The Role of Plasmodesmata in the Electrotonic Transmission of Action Potentials

  • Roger M. Spanswick


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.


Specific Resistance Electrical Coupling Internodal Cell Intercellular Transport Characean Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Arisz WH (1960) Symplasmitischer Salztransport in Vallineria-Blattern. Protoplasma 52:309–343CrossRefGoogle Scholar
  2. Badelt K, White RG, Overall RL, Vesk M (1994) Ultrastructural specialization of the cell wall sleeve around plasmodesmata. Am J Bot 81:1422–1427CrossRefGoogle Scholar
  3. Baluška F, Volkmann D, Menzel D (2005) Plant synapses: actin-based domains for cell-to-cell communication. Trends Plant Sci 10:106–111PubMedCrossRefGoogle Scholar
  4. Beebe DU, Turgeon R (1991) Current perspectives on plasmodesmata: structure and function. Physiol Plant 83:194–199CrossRefGoogle Scholar
  5. Bell K, Oparka K (2011) Imaging plasmodesmata. Protoplasma 248:9–25PubMedCrossRefGoogle Scholar
  6. Bierberg W (1909) Die Beduetung der Protoplasmarotation für der Stofftransport in den Pflanzen. Flora 99:52–80Google Scholar
  7. Blackman LM, Overall RL (1998) Immunolocalization of the cytoskeleton to plasmodesmata of Chara corallina. Plant J 14:733–741CrossRefGoogle Scholar
  8. Blackman LM, Overall RL (2001) Structure and function of plasmodesmata. Austr J Plant Physiol 28:709–727Google Scholar
  9. Blake IO (1979) The effect of cell excision and microelectrode perforation on membrane resistance measurements of Nitella translucens. Biochim Biophys Acta 554:62–67PubMedCrossRefGoogle Scholar
  10. Bostrom TE, Walker NA (1975) Intercellular transport in plants. I. The rate of transport of chloride and the electrical resistance. J Exp Bot 26:767–782CrossRefGoogle Scholar
  11. 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 248:61–74PubMedCrossRefGoogle Scholar
  12. Cao J, Cole IB, Murch SJ (2006) Neurotransmitters, neuroregulators and neurotoxins in the life of plants. Can J Plant Sci 86:1183–1188CrossRefGoogle Scholar
  13. Cleland RE, Fujiwara T, Lucas WJ (1994) Plasmodesmal-mediated cell-to-cell transport in wheat roots is modulated by anaerobic stress. Protoplasma 178:81–85PubMedCrossRefGoogle Scholar
  14. Conti F, De Felice LJ, Wanke E (1975) Potassium and sodium ion current noise in the membrane of the squid giant axon. J Physiol 248:45–82PubMedGoogle Scholar
  15. 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 65:509–511CrossRefGoogle Scholar
  16. 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 87:3284–3288PubMedCrossRefGoogle Scholar
  17. Ding B, Itaya A, Woo Y-M (1999) Plasmodesmata and cell-to-cell communication in plants. Int Rev Cytol 190:251–316CrossRefGoogle Scholar
  18. Ding B, Turgeon R, Parthasarathy MV (1992) Substructure of freeze-substituted plasmodesmata. Protoplasma 169:28–41CrossRefGoogle Scholar
  19. 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 30:739–748Google Scholar
  20. Drake GA (1979) Electrical coupling, potentials, and resistances in oat coleoptiles: effects of azide and cyanide. J Exp Bot 30:719–725CrossRefGoogle Scholar
  21. Drake GA, Carr DJ, Anderson WP (1978) Plasmolysis, plasmodesmata, and the electrical coupling of oat coleoptile cells. J Exp Bot 29:1205–1214CrossRefGoogle Scholar
  22. Etherton B, Rubinstein B (1978) Evidence for amino acid-H+ co-transport in oat coleoptiles. Plant Physiol 61:933–937PubMedCrossRefGoogle Scholar
  23. Faulkner C, Maule A (2011) Opportunities and successes in the search for plasmodesmal proteins. Protoplasma 248:27–38PubMedCrossRefGoogle Scholar
  24. Felle HH, Zimmermann MR (2007) Systemic signalling in barley through action potentials. Planta 226:203–214PubMedCrossRefGoogle Scholar
  25. Fernandez-Calvino L, Faulkner C, Walshaw J, Saalbach G, Bayer E, Benitez-Alfonso Y, Maule M (2011) Arabidopsis plasmodesmal proteome. PLoS ONE 6:e18880Google Scholar
  26. 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 52:1209–1214CrossRefGoogle Scholar
  27. 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 188:180–185CrossRefGoogle Scholar
  28. Fromm J, Lautner S (2007) Electrical signals and their physiological significance in plants. Plant Cell Environ 30:249–257PubMedCrossRefGoogle Scholar
