Skip to main content
SpringerLink
Log in

Theoretical Analysis of the Influence of Fluctuations in the Activity of the Plasma Membrane H+-ATPase on Low-Temperature-Induced Electrical Responses in a Plant Cell

  • Published:
Biochemistry (Moscow), Supplement Series A: Membrane and Cell Biology Aims and scope

Abstract

Fluctuations in physiological processes are a key property of biosystems; these fluctuations can play both positive and negative roles in living organisms. In particular, fluctuations in the activity of ion channels can increase sensitivity of the receptors and modulate the activity of neural networks. At the same time, a possible influence of fluctuations on the electrical activity in plants has not been investigated as yet. The aim of this work was a theoretical analysis of the influence of fluctuations in the plasma membrane H+‑ATPase activity on the low-temperature-induced electrical responses in a plant cell. The mathematical model of plant electrogenesis developed by the authors earlier, which was modified by description of fluctuations in the H+-ATPase activity, was used in this study. Fluctuations in the H+-ATPase activity were described by multiplying the H+ flux through the H+-ATPase by an additional random value with a normal distribution (its specific values were recalculated every 1 s; the mean value was 1). The analysis of the model has shown that an increase in the magnitude of fluctuations in the H+-ATPase activity was accompanied by (i) a non-linear increase of fluctuations in the membrane potential at rest; (ii) a decrease in the threshold of generation of simulated action potential when analyzing individual cells simulated by the model; and (iii) modification of low-temperature-induced changes in the membrane potential when averaging electrical activity over a large sample of cells. The obtained results theoretically predict that fluctuations in the H+-ATPase activity can decrease the threshold of generation of electrical responses in a plant cell upon cooling.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.
Fig. 8.

Similar content being viewed by others

REFERENCES

  1. Opritov V.A., Piatigin S.S., Retivin V.G. 1991. Bioelectrogenez vysshikh rasteniy (Bioelectrogenesis in high plants). Moscow: Nauka.

  2. Pyatygin S. S. 2003. Electrogenesis of plant cells under stress. Uspekhi Sovremennoy Biologii (Rus.).123, 552–562.

    Google Scholar 

  3. Krol E., Dziubińska H., Trebacz K. 2004. Low-temperature-induced transmembrane potential changes in mesophyll cells of Arabidopsis thaliana, Helianthus annuus and Vicia faba.Physiol. Plant.120, 265–270.

    Article  CAS  PubMed  Google Scholar 

  4. Zatsepina G.N., Bezmaternykh P.M., Kolomiets A.A., Tulsky C.B., Tsaplev Yu.B. 1992. Electricheskaya systema regulatsii protsessov zhiznedeyatel’nosti (Electrical system of regulation of life processes). Moscow: MSU Publishing house.

  5. Zatsepina G.N., Tsaplev Yu.B. 1987. Dependence of tradescantia roots regeneration from pH, the amplitude of variable potential and constant electric field of the plant. Biofizika (Rus.). 32, 492–495.

    Google Scholar 

  6. Zatsepina G.N., Kolomiets A.A., Ponomarev E.E. 1991. Correlation between the constant electric field of the sour cherry stalk and the physiological state of the plant. Biofizika (Rus.). 36, 895–898.

    Google Scholar 

  7. Zatsepina G. N., Tsogbadrakh M., Tulsky C. B. 1991. Influence of a constant electric field and pH of the solution washing the roots on the regeneration process of the leaf and root of phyllocactus. Biofizika (Rus.). 36, 133–136.

    Google Scholar 

  8. Davies E. 2006. Electrical signals in plants: Facts and hypotheses. In: Plant electrophysiology. Theory and methods. Ed. Volkov A.G. Berlin, Heidelberg, New York: Springer-Verlag, p. 407–422.

    Google Scholar 

  9. Fromm J., Lautner S. 2007. Electrical signals and their physiological significance in plants. Plant. Cell. Environ. 30, 249–257.

