Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Electrical signalling in Nitellopsis obtusa: potential biomarkers of biologically active compounds

Vilma Kisnieriene A B , Indre Lapeikaite A and Vilmantas Pupkis A
+ Author Affiliations
- Author Affiliations

A Department of Neurobiology and Biophysics, Faculty of Natural Science, Vilnius University, Vilnius, Sauletekio av. 7, LT-10257, Lithuania.

B Corresponding author. Email: vilma.kisnieriene@gf.vu.lt

This paper originates from a presentation at the Fourth International Symposium on Plant Signaling and Behavior, Komarov Botanical Institute RAS/Russian Science Foundation, Saint Petersburg, Russia, 1923 June 2016.

Functional Plant Biology - https://doi.org/10.1071/FP16339
Submitted: 30 September 2016  Accepted: 19 February 2017   Published online: 19 April 2017

Abstract

The Nitellopsis obtusa (N.A.Desvaux) J.Groves cell provides a model system for complex investigation of instantaneous effects of various biologically active compounds (BC) on the generation of plant bioelectrical signals in vivo. Experimental evidence using multiple electrical signals as biomarkers of the effects of BC (acetylcholine, asparagine, glutamate, nicotine, aluminium, nickel and cadmium ions) is provided. The effect of BC on membrane transport systems involved in the cell excitability were tested by current clamp, voltage clamp and patch clamp methods. Membrane potential (MP) alterations and action potential (AP) patterns in response to BC were shown to represent the cell state. High discretisation frequency allows precise, high time resolution analysis of real-time processes measuring changes in excitation threshold, AP amplitude and velocity of repolarisation values after application of BC indicating the effect on ion channels involved in AP generation. Application of voltage clamp revealed that changes in AP peak value were caused not only by increment in averaged maximum amplitude of the Cl current, but in prolonged Cl channels’ opening time also. The cytoplasmic droplet can serve as a model system in which the effects of BC on single tonoplast ion channel can be studied by patch clamping. Investigation of electrical cell-to-cell communication revealed evidence on the electrical signal transduction through plasmodesmata.

Additional keywords: action potential, Characeae, ion channels, plant electrophysiology, voltage-clamp.


References

Beilby MJ (2007) Action potential in charophytes. International Review of Cytology 257, 43–82.
Action potential in charophytes.CrossRef | 1:CAS:528:DC%2BD2sXmt1Glurc%3D&md5=ab80b438d81a71b8cf139135f07e31e1CAS |

Beilby MJ (2016) Multi-scale Characean experimental system: from electrophysiology of membrane transporters to cell-to-cell connectivity, cytoplasmic streaming and auxin metabolism. Frontiers in Plant Science 7, 1052
Multi-scale Characean experimental system: from electrophysiology of membrane transporters to cell-to-cell connectivity, cytoplasmic streaming and auxin metabolism.CrossRef |

Beilby MJ, Al Khazaaly SA (2016) Re-modeling Chara action potential: I. from Thiel model of Ca2+ transient to action potential form. AIMS Biophysics 3, 431–449.
Re-modeling Chara action potential: I. from Thiel model of Ca2+ transient to action potential form.CrossRef |

Beilby MJ, Casanova MT (2014) ‘The physiology of Characean cells.’ (Springer: Berlin)

Beilby MJ, Mimura T, Shimmen T (1993) The proton pump, high pH channels, and excitation: voltage clamp studies of intact and perfused cells of Nitellopsis obtusa. Protoplasma 175, 144–152.
The proton pump, high pH channels, and excitation: voltage clamp studies of intact and perfused cells of Nitellopsis obtusa.CrossRef | 1:CAS:528:DyaK2cXivFeqtbs%3D&md5=a2a5195550d545ae84816aab32261eceCAS |

