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Determining the fluxes of ions (Pb2+, Cu2+ and Cd2+) at the root surface of wetland plants using the scanning ion-selective electrode technique

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Abstract

Background and aims

Measuring specific ion fluxes from different regions of the root under practical physiological conditions is crucial for understanding metal uptake mechanisms by plants.

Methods

We developed and tested a neutral carrier-based liquid-membrane Pb2+ and Cu2+ ion selective microelectrode (ISME) to investigate ion-transport processes along the roots of three common wetland plant species.

Results

The Pb2+ and Cu2+ ISME exhibited a Nernstian response with Pb2+ and Cu2+ activities as low as 1.0 nM and 1.0 μM in deionized water and simulated soil solution, respectively. Phragmites australis had a region of Cu2+ release for approximately the first 200 μm, while it exhibited Pb2+ and Cd2+ outward net flux up to the first 500 μm. Although in older sections of the root of Phragmites australis there were areas of influx of Cu2+, Pb2+ and Cd2+, the overall influx was much smaller than that of Typha latifolia or Canna indica. Such a reduced uptake and/or an increased efflux of metal ions across the root-cell plasma-membrane might explain the higher resistance of Phragmites australis to metals, at least in part.

Conclusions

The Pb2+ and Cu2+ ISMEs are shown to permit detailed investigation of heavy-metal ion transport in plant roots, especially for plants used for phytoremediation.

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References

  • Amman D, Chao P, Simon W (1987) Valinomycin-based K+ selective microelectrodes with low electrical membrane resistance. Neurosci Lett 74:221–226

    Article  Google Scholar 

  • Bakker E (1996) Determination of improved selectivity coefficients of polymer membrane ion-selective electrodes by conditioning with a discriminated ion. J Electrochem Soc 143:L83–L85

    Article  CAS  Google Scholar 

  • Bakker E (1997a) Selectivity of liquid membrane ion-selective electrodes. Electroanalysis 9:7–12

    Article  CAS  Google Scholar 

  • Bakker E (1997b) Determination of unbiased selectivity coefficients of neutral carrier-based cation-selective electrodes. Anal Chem 69:1061–1069

    Article  CAS  Google Scholar 

  • Ceresa A, Pretsch E (1999) Determination of formal complex formation constants of various Pb2+ ionophores in the sensor membrane phase. Anal Chim Acta 395:41–52

    Article  CAS  Google Scholar 

  • Ceresa A, Bakker E, Hattendorf B, Gunther D, Pretsch E (2001) Potentiometric polymeric membrane electrodes for measurement of environmental samples at trace levels: new requirements for selectivities and measuring protocols, and comparison with ICPMS. Anal Chem 73:343–351

    Article  CAS  PubMed  Google Scholar 

  • Deng H, Ye ZH, Wong MH (2004) Accumulation of lead, zinc, copper and cadmium by 12 wetland plant species thriving in metal-contaminated sites in China. Environ Pollut 132:29–40

    Article  CAS  PubMed  Google Scholar 

  • Dunbabin JS, Bowmer KH (1992) Potential use of constructed wetlands for treatment of industrial wastewaters containing metals. Sc Total Environ 111:151–168

    Article  CAS  Google Scholar 

  • Farrell RE, McArthur DFE, Van Rees KCJ (2005) Net Cd2+ flux at the root surface of durum wheat (Triticum turgidum L. Var. Durum) cultivars in relation to cultivar differences in Cd accumulation. Can J Plant Sci 85:103–107

    Article  CAS  Google Scholar 

  • Fitzgerald EJ, Caffrey JM, Nesaratna ST, McLoughlin P (2003) Copper and lead concentrations in salt marsh plants on the Suir estuary, Ireland. Environ Pollut 123:67–74

    Article  CAS  PubMed  Google Scholar 

  • Hoagland DR, Arnon DI (1938) The water-culture method for growing plants without soil. Circular 347, University of California, College of Agriculture, Berkeley

