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The effect of acetylcholine on Characeae K+ channels at rest and during action potential generation

  • Research Article
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Central European Journal of Biology

Abstract

The role of acetylcholine (ACh) as a signalling molecule in plants was investigated using a model system of Characeae cells. The effect of ACh on conductance of K+ channels in Nitella flexilis cells and on the action potential generation in Nitellopsis obtusa cells after H+-ATPase inhibition, where repolarization occurs after the opening of outward rectifying K+ channels, was investigated. Voltage-clamp method based on only one electrode impalement was used to evaluate the activity of separate potassium ion transport system at rest. We found that ACh at high concentrations (1 mM and 5 mM) activates K+ channels as the main membrane transport system at the resting state involved in electrogenesis of Characeaen membrane potential. We observed that ACh caused an increase in duration of AP repolarization of cells in K+ state when plasmalemma electrical characteristics are determined by large conductance K+ channels irrespective of whether AP were spontaneous or electrically evoked. These results indicate interference of ACh with electrical cellular signalling pathway in plants.

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References

  1. Wessler I., Kirkpatrick C.J., Acetylcholine beyond neurons: the non-neuronal cholinergic system in humans, Br. J. Pharmacol., 2008, 154, 1558–1571

    Article  PubMed  CAS  Google Scholar 

  2. Resende R.R., Adhikari A., Cholinergic receptor pathways involved in apoptosis, cell proliferation and neuronal differentiation, Cell Commun. Signal., 2009, 7–20

  3. Arias H.R., Richards V.E., Ng D., Ghafoori M.E., Le V., Mousa S.A., Role of non-neuronal nicotinic acetylcholine receptors in angiogenesis, Int. J. Biochem. Cell Biol., 2009, 41, 1441–1451

    Article  PubMed  CAS  Google Scholar 

  4. Rodriguez-Diaz R., Dando R., Jacques-Silva M.C., Fachado A., Molina J., Abdulreda M.H., et al., Alpha cells secrete acetylcholine as a nonneuronal paracrine signal priming beta cell function in humans, Nat. Med., 2011, 17, 888–892

    Article  PubMed  CAS  Google Scholar 

  5. Roshchina V.V., Neurotransmitters in plant life, Science publishers, USA, 2001

    Google Scholar 

  6. Wessler I., Kilbinger H., Bittinger F., Kirkpatrick C.J., The biological role of non-neuronal acetylcholine in plants and humans, Jpn. J. Pharmacol., 2001, 85, 2–10

    Article  PubMed  CAS  Google Scholar 

  7. Hartmann E., Gupta R., Acetylcholine as a signaling system in plants, In: Boss W.E., Marre, D.J. Liss A.R. (Eds.), Second Messengers in Plant Growth and Development, Oxford, 1989

    Google Scholar 

  8. Horiuchi Y., Kimura R., Kato N., Fujii T., Seki M., Endo T., et al., Evolutional study on acetylcholine expression, Life Sci., 2003, 72, 1745–1756

    Article  PubMed  CAS  Google Scholar 

  9. Davies E., New functions for electrical signals in plants, New Phytologist, 2004, 161, 607–610

    Article  Google Scholar 

  10. Knight H., Knight M. R., Abiotic stress signalling pathways: specificity and cross-talk, Trends Plant Sci., 2001, 6, 262–267

    Article  PubMed  CAS  Google Scholar 

  11. Sanders D., Brownlee C., Harper J. F., Communicating with calcium, Plant Cell, 1999, 11, 691–706

    PubMed  CAS  Google Scholar 

  12. Zimmermann S., Ehrhardt T., Plesch G., Mueller-Roeber B., Ion channels in plant signaling, Cell Mol. Life Sci., 1999, 55, 183–203

    Article  CAS  Google Scholar 

  13. Beilby M. J., Action potential in Charophytes, Int. Rev. Cytol., 2007, 257, 43–82

    Article  PubMed  CAS  Google Scholar 

  14. Hille B., Ion Channels of Excitable Membranes, 3rd ed, Sinauer Associates Inc., Sunderland, MA, 2001

    Google Scholar 

  15. Sondergaard T.E., Schulz A., Palmgren M.G., Energization of transport processes in plants. Roles of the plasma membrane H+-ATPase, Plant Physiol., 2004, 136, 2475–2482