    Article  CAS  PubMed  Google Scholar 

  10. Sukhov V. 2016. Electrical signals as mechanism of photosynthesis regulation in plants. Photosynth. Res.130, 373–387.

    Article  CAS  PubMed  Google Scholar 

  11. Sukhov V., Sukhova E., Vodeneev V. 2019. Long-distance electrical signals as a link between the local action of stressors and the systemic physiological responses in higher plants. Progr. Biophys. Mol. Biol.146, 63–84.

    Article  CAS  Google Scholar 

  12. Peña-Cortés H., Fisahn J., Willmitzer L. 1995. Signals involved in wound-induced proteinase inhibitor II gene expression in tomato and potato plants. Proc. Natl. Acad. Sci. USA.92, 4106–4113.

    Article  PubMed  Google Scholar 

  13. Mousavi S.A., Chauvin A., Pascaud F., Kellenberger S., Farmer E.E. 2013. Glutamate receptor-like genes mediate leaf-to-leaf wound signalling. Nature. 500, 422–426.

    Article  CAS  PubMed  Google Scholar 

  14. Hlavácková V., Krchnák P., Naus J., Novák O., Spundová M., Strnad M. 2006. Electrical and chemical signals involved in short-term systemic photosynthetic responses of tobacco plants to local burning. Planta. 225, 235–244.

    Article  PubMed  CAS  Google Scholar 

  15. Hlavinka J., Nožková-Hlaváčková V., Floková K., Novák O., Nauš J. 2012. Jasmonic acid accumulation and systemic photosynthetic and electrical changes in locally burned wild type tomato, ABA-deficient sitiens mutants and sitiens pre-treated by ABA. Plant Physiol. Biochem.54, 89–96.

    Article  CAS  PubMed  Google Scholar 

  16. Krausko M., Perutka Z., Šebela M., Šamajová O., Šamaj J., Novák O., Pavlovič A. 2017. The role of electrical and jasmonate signalling in the recognition of captured prey in the carnivorous sundew plant Drosera capensis.New Phytol. 213, 1818–1835.

    Article  CAS  PubMed  Google Scholar 

  17. Pavlovič A., Jakšová J., Novák O. 2017. Triggering a false alarm: Wounding mimics prey capture in the carnivorous Venus flytrap (Dionaea muscipula). New Phytol. 216, 927–938.

    Article  PubMed  CAS  Google Scholar 

  18. Krupenina N.A., Bulychev A.A. 2007. Action potential in a plant cell lowers the light requirement for non-photochemical energy-dependent quenching of chlorophyll fluorescence. Biochim. Biophys. Acta.1767, 781–788.

    Article  CAS  PubMed  Google Scholar 

  19. Krupenina N.A., Bulychev A.A., Roelfsema M.R.G., Schreiber U. 2008. Action potential in Chara cells intensifies spatial patterns of photosynthetic electron flow and non-photochemical quenching in parallel with inhibition of pH banding. Photochem. Photobiol. Sci.7, 681–688.

    Article  CAS  PubMed  Google Scholar 

  20. Pavlovič A., Slováková L., Pandolfi C., Mancuso S. 2011. On the mechanism underlying photosynthetic limitation upon trigger hair irritation in the carnivorous plant Venus flytrap (Dionaea muscipula Ellis). J. Exp. Bot.62, 1991–2000.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Sukhov V., Sherstneva O., Surova L., Katicheva L., Vodeneev V. 2014. Proton cellular influx as a probable mechanism of variation potential influence on photosynthesis in pea. Plant. Cell. Environ.37, 2532–2541.

    Article  CAS  PubMed  Google Scholar 

  22. Sukhova E., Mudrilov M., Vodeneev V., Sukhov V. 2018. Influence of the variation potential on photosynthetic flows of light energy and electrons in pea. Photosynth. Res. 136, 215–228.