  • Kamata S, Onoyama K (1991) Lead-selective membrane electrode using methylene bis(diisobuty1dithiocarbamate) neutral carrier. Anal Chem 33:1295–1298

    Article  Google Scholar 

  • Kochian LV, Shaff JE, Kuhtreiber WM, Jaffe LF, Lucas WJ (1992) Use of an extracellular ionselective vibrating microelectrode system for the quantification of K+, H+ and Ca2+ fluxes in maize roots and maize suspension cells. Planta 188:601–610

    Article  CAS  PubMed  Google Scholar 

  • Kozłowska M, Jóźwiak A, Szpakowska B, Goliński P (2009) Biological aspects of cadmium and lead uptake by Phragmites australis (Cav. Trin ex Steudel) in natural water ecosystem. J Elem 14:299–312

    Google Scholar 

  • Kühtreibe WM, Jaffe LF (1990) Detection of extracellular calcium gradients with a calcium-specific vibrating electrode. J Cell Biol 110:1565–1573

    Article  Google Scholar 

  • Lerchi M, Bakker E, Rusterholz B, Simon W (1992) Lead-selective bulk optodes based on neutral ionophores with subnanomolar detection limits. Anal Chem 64:1534–1540

    Article  CAS  Google Scholar 

  • Li L, Liu X, Peijnenburg W, Zhao J, Chen X, Yu J, Wu H (2012) Pathways of cadmium fluxes in the root of the halophyte Suaeda salsa. Ecotoxicol Environ Saf 75:1–7

    Article  PubMed  Google Scholar 

  • Ma WW, Xu WZ, Xu H, Chen YS, He ZY, Ma M (2010) Nitric oxide modulates cadmium influx during cadmium-induced programmed cell death in tobacco BY-2 cells. Planta 232:325–335

    Article  CAS  PubMed  Google Scholar 

  • Mancuso S, Papeschi G, Marras AM (2000) A polarographic, oxygen-selective, vibrating microelectrode system for the spatial and temporal characterisation of transmembrane oxygen fluxes in plants. Planta 211:384–389

    Article  CAS  PubMed  Google Scholar 

  • Mancuso S, Marras AM, Magnus V, Baluska F (2005) Non invasive and continuous recordings of auxin fluxes in intact root apex with a carbon nanotube-modified and self-referencing microelectrode. Anal Biochem 341:344–351

    Article  CAS  PubMed  Google Scholar 

  • McLamore ES, Porterfield DM, Banks MK (2009) Non-invasive selfreferencing electrochemical sensors for quantifying real-time biofilm analyte flux. Biotechnol Bioeng 102:791–799

    Article  CAS  PubMed  Google Scholar 

  • McNaughton SJ, Folsom TC, Lee T, Park F, Price C, Roeder D, Schmitz J, Stockwell C (1974) Heavy metal tolerance in Typha latifolia without the evolution of tolerant races. Ecology 55:1163–1165

    Article  CAS  Google Scholar 

  • Migocka M, Papierniak A, Kosatka E, Klobus G (2011) Comparative study of the active cadmium efflux systems operating at the plasma membrane and tonoplast of cucumber root cells. J Exp Bot 62:4903–4916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Newman IA (2001) Ion transport in roots: measurement of fluxes using ion-selective microelectrodes to characterize transporter function. Plant Cell Environ 24:1–14

    Article  CAS  PubMed  Google Scholar 

  • Newman IA, Kochian LV, Grusak MA, Lucas WJ (1987) Fluxes of H+ and K+ in corn roots. Characterisation and stoichiometries using ion-selective microelectrodes. Plant Physiol 84:1177–1184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Papernik LA, Shaff JE, Jones DL (1996) Kochian LV (1996) use of vibrating ion selective microelectrodes to study the physiology of heavy metal transport into roots. Plant Physiol (rockville) 111(2 Suppl):54

    Google Scholar 

  • Papeschi G, Mancuso S, Marras AM (2000) Electrochemical behaviour of a Cu/CuSe microelectrode and its application in detecting temporal and spatial localization of copper (II) fluxes along Olea europaea roots. J Solid State Electrochem 4:325–329

