Plant Electrophysiology: Early Stages of the Plant Response to Chemical Signals

  • Simon A. Zebelo
  • Massimo E. MaffeiEmail author
Part of the Signaling and Communication in Plants book series (SIGCOMM)


Plant defence strategies start at the plant cell plasma membrane, where volatile organic compounds (VOCs) induced by insect herbivores or plant pathogens interact chemically and trigger plant signalling molecules. The earliest plant responses for the perception of VOCs are ion flux imbalances generated in the plant cell plasma membrane at the perception zone. This different charge distribution generates variation in the plasma transmembrane potential (Vm), which is the first event preceding the regulation of signal transduction pathways and gene expression. Change in the Vm can be through either an increase (hyperpolarization) or a decrease (depolarization) in the membrane potential. Here, we review recent advances in electrophysiological methods for the study of the early events of VOC perception and the correlation between Vm depolarization and plant signal transduction pathways leading to changes in gene expression.


Plasma membrane potential Volatile organic compounds (VOCs) Herbivores Pathogens Electrophysiology Early events 


  1. Alborn HT, Hansen TV, Jones TH, Bennett DC, Tumlinson JH, Schmelz EA, Teal PEA (2007) Disulfooxy fatty acids from the American bird grasshopper Schistocerca americana, elicitors of plant volatiles. Proc Natl Acad Sci USA 104(32):12976–12981CrossRefPubMedPubMedCentralGoogle Scholar
  2. Arimura G, Maffei ME (2010) Calcium and secondary CPK signaling in plants in response to herbivore attack. Biochem Biophys Res Commun 400(4):455–460CrossRefPubMedGoogle Scholar
  3. Aslam SN, Erbs G, Morrissey KL, Newman MA, Chinchilla D, Boller T, Molinaro A, Jackson RW, Cooper RM (2009) Microbe-associated molecular pattern (MAMP) signatures, synergy, size and charge: influences on perception or mobility and host defence responses. Mol Plant Pathol 10(3):375–387CrossRefPubMedGoogle Scholar
  4. Baunsgaard L, Fuglsang AT, Jahn T, Korthout HAAJ, de Boer AH, Palmgren MG (1998) The 14-3-3 proteins associate with the plant plasma membrane H+-ATPase to generate a fusicoccin binding complex and a fusicoccin responsive system. Plant J 13(5):661–671CrossRefPubMedGoogle Scholar
  5. Blume B, Nurnberger T, Nass N, Scheel D (2000) Receptor-mediated increase in cytoplasmic free calcium required for activation of pathogen defense in parsley. Plant Cell 12(8):1425–1440CrossRefPubMedPubMedCentralGoogle Scholar
  6. Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406CrossRefPubMedGoogle Scholar
  7. Bourque S, Lemoine R, Sequeira-Legrand A, Fayolle U, Delrot S, Pugin A (2002) The elicitor cryptogein blocks glucose transport in tobacco cells. Plant Physiol 130(4):2177–2187CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bricchi I, Leitner M, Foti M, Mithöfer A, Boland W, Maffei ME (2010) Robotic mechanical wounding (MecWorm) versus herbivore-induced responses: early signaling and volatile emission in Lima bean (Phaseolus lunatus L.). Planta 232(3):719–729CrossRefPubMedGoogle Scholar
  9. Bricchi I, Bertea CM, Occhipinti A, Paponov IA, Maffei ME (2012) Dynamics of membrane potential variation and gene expression induced by Spodoptera littoralis, Myzus persicae, and Pseudomonas syringae in Arabidopsis. PLoS One 7(10)Google Scholar
  10. Bricchi I, Occhipinti A, Bertea CM, Zebelo SA, Brillada C, Verrillo F, De Castro C, Molinaro A, Faulkner C, Maule AJ, Maffei ME (2013) Separation of early and late responses to herbivory in Arabidopsis by changing plasmodesmal function. Plant J 73(1):14–25CrossRefPubMedGoogle Scholar
  11. Cao J, Cole IB, Murch SJ (2006) Neurotransmitters, neuroregulators and neurotoxins in the life of plants. Can J Plant Sci 86(4):1183–1188CrossRefGoogle Scholar
  12. Consales F, Schweizer F, Erb M, Gouhier-Darimont C, Bodenhausen N, Bruessow F, Sobhy I, Reymond P (2012) Insect oral secretions suppress wound-induced responses in Arabidopsis. J Exp Bot 63(2):727–737CrossRefPubMedGoogle Scholar
  13. Duclohier H, Alder G, Kociolek K, Leplawy MT (2003) Channel properties of template assembled alamethicin tetramers. J Pept Sci 9(11–12):776–783CrossRefPubMedGoogle Scholar
  14. Elmore JM, Coaker G (2011) The role of the plasma membrane H+-ATPase in plant–microbe interactions. Mol Plant 4(3):416–427CrossRefPubMedPubMedCentralGoogle Scholar
  15. Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH (2004) Airborne signals prime plants against insect herbivore attack. Proc Natl Acad Sci USA 101(6):1781–1785CrossRefPubMedPubMedCentralGoogle Scholar
  16. Felle HH, Zimmermann MR (2007) Systemic signalling in barley through action potentials. Planta 226(1):203–214CrossRefPubMedGoogle Scholar