    Article  CAS  PubMed  Google Scholar 

  23. Kaiser H., Grams T.E., 2006. Rapid hydropassive opening and subsequent active stomatal closure follow heat-induced electrical signals in Mimosa pudica.J. Exp. Bot.57, 2087–2092.

    Article  CAS  PubMed  Google Scholar 

  24. Surova L. M., Sherstneva O. N., Mysiagin S. A., Vodeneev V. A., Sukhov V. S. 2019. The effect of local damage on the transpiration of pea leaves at different air humidity. Fiziologiya rasteniy (Rus.). 66, 58–65.

  25. Filek M., Kościelniak J. 1997. The effect of wounding the roots by high temperature on the respiration rate of the shoot and propagation of electric signal in horse bean seedlings (Vicia faba L. minor). Plant Sci. 123, 39–46.

    Article  CAS  Google Scholar 

  26. Surova L., Sherstneva O., Vodeneev V., Katicheva L., Semina M., Sukhov V. 2016. Variation potential-induced photosynthetic and respiratory changes increase ATP content in pea leaves. J. Plant Physiol.202, 57–64.

    Article  CAS  PubMed  Google Scholar 

  27. Sukhov V., Surova L., Sherstneva O., Vodeneev V. 2014. Influence of variation potential on resistance of the photosynthetic machinery to heating in pea. Physiol. Plant.152, 773–783.

    Article  CAS  PubMed  Google Scholar 

  28. Sukhov V., Surova L., Sherstneva O., Bushueva A., Vodeneev V. 2015. Variation potential induces decreased PSI damage and increased PSII damage under high external temperatures in pea. Funct. Plant. Biol.42, 727–736.

    Article  PubMed  Google Scholar 

  29. Surova L., Sherstneva O., Vodeneev V., Sukhov V. 2016. Variation potential propagation decreases heat-related damage of pea photosystem I by 2 different pathways. Plant Sign. Behav. 11, e1145334.

    Article  CAS  Google Scholar 

  30. Sukhov V., Gaspirovich V., Mysyagin S., Vodeneev V. 2017. High-temperature tolerance of photosynthesis can be linked to local electrical responses in leaves of pea. Front. Physiol. 8, 763.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Felle H.H., Zimmermann M.R. 2007. Systemic signalling in barley through action potentials. Planta. 226, 203–214.

    Article  CAS  PubMed  Google Scholar 

  32. Vodeneev V., Akinchits E., Sukhov V. 2015. Variation potential in higher plants: Mechanisms of generation and propagation. Plant. Signal. Behav.10, e1057365.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Vodeneev V. A., Opritov V. A., Pyatygin S. S. 2006. Reversible change in intracellular pH when generating an action potential in the higher plant Cucurbita pepo. Fiziologiya rasteniy (Rus.). 53, 538–545.

  34. Zimmermann M.R., Maischak H., Mithöfer A., Boland W., Felle H.H. 2009. System potentials, a novel electrical long-distance apoplastic signal in plants, induced by wounding. Plant Physiol. 149, 1593–1600.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Zimmermann M.R., Mithöfer A., Will T., Felle H.H., Furch A.C. 2016. Herbivore-triggered electrophysiological reactions: Candidates for systemic signals in higher plants and the challenge of their identification. Plant Physiol. 170, 2407–2419.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Sukhov V., Sherstneva O., Surova L., Katicheva L., Vodeneev V. 2014. Proton cellular influx as a probable mechanism of variation potential influence on photosynthesis in pea. Plant. Cell. Environ.37, 2532–2541.

    Article  CAS  PubMed  Google Scholar 

  37. Sherstneva O.N., Vodeneev V.A., Katicheva L.A., Surova L.M., Sukhov V.S. 2015. Participation of changes in intra- and extracellular pH in the development of photosynthetic response caused by variable potential in pumpkin seedlings. Biokhimiya (Rus.). 8, 920–930.