    Article  CAS  Google Scholar 

  • Pineros MA, ShaV JE, Kochian V (1998) Development, characterization, and application of a cadmium-selective microelectrode for the measurement of cadmium fluxes in roots of Thlaspi species and wheat. Plant Physiol 116:1393–1401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rai PK (2008) Heavy metal pollution in aquatic ecosystems and its phytoremediation using wetland plants: an ecosustainable approach. Int J Phytoremediation 10:131–158

    PubMed  Google Scholar 

  • Ramos AC, Lima PT, Dias PN, Kasuya MCM, Feij o JA (2009) A pH signaling mechanism involved in the spatial distribution of calcium and anion fluxes in ectomycorrhizal roots. New Phytol 181: 448–462

  • Redjala T, Sterckeman T, Morel JL (2009) Cadmium uptake by roots: Contribution of apoplast and of high- and low-affinity membrane transport systems. Environ Exp Bot 67(1):235–242

    Article  CAS  Google Scholar 

  • Redjala T, Sterckeman T, Morel JL (2010) Determination of the different components of cadmium short-term uptake by roots. J Plant Nutr Soil Sci 173(6):935–945

    Article  CAS  Google Scholar 

  • Ryan PR, Newman IA, Arif I (1992) Rapid calcium exchange for protons and potassium in cell walls of Chara. Plant Cell Environ 15:675–683

    Article  CAS  Google Scholar 

  • Sasmaz A, Obek E, Hasar H (2008) The accumulation of heavy metals in Typha latifolia L. Grown in a stream carrying secondary treated effluent. Ecol Eng 33:278–284

    Article  Google Scholar 

  • Shabala S, Newman IA (1997) Proton and calcium flux oscillations in the elongation region correlate with root nutation. Physiol Plant 100:917–926

    Article  CAS  PubMed  Google Scholar 

  • Shabala S, Newman IA, Morris J (1997) Oscillations in H+ and Ca2+ ion fluxes around the elongation region of corn roots and effects of external pH. Plant Physiol 113:111–118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shamsipur M, Javanbakht M, Mousavi MF, Ganjali MR, Lippolis V, Garau A, Tei L (2001) Copper (II) -selective membrane electrodes based on some recently synthesized mixed aza-thioether crowns containing a 1, 10-phenanthroline sub-unit. Talanta 55:1047–1054

    Article  CAS  PubMed  Google Scholar 

  • Smith PJS, Sanger RH, Jaffe LF (1994) The vibrating Ca2+ electrode: a new technique for detecting plasma membrane regions of Ca2+ influx and efflux. Methods Cell Biol 40:115–134

    Article  CAS  PubMed  Google Scholar 

  • Smith PJ, Hammar K, Porterfield DM, Sanger RH, Trimarchi JR (1999) Self-referencing, non-invasive, ion selective electrode for single cell detection of trans-plasma membrane calcium flux. Microsc Res Tech 46:398–417

    Article  CAS  PubMed  Google Scholar 

  • Taylor GJ, Crowder AA (1983) Uptake and accumulation of heavy metals by Typha latifolia in wetlands of the Sudbury, Ontario region. Can J Bot 61:63–73

    Article  CAS  Google Scholar 

  • Taylor GJ, Crowder AA (1984) Copper and nickel tolerance in Typha latifolia clones from contaminated and uncontaminated environments. Can J Bot 62:1304–1308

    Article  CAS  Google Scholar 

  • Van der Werff M (1991) Common reed. In: Rozema, J.; Verkleij, J. A. C. Eds. Ecological responses to environmental stress. Dordrecht, the Netherlands, Kluwer Academic Publishers, 1991, 172–182

  • van Hoof NALM, Koevoets PLM, Hakvoort HWJ, Bookum WM, Schate H, Verkleij JAC, Ernst WHO (2001) Enhanced ATP-dependent copper efflux across the root cell plasma membrane in copper-tolerant Silene vulgaris. Physiol Plant 113:225–232

