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Emergent Oscillatory Properties in Modelling Ion Transport of Guard Cells

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Rhythms in Plants

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Abstract

Transport across eukaryotic cell membranes, including those of plant cells, is so complex that it defies intuitive understanding. Quantitative systems modelling is essential in these circumstances, to test our understanding of the system through the experimental scrutiny of predictions. OnGuard is the first, fully integrated and quantitative modelling package developed for the study of cellular homoeostasis in guard cells and its relevance to stomatal aperture dynamics. It offers a unique tool for exploring the properties arising from interactions between plasma membrane and tonoplast transporters with the processes involved in the control of pH, ionic and neutral osmolite concentrations, membrane potentials and ion buffering in cytoplasm and vacuole. OnGuard has already yielded detail sufficient to guide phenotypic and mutational studies, opening the way towards ‘reverse-engineering’ of stomatal guard cells with the aim of improving water-use efficiency. We focus here on the fundamental insights OnGuard models offer for understanding the physiological phenomena of oscillations in membrane voltage, cytosolic-free Ca2+ concentration, and their roles in stomatal movements. OnGuard models faithfully reproduce differences in stomatal closure with oscillation frequency, much as observed in vivo and including an optimal cycle period. Analysis shows that these oscillations arise from the balance of transport activities at the plasma membrane and tonoplast to generate a range of resonant frequencies. The lowest frequencies are of sufficient duration to permit substantial changes in cytosolic-free Ca2+ concentration. Thus, we demonstrate the oscillations as an emergent property of the system of transport at the two dominant membranes of the guard cell.

Carla Minguet-Parramona and Yizhou Wang are co-first authors

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Acknowledgments

This work was supported by BBSRC grants BB/L019205/1 and BB/M001601/1 to MRB, BB/L001276/1 to MRB and SR, BB/I001187/1 to HG and TL, and EU OPTIMA project 289642 PhD studentship to CM-P.

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Authors and Affiliations

  1. Laboratory of Plant Physiology and Biophysics, University of Glasgow, Bower Building, Glasgow, G12 8QQ, UK

    Carla Minguet-Parramona, Yizhou Wang, Adrian Hills & Michael R. Blatt

  2. Biological Sciences, University of Essex, Wivenhoe Park, Colchester, CO4 3SQ, UK

    Silvere Vialet-Chabrand & Tracy Lawson

  3. Plant Sciences, University of Cambridge, Downing Street, Cambridge, CB2 3EA, UK

    Howard Griffiths

  4. Physiological Laboratory, University of Cambridge, Downing Street, Cambridge, CB2 3EG, UK

    Virgilio Lew

  5. Computing Science, University of Glasgow, Alwyn Williams Building, Glasgow, G12 8QQ, UK

    Simon Rogers

Authors
  1. Carla Minguet-Parramona
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  2. Yizhou Wang
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  3. Adrian Hills
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  4. Silvere Vialet-Chabrand
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  5. Howard Griffiths
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  6. Simon Rogers
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  7. Tracy Lawson
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  8. Virgilio Lew
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  9. Michael R. Blatt
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Corresponding author

Correspondence to Michael R. Blatt .

Editor information

Editors and Affiliations

  1. Dipartimento di Scienze delle Produzioni Agroalimentari e dell'Ambiente, LINV–International Lab for Plant Neurobiology, University of Florence, Sesto Fiorentino, Italy

    Stefano Mancuso

  2. School of Land and Food, University of Tasmania, Hobart, Tasmania, Australia

    Sergey Shabala

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Minguet-Parramona, C. et al. (2015). Emergent Oscillatory Properties in Modelling Ion Transport of Guard Cells. In: Mancuso, S., Shabala, S. (eds) Rhythms in Plants. Springer, Cham. https://doi.org/10.1007/978-3-319-20517-5_12

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