Generation, Transmission, and Physiological Effects of Electrical Signals in Plants

Chapter

Abstract

This review explores the relationship between electrical long-distance signaling and the potential consequences for physiological processes in plants. Electrical signals such as action potentials (APs) and variation potentials (VPs) can be generated by spontaneous changes in temperature, light, touch, soil water content, by electrical as well as chemical stimulation or by wounding. An AP is evoked when the stimulus is sufficiently great to depolarize the membrane to below a certain threshold, while VPs are mostly induced by wounding, which induces a hydraulic wave transmitted through the xylem, thereby causing a local electrical response in the neighboring symplastic cells. Once generated, the signal can be transmitted over short distances from cell-to-cell through plasmodesmata, and after having reached the phloem it can also be propagated over long distances along the sieve tube plasma membrane. Such electrical messages may have a large impact on distant cells, as numerous well-documented physiological effects of long-distance electrical signaling have been shown. Electrical signals, for instance, affect phloem transport as well as photosynthesis, respiration, nutrient uptake, and gene expression.

Keywords

Wood Formation Sieve Tube Sieve Element Chloroplast Movement Phloem Transport 
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.

References

  1. Ache P, Becker D, Ivashikina N, Dietrich P, Roelfsema MRG, Hedrich R (2000) GORK, a delayed outward rectifier expressed in guard cells of Arabidopsis thaliana, is a K+ selective, K+ sensing ion channel. FEBS Lett 486:93–98PubMedGoogle Scholar
  2. Ache P, Becker D, Deeken R, Dreyer I, Weber H, Fromm J, Hedrich R (2001) VFK1, a Vicia faba K+ channel involved in phloem unloading. Plant J 27:571–580PubMedGoogle Scholar
  3. Ache P, Fromm J, Hedrich R (2010) Potassium-dependent wood formation in poplar: seasonal aspects and environmental limitations. Plant Biol 12:259–267PubMedGoogle Scholar
  4. Adrian ED, Bronk DW (1928) The discharge of impulses in motor nerve fibres. I. Impulses in single fibres of the phrenic nerve. J Physiol 66:81–101PubMedGoogle Scholar
  5. Arend M, Weisenseel MH, Brummer M, Osswald W, Fromm J (2002) Seasonal changes of plasma membrane H+-ATPase and endogenous ion current during growth in poplar plants. Plant Physiol 129:1651–1663PubMedGoogle Scholar
  6. Arend M, Monshausen G, Wind C, Weisenseel MH, Fromm J (2004) Effect of potassium deficiency on the plasma membrane H+-ATPase of the wood ray parenchyma in poplar. Plant Cell Environ 27:1288–1296Google Scholar
  7. Arend M, Stinzing A, Wind C, Langer K, Latz A, Ache P, Fromm J, Hedrich R (2005) Polar-localised poplar K+ channel capable of controlling electrical properties of wood-forming cells. Planta 223:140–148PubMedGoogle Scholar
  8. Beilby MJ, Coster HGL (1979) The action potential in Chara corallina. II. Two activation-inactivation transients in voltage clamps of plasmalemma. Austr J Plant Phys 6:329–335Google Scholar
  9. Beyhl D, Hörtensteiner S, Martinoia E, Farmer EE, Fromm J, Marten I, Hedrich R (2009) The fou2 mutation in the major vacuolar cation channel TPC1 confers tolerance to inhibitory luminal calcium. Plant J 58:715–723PubMedGoogle Scholar
  10. Bulychev AA, Kamzolkina NA (2006) Effect of action potential on photosynthesis and spatially distributed H+ fluxes in cells and chloroplasts of Chara corallina. Russ J Plant Physiol 53:5–14Google Scholar
