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Silver ions increase plasma membrane permeability through modulation of intracellular calcium levels in tobacco BY-2 cells

Plant Cell Reports volume 37, pages 809–818 (2018)Cite this article

Abstract

Key message

Silver ions increase plasma membrane permeability for water and small organic compounds through their stimulatory effect on plasma membrane calcium channels, with subsequent modulation of intracellular calcium levels and ion homeostasis.

Abstract

The action of silver ions at the plant plasma membrane is largely connected with the inhibition of ethylene signalling thanks to the ability of silver ion to replace the copper cofactor in the ethylene receptor. A link coupling the action of silver ions and cellular auxin efflux has been suggested earlier by their possible direct interaction with auxin efflux carriers or by influencing plasma membrane permeability. Using tobacco BY-2 cells, we demonstrate here that besides a dramatic increase of efflux of synthetic auxins 2,4-dichlorophenoxyacetic acid (2,4-D) and 1-naphthalene acetic acid (NAA), treatment with AgNO3 resulted in enhanced efflux of the cytokinin trans-zeatin (tZ) as well as the auxin structural analogues tryptophan (Trp) and benzoic acid (BA). The application of AgNO3 was accompanied by gradual water loss and plasmolysis. The observed effects were dependent on the availability of extracellular calcium ions (Ca2+) as shown by comparison of transport assays in Ca2+-rich and Ca2+-free buffers and upon treatment with inhibitors of plasma membrane Ca2+-permeable channels Al3+ and ruthenium red, both abolishing the effect of AgNO3. Confocal microscopy of Ca2+-sensitive fluorescence indicator Fluo-4FF, acetoxymethyl (AM) ester suggested that the extracellular Ca2+ availability is necessary to trigger the response to silver ions and that the intracellular Ca2+ pool alone is not sufficient for this effect. Altogether, our data suggest that in plant cells the effects of silver ions originate from the primal modification of the internal calcium levels, possibly by their interaction with Ca2+-permeable channels at the plasma membrane.

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Acknowledgements

The work was supported by the Ministry of Education, Youth and Sports of Czech Republic, Project MSM/LO1417 (JP), Czech Science Foundation Project GA16-10948S (PK, ML, JP) and by a grant from Ghent University (Bijzonder Onderzoeksfonds, Bilateral Cooperation, BILA-06) to DVDS. FV was a post-doctoral fellow of the Fund for Scientific Research—Flanders (FWO). IEB Imaging Facility is supported by Operational Programme Prague—Competitiveness, Project No. CZ.2.16/3.1.00/21519. The authors would like to thank Dr. Edita Tylová for her critical reading of the manuscript.

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  1. Petr Klíma and Martina Laňková contributed equally to this paper.

Authors and Affiliations

  1. Laboratory of Hormonal Regulations in Plants, Institute of Experimental Botany of the Czech Academy of Sciences, Rozvojová 263, 165 02, Prague 6, Czech Republic

    Petr Klíma, Martina Laňková & Jan Petrášek

  2. Laboratory of Functional Plant Biology, Department of Biology, Ghent University, K. L. Ledeganckstraat 35, Ghent, Belgium

    Filip Vandenbussche & Dominique Van Der Straeten

  3. Department of Experimental Plant Biology, Faculty of Science, Charles University, Viničná 5, 128 44, Prague 2, Czech Republic

    Jan Petrášek

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  1. Petr Klíma
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  2. Martina Laňková
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Correspondence to Jan Petrášek.

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Communicated by Attila Feher.

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Klíma, P., Laňková, M., Vandenbussche, F. et al. Silver ions increase plasma membrane permeability through modulation of intracellular calcium levels in tobacco BY-2 cells. Plant Cell Rep 37, 809–818 (2018). https://doi.org/10.1007/s00299-018-2269-6

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  • DOI: https://doi.org/10.1007/s00299-018-2269-6

Keywords

  • Silver ions
  • Calcium
  • Tobacco BY-2 cells
  • Transmembrane transport
  • Ethylene
  • Auxin