    Article  PubMed  CAS  Google Scholar 

  16. Zingarelli L., Marre M.T., Massardi F., Lado P., Effects of hyper-osmotic stress on K+ fluxes, H+ extrusion, transmembrane electric potential difference and comparison with the effects of fusicoccin, Physiol. Plant, 1999, 106, 287–295

    Article  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  18. Kishimoto U., Takeuchi Y., Ohkawa T.A., Kami-ike N., A kinetic analysis of the electrogenic pump of Chara corallina: III. Pump activity during the action potential, J. Membr. Biol., 1985, 86, 27–36

    Article  CAS  Google Scholar 

  19. Sukhov V.S., Vodeneev V.A., A mathematical model of action potential in cells of vascular plants, J. Membr. Biol., 2009, 232, 59–67

    Article  PubMed  CAS  Google Scholar 

  20. Johnson B.R., Wyttenbach R.A., Wayne R., Hoy R.R., Action potentials in a giant algal cell: a comparative approach to mechanisms and evolution of excitability, J. Undergrad. Neurosci. Educ., 2002, 1, 23–27

    Google Scholar 

  21. Thiel G., Homann U., Plieth C., Ion channel activity during the action potential in Chara: a new insight with new techniques, J. Exp. Bot., 1997, 48, 609–622

    Article  PubMed  CAS  Google Scholar 

  22. Gong X.-Q., Bisson M.A., Acetylcholine-activated Cl channel in the Chara tonoplast, J. Membr. Biol., 2002, 188, 107–113

    Article  PubMed  CAS  Google Scholar 

  23. Volkov A.G., Plant electrophysiology — Theory and Methods, Springer-Verlag, Berlin, 2006

    Book  Google Scholar 

  24. Sokolik A.I., Yurin V.M., Potasium channels in plasmalema of Nitella cells at rest, J. Membr. Biol., 1986, 89, 9–22

    Article  CAS  Google Scholar 

  25. Yurin V.M., Sokolik A.I., Kudryashov A.P., Regulation of ion transport through plant cell membranes, Science and Engineering, Minsk, 1991

    Google Scholar 

  26. Kisnieriene V., Sakalauskas V., The effect of aluminium on bioelectrical activity of the Nitellopsis obtusa cell membrane after H+-ATPase inhibition, Cent. Eur. J. Biol., 2007, 2, 222–232

    Article  CAS  Google Scholar 

  27. Beilby M.J., Shepherd V.A., The characteristics of Ca2+-activated Cl channels of the salt-tolerant Charophyte Lamprothamnium, Plant Cell Environ., 2006, 29, 764–777

    Article  PubMed  CAS  Google Scholar 

  28. Jaffe M.J., Evidence for the regulation of phytochrome-mediated process in bean roots by the neurohumor, acetylcholine, Plant Physiol., 1970, 46, 768–777

    Article  PubMed  CAS  Google Scholar 

  29. Tretyn A., Influence of red light and acetylcholine on 45Ca2+ uptake by oat coleoptile cells, Cell Biol. Int. Rep., 1987, 11, 887–896

    Article  CAS  Google Scholar 

  30. Lunevsky V.Z., Zherelova O.M., Vostrikov I.Y., Berestovsky G.N., Excitation of Characeae cell membranes as a result of activation of calcium and chloride channels, J. Membr. Biol., 1983, 72, 43–58

    Article  Google Scholar 

  31. Kisnierienė V., Sakalauskas V., Pleskačiauskas A., Yurin V., Rukšėnas O., The combined effect of Cd2+ and ACh on action potentials of Nitellopsis obtusa cells, Cent. Eur. J. Biol., 2009, 4, 343–350

    Article  Google Scholar 

  32. Tsutsui I., Ohkawa T., Regulation of the H+ pump activity in the plasma membrane of internally perfused Chara coralline, Plant Cell Physiol., 2001, 42, 531–537

    Article  PubMed  CAS  Google Scholar 

  33. Hirschi K., Vacuolar H+/Ca2+ transport: who’s directing the traffic?, Trends Plant Sci., 2001, 6, 100–104

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Vilma Kisnieriene.

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Kisnieriene, V., Ditchenko, T.I., Kudryashov, A.P. et al. The effect of acetylcholine on Characeae K+ channels at rest and during action potential generation. cent.eur.j.biol. 7, 1066–1075 (2012). https://doi.org/10.2478/s11535-012-0085-5

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  • DOI: https://doi.org/10.2478/s11535-012-0085-5

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