Berecki G, Eijken M, Van Iren F, Van Duijn B (2001) Tonoplast anion channel activity modulation by pH in Chara corallina. Journal of Membrane Biology 184, 131–141.
Tonoplast anion channel activity modulation by pH in Chara corallina.CrossRef | 1:CAS:528:DC%2BD3MXos1Khsro%3D&md5=6554230d140b230ebe0f5678d0b576f3CAS |

Berestovsky G, Kataev A (2005) Voltage-gated calcium and Ca2+-activated chloride channels and Ca2+ transients: voltage-clamp studies of perfused and intact cells of Chara. European Biophysics Journal 34, 973–986.
Voltage-gated calcium and Ca2+-activated chloride channels and Ca2+ transients: voltage-clamp studies of perfused and intact cells of Chara.CrossRef | 1:CAS:528:DC%2BD2MXht1SksbvK&md5=65ad3dedd71d333ec9af2acb5e969f89CAS |

Bertl A (1989) Current-voltage relationships of a sodium-sensitive potassium channel in the tonoplast of Chara corallina. Journal of Membrane Biology 109, 9–19.
Current-voltage relationships of a sodium-sensitive potassium channel in the tonoplast of Chara corallina.CrossRef | 1:CAS:528:DyaL1MXkvFans74%3D&md5=9d9213463039005ab8363b6b949d4f50CAS |

Böhm J, Scherzer S, Krol E, Kreuzer I, von Meyer K, Lorey C, Mueller TD, Shabala L, Monte I, Solano R, Al-Rasheid KA, Rennenberg H, Shabala S, Neher E, Hedrich R (2016) The Venus flytrap Dionaea muscipula counts prey-induced action potentials to induce sodium uptake. Current Biology 26, 286–295.
The Venus flytrap Dionaea muscipula counts prey-induced action potentials to induce sodium uptake.CrossRef |

Clabeaux BL, Navarro DA, Aga DS, Bisson MA (2011) Cd tolerance and accumulation in the aquatic macrophyte, Chara australis: potential use for charophytes in phytoremediation. Environmental Science & Technology 45, 5332–5338.
Cd tolerance and accumulation in the aquatic macrophyte, Chara australis: potential use for charophytes in phytoremediation.CrossRef | 1:CAS:528:DC%2BC3MXmtVCmt7Y%3D&md5=7f577ecb389256dca14ec83c08ffd27bCAS |

Davies E (2004) New functions for electrical signals in plants. New Phytologist 161, 607–610.
New functions for electrical signals in plants.CrossRef |

Davies E, Stankovic B (2006) Electrical signals, the cytoskeleton, and gene expression: a hypothesis on the coherence of the cellular responses to environmental insult. In ‘Communication in Plants – Neuronal Aspects of Plant Life’. (Eds F Baluska, S Mancuso, D Volkmann) pp. 309–320. (Springer Verlag: Berlin Heidelberg)

De Boer AH, Van Duijn B, Giesberg P, Wegner L, Obermeyer G, Köhler K, Linz KW (1994) Laser microsurgery: a versatile tool in plant (electro) physiology. Protoplasma 178, 1–10.
Laser microsurgery: a versatile tool in plant (electro) physiology.CrossRef |

Felle HH, Zimmermann MR (2007) Systemic signalling in barley through action potentials. Planta 226, 203–214.
Systemic signalling in barley through action potentials.CrossRef | 1:CAS:528:DC%2BD2sXltlSrsbw%3D&md5=2bc3de348e83fd0e0fd9d6e0796050adCAS |

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 Physiology 45, 456–459.
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.CrossRef | 1:CAS:528:DC%2BD2cXjsFKhtb8%3D&md5=1c627ef6764a46d41e312fe3f64d510dCAS |

Fromm J, Lautner S (2007) Electrical signals and their physiological significance in plants. Plant, Cell & Environment 30, 249–257.
Electrical signals and their physiological significance in plants.CrossRef | 1:CAS:528:DC%2BD2sXjtlemu74%3D&md5=0f339e0dc380598533a73d13f28df4ebCAS |

