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The Role of Plasmodesmata in the Electrotonic Transmission of Action Potentials

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Plant Electrophysiology

Abstract

The mounting evidence for the transmission of action potentials from cell to cell in a range of plants has exposed our lack of knowledge concerning the mechanism of transmission. While variation potentials (also known as slow wave potentials) involve chemicals released from damaged tissues and/or associated hydrodynamic changes, there is little or no evidence for the involvement of chemicals in the intercellular transmission of action potentials in plants. Plasmodesmata provide electrical connections between plant cells, as demonstrated by experiments in which current injected into one cell can produce a change in potential in a neighboring cell (electrical coupling). The evidence available to date supports a mechanism for electrotonic coupling of cells in transmission of action potentials rather than a direct transmission of excitation along the plasma membranes in the plasmodesmatal pores.

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References

  • Arisz WH (1960) Symplasmitischer Salztransport in Vallineria-Blattern. Protoplasma 52:309–343

    Article  Google Scholar 

  • Badelt K, White RG, Overall RL, Vesk M (1994) Ultrastructural specialization of the cell wall sleeve around plasmodesmata. Am J Bot 81:1422–1427

    Article  Google Scholar 

  • BaluÅ¡ka F, Volkmann D, Menzel D (2005) Plant synapses: actin-based domains for cell-to-cell communication. Trends Plant Sci 10:106–111

    Article  PubMed  Google Scholar 

  • Beebe DU, Turgeon R (1991) Current perspectives on plasmodesmata: structure and function. Physiol Plant 83:194–199

    Article  CAS  Google Scholar 

  • Bell K, Oparka K (2011) Imaging plasmodesmata. Protoplasma 248:9–25

    Article  PubMed  Google Scholar 

  • Bierberg W (1909) Die Beduetung der Protoplasmarotation für der Stofftransport in den Pflanzen. Flora 99:52–80

    Google Scholar 

  • Blackman LM, Overall RL (1998) Immunolocalization of the cytoskeleton to plasmodesmata of Chara corallina. Plant J 14:733–741

    Article  CAS  Google Scholar 

  • Blackman LM, Overall RL (2001) Structure and function of plasmodesmata. Austr J Plant Physiol 28:709–727

    CAS  Google Scholar 

  • Blake IO (1979) The effect of cell excision and microelectrode perforation on membrane resistance measurements of Nitella translucens. Biochim Biophys Acta 554:62–67

    Article  PubMed  CAS  Google Scholar 

  • Bostrom TE, Walker NA (1975) Intercellular transport in plants. I. The rate of transport of chloride and the electrical resistance. J Exp Bot 26:767–782

    Article  CAS  Google Scholar 

  • Burch-Smith TM, Stonebloom S, Xu M, Zambryski PC (2011) Plasmodesmata during development: re-examination of the importance of primary, secondary, and branched plasmodesmata structure versus function. Protoplasma 248:61–74

    Article  PubMed  CAS  Google Scholar 

  • Cao J, Cole IB, Murch SJ (2006) Neurotransmitters, neuroregulators and neurotoxins in the life of plants. Can J Plant Sci 86:1183–1188

    Article  CAS  Google Scholar 

  • Cleland RE, Fujiwara T, Lucas WJ (1994) Plasmodesmal-mediated cell-to-cell transport in wheat roots is modulated by anaerobic stress. Protoplasma 178:81–85

    Article  PubMed  CAS  Google Scholar 

  • Conti F, De Felice LJ, Wanke E (1975) Potassium and sodium ion current noise in the membrane of the squid giant axon. J Physiol 248:45–82

    PubMed  CAS  Google Scholar 

  • Coté R, Thain J, Fensom DS (1987) Increase in electrical resistance of plasmodesmata of Chara induced by an applied pressure gradient across nodes. Can J Bot 65:509–511

    Article  Google Scholar 

  • Deom CM, Schubert KR, Wolf S, Holt CA, Lucas WJ, Beachy RN (1990) Molecular characterization and biological function of the movement protein of tobacco virus in transgenic plants. Proc Nat Acad Sci USA 87:3284–3288

    Article  PubMed  CAS  Google Scholar 

  • Ding B, Itaya A, Woo Y-M (1999) Plasmodesmata and cell-to-cell communication in plants. Int Rev Cytol 190:251–316

    Article  CAS  Google Scholar 

  • Ding B, Turgeon R, Parthasarathy MV (1992) Substructure of freeze-substituted plasmodesmata. Protoplasma 169:28–41