  29. Fromm J, Spanswick RM (1993) Characteristics of action potentials in willow (Salix viminalis L.). J Exp Bot 44:1119–1125CrossRefGoogle Scholar
  30. Furshpan EJ, Potter DD (1968) Low resistance junctions between cells in embryos and tissue culture. Curr Topics Dev Biol 3:95–127CrossRefGoogle Scholar
  31. Goodwin PB (1983) Molecular size limit for movement in the symplast of the Elodea leaf. Planta 157:124–130CrossRefGoogle Scholar
  32. Hepler PK (1982) Endoplasmic reticulum in the formation of the cell plate and plasmodesmata. Protoplasma 111:121–133CrossRefGoogle Scholar
  33. Hille B (2001) Ionic channels of excitable membranes, 3rd edn. Sinauer Associates, SunderlandGoogle Scholar
  34. Holdaway-Clarke TL (2005) Regulation of plasmodesmal conductance. In: Oparka K (ed) Plasmodesmata. Blackwell Publishing Ltd., Oxford, pp 279–297CrossRefGoogle Scholar
  35. 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 210:329–335PubMedCrossRefGoogle Scholar
  36. Holdaway-Clarke TL, Walker NA, Overall RL (1996) Measurement of the electrical resistance of plasmodesmata and membranes of corn suspension-culture cells. Planta 199:537–544CrossRefGoogle Scholar
  37. Jefferys JGR (1995) Nonsynaptic modulation of neuronal ctivity in the brain—Electric currents and extracellular ions. Physiol Rev 75:689–723PubMedGoogle Scholar
  38. Kanno Y, Lowenstein WR (1964) Low-resistance coupling between gland cells. Some observations on intercellular contact membranes and intercellular space. Nature 201:194–195PubMedCrossRefGoogle Scholar
  39. Kinraide TB, Etherton B (1980) Electrical evidence for different mechanisms of uptake for basic, neutral, and acidic amino acids in oat coleoptiles. Plant Physiol 65:1085–1089PubMedCrossRefGoogle Scholar
  40. 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 164:773–784PubMedCrossRefGoogle Scholar
  41. Lew R (1994) Regulation of electrical coupling between Arabidopsis root hairs. Planta 193:67–73CrossRefGoogle Scholar
  42. 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 225:67–76PubMedCrossRefGoogle Scholar
  43. Littlefield L, Forsberg C (1965) Absorption and translocation of phosphorus-32 by Chara globularis Thuill. Physiol Plant 18:291–296CrossRefGoogle Scholar
  44. 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 335–356CrossRefGoogle Scholar
  45. Lou CH (1955) Protoplasmic continuity in plants. Acta Bot Sinica 4:183–222Google Scholar
  46. Lucas WJ, Ham B-K, Kim J-Y (2009) Plasmodesmata—bridging the gap between neighboring plant cells. Trends Cell Biol 19:495–503PubMedCrossRefGoogle Scholar
  47. Malone M (1996) Rapid, long-distance signal transmission in higher plants. Adv Bot Res 22:163–228CrossRefGoogle Scholar
  48. McLean BG, Hempel FD, Zambryski PC (1997) Plant intercellular communication via plasmodesmata. Plant Cell 9:1043–1054PubMedCrossRefGoogle Scholar
  49. Minorsky PV, Spanswick RM (1989) Electrophysiological evidence for a role for calcium in temperature sensing by roots of cucumber seedlings. Plant Cell Environ 12:137–143CrossRefGoogle Scholar
  50. Murch SJ (2006) Neurotransmitters, neuroregulators and neurotoxins in plants. In: Baluška F, Mancuso S, Volkmann D (eds) Communication in plants. Springer, Berlin, pp 137–151CrossRefGoogle Scholar
  51. Overall RL, Blackman LM (1996) A model of the macromolecular structure of plasmodesmata. Trends Plant Sci 1:307–311Google Scholar
  52. Overall RL, Gunning BES (1982) Intercellular communication in Azolla roots: II Electrical coupling. Protoplasma 111:151–160CrossRefGoogle Scholar
  53. Overall RL, Wolfe J, Gunning BES (1982) Intercellular communication in Azolla roots: I Ultrastructure of plasmodesmata. Protoplasma 111:134–150CrossRefGoogle Scholar
  54. Pickard BG (1973) Action potentials in higher plants. Bot Rev 39:172–201CrossRefGoogle Scholar
  55. Pickard BG (2007) Delivering force and amplifying signals in plant mechanosensing. Curr Top Membr 58:361–392CrossRefGoogle Scholar
  56. Ping Z, Mimura T, Tazawa M (1990) Jumping transmission of action potential between separately placed internodal cells of Chara corallina. Plant Cell Physiol 31:299–302Google Scholar
  57. Racusen RH (1976) Phytochrome control of electrical potentials and intercellular coupling in oat coleoptile tissue. Planta 132:25–29CrossRefGoogle Scholar