Gallé A, Lautner S, Flexas J, Fromm J (2015) Environmental stimuli and physiological responses: the current view on electrical signalling. Environmental and Experimental Botany 114, 15–21.
Environmental stimuli and physiological responses: the current view on electrical signalling.CrossRef |

Gong XQ, Bisson MA (2002) Acetylcholine-activated Cl channel in the Chara tonoplast. Journal of Membrane Biology 188, 107–113.
Acetylcholine-activated Cl channel in the Chara tonoplast.CrossRef | 1:CAS:528:DC%2BD38XlvFeru7s%3D&md5=ea3d5e8e290a00a93057cb5040fcd2ccCAS |

Grams TE, 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 & Environment 32, 319–326.
Heat-induced electrical signals affect cytoplasmic and apoplastic pH as well as photosynthesis during propagation through the maize leaf.CrossRef | 1:CAS:528:DC%2BD1MXkslKjsrk%3D&md5=fe456415cf21baa5c86d64e05d382aa7CAS |

Gyenes M, Saxena R (1984) Excitable active electrogenic ion-transport units in the plasmalemma of Nitellopsis obtusa. Journal of Experimental Botany 35, 1323–1331.
Excitable active electrogenic ion-transport units in the plasmalemma of Nitellopsis obtusa.CrossRef | 1:CAS:528:DyaL2cXmtVOrs7Y%3D&md5=1cb81a78681998c4786a2765e69b9bddCAS |

Hedrich R, Salvador-Recatalà V, Dreyer I (2016) Electrical wiring and long-distance plant communication. Trends in Plant Science 21, 376–387.
Electrical wiring and long-distance plant communication.CrossRef | 1:CAS:528:DC%2BC28Xit1SitLk%3D&md5=3a059bb7760868eb9e58b765d6664187CAS |

Kamiya N, Kuroda K (1957) Cell operation in Nitella. I. Cell amputation and effusion of the endoplasm. Proceedings of the Japan Academy 33, 149–152.

Katicheva L, Sukhov V, Akinchits E, Vodeneev V (2014) Ionic nature of burn-induced variation potential in wheat leaves. Plant & Cell Physiology 55, 1511–1519.
Ionic nature of burn-induced variation potential in wheat leaves.CrossRef | 1:CAS:528:DC%2BC28XhtlWmtb7N&md5=ed715655998d23c258b4616a849fcdc8CAS |

Katsuhara M, Mimura T, Tazawa M (1990) ATP-regulated ion channels in the plasma membrane of a Characeae alga, Nitellopsis obtusa. Plant Physiology 93, 343–346.
ATP-regulated ion channels in the plasma membrane of a Characeae alga, Nitellopsis obtusa.CrossRef | 1:CAS:528:DyaK3cXktlOrtbo%3D&md5=a14116f8bf833919a8836b830d94b0b0CAS |

Kikuyama M, Tazawa M (1998) Temporal relationship between action potential and Ca2+ transient in Characean cells. Plant & Cell Physiology 39, 1359–1366.
Temporal relationship between action potential and Ca2+ transient in Characean cells.CrossRef | 1:CAS:528:DyaK1MXhsF2luw%3D%3D&md5=49dfac9fc3b8fcec4ab398115a91fadcCAS |

Kisnieriene V, Lapeikaite I (2015) When chemistry meets biology: the case of aluminium – a review. Chemija 26, 148–158.

Kisnieriene V, Sakalauskas V (2005) Al3+ induced membrane potential changes in Nitellopsis obtusa cells. Biologija 1, 31–34.

Kisnierienë V, Sakalauskas V (2007) The effect of aluminium on bioelectrical activity of the Nitellopsis obtusa cell membrane after H+-ATPase inhibition. Central European Journal of Biology 2, 222–232.