  11. Canny MJP (1975) Mass transfer. In: Zimmermann HM, Milburn JA (eds) Encyclopedia of plant physiology. Springer, Berlin, pp 139–153Google Scholar
  12. Carpaneto A, Geiger D, Bamberg E, Sauer N, Fromm J, Hedrich R (2005) Phloem-localized, proton-coupled sucrose carrier ZmSUT1 mediates sucrose efflux under control of sucrose gradient and pmf. J Biol Chem 280:21437–21443PubMedGoogle Scholar
  13. Carpaneto A, Ivashikina N, Levchenko V, Krol E, Zhu J-K, Hedrich R (2007) Cold transiently activates calcium-permeable channels in Arabidopsis mesophyll cells. Plant Physiol 143:487–494PubMedGoogle Scholar
  14. Cosgrove DJ, Hedrich R (1991) Stretch-activated chloride, potassium, and calcium channels coexisting in plasma membranes of guard cells of Vicia faba L. Planta 186:143–153PubMedGoogle Scholar
  15. Davies E (1987) Action potentials as multifunctional signals in plants: a unifying hypothesis to explain apparently disparate wound responses. Plant Cell Environ 10:623–631Google Scholar
  16. Davies E (1993) Intercellular and intracellular signals in plants and their transduction via the membrane—cytoskeleton interface. Semin Cell Biol 4:139–147PubMedGoogle Scholar
  17. Davies E (2004) New functions for electrical signals in plants. New Phytol 161:607–610Google Scholar
  18. Davies E, Ramaiah KVA, Abe S (1986) Wounding inhibits protein synthesis yet stimulates polysome formation in aged, excised pea epicotyls. Plant Cell Physiol 27:1377–1386Google Scholar
  19. Davies E, Stankovic B (2006) Electrical signals, the cytoskeleton, and gene expression: a hypothesis on the coherence of cellular processes to environmental insult. In: Baluska F, Mancuso S, Volkmann D (eds) Communication in plants—neuronal aspects of plant life. Springer, Berlin, pp 309–320Google Scholar
  20. Davies WJ, Zhang J (1991) Root signals and the regulation of growth and development of plants in drying soil. Annu Rev Plant Physiol Plant Mol Biol 42:55–76Google Scholar
  21. Deeken R, Geiger D, Fromm J, Koroleva O, Ache P, Langenfeld-Heyser R, Sauer N, May ST, Hedrich R (2002) Loss of the AKT2/3 potassium channel affects sugar loading into the phloem of Arabidopsis. Planta 216:334–344PubMedGoogle Scholar
  22. Demidchik V, Maathuis FJM (2007) Physiological roles of non-selective cation channels in plants: from salt stress to signalling and development. New Phytol 175:387–404PubMedGoogle Scholar
  23. Ding JP, Pickard BG (1993) Modulation of mechanosensitive calcium-selective cation channels by temperature. Plant J 3:713–720PubMedGoogle Scholar
  24. Dutta R, Robinson KR (2004) Identification and characterization of stretch-activated ion channels in pollen protoplasts. Plant Physiol 135:1398–1406PubMedGoogle Scholar
  25. Dziubinska H, Trebacz K, Zawadzki T (1989) The effect of excitation on the rate of respiration in the liverwort Conocephalum conicum. Physiol Plant 75:417–423Google Scholar
  26. Eschrich W, Fromm J, Evert RF (1988) Transmission of electric signals in sieve tubes of zucchini plants. Bot Acta 101:327–331Google Scholar
  27. Evert RF, Eschrich W, Eichhorn SE (1973) P-protein distribution in mature sieve elements of Cucurbita maxima. Planta 109:193–210Google Scholar
  28. Evert R (1990) Dicotyledons. In: Behnke H-D, Sjolund RD (eds) Sieve elements—comparative structure, induction and development. Springer, Berlin, pp 103–137Google Scholar
  29. Filek M, Koscielniak J (1997) The effect of wounding the roots by high temperature on the respiration rate of the shoot and propagation of electric signal in horse bean seedlings (Vicia faba L. Minor). Plant Science 123:39–46 Google Scholar
  30. Findlay GP (1961) Voltage-clamp experiments with Nitella. Nature 191:812–814Google Scholar