    Article  Google Scholar 

  • Ding D-Q, Tazawa M (1989) Influence of cytoplasmic streaming and turgor pressure gradient on the transnodal transport of rubidium and electrical conductance in Chara corallina. Plant Cell Physiol 30:739–748

    Google Scholar 

  • Drake GA (1979) Electrical coupling, potentials, and resistances in oat coleoptiles: effects of azide and cyanide. J Exp Bot 30:719–725

    Article  CAS  Google Scholar 

  • Drake GA, Carr DJ, Anderson WP (1978) Plasmolysis, plasmodesmata, and the electrical coupling of oat coleoptile cells. J Exp Bot 29:1205–1214

    Article  Google Scholar 

  • Etherton B, Rubinstein B (1978) Evidence for amino acid-H+ co-transport in oat coleoptiles. Plant Physiol 61:933–937

    Article  PubMed  CAS  Google Scholar 

  • Faulkner C, Maule A (2011) Opportunities and successes in the search for plasmodesmal proteins. Protoplasma 248:27–38

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Fernandez-Calvino L, Faulkner C, Walshaw J, Saalbach G, Bayer E, Benitez-Alfonso Y, Maule M (2011) Arabidopsis plasmodesmal proteome. PLoS ONE 6:e18880

    Google Scholar 

  • Fischer RA, Dainty J, Tyree MT (1976) A quantitative investigation of symplasmic transport in Chara corallina. I. Ultrastructure of the nodal complex cell walls. Can J Bot 52:1209–1214

    Article  Google Scholar 

  • Fleurat-Lessard P, Bouché-Pillon S, Leloup C, Lucas WJ, Serrano R, Bonnemain J-L (1995) Absence of plasma membrane H+-ATPase in plasmodesmata located in pit-fields of the young reactive pulvinus of Mimosa pudica L. Protoplasma 188:180–185

    Article  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 

  • Fromm J, Spanswick RM (1993) Characteristics of action potentials in willow (Salix viminalis L.). J Exp Bot 44:1119–1125

    Article  Google Scholar 

  • Furshpan EJ, Potter DD (1968) Low resistance junctions between cells in embryos and tissue culture. Curr Topics Dev Biol 3:95–127

    Article  CAS  Google Scholar 

  • Goodwin PB (1983) Molecular size limit for movement in the symplast of the Elodea leaf. Planta 157:124–130

    Article  CAS  Google Scholar 

  • Hepler PK (1982) Endoplasmic reticulum in the formation of the cell plate and plasmodesmata. Protoplasma 111:121–133

    Article  Google Scholar 

  • Hille B (2001) Ionic channels of excitable membranes, 3rd edn. Sinauer Associates, Sunderland

    Google Scholar 

  • Holdaway-Clarke TL (2005) Regulation of plasmodesmal conductance. In: Oparka K (ed) Plasmodesmata. Blackwell Publishing Ltd., Oxford, pp 279–297

    Chapter  Google Scholar 

  • Holdaway-Clarke TL, Walker NA, Hepler PK, Overall RL (2000) Physiological elevations in cytoplasmic free calcium by cold or ion injection result in transient closure of higher plant plasmodesmata. Planta 210:329–335

    Article  PubMed  CAS  Google Scholar 

  • Holdaway-Clarke TL, Walker NA, Overall RL (1996) Measurement of the electrical resistance of plasmodesmata and membranes of corn suspension-culture cells. Planta 199:537–544

    Article  Google Scholar 

  • Jefferys JGR (1995) Nonsynaptic modulation of neuronal ctivity in the brain—Electric currents and extracellular ions. Physiol Rev 75:689–723

    PubMed  CAS  Google Scholar 

  • Kanno Y, Lowenstein WR (1964) Low-resistance coupling between gland cells. Some observations on intercellular contact membranes and intercellular space. Nature 201:194–195

    Article  PubMed  CAS  Google Scholar 

  • Kinraide TB, Etherton B (1980) Electrical evidence for different mechanisms of uptake for basic, neutral, and acidic amino acids in oat coleoptiles. Plant Physiol 65:1085–1089

    Article  PubMed  CAS  Google Scholar 

  • Krol E, Dziubinska H, Trebacz K, Koselski M, Stolarz M (2007) The influence of glutamic acid and aminoacetic acids on the excitability of the liverwort Conocephalum conicum. J Plant Physiol 164:773–784

    Article  PubMed  CAS  Google Scholar 

  • Lew R (1994) Regulation of electrical coupling between Arabidopsis root hairs. Planta 193:67–73

