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Simulation of Variation Potential in Higher Plant Cells

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Variation potential (VP), a propagating electrical signal unique to plants, induces a number of changes in many physiological processes. However, the mechanisms of its generation and propagation are still under discussion and require experimental and theoretical analysis, including VP simulations. The mathematical model for VP formation in plants has been worked out and is based on our previous description of electrophysiological processes in higher plant cells, including plasma membrane ion transport systems (K+, Cl and Ca2+ channels, H+ and Ca2+-ATPase, 2H+/Cl symporter and H+/K+ antiporter) and their regulation, ion concentration changes in cells and extracellular spaces and buffers in cytoplasm and apoplast. In addition, the VP model takes into account wound substance diffusion, which is described by a one-dimensional diffusion equation, and ligand-gated Ca2+ channels, which are activated by this substance. The VP model simulates the experimental dependence of amplitude, velocity and shape of VP on the distance from the wounding site and describes the influence of metabolic inhibitors, divalent cation chelators and anion channel blockers on the generation of this electrical reaction, as shown in experiments. Thus, our model favorably simulates VP in plants and theoretically supports the role of wound substance diffusion and Ca2+ influx in VP development.

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References

  • Beilby MJ (1982) Cl channels in Chara. Philos Trans R Soc Lond B Biol Sci 299:435–445

    Article  CAS  Google Scholar 

  • Beilby MJ (2007) Action potential in charophytes. Int Rev Cytol 257:43–82

    Article  PubMed  CAS  Google Scholar 

  • Beilby MJ, Shepherd VA (2001) Modeling the current–voltage characteristics of charophyte membranes. II. The effect of salinity on membranes of Lamprothamnium papulosum. J Membr Biol 181:77–89

    PubMed  CAS  Google Scholar 

  • Beilby MJ, Shepherd VA (2006) The characteristics of Ca++-activated Cl channels of salt-tolerant charophyte Lamprothamnium. Plant Cell Environ 29:764–777

    Article  PubMed  CAS  Google Scholar 

  • Berestovsky GN, Kataev AA (2005) Voltage-gated calcium and Ca2+-activated chloride channels and Ca2+ transients: voltage-clamp studies of perfused and intact cells of Chara. Eur Biophys J 34:973–986

    Article  PubMed  CAS  Google Scholar 

  • Codling EA, Plank MJ, Benhamou S (2008) Random walk models in biology. J R Soc Interface 5:813–834

    Article  PubMed  Google Scholar 

  • Davies E (2006) Electrical signals in plants: facts and hypotheses. In: Volkov AG (ed) Plant electrophysiology. Theory and methods, Springer-Verlag, Berlin, pp 407–422

    Chapter  Google Scholar 

  • De Nisi P, Dell’Orto M, Pirovano L, Zocchi G (1999) Calcium-dependent phosphorylation regulates the plasma-membrane H+-ATPase activity of maize (Zea mays L.) roots. Planta 209:187–194

    Article  PubMed  Google Scholar 

  • Dziubinska H, Filek M, Koscielniak J, Trebacz K (2003) Variation and action potentials evoked by thermal stimuli accompany enhancement of ethylene emission in distant non-stimulated leaves of Vicia faba minor seedlings. J Plant Physiol 160:1203–1210

    Article  PubMed  CAS  Google Scholar 

  • Felle HH, Zimmermann MR (2007) Systemic signaling in barley through action potentials. Planta 226:203–214

    Article  PubMed  CAS  Google Scholar 

  • Filek M, Koscielniak 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 

  • Fisahn J, Herde O, Willmitzer L, Peña-Cortés H (2004) Analysis of the transient increase in cytosolic Ca2+ during the action potential of higher plants with high temporal resolution: requirement of Ca2+ transients for induction of jasmonic acid biosynthesis and PINII gene expression. Plant Cell Physiol 45:456–459

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Grams TEE, Koziolek C, Lautner S, Matyssek R, Fromm J (2007) Distinct roles of electric and hydraulic signals on the reaction of leaf gas exchange upon re-irrigation in Zea mays L. Plant Cell Environ 30:79–84

    Article  PubMed  Google Scholar 

  • Grams TEE, Lautner S, Felle HH, Matyssek R, Fromm J (2009) Heat-induced electrical signals affect cytoplasmic and apoplastic pH as well as photosynthesis during propagation through the maize leaf. Plant Cell Environ 32:319–326

    Article  PubMed  CAS  Google Scholar 

  • Hansen U-P, Gradmann D, Sanders D, Slayman CL (1981) Interpretation of current–voltage relationships for “active” ion transport systems: I. Steady-state reaction-kinetic analysis of class-I mechanisms. J Membr Biol 63:165–190

    Article  PubMed  CAS  Google Scholar 

  • Hlaváčková V, Krchňák P, Nauš J, Novák O, Špundová 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  Google Scholar 

  • Julien JL, Desbiez MO, de Jaeger G, Frachisse JM (1991) Characteristics of the wave of depolarization induced by wounding in Bidens pilosa L. J Exp Bot 42:131–137

    Article  Google Scholar 

  • Kinoshita T, Nishimura M, Shimazaki K (1995) Cytosolic concentration of Ca2+ regulates the plasma membrane H+-ATPase in guard cells of fava bean. Plant Cell 7:1333–1342

    PubMed  CAS  Google Scholar 

  • Koziolek C, Grams TEE, Schreiber U, Matyssek R, Fromm J (2003) Transient knockout of photosynthesis mediated by electrical signals. New Phytol 161:715–722

    Article  Google Scholar 

  • Lautner S, Grams TEE, Matyssek R, Fromm J (2005) Characteristics of electrical signals in poplar and responses in photosynthesis. Plant Physiol 138:2200–2209

