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BY-NC-ND 3.0 license Open Access Published by De Gruyter Open Access October 10, 2012

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

  • Vilma Kisnieriene EMAIL logo , Tatiana Ditchenko , Anatoly Kudryashov , Vidmantas Sakalauskas , Vladimir Yurin and Osvaldas Ruksenas
From the journal Open Life Sciences

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.

[1] Wessler I., Kirkpatrick C.J., Acetylcholine beyond neurons: the non-neuronal cholinergic system in humans, Br. J. Pharmacol., 2008, 154, 1558–1571 http://dx.doi.org/10.1038/bjp.2008.18510.1038/bjp.2008.185Search in 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 10.1186/1478-811X-7-20Search in Google Scholar

[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 http://dx.doi.org/10.1016/j.biocel.2009.01.01310.1016/j.biocel.2009.01.013Search in 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 http://dx.doi.org/10.1038/nm.237110.1038/nm.2371Search in Google Scholar

[5] Roshchina V.V., Neurotransmitters in plant life, Science publishers, USA, 2001 10.1201/9781482279856Search in 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 http://dx.doi.org/10.1254/jjp.85.210.1254/jjp.85.2Search in 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 Search in 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 http://dx.doi.org/10.1016/S0024-3205(02)02478-510.1016/S0024-3205(02)02478-5Search in Google Scholar

[9] Davies E., New functions for electrical signals in plants, New Phytologist, 2004, 161, 607–610 http://dx.doi.org/10.1111/j.1469-8137.2003.01018.x10.1111/j.1469-8137.2003.01018.xSearch in Google Scholar

[10] Knight H., Knight M. R., Abiotic stress signalling pathways: specificity and cross-talk, Trends Plant Sci., 2001, 6, 262–267 http://dx.doi.org/10.1016/S1360-1385(01)01946-X10.1016/S1360-1385(01)01946-XSearch in Google Scholar

[11] Sanders D., Brownlee C., Harper J. F., Communicating with calcium, Plant Cell, 1999, 11, 691–706 10.1105/tpc.11.4.691Search in Google Scholar PubMed PubMed Central

[12] Zimmermann S., Ehrhardt T., Plesch G., Mueller-Roeber B., Ion channels in plant signaling, Cell Mol. Life Sci., 1999, 55, 183–203 http://dx.doi.org/10.1007/s00018005028410.1007/s000180050284Search in Google Scholar

[13] Beilby M. J., Action potential in Charophytes, Int. Rev. Cytol., 2007, 257, 43–82 http://dx.doi.org/10.1016/S0074-7696(07)57002-610.1016/S0074-7696(07)57002-6Search in Google Scholar

[14] Hille B., Ion Channels of Excitable Membranes, 3rd ed, Sinauer Associates Inc., Sunderland, MA, 2001 Search in 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 http://dx.doi.org/10.1104/pp.104.04823110.1104/pp.104.048231Search in Google Scholar PubMed PubMed Central

[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 http://dx.doi.org/10.1034/j.1399-3054.1999.106305.x10.1034/j.1399-3054.1999.106305.xSearch in 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 http://dx.doi.org/10.1016/j.jtbi.2011.09.01910.1016/j.jtbi.2011.09.019Search in Google Scholar PubMed

[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 http://dx.doi.org/10.1007/BF0187160710.1007/BF01871607Search in 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 http://dx.doi.org/10.1007/s00232-009-9218-910.1007/s00232-009-9218-9Search in Google Scholar PubMed

[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 Search in 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 http://dx.doi.org/10.1093/jxb/48.Special_Issue.60910.1093/jxb/48.Special_Issue.609Search in Google Scholar PubMed

[22] Gong X.-Q., Bisson M.A., Acetylcholine-activated Cl− channel in the Chara tonoplast, J. Membr. Biol., 2002, 188, 107–113 http://dx.doi.org/10.1007/s00232-001-0177-z10.1007/s00232-001-0177-zSearch in Google Scholar PubMed

[23] Volkov A.G., Plant electrophysiology — Theory and Methods, Springer-Verlag, Berlin, 2006 http://dx.doi.org/10.1007/978-3-540-37843-310.1007/978-3-540-37843-3Search in 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 http://dx.doi.org/10.1007/BF0187089210.1007/BF01870892Search in 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 Search in 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 http://dx.doi.org/10.2478/s11535-007-0009-y10.2478/s11535-007-0009-ySearch in 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 http://dx.doi.org/10.1111/j.1365-3040.2005.01437.x10.1111/j.1365-3040.2005.01437.xSearch in 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 http://dx.doi.org/10.1104/pp.46.6.76810.1104/pp.46.6.768Search in 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 http://dx.doi.org/10.1016/0309-1651(87)90123-810.1016/0309-1651(87)90123-8Search in 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 http://dx.doi.org/10.1007/BF0187031310.1007/BF01870313Search in 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 http://dx.doi.org/10.2478/s11535-009-0028-y10.2478/s11535-009-0028-ySearch in 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 http://dx.doi.org/10.1093/pcp/pce06810.1093/pcp/pce068Search in Google Scholar

[33] Hirschi K., Vacuolar H+/Ca2+ transport: who’s directing the traffic?, Trends Plant Sci., 2001, 6, 100–104 http://dx.doi.org/10.1016/S1360-1385(00)01863-X10.1016/S1360-1385(00)01863-XSearch in Google Scholar

Published Online: 2012-10-10
Published in Print: 2012-12-1

© 2012 Versita Warsaw

This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.

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