  58. Reid RJ, Overall RL (1992) Intercellular communication in Chara: factors affecting transnodal electrical resistance and solute fluxes. Plant Cell Environ 15:507–517CrossRefGoogle Scholar
  59. Roy S, Watada AE, Wergin WP (1997) Characterization of the cell wall microdomain surrounding plasmodesmata in apple fruit. Plant Physiol 114:539–547PubMedGoogle Scholar
  60. Schönknecht G, Brown JE, Verchot-Lubicz J (2008) Plasmodesmata transport of GFP alone or fused to potato virus X TGBp1 is diffusion driven. Protoplasma 232:143–152PubMedCrossRefGoogle Scholar
  61. Shimmen T (2003) Studies on mechano-perception in the Characeae: transduction of pressure signals into electrical signals. Plant Cell Physiol 44:1215–1224PubMedCrossRefGoogle Scholar
  62. Sibaoka T (1966) Action potentials in plant cells. Symp Soc Exp Biol 20:49–73PubMedGoogle Scholar
  63. Sibaoka T, Tabata T (1981) Electrotonic coupling between adjacent internodal cells of Chara braunii: transmission of action potentials beyond the node. Plant Cell Physiol 22:397–411Google Scholar
  64. Skierczynska J (1968) Some of the electrical characteristics of the cell membrane of Chara australis. J Exp Bot 19:389–406CrossRefGoogle Scholar
  65. Spanswick RM (1972) Electrical coupling between the cells of higher plants: a direct demonstration of intercellular transport. Planta 102:215–227CrossRefGoogle Scholar
  66. Spanswick RM (1974) Symplasmic transport in plants. Symp Soc Exp Biol 28:127–137PubMedGoogle Scholar
  67. Spanswick RM (1976) Plasmodesmata and symplasmic transport. Encyclopedia of Plant Physiology, New Series IIB:35–53Google Scholar
  68. Spanswick RM, Costerton JWF (1967) Plasmodesmata in Nitella translucens: structure and electrical resistance. J Cell Sci 2:451–464PubMedGoogle Scholar
  69. 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 103:51–58CrossRefGoogle Scholar
  70. 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 146:529–538PubMedCrossRefGoogle Scholar
  71. Stolarz M, Król E, Dziubińska H, Kurenda A (2010) Glutamate induces series of action potentials and a decrease in circumnutation rate in Helianthus annuus. Physiol Plant 138:329–338PubMedCrossRefGoogle Scholar
  72. 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 31:575–579Google Scholar
  73. Taiz L, Jones RL (1973) Plasmodesmata and an associated cell wall component in barley aleurone tissue. Am J Bot 60:67–75CrossRefGoogle Scholar
  74. Tangl E (1879) Über offene Kommunikation zwichen den Zellen des Endosperms einiger Samen. Jahrbücher für wissenschaftliche Botanik 12:170–190Google Scholar
  75. 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 113:193–201CrossRefGoogle Scholar
  76. 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 52:1325–1334CrossRefGoogle Scholar
  77. Ueki S, Citovsky V (2011) To gate, or not to gate: regulatory mechanisms for intercellular protein transport and virus movement in plants. Mol Plant 4:782–793PubMedCrossRefGoogle Scholar
  78. 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 181:210–218PubMedCrossRefGoogle Scholar
  79. 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 51–65Google Scholar
  80. 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 54:2651–2661CrossRefGoogle Scholar
  81. Veenstra RD (2000) Ion permeation through connexin gap junction channels: effects on conductance and selectivity. Curr Topics Membr 49:95–129CrossRefGoogle Scholar
  82. White RG, Barton DA (2011) The cytoskeleton in plasmodesmata: a role in intercellular transport? J Exp Bot 62:5249–5266PubMedCrossRefGoogle Scholar
  83. Williams SE, Spanswick RM (1976) Propagation of the neuroid action potential of the carnivorous plant Drosera. J Comp Physiol A 108:211–223CrossRefGoogle Scholar
  84. Wolf S, Deom CM, Beachy RN, Lucas WJ (1989) Movement protein of tobacco mosaic virus modifies plasmodesmatal size exclusion limit. Science 246:377–379PubMedCrossRefGoogle Scholar
  85. Zambryski PC, Crawford K (2000) Plasmodesmata: gatekeepers for cell-to-cell transport of developmental signals in plants. Annu Rev Cell Dev Biol 16:393–421PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Department of Biological and Environmental EngineeringCornell UniversityIthacaUSA

Personalised recommendations