    Article  PubMed  CAS  Google Scholar 

  • Lewis BD, Karlin-Neumann G, Davis RW, Spalding EP (1997) Ca2+-activated anion channels and membrane depolarizations induced by blue light and cold in Arabidopsis seedlings. Plant Physiol 114:1327–1328

    Article  PubMed  CAS  Google Scholar 

  • Malone M, Stankovic B (1991) Surface potentials and hydraulic signals in wheat leaves following localized wounding by heat. Plant Cell Environ 14:431–436

    Article  Google Scholar 

  • Mancuso S (1999) Hydraulic and electrical transmission of wound-induced signals in Vitis vinifera. Aust J Plant Physiol 26:55–61

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Retivin VG, Opritov VA, Lobov SA (2001) A computer electrophysiological investigation of action potential propagation in stem of pumpkin seedling. Vestnik of NNSU [in Russian]. Seriya Biologiya 1:190–197

    Google Scholar 

  • Rhodes JD, Thain JF, Wildon DC (1999) Evidence for physically distinct systemic signalling pathways in the wounded tomato plant. Ann Bot 84:109–116

    Article  CAS  Google Scholar 

  • Ricca U (1916) Soluzione d’un problema di fisiologia: la propagazione di stimulo nella Mimosa. Nuovo G Bot Ital 23:51–170

    Google Scholar 

  • Shimmen T (2002) Electrical perception of “death message” in Chara: analysis of rapid component and ionic process. Plant Cell Physiol 43:1575–1584

    Article  PubMed  CAS  Google Scholar 

  • Sibaoka T (1997) Application of leaf extract causes repetitive action potentials in Biophytum sensitivum. J Plant Res 110:485–487

    Article  Google Scholar 

  • Smith JR, Beilby MJ (1983) Inhibition of electrogenic transport associated with the action potential in Chara. J Membr Biol 71:131–140

    Article  Google Scholar 

  • Stahlberg R, Cosgrove DJ (1992) Rapid alteration in growth rate and electric potentials upon stem excision in pea seedlings. Planta 187:523–531

    Article  PubMed  CAS  Google Scholar 

  • Stahlberg R, Cosgrove DJ (1996) Induction and ionic basis of slow wave potentials in seedlings of Pisum sativum L. Planta 200:416–425

    Article  PubMed  CAS  Google Scholar 

  • Stahlberg R, Cosgrove DJ (1997) The propagation of slow wave potentials in pea epicotyls. Plant Physiol 113:209–217

    PubMed  CAS  Google Scholar 

  • Stahlberg R, Robert E, Cleland RE, van Volkenburgh E (2006) Slow wave potentials—a propagating electrical signal unique to higher plants. In: Baluška F, Mancuso S, Volkmann D (eds) Communication in plants. Neuronal aspects of plant life, Springer-Verlag, Berlin, pp 291–309

    Chapter  Google Scholar 

  • Stanković B, Davies E (1996) Both action potentials and variation potentials induce proteinase inhibitor gene expression in tomato. FEBS Lett 390:275–279

    Article  PubMed  Google Scholar 

  • Sukhov V, Vodeneev V (2009) A mathematical model of action potential in cells of vascular plants. J Membr Biol 232:59–67

    Article  PubMed  CAS  Google Scholar 

  • Sukhov V, Nerush V, Orlova L, Vodeneev V (2011) Simulation of action potential propagation in plants. J Theor Biol 291:47–55

    Article  PubMed  Google Scholar 

  • Sukhov V, Orlova L, Mysyagin S, Sinitsina J, Vodeneev V (2012) Analysis of the photosynthetic response induced by variation potential in geranium. Planta 235:703–712

    Article  PubMed  CAS  Google Scholar 

  • Trebacz K, Dziubinska H, Krol E (2006) Electrical signals in long-distance communication in plants. In: Baluška F, Mancuso S, Volkmann D (eds) communication in plants. Neuronal aspects of plant life. Springer-Verlag, Berlin-Heidelberg, pp 277–290

    Chapter  Google Scholar 

  • Umrath K (1959) Der Erregungsvorgang. In: Ruhland W (ed) Handbuch der pflanzenphysiologie, vol 17. Springer, Berlin, pp 24–110

    Google Scholar 

  • Vodeneev VA, Opritov VA, Pyatygin SS (2006) Reversible changes of extracellular pH during action potential generation in a higher plant Cucurbita pepo. Russ J Plant Physiol 53:481–487

    Article  CAS  Google Scholar 

  • Vodeneev VA, Akinchits EK, Orlova LA, Sukhov VS (2011) The role of Ca2+, H+, and Cl ions in generation of variation potential in pumpkin plants. Russ J Plant Physiol 58:974–981

    Article  CAS  Google Scholar 

  • Vodeneev V, Orlova A, Morozova E, Orlova L, Akinchits E, Orlova O, Sukhov V (2012) The mechanism of propagation of variation potentials in wheat leaves. J Plant Physiol 169:949–954

    Article  PubMed  CAS  Google Scholar 

  • Zawadzki T, Trebacz K (1985) Extra- and intracellular measurements of action potentials in the liverwort Conocephalum conicum. Physiol Plant 64:477–481

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the Russian Foundation for Basic Research, project 12-04-00837-a, and the Ministry of Education and Science of Russian Federation, project MK-1869.2012.4.

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Correspondence to Vladimir Sukhov.

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Sukhov, V., Akinchits, E., Katicheva, L. et al. Simulation of Variation Potential in Higher Plant Cells. J Membrane Biol 246, 287–296 (2013). https://doi.org/10.1007/s00232-013-9529-8

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  • DOI: https://doi.org/10.1007/s00232-013-9529-8

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