  31. Findlay GP (1962) Calcium ions and the action potential in Nitella. Aust J Biol Sci 15:69–82Google Scholar
  32. Fisahn J, Herde O, Willmitzer L, Pena-Cortes 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 Physiol 45:456–459PubMedGoogle Scholar
  33. Forterre Y, Skothelm JM, Dumals J, Mahadevan L (2005) How the venus flytrap snaps. Nature 433:421–425PubMedGoogle Scholar
  34. Fromm J (1991) Control of phloem unloading by action potentials in Mimosa. Physiol Plant 83:529–533Google Scholar
  35. Fromm J (2010) Wood formation of trees in relation to potassium and calcium nutrition. Tree Physiol 30:1140–1147PubMedGoogle Scholar
  36. Fromm J, Bauer T (1994) Action potentials in maize sieve tubes change phloem translocation. J Exp Bot 45:463–469Google Scholar
  37. Fromm J, Eschrich W (1988a) Transport processes in stimulated and non-stimulated leaves of Mimosa pudica. I. The movement of 14C-labelled photoassimilates. Trees 2:7–17Google Scholar
  38. Fromm J, Eschrich W (1988b) Transport processes in stimulated and non-stimulated leaves of Mimosa pudica. II. Energesis and transmission of seismic stimulations. Trees 2:18–24Google Scholar
  39. Fromm J, Eschrich W (1988c) Transport processes in stimulated and non-stimulated leaves of Mimosa pudica. III. Displacement of ions during seismonastic leaf movements. Trees 2:65–72Google Scholar
  40. Fromm J, Eschrich W (1989) Correlation of ionic movements with phloem unloading and loading in barley leaves. Plant Physiol Biochem 27:577–585Google Scholar
  41. Fromm J, Eschrich W (1990) Seismonastic movements in Mimosa. In: Satter RL, Gorton HL, Vogelmann TC (eds) The pulvinus: motor organ for leaf movement. Americ Soc Plant Physiol, Rockville, pp 25–43Google Scholar
  42. Fromm J, Eschrich W (1993) Electric signals released from roots of willow (Salix viminalis L.) change transpiration and photosynthesis. J Plant Physiol 141:673–680Google Scholar
  43. Fromm J, Fei H (1998) Electrical signaling and gas exchange in maize plants of drying soil. Plant Sci 132:203–213Google Scholar
  44. Fromm J, Lautner S (2005) Characteristics and functions of phloem-transmitted electrical signals in higher plants. In: Baluska F, Mancuso S, Volkmann D (eds) Communication in plants–neuronal aspects of plant life. Springer, Heidelberg, pp 321–332Google Scholar
  45. Fromm J, Lautner S (2007) Electrical signals and their physiological significance in plants. Plant Cell Environm 30:249–257Google Scholar
  46. Fromm J, Spanswick R (1993) Characteristics of action potentials in willow (Salix viminalis L.). J Exp Bot 44:1119–1125Google Scholar
  47. Fromm J, Hajirezaei M, Wilke I (1995) The biochemical response of electrical signaling in the reproductive system of Hibiscus plants. Plant Physiol 109:375–384PubMedGoogle Scholar
  48. Fromm J, Meyer AJ, Weisenseel MH (1997) Growth, membrane potential and endogenous ion currents of willow (Salix viminalis) roots are all affected by abscisic acid and spermine. Physiol Plant 99:529–537Google Scholar
  49. Furch ACU, Hafke JB, Schulz A, van Bel AJE (2007) Ca2+-mediated remote control of reversible sieve tube occlusion in Vicia faba. J Exp Bot 58:2827–2838PubMedGoogle Scholar
  50. Furch ACU, van Bel AJE, Fricker MD, Felle HH, Fuchs M, Hafke JB (2009) Sieve element Ca2+ channels as relay stations between remote stimulus and sieve tube occlusion. Plant Cell 21:2118–2131PubMedGoogle Scholar
  51. Furch ACU, Zimmermann MR, Will T, Hafke JB, van Bel AJE (2010) Remote-controlled stop of mass flow by biphasic occlusion in Cucurbita maxima. J Exp Bot 61:3697–3708PubMedGoogle Scholar