    Article  CAS  Google Scholar 

  • Liarzi O, Epel BL (2005) Development of a quantitative tool for measuring changes in the coefficient of conductivity of plasmodesmata induced by developmental, biotic, and abiotic signals. Protoplasma 225:67–76

    Article  PubMed  CAS  Google Scholar 

  • Littlefield L, Forsberg C (1965) Absorption and translocation of phosphorus-32 by Chara globularis Thuill. Physiol Plant 18:291–296

    Article  CAS  Google Scholar 

  • Loewenstein WR (1978) Cell-to-cell communication. Permeability, formation, genetics, and functions of the cell–cell membrane channel. In: Andreoli TE, Hoffman JF, Fanestil DD (eds) Membrane physiology. Plenum Press, New York, pp 335–356

    Chapter  Google Scholar 

  • Lou CH (1955) Protoplasmic continuity in plants. Acta Bot Sinica 4:183–222

    Google Scholar 

  • Lucas WJ, Ham B-K, Kim J-Y (2009) Plasmodesmata—bridging the gap between neighboring plant cells. Trends Cell Biol 19:495–503

    Article  PubMed  CAS  Google Scholar 

  • Malone M (1996) Rapid, long-distance signal transmission in higher plants. Adv Bot Res 22:163–228

    Article  CAS  Google Scholar 

  • McLean BG, Hempel FD, Zambryski PC (1997) Plant intercellular communication via plasmodesmata. Plant Cell 9:1043–1054

    Article  PubMed  CAS  Google Scholar 

  • Minorsky PV, Spanswick RM (1989) Electrophysiological evidence for a role for calcium in temperature sensing by roots of cucumber seedlings. Plant Cell Environ 12:137–143

    Article  CAS  Google Scholar 

  • Murch SJ (2006) Neurotransmitters, neuroregulators and neurotoxins in plants. In: BaluÅ¡ka F, Mancuso S, Volkmann D (eds) Communication in plants. Springer, Berlin, pp 137–151

    Chapter  Google Scholar 

  • Overall RL, Blackman LM (1996) A model of the macromolecular structure of plasmodesmata. Trends Plant Sci 1:307–311

    Google Scholar 

  • Overall RL, Gunning BES (1982) Intercellular communication in Azolla roots: II Electrical coupling. Protoplasma 111:151–160

    Article  Google Scholar 

  • Overall RL, Wolfe J, Gunning BES (1982) Intercellular communication in Azolla roots: I Ultrastructure of plasmodesmata. Protoplasma 111:134–150

    Article  Google Scholar 

  • Pickard BG (1973) Action potentials in higher plants. Bot Rev 39:172–201

    Article  Google Scholar 

  • Pickard BG (2007) Delivering force and amplifying signals in plant mechanosensing. Curr Top Membr 58:361–392

    Article  CAS  Google Scholar 

  • Ping Z, Mimura T, Tazawa M (1990) Jumping transmission of action potential between separately placed internodal cells of Chara corallina. Plant Cell Physiol 31:299–302

    Google Scholar 

  • Racusen RH (1976) Phytochrome control of electrical potentials and intercellular coupling in oat coleoptile tissue. Planta 132:25–29

    Article  CAS  Google Scholar 

  • Reid RJ, Overall RL (1992) Intercellular communication in Chara: factors affecting transnodal electrical resistance and solute fluxes. Plant Cell Environ 15:507–517

    Article  Google Scholar 

  • Roy S, Watada AE, Wergin WP (1997) Characterization of the cell wall microdomain surrounding plasmodesmata in apple fruit. Plant Physiol 114:539–547

    PubMed  CAS  Google Scholar 

  • Schönknecht G, Brown JE, Verchot-Lubicz J (2008) Plasmodesmata transport of GFP alone or fused to potato virus X TGBp1 is diffusion driven. Protoplasma 232:143–152

    Article  PubMed  Google Scholar 

  • Shimmen T (2003) Studies on mechano-perception in the Characeae: transduction of pressure signals into electrical signals. Plant Cell Physiol 44:1215–1224

    Article  PubMed  CAS  Google Scholar 

  • Sibaoka T (1966) Action potentials in plant cells. Symp Soc Exp Biol 20:49–73

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Skierczynska J (1968) Some of the electrical characteristics of the cell membrane of Chara australis. J Exp Bot 19:389–406

    Article  Google Scholar 

  • Spanswick RM (1972) Electrical coupling between the cells of higher plants: a direct demonstration of intercellular transport. Planta 102:215–227

    Article  CAS  Google Scholar 

  • Spanswick RM (1974) Symplasmic transport in plants. Symp Soc Exp Biol 28:127–137