Kisnieriene V, Beitas K, Sakalauskas V, Daktariunas (2008) Information technologies for biology education: computerized electrophysiology of plant cells. Informatics in Education 7, 91–104.

Kisnieriene V, Sakalauskas V, Pleskačiauskas A, Yurin V, Rukšɹnas O (2009) The combined effect of Cd2+ and ACh on action potentials of Nitellopsis obtusa cells. Central European Journal of Biology 4, 343–350.

Kisnieriene V, Ditchenko T, Kudryashov A, Sakalauskas V, Yurin V, Ruksenas O (2012) The effect of acetylcholine on Characeae K+ channels at rest and during action potential generation. Central European Journal of Biology 7, 1066–1075.

Kisnieriene V, Burneika J, Lapeikaite I, Sevriukova O, Daktariunas A (2014) Investigation of membrane potential changes in Nitellopsis obtusa cells induced by blue and red light stimulation. Biologija 60, 71–78.
Investigation of membrane potential changes in Nitellopsis obtusa cells induced by blue and red light stimulation.CrossRef | 1:CAS:528:DC%2BC2cXhvFejtLbL&md5=b4abb09c48ef87635da781659fa2536bCAS |

Kisnieriene V, Lapeikaite I, Sevriukova O, Ruksenas O (2016) The effects of Ni2+ on electrical signaling of Nitellopsis obtusa cells. Journal of Plant Research 129, 551–558.
The effects of Ni2+ on electrical signaling of Nitellopsis obtusa cells.CrossRef | 1:CAS:528:DC%2BC28XivFOlurY%3D&md5=177f50907cd4e14b27e308002ec05ec8CAS |

Koselski M, Trebacz K, Dziubinska H (2013) Cation-permeable vacuolar ion channels in the moss Physcomitrella patens: a patch-clamp study. Planta 238, 357–367.
Cation-permeable vacuolar ion channels in the moss Physcomitrella patens: a patch-clamp study.CrossRef | 1:CAS:528:DC%2BC3sXhtFKnu7rJ&md5=e06d0cb799d8ad89b2d1310752ad83aaCAS |

Kourie JI (1994) Transient Cl and K+ currents during the action potential in Chara inflata (effects of external sorbitol, cations, and ion channel blockers). Plant Physiology 106, 651–660.
Transient Cl and K+ currents during the action potential in Chara inflata (effects of external sorbitol, cations, and ion channel blockers).CrossRef | 1:CAS:528:DyaK2cXmslKrsr0%3D&md5=bb9b8a7d55b67ffab5c5ae2c7718013eCAS |

Król E, Dziubińska H, Trębacz K (2010) What do plants need action potentials for? In ‘Action potential: biophysical and cellular context, initiation, phases and propagation’. (Ed. ML DuBois) pp. 1–26. (Nova Science Publishers: New York)

Kurtyka R, Burdach Z, Karcz W (2011) Effect of cadmium and lead on the membrane potential and photoelectric reaction of Nitellopsis obtusa cells. General Physiology and Biophysics 30, 52–58.
Effect of cadmium and lead on the membrane potential and photoelectric reaction of Nitellopsis obtusa cells.CrossRef | 1:CAS:528:DC%2BC3MXnvVeju7c%3D&md5=945b365a057e9f42f51cbe47d063402dCAS |

Lühring H (1986) Recording of single K+ channels in the membrane of cytoplasmic drop of Chara australis. Protoplasma 133, 19–28.
Recording of single K+ channels in the membrane of cytoplasmic drop of Chara australis.CrossRef |

Lühring H, Witzemann V (1995) Internodal cells of the giant green alga Chara as an expression system for ion channels. FEBS Letters 361, 65–69.
Internodal cells of the giant green alga Chara as an expression system for ion channels.CrossRef |

Lunevsky VZ, Zherelova OM, Vostrikov IY, Berestovsky GN (1983) Excitation of Characeae cell membranes as a result of activation of calcium and chloride channels. Journal of Membrane Biology 72, 43–58.
Excitation of Characeae cell membranes as a result of activation of calcium and chloride channels.CrossRef |

McCourt RM, Delwiche CF, Karol KG (2004) Charophyte algae and land plant origins. Trends in Ecology & Evolution 19, 661–666.
Charophyte algae and land plant origins.CrossRef |

Mimura T, Tazawa M (1986) Light-induced membrane hyperpolarization and adenine nucleotide levels in perfused Characean cells. Plant & Cell Physiology 27, 319–330.