  52. Gaffey CT, Mullins LJ (1958) Ion fluxes during the action potential in Chara. J Physiol 144:505–524PubMedGoogle Scholar
  53. Gamalei YV, Fromm J, Krabel D, Eschrich W (1994) Chloroplast movement as response to wounding in Elodea canadensis. J Plant Physiol 144:518–524Google Scholar
  54. Gaymard F, Pilot G, Lacombe B, Bouchez D, Bruneau D, Boucherez J, Michaux-Ferriere N, Thibaud JB, Sentenac H (1998) Identification and disruption of a plant shaker-like outward channel involved in K+ release into the xylem sap. Cell 94:647–655PubMedGoogle Scholar
  55. Grams TEE, Koziolek C, Lautner S, Matyssek R, Fromm J (2007) Distinct roles of electric and hydraulic signals on the reaction of leaf gas exchange upon re-irrigation in Zea mays L. Plant Cell Environ 30:79–84PubMedGoogle Scholar
  56. Grams TEE, 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 Environ 32:319–326PubMedGoogle Scholar
  57. Gurovich LA, Hermosilla P (2009) Electric signalling in fruit trees in response to water applications and light-darkness conditions. J Plant Physiol 166:290–300PubMedGoogle Scholar
  58. Gustin MC, Zhou XL, Martinac B, Kung C (1988) A mechanosensitive ion channel in the yeast plasma membrane. Science 242:762–765PubMedGoogle Scholar
  59. Hamilton DWA, Hills A, Kohler B, Blatt MR (2000) Ca2+ channels at the plasma membrane of stomatal guard cells are activated by hyperpolarization and abscisic acid. Proc Natl Acad Sci USA 97:4867–4972Google Scholar
  60. Hayama T, Shimmen T, Tazawa M (1979) Participation of Ca2+ in cessation of cytoplasmic streaming induced by membrane excitation in Characeae internodal cells. Protoplasma 99:305–321Google Scholar
  61. Hörmann G (1898) Studien über die Protoplasmaströmung bei den Characaean. Gustav Fischer Verlag, JenaGoogle Scholar
  62. Hodick D, Sievers A (1988) The action potential of Dionaea muscipula Ellis. Planta 174:8–18Google Scholar
  63. Hope AB (1961) Ionic relations of cells of Chara corallina. V. The action potential. Aust J Biol Sci 14:312–322Google Scholar
  64. Kayler Z, Gessler A, Buchmann N (2010) What is the speed of link between aboveground and belowground processes? New Phytol 187:885–888PubMedGoogle Scholar
  65. Kempers R, Ammerlaan A, van Bel AJE (1998) Symplasmic constriction and ultrastructural features of the sieve element/companion cell complex in the transport phloem of apoplasmically and symplasmically phloem-loading species. Plant Physiol 116:271–278Google Scholar
  66. Kiegle E, Gilliham M, Haseloff J, Tester M (2000) Hyperpolarisation activated calcium currents found only in cells from the elongation zone of Arabidopsis thaliana roots. Plant J 21:225–229PubMedGoogle Scholar
  67. Kishimoto U (1968) Response of Chara internodes to mechanical stimulation. Ann Rep Biol Works Fac Sci Osaka Univ 16:61–66Google Scholar
  68. Knoblauch M, Peters WS, Ehlers K, van Bel AJE (2001) Reversible calcium-regulated stopcocks in legume sieve tubes. Plant Cell 13:1221–1230PubMedGoogle Scholar
  69. Koziolek C, Grams TEE, Schreiber U, Matyssek R, Fromm J (2004) Transient knockout of photosynthesis mediated by electrical signals. New Phytol 161:715–722Google Scholar
  70. Langer K, Ache P, Geiger D, Stinzing A, Arend M, Wind C, Regan S, Fromm J, Hedrich R (2002) Poplar potassium transporters capable of controlling K+ homeostasis and K+ dependent xylogenesis. Plant J 32:997–1009PubMedGoogle Scholar
  71. Lautner S, Grams TEE, Matyssek R, Fromm J (2005) Characteristics of electrical signals in poplar and responses in photosynthesis. Plant Physiol 138: 2200–2209Google Scholar