    PubMed  Google Scholar 

  • Spanswick RM (1976) Plasmodesmata and symplasmic transport. Encyclopedia of Plant Physiology, New Series IIB:35–53

    Google Scholar 

  • Spanswick RM, Costerton JWF (1967) Plasmodesmata in Nitella translucens: structure and electrical resistance. J Cell Sci 2:451–464

    PubMed  CAS  Google Scholar 

  • Stankovic’ B, Witters DL, Zawadzki T, Davies E (1998) Action potentials and variation potentials in sunflower: an analysis of their relationships and distinguishing characteristics. Physiol Plant 103:51–58

    Article  Google Scholar 

  • Stephens N, Qi Z, Spalding EP (2008) Glutamate receptor subtypes evidenced by differences in desensitizatiion and dependence on the GLR3.3 and GLR3.4 genes. Plant Physiol 146:529–538

    Article  PubMed  CAS  Google Scholar 

  • Stolarz M, Król E, DziubiÅ„ska H, Kurenda A (2010) Glutamate induces series of action potentials and a decrease in circumnutation rate in Helianthus annuus. Physiol Plant 138:329–338

    Article  PubMed  CAS  Google Scholar 

  • Tabata T (1990) Ephaptic transmission and conduction velocity of an action potential in Chara internodal cells placed in parallel and in contact with one another. Plant Cell Physiol 31:575–579

    Google Scholar 

  • Taiz L, Jones RL (1973) Plasmodesmata and an associated cell wall component in barley aleurone tissue. Am J Bot 60:67–75

    Article  CAS  Google Scholar 

  • Tangl E (1879) Ãœber offene Kommunikation zwichen den Zellen des Endosperms einiger Samen. Jahrbücher für wissenschaftliche Botanik 12:170–190

    Google Scholar 

  • Tucker EB (1982) Translocation in the staminal hairs of Setcreasea pupurea. I. A study of cell ultrastructure and cell-to-cell passage of molecular probes. Protoplasma 113:193–201

    Article  CAS  Google Scholar 

  • Tyree MT, Fischer RA, Dainty J (1974) A quantitative investigation of symplasmic transport in Chara corallina. II. The symplasmic transport of chloride. Can J Bot 52:1325–1334

    Article  CAS  Google Scholar 

  • Ueki S, Citovsky V (2011) To gate, or not to gate: regulatory mechanisms for intercellular protein transport and virus movement in plants. Mol Plant 4:782–793

    Article  PubMed  CAS  Google Scholar 

  • van Bel AJE, Knoblauch M, Furch ACU, Hafke JB (2011) (Questions)n on phloem biology. 1. Electropotential waves, Ca2+ fluxes and cellular cascades along the propagation pathway. Plant Sci 181:210–218

    Article  PubMed  Google Scholar 

  • van Rijen HVM, Wilders R, Jongsma HJ (1999) Electrical coupling. In: van Bel AJE, van Kesteren WJP (eds) Plasmodesmata. Structure, function, role in cell communication. Springer, Berlin, pp 51–65

    Google Scholar 

  • Van Sambeek JW, Pickard BG (1976) Modification of rapid electrical, metabolic, transpirational, and photosynthetic changes by factors released from wounds. II. Mediation of the variation potential by Ricca’s factor. Can J Bot 54:2651–2661

    Article  Google Scholar 

  • Veenstra RD (2000) Ion permeation through connexin gap junction channels: effects on conductance and selectivity. Curr Topics Membr 49:95–129

    Article  CAS  Google Scholar 

  • White RG, Barton DA (2011) The cytoskeleton in plasmodesmata: a role in intercellular transport? J Exp Bot 62:5249–5266

    Article  PubMed  CAS  Google Scholar 

  • Williams SE, Spanswick RM (1976) Propagation of the neuroid action potential of the carnivorous plant Drosera. J Comp Physiol A 108:211–223

    Article  Google Scholar 

  • Wolf S, Deom CM, Beachy RN, Lucas WJ (1989) Movement protein of tobacco mosaic virus modifies plasmodesmatal size exclusion limit. Science 246:377–379

    Article  PubMed  CAS  Google Scholar 

  • Zambryski PC, Crawford K (2000) Plasmodesmata: gatekeepers for cell-to-cell transport of developmental signals in plants. Annu Rev Cell Dev Biol 16:393–421

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Roger M. Spanswick .

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Spanswick, R.M. (2012). The Role of Plasmodesmata in the Electrotonic Transmission of Action Potentials. In: Volkov, A. (eds) Plant Electrophysiology. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-29110-4_9

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