    Google Scholar 

  38. Sherstneva O. N., Surova L. M., Vodeneev V. A., Plotnikova Yu. I., Bushueva A.V., Sukhov V. S. 2015. The role of intracellular and extracellular protons in inducing photosynthetic response by variable potential in pea seedlings. Biol. membrany (Rus.). 32, 446–454.

  39. Sherstneva O.N., Vodeneev V.A., Surova L.M., Novikova E.M., Sukhov V.S. 2016. Using a mathematical model of variable potential to analyze its effect on photosynthesis in higher plants. Biol. membrany (Rus.). 33, 293–302.

  40. Sukhova E.M., Sukhov V.S. 2018. Dependence of CO2 uptake in a plant cell on the activity of H+-ATPase of the plasma membrane. Theoretical analysis. Biol. membrany (Rus.). 35, 52–65.

  41. Opritov V.A. 1998. Functional aspects of bioelectrogenesis in higher plants In: 59th Timiryazev reading. N. Novgorod: NNSU Publishing house, p. 46.

    Google Scholar 

  42. Krol E., Trebacz K. 1999. Calcium-dependent voltage transients evoked by illumination in the liverwort Conocephalum conicum. Plant Cell Physiol. 40, 17–24.

    Article  CAS  Google Scholar 

  43. Pyatygin S. S. 2004. The role of the plasma membrane in the perception of cold effects on plant cells. Biol. membrany (Rus.). 21, 442–449.

  44. Pyatygin S. S., Vodeneev V. A., Opritov V. A. 2006. Depolarization of the plasma membrane as a universal primary bioelectric reaction of plant cells to the action of various factors. Uspekhi Sovremennoy Biologii (Rus.). 126, 493–502.

    Google Scholar 

  45. Gammaitoni L., Hanggi P., Jung P., Marchesoni F. 1998. Stochastic resonance. Rev. Mod. Phys. 70, 223–287.

    Article  CAS  Google Scholar 

  46. Paulsson J., Berg O.G., Ehrenberg M. 2000. Stochastic focusing: Fluctuation-enhanced sensitivity of intracellular regulation. Proc. Natl. Acad. Sci. USA.97, 7148–7153

    Article  CAS  PubMed  Google Scholar 

  47. Berg O.G., Paulsson J., Ehrenberg M. 2000. Fluctuations and quality of control in biological cells: Zero-order ultrasensitivity reinvestigated. Biophys. J.79, 1228–1236.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Berg O.G., Paulsson J., Ehrenberg M. 2000. Fluctuations in repressor control: Thermodynamic constraints on stochastic focusing. Biophys. J.79, 2944–2953.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Rao C.V., Wolf D.M., Arkin P.A. 2002. Control, exploitation and tolerance of intracellular noise. Nature. 420, 231–237.

    Article  CAS  PubMed  Google Scholar 

  50. Steuer R., Zhou C., Kurths J. 2003. Constructive effects of fluctuations in genetic and biochemical regulatory systems. BioSystems. 72, 241–251.

    Article  CAS  PubMed  Google Scholar 

  51. Wellens T., Shatokhin V., Buchleitner A. 2004. Stochastic resonance. Rep. Prog. Phys. 67, 45–105.

    Article  Google Scholar 

  52. Fulinski A. 1997. Active transport in biological membranes and stochastic resonances. Phys. Rev. Lett. 79, 4926–4929.

    Article  CAS  Google Scholar 

  53. Volkov E.I., Ullner E., Zaikin A.A., Kurths J. 2003. Frequency-dependent stochastic resonance in inhibitory coupled excitable systems. Phys. Rev. E.68, 061112.

    Article  CAS  Google Scholar 

  54. Beilby M. J. 1982. C1– channels in Chara. R. Soc. London B.299, 435–445.

    CAS  Google Scholar 

  55. Mummert H., Gradmann D. 1991. Action potentials in Acetabularia: Measurement and simulation of voltage-gated fluxes. J. Membr. Biol. 124, 265–273.