  72. Lunevsky VZ, Zherelova OM, Vostrikov IY, Berestovsky GN (1983) Excitation of Characeae cell membranes as a result of activation of calcium and chloride channels. J Membr Biol 72:43–58Google Scholar
  73. Mansfield TA, Hetherington AM, Atkinson CJ (1990) Some current aspects of stomatal physiology. Annu Rev Plant Physiol Plant Mol Biol 41:55–75Google Scholar
  74. Martinac B, Buechner M, Delcour AH, Adler J, Kung C (1987) Pressure-sensitive ion channel in Escherichia coli. Proc Natl Acad Sci USA 84:2297–2301PubMedGoogle Scholar
  75. McCormack E, Velasquez L, Delk NA, Braam J (2006) Touch-responsive behaviours and gene expression in plants. In: Baluska F, Mancuso S, Volkmann D (eds) Communication in plants—neuronal aspects of plant life. Springer, Berlin, pp 249–260Google Scholar
  76. Mencuccini M, Hölttä T (2010) The significance of phloem transport for the speed with which canopy photosynthesis and belowground respiration are linked. New Phytol 185:189–203PubMedGoogle Scholar
  77. Minchin PEH, Thorpe MR (1983) A rate of cooling response in phloem translocation. J Exp Bot 34:529–536Google Scholar
  78. Mühling KH, Sattelmacher B (1997) Determination of apoplastic K+ in intact leaves by ratio imaging of PBFI fluorescence. J Exp Bot 48:1609–1614Google Scholar
  79. Mummert E, Gradmann D (1976) Voltage dependent potassium fluxes and the significance of action potentials in Acetabularia. Biochim Biophys Acta 443:443–450PubMedGoogle Scholar
  80. Nick P (2008) Microtubules as sensors for abiotic stimuli. In: Nick P (ed) Plant microtubules, 2nd edn. Springer, Berlin, pp 175–203Google Scholar
  81. Oda K (1976) Simultaneous recording of potassium and chloride effluxes during an action potential in Chara corallina. Plant Cell Physiol 17:1085–1088Google Scholar
  82. Oyarce P, Gurovich L (2010) Electrical signals in avocado trees. Plant Signaling Behav 5(1):34–41Google Scholar
  83. Plieth C, Hansen U-P, Knight H, Knight MR (1999) Temperature sensing by plants: the primary characteristics of signal perception and calcium response. Plant J 18:491–497PubMedGoogle Scholar
  84. Preiss J, Robinson N, Spilatro S, McNamara K (1985) Starch synthesis and its regulation. In: Heath R, Preiss J (eds) Regulation of carbon partitioning in photosynthetic tissue. Amer Soc Plant Physiol, Rockville, pp 1–26Google Scholar
  85. Pyatygin SS, Opritov VA, Vodeneev VA (2008) Signaling role of action potential in higher plants. Russ J Plant Physiol 55:285–291Google Scholar
  86. Rhodes J, Thain JF, Wildon DC (1996) The pathway for systemic electrical signal transduction in the wounded tomato plant. Planta 200:50–57Google Scholar
  87. Rienmüller F, Beyhl D, Lautner S, Fromm J, Al-Rasheid KAS, Ache P, Farmer EE, Marten I, Hedrich R (2010) Guard cell-specific calcium sensitivity of high density and activity SV/TPC1 channels. Plant Cell Physiol 51(9):1548–1554PubMedGoogle Scholar
  88. Schurr U, Gollan T (1990) Composition of xylem sap of plants experiencing root water stress: a descriptive study. In: Davies WJ, Jeffcoat B (eds) Importance of root to shoot communication in the response to environmental stress. Br Soc Plant Growth Regul, Bristol, pp 201–214Google Scholar
  89. Shabala S, Pang J, Zhou M, Shabala L, Cuin TA, Nick P, Wegner LH (2009) Electrical signalling and cytokinins mediate effects of light and root cutting on ion uptake in intact plants. Plant Cell Environ 32:194–207PubMedGoogle Scholar
  90. Shiina T, Tazawa M (1986) Action potential in Luffa cylindrica and its effects on elongation growth. Plant Cell Physiol 27:1081–1089Google Scholar
  91. Shvetsova T, Mwesigwa J, Labady A, Kelly S, Thomas D, Lewis K, Volkov AG (2002) Soybean electrophysiology: effects of acid rain. Plant Sci 162:723–731Google Scholar
