ion (Ca2+, Cu2+, Cd2+ or Ni2+) interactions and their effectiveness on rhizotoxicity. Plant Soil 334, 277–288 (2010). https://doi.org/10.1007/s11104-010-0381-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-010-0381-7

Keywords