    Article  CAS  PubMed  Google Scholar 

  56. Gradmann D. 2001. Impact of apoplast volume on ionic relations in plant cells. J. Membr. Biol. 184, 61–69.

    Article  CAS  PubMed  Google Scholar 

  57. Sukhov V., Vodeneev V. 2009. Mathematical model of action potential in cells of vascular plants. J. Membr. Biol. 232, 59–67.

    Article  CAS  PubMed  Google Scholar 

  58. Sukhov V., Nerush V., Orlova L., Vodeneev V. Simulation of action potential propagation in plants. J. Theor. Biol. 291, 47–55.

  59. Sukhov V., Akinchits E., Katicheva L., Vodeneev, V. 2013. Simulation of variation potential in higher plant cells. J. Membr. Biol.246, 287–296.

    Article  CAS  PubMed  Google Scholar 

  60. Beilby M.J., Al Khazaaly S. 2016. Re-modeling Chara action potential: I. From Thiel model of Ca2+ transient to action potential form. AIMS Biophysics. 3, 431–449.

    Article  CAS  Google Scholar 

  61. Beilby M.J., Al Khazaaly, S. 2017. Re-modeling Chara action potential: II. The action potential form under salinity stress. AIMS Biophysics. 4, 298–315.

    Article  CAS  Google Scholar 

  62. Evans M.J., Morris R.J. 2017. Chemical agents transported by xylem mass flow propagate variation potentials. Plant J.91, 1029–1037.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Novikova E. M., Vodeneev V. A., Sukhov V. S. 2017. Development of a mathematical model of the action potential of higher plants, taking into account the role of the vacuole in generating an electrical signal. Biol. membrany (Rus.). 34, 109–125.

  64. Sukhova E., Akinchits E., Sukhov V. 2017. Mathematical models of electrical activity in plants. J. Membr. Biol. 250, 407–423.

    Article  CAS  PubMed  Google Scholar 

  65. Blyth M.G., Morris R.J. 2019. Shear-enhanced dispersion of a wound substance as a candidate mechanism for variation potential transmission. Front. Plant. Sci. 10, 1393.

    Article  PubMed  PubMed Central  Google Scholar 

  66. Sukhov V. S., Vodeneev V. A., Opritov V. A. 2008. Analysis of the influence of the level of fluctuation in the plant body on its resistance to stress factors. Nelineyniy mir (Rus.). 6, 713–717.

Download references

ACKNOWLEDGMENTS

The development of mathematical model of generation of electric cold-induced reactions in fluctuations of the activity H+-ATPase, as well as analysis of the impact of such fluctuations on the parameters of electrical responses was performed with financial support of the Russian Foundation for Basic Research (project no. 19-04-00614a). The analysis of the possibility of spontaneous generation of responses with an increase in the amplitude of fluctuations was carried out with financial support of the grant of the President of the Russian Federation to support young candidates of science (project no. MK-2707.2019.11.)

Author information

Authors and Affiliations

  1. Lobachevsky State University of Nizhni Novgorod, 603950, Nizhni Novgorod, Russia

    V. S. Sukhov, E. M. Sukhova, D. A. Ratnitsyna, M. A. Grinberg, L. M. Yudina & V. A. Vodeneev

Authors
  1. V. S. Sukhov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. M. Sukhova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. A. Ratnitsyna
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. A. Grinberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. L. M. Yudina
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. V. A. Vodeneev
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to V. S. Sukhov.

Ethics declarations

The authors declare that they have no conflict of interest.

This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by E. Puchkov

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sukhov, V.S., Sukhova, E.M., Ratnitsyna, D.A. et al. Theoretical Analysis of the Influence of Fluctuations in the Activity of the Plasma Membrane H+-ATPase on Low-Temperature-Induced Electrical Responses in a Plant Cell. Biochem. Moscow Suppl. Ser. A 14, 298–309 (2020). https://doi.org/10.1134/S1990747820030125

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1990747820030125

Keywords:

Search

Navigation