  92. Sibaoka T (1969) Physiology of rapid movements in higher plants. Ann Rev Plant Physiol 20:165–184Google Scholar
  93. Sibaoka T (1973) Transmission of action potentials in Biophytum. Bot Mag 86:51–61Google Scholar
  94. Simons P (1992) The action plant. Movement and nervous behaviour in plants. Blackwell Publishing, OxfordGoogle Scholar
  95. Sinyukhin AM, Britikov EA (1967) Action potentials in the reproductive system of plants. Nature 215:1278–1280Google Scholar
  96. Spanjers AW (1981) Bioelectric potential changes in the style of Lilium longiflorum Thunb. after self- and cross-pollination of the stigma. Planta 153:1–5Google Scholar
  97. Spanswick RM (1972) Electrical coupling between cells of higher plants: a direct demonstration of intercellular communication. Planta 102:215–227Google Scholar
  98. Spanswick RM, Costerton JWF (1967) Plasmodesmata in Nitella translucens: structure and electrical resistance. J Cell Sci 2:451–464PubMedGoogle Scholar
  99. Spyropoulos CS, Tasaki I, Hayward G (1961) Fractination of tracer effluxes during action potential. Science 133:2064–2065PubMedGoogle Scholar
  100. Stahlberg E, Cosgrove DJ (1997) The propagation of slow wave potentials in pea epicotyls. Plant Physiol 113:33–41Google Scholar
  101. Stahlberg R, Cleland RE, van Volkenburgh E (2006) Slow wave potentials—a propagating electrical signal unique to higher plants. In: Baluska F, Mancuso S, Volkmann D (eds) Communication in plants—neuronal aspects of plant life. Springer, Berlin, pp 291–308Google Scholar
  102. Stankovic B, Davies E (1996) Both action potentials and variation potentials induce proteinase inhibitor gene expression in tomato. FEBS Lett 390:275–279PubMedGoogle Scholar
  103. Stankovic B, Davies E (1997) Intercellular communication in plants: electrical stimulation of proteinase inhibitor gene expression in tomato. Planta 202:402–406Google Scholar
  104. Szmelcman S, Adler J (1976) Change in membrane potential during bacterial chemotaxis. Proc Natl Acad Sci USA 73:4387–4391PubMedGoogle Scholar
  105. Tazawa M, Shimmen T, Mimura T (1987) Membrane control in the Characeae. Annu Rev Plant Physiol 38:95–117Google Scholar
  106. Thion L, Mazars C, Nacry P, Bouchez D, Moreau M, Ranjeva R, Thuleau P (1998) Plasma membrane depolarization-activated calcium channels stimulated by microtubule-depolymerizing drugs in wild-type Arabidopsis thaliana protoplasts, display constitutively large activities and a longer half-life in ton 2 mutant cells affected in the organization of the cortical microtubules. Plant J 13: 603–610Google Scholar
  107. Thorpe MREH, Foeller J, van Bel AJE, Hafke JB (2010) Rapid cooling triggers forisome dispersion just before phloem transport stops. Plant Cell Environ 33:259–271PubMedGoogle Scholar
  108. Thorsch J, Esau K (1981) Nuclear generation and the association of endoplasmic reticulum with the nuclear envelope and microtubules in maturing sieve elements of Gossypium hirsutum. J Ultrastr Res 74:195–204Google Scholar
  109. Thuleau P, Moreau M, Schroeder JI, Ranjeva R (1994) Recruitment of plasma membrane voltage-dependent calcium-permeable channels in carrot cells. EMBO J 13:5843–5847PubMedGoogle Scholar
  110. Van Bel AJE (1993) The transport phloem. Specifics of its functioning. Prog Bot 54:134–150Google Scholar
  111. Van Bel AJE, Ehlers K (2005) Electrical signalling via plasmodesmata. In: Oparka KJ (ed) Plasmodesmata, Blackwell Publishing, Oxford, pp 263–278Google Scholar