Mousavi SA, Chauvin A, Pascaud F, Kellenberger S, Farmer EE (2013) Glutamate receptor-like genes mediate leaf-to-leaf wound signalling. Nature 500, 422–426.
Glutamate receptor-like genes mediate leaf-to-leaf wound signalling.CrossRef | 1:CAS:528:DC%2BC3sXhtlWjtrbJ&md5=ac068796f33d29f0226c8dcd96dd3f16CAS |

Sakano K, Tazawa M (1986) Tonoplast origin of the envelope membrane of cytoplasmic droplets prepared from Chara internodal cells. Protoplasma 131, 247–249.
Tonoplast origin of the envelope membrane of cytoplasmic droplets prepared from Chara internodal cells.CrossRef |

Sevriukova O, Kanapeckaite A, Lapeikaite I, Kisnieriene V, Ladygiene R, Sakalauskas V (2014a) Charophyte electrogenesis as a biomarker for assessing the risk from low-dose ionizing radiation to a single plant cell. Journal of Environmental Radioactivity 136, 10–15.
Charophyte electrogenesis as a biomarker for assessing the risk from low-dose ionizing radiation to a single plant cell.CrossRef | 1:CAS:528:DC%2BC2cXhtFOrsLzM&md5=478054dc06d7444ce96bee644e6f1c2bCAS |

Sevriukova O, Kanapeckaite A, Kisnieriene V, Ladygiene R, Lapeikaite I, Sakalauskas V (2014b) Modifying action of tritium on the charophytes bioelectrical response to anthropogenic pollution. Trace Elements and Electrolytes 31, 60–66.
Modifying action of tritium on the charophytes bioelectrical response to anthropogenic pollution.CrossRef | 1:CAS:528:DC%2BC2cXosVyntbs%3D&md5=9dc03d9499da4c5b84a519ca70ac836dCAS |

Shabala S, Shabala L, Gradmann D, Chen Z, Newman I, Mancuso S (2006) Oscillations in plant membrane transport: model predictions, experimental validation, and physiological implications. Journal of Experimental Botany 57, 171–184.
Oscillations in plant membrane transport: model predictions, experimental validation, and physiological implications.CrossRef | 1:CAS:528:DC%2BD2MXhtlCmsbvE&md5=2eabe5f69597d4ef51a068eae55da2a0CAS |

Shiina T, Tazawa M (1987) Ca2+-activated Cl channel in plasmalemma of Nitellopsis obtusa. The Journal of Membrane Biology 99, 137–146.
Ca2+-activated Cl channel in plasmalemma of Nitellopsis obtusa.CrossRef | 1:CAS:528:DyaL1cXnt1aisw%3D%3D&md5=0d0f2cc2b3fd5c1259b28f426d8aa63bCAS |

Shimmen T (1996) Studies on mechano-perception in characean cells: development of a monitoring apparatus. Plant & Cell Physiology 37, 591–597.
Studies on mechano-perception in characean cells: development of a monitoring apparatus.CrossRef | 1:CAS:528:DyaK28Xks1Ons7g%3D&md5=3151a732b9faf9ec6b7a83038b95e020CAS |

Shimmen T, Mimura T, Kikuyama M, Tazawa M (1994) Characean cells as a tool for studying electrophysiological characteristics of plant cells. Cell Structure and Function 19, 263–278.
Characean cells as a tool for studying electrophysiological characteristics of plant cells.CrossRef | 1:STN:280:DyaK2M7ltlOktw%3D%3D&md5=b5d190c963c8aed7faffcfd548e8b77aCAS |

Sibaoka T, Tabata T (1981) Electrotonic coupling between adjacent internodal cells of Chara braunii: transmission of action potentials beyond the node. Plant & Cell Physiology 22, 397–411.