    Article  PubMed  Google Scholar 

  • Wenzel WW (2009) Rhizosphere processes and management in plant-assisted bioremediation (phytoremediation) of soils. Plant Soil 321:385–408

    Article  CAS  Google Scholar 

  • Wu SC, Horng JL, Liu ST, Hwang PP, Wen ZH, Lin CS, Lin LY (2010) Ammonium-dependent sodium uptake in mitochondrion-rich cells of medaka (Oryzias latipes) larvae. Am J Physiol Cell Physiol 298:C237–C250

    Article  CAS  PubMed  Google Scholar 

  • Ye ZH (1995) Heavy metal tolerance, uptake and accumulation in populations of Typha latifolia L. and Phragmites australis (Cav.) Trin. ex Steudel. PhD Thesis, University of Sheffield, UK

  • Ye ZH, Chen GZ, Lan CY, Li LC (1992a) Effect of treating Pb/Zn mine wastewater with T. latifolia purification pond system. Chinese Journal of Applied Eco 3:190–194 [in Chinese]

    Google Scholar 

  • Ye ZH, Chen GZ, Lan CY, Li LC (1992b) The accumulation and distribution of heavy metals in Typha latifolia from Pb/Zn mine waste water. Acta Phytoecologica et Geobotanica Sinica 16:72–79 [in Chinese]

    Google Scholar 

  • Ye ZH, Baker AJ, Wong MH, Willis AJ (1997a) Zinc, lead and cadmium tolerance, uptake and accumulation by the common reed, Phragmites australis (Cav.) Trin. Ex Steudel. Ann Bot 80:363–370

    Article  CAS  Google Scholar 

  • Ye ZH, Baker AJ, Wong MH, Willis AJ (1997b) Zinc, lead and cadmium tolerance, uptake and accumulation by Typha latifolia. New Phytol 136:469–480

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study is supported by the National Natural Science Foundation (No. Y311111031 and 41230858), a grant from the National High Technology Research and Development Program of China (863 Program) (2012AA06A204-4) and the Scientific Research Equipments Development Program of CAS (YZ201558). This is also supported by the project of “Research on Migration/Transformation and Safety Threshold of Heavy Metals in Farmland Systems” (2016YFD0800405), National Key Research and Development Program of China. We want to thank Dr. Ian Newman and Dr. Sergey Shabala from University of Tasmania, Australia and Prof. Peter J S Smith from University of Southampton, UK for their valuable comments in the improvement of the manuscript. The authors also thank Prof. Michael O’Donnell from McMaster University for his constructive comments on an earlier version of the manuscript.

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Authors and Affiliations

  1. Key Laboratory of Coastal Zone Environmental Processes and Ecological Remediation, Yantai Institute of Coastal Zone Research (YIC), Chinese Academy of Sciences (CAS); Shandong Provincial Key Laboratory of Coastal Zone Environmental Processes, YICCAS, No.17, Chunhui Road, Yantai, 264003, People’s Republic of China

    Lian-Zhen Li, Shun-Yang Yu & Yong-Ming Luo

  2. Laboratory for Ecological Risk Assessment, National Institute of Public Health and the Environment, P.O. Box 1, 3720, BA, Bilthoven, The Netherlands

    Willie J. G. M. Peijnenburg

  3. Institute of Environmental Sciences (CML), Leiden University, Leiden, The Netherlands

    Willie J. G. M. Peijnenburg

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  1. Lian-Zhen Li
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  2. Shun-Yang Yu
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  3. Willie J. G. M. Peijnenburg
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  4. Yong-Ming Luo
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Correspondence to Yong-Ming Luo.

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Responsible Editor: Robert Reid.

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Li, LZ., Yu, SY., Peijnenburg, W.J.G.M. et al. Determining the fluxes of ions (Pb2+, Cu2+ and Cd2+) at the root surface of wetland plants using the scanning ion-selective electrode technique. Plant Soil 414, 1–12 (2017). https://doi.org/10.1007/s11104-016-3109-5

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  • DOI: https://doi.org/10.1007/s11104-016-3109-5

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