  112. Van Bel AJE, Van Rijen HVM (1994) Microelectrode-recorded development of symplasmic autonomy of the sieve element/companion cell complex in the stem phloem of Lupinus luteus. Planta 192:165–175Google Scholar
  113. Van Sambeek JW, Pickard BG (1976) Mediation of rapid electrical, metabolic, transpirational and photosynthetic changes by factors released from wounds. I. Variation potentials and putative action potentials in intact plants. Can J Bot 54:2642–2650Google Scholar
  114. Volk G, Franceschi VR (2000) Localization of a calcium-channel-like protein in the sieve element plasma membrane. Aust J Plant Physiol 27:779–786Google Scholar
  115. Volkov AG, Dunkley TC, Morgan SA, Ruff D II, Boyce YL, Labady AJ (2004) Bioelectrochemical signaling in green plants induced by photosensory systems. Bioelectrochem 63:91–94Google Scholar
  116. Volkov AG, Adesina T, Markin VS, Jovanov E (2008a) Kinetics and mechanism of Dionaea muscipula trap closing. Plant Physiol 146:694–702PubMedGoogle Scholar
  117. Volkov AG, Coopwood KJ, Markin VS (2008b) Inhibition of the Dionaea muscipula Ellis trap closure by ion and water channel blockers and uncouplers. Plant Sci 175:642–649Google Scholar
  118. Volkov AG, Adesina T, Jovanov E (2008c) Charge induced closing of Dionaea muscipula Ellis trap. Bioelectrochemistry 74:16–21PubMedGoogle Scholar
  119. Volkov AG, Carrell H, Baldwin A, Markin VS (2009a) Electrical memory in Venus flytrap. Bioelectrochemistry 75:142–147PubMedGoogle Scholar
  120. Volkov AG, Carrell H, Markin VS (2009b) Biologically closed electrical circuits in Venus flytrap. Plant Physiol 149:1661–1667PubMedGoogle Scholar
  121. Volkov AG, Foster JC, Ashby TA, Walker RK, Johnson JA, Markin VS (2010) Mimosa pudica: Electrical and mechanical stimulation of plant movements. Plant Cell Environ 33:163–173PubMedGoogle Scholar
  122. White PJ, Ridout MS (1999) An energy-barrier model for the permeation of monovalent and divalent cations through the maxi cation channel in the plasma membrane of rye roots. J Membr Biol 168:63–75PubMedGoogle Scholar
  123. White PJ (2004) Calcium signals in root cells: the roles of plasma membrane calcium channels. Biol Plant 59:77–83Google Scholar
  124. White PJ (2009) Depolarization-activated calcium channels shape the calcium signatures induced by low-temperature stress. New Phytol 183:6–8PubMedGoogle Scholar
  125. Wildon DC, Thain JF, Minchin PEH, Gubb IR, Reilly AJ, Skipper YD, Doherty HM, Odonnell PJ, Bowles DJ (1992) Electrical signaling and systemic proteinase-inhibitor induction in the wounded plant. Nature 360:62–65Google Scholar
  126. Williams SE, Pickard BG (1972a) Properties of action potentials in Drosera tentacles. Planta 103:193–221Google Scholar
  127. Williams SE, Pickard BG (1972b) Receptor potentials and action potentials in Drosera tentacles. Planta 103:222–240Google Scholar
  128. Wind C, Arend M, Fromm J (2004) Potassium-dependent cambial growth in poplar. Plant Biol 6:30–37PubMedGoogle Scholar
  129. Woodley SJ, Fensom DS, Thompson RG (1976) Biopotentials along the stem of Helianthus in association with short-term translocation of 14C and chilling. Can J Bot 54:1246–1256Google Scholar
  130. Wright JP, Fisher DB (1981) Measurement of the sieve tube membrane potential. Plant Physiol 67:845–848PubMedGoogle Scholar
  131. Zawadzki T, Davies E, Dziubinska H, Trebacz K (1991) Characteristics of action potentials in Helianthus annuus. Physiol Plant 83:601–604Google Scholar

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© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Institute for Wood BiologyUniversität HamburgHamburgGermany

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