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

Sukhov V (2016) Electrical signals as mechanism of photosynthesis regulation in plants. Photosynthesis Research 130, 373–387.
Electrical signals as mechanism of photosynthesis regulation in plants.CrossRef | 1:CAS:528:DC%2BC28XnsV2it7g%3D&md5=0d71c50732cbe1405a5ecede64987c3aCAS |

Sukhov V, Nerush V, Orlova L, Vodeneev V (2011) Simulation of action potential propagation in plants. Journal of Theoretical Biology 291, 47–55.
Simulation of action potential propagation in plants.CrossRef |

Tazawa M, Kikuyama M (2003) Is Ca2+ release from internal stores involved in membrane excitation in characean cells? Plant & Cell Physiology 44, 518–526.
Is Ca2+ release from internal stores involved in membrane excitation in characean cells?CrossRef | 1:CAS:528:DC%2BD3sXkt1OhsLw%3D&md5=dc8a7406486a8c9ea7a06b801e46d860CAS |

Thiel G, Homann U, Plieth C (1997) Ion channel activity during the action potential in Chara: new insights with new techniques. Journal of Experimental Botany 48, 609–622.
Ion channel activity during the action potential in Chara: new insights with new techniques.CrossRef | 1:CAS:528:DyaK2sXjs1eqtbs%3D&md5=49df27adc81576097ae09e2790ca421bCAS |

Trebacz K, Simonis W, Schonknecht G (1997) Effects of anion channel inhibitors on light-induced potential changes in the liverwort Conocephalum conicum. Plant & Cell Physiology 38, 550–557.
Effects of anion channel inhibitors on light-induced potential changes in the liverwort Conocephalum conicum.CrossRef | 1:CAS:528:DyaK2sXjtl2qtb0%3D&md5=9a9fe969e0233db0bbc086cd343f7c45CAS |

Tsutsui I, Ohkawa TA, Nagai R, Kishimoto U (1987) Role of calcium ion in the excitability and electrogenic pump activity of the Chara corallina membrane: I. Effects of La3+, verapamil, EGTA, W-7, and TFP on the action potential. Journal of Membrane Biology 96, 65–73.
Role of calcium ion in the excitability and electrogenic pump activity of the Chara corallina membrane: I. Effects of La3+, verapamil, EGTA, W-7, and TFP on the action potential.CrossRef | 1:CAS:528:DyaL2sXksFGqu70%3D&md5=286282cbea62329f30f3a62cdb5f46e8CAS |

Tyerman SD, Findlay GP (1989) Current-voltage curves of single Cl- channels which coexist with two types of K+ channel in the tonoplast of Chara corallina. Journal of Experimental Botany 40, 105–117.
Current-voltage curves of single Cl- channels which coexist with two types of K+ channel in the tonoplast of Chara corallina.CrossRef |

Vodeneev V, Akinchits E, Sukhov V (2015) Variation potential in higher plants: mechanisms of generation and propagation. Plant Signaling & Behavior 10, e1057365
Variation potential in higher plants: mechanisms of generation and propagation.CrossRef |

Wacke M, Thiel G (2001) Electrically triggered all-or-none Ca2+-liberation during action potential in the giant alga Chara. Journal of General Physiology 118, 11–22.
Electrically triggered all-or-none Ca2+-liberation during action potential in the giant alga Chara.CrossRef | 1:CAS:528:DC%2BD3MXlt1yqs7o%3D&md5=6dc852a5ac1be035e22251848740d082CAS |



Export Citation