  17. Felton G (2008) Caterpillar secretions and induced plant responses. In: Schaller A (ed) Induced plant resistance to herbivory. Springer, Dordrecht, pp 369–387CrossRefGoogle Scholar
  18. 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(4):456–459CrossRefPubMedGoogle Scholar
  19. Fromm J, Bauer T (1994) Action-potentials in maize sieve tubes change phloem translocation. J Exp Bot 45(273):463–469CrossRefGoogle Scholar
  20. Fromm J, Lautner S (2007) Electrical signals and their physiological significance in plants. Plant Cell Environ 30(3):249–257CrossRefPubMedGoogle Scholar
  21. Geiger D, Becker D, Vosloh D, Gambale F, Palme K, Rehers M, Anschuetz U, Dreyer I, Kudla J, Hedrich R (2009) Heteromeric AtKC1.AKT1 channels in Arabidopsis roots facilitate growth under K+-limiting conditions. J Biol Chem 284(32):21288–21295CrossRefPubMedPubMedCentralGoogle Scholar
  22. Gelli A, Higgins VJ, Blumwald E (1997) Activation of plant plasma membrane Ca2+-permeable channels by race-specific fungal elicitors. Plant Physiol 113(1):269–279PubMedPubMedCentralGoogle Scholar
  23. Halitschke R, Schittko U, Pohnert G, Boland W, Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. Plant Physiol 125(2):711–717CrossRefPubMedPubMedCentralGoogle Scholar
  24. Heil M, Silva Bueno JC (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci USA 104(13):5467–5472CrossRefPubMedPubMedCentralGoogle Scholar
  25. Imbiscuso G, Trotta A, Maffei M, Bossi S (2009) Herbivory induces a ROS burst and the release of volatile organic compounds in the fern Pteris vittata L. J Plant Interact 4(1):15–22CrossRefGoogle Scholar
  26. Jeworutzki E, Roelfsema MRG, Anschutz U, Krol E, Elzenga JTM, Felix G, Boller T, Hedrich R, Becker D (2010) Early signaling through the Arabidopsis pattern recognition receptors FLS2 and EFR involves Ca2+-associated opening of plasma membrane anion channels. Plant J 62(3):367–378CrossRefPubMedGoogle Scholar
  27. Kato T, Shiraishi T, Toyoda K, Saitoh K, Satoh Y, Tahara M, Yamada T, Oku H (1993) Inhibition of ATPase activity in pea plasma-membranes by fungal suppressors from Mycosphaerella pinodes and their peptide moieties. Plant Cell Physiol 34(3):439–445PubMedGoogle Scholar
  28. Keinath NF, Kierszniowska S, Lorek J, Bourdais G, Kessler SA, Shimosato-Asano H, Grossniklaus U, Schulze WX, Robatzek S, Panstruga R (2010) PAMP (pathogen-associated molecular pattern)-induced changes in plasma membrane compartmentalization reveal novel components of plant immunity. J Biol Chem 285(50):39140–39149CrossRefPubMedPubMedCentralGoogle Scholar
  29. Knogge W (1996) Fungal infection of plants. Plant Cell 8(10):1711–1722CrossRefPubMedPubMedCentralGoogle Scholar
  30. Lebaudy A, Very AA, Sentenac H (2007) K+ channel activity in plants: genes, regulations and functions. FEBS Lett 581(12):2357–2366CrossRefPubMedGoogle Scholar
  31. Lecourieux D, Lamotte O, Bourque S, Wendehenne D, Mazars C, Ranjeva R, Pugin A (2005) Proteinaceous and oligosaccharidic elicitors induce different calcium signatures in the nucleus of tobacco cells. Cell Calcium 38(6):527–538CrossRefPubMedGoogle Scholar
  32. Luhring H, Nguyen VD, Schmidt L, Rose USR (2007) Caterpillar regurgitant induces pore formation in plant membranes. FEBS Lett 581(28):5361–5370CrossRefPubMedGoogle Scholar
  33. Maathuis JM, Ichida AM, Sanders D, Schroeder JI (1997) Roles of higher plant K+ channels. Plant Physiol 114(4):1141–1149CrossRefPubMedPubMedCentralGoogle Scholar
  34. Maffei M, Bossi S (2006) Electrophysiology and plant responses to biotic stress. In: Volkov A (ed) Plant electrophysiology. Springer, Berlin, Heidelberg, pp 461–481CrossRefGoogle Scholar
  35. Maffei M, Camusso W, Sacco S (2001) Effect of Mentha x piperita essential oil and monoterpenes on cucumber root membrane potential. Phytochemistry 58(5):703–707CrossRefPubMedGoogle Scholar
  36. Maffei M, Bossi S, Spiteller D, Mithöfer A, Boland W (2004) Effects of feeding Spodoptera littoralis on lima bean leaves. I. Membrane potentials, intracellular calcium variations, oral secretions, and regurgitate components. Plant Physiol 134(4):1752–1762CrossRefPubMedPubMedCentralGoogle Scholar
  37. Maffei ME, Mithofer A, Arimura GI, Uchtenhagen H, Bossi S, Bertea CM, Cucuzza LS, Novero M, Volpe V, Quadro S, Boland W (2006) Effects of feeding Spodoptera littoralis on lima bean leaves. III. Membrane depolarization and involvement of hydrogen peroxide. Plant Physiol 140(3):1022–1035CrossRefPubMedPubMedCentralGoogle Scholar
  38. Maffei ME, Mithöfer A, Boland W (2007a) Before gene expression: early events in plant–insect interaction. Trends Plant Sci 12(7):310–316CrossRefPubMedGoogle Scholar
  39. Maffei ME, Mithöfer A, Boland W (2007b) Insects feeding on plants: rapid signals and responses preceding the induction of phytochemical release. Phytochemistry 68(22–24):2946–2959CrossRefPubMedGoogle Scholar
  40. Maffei ME, Arimura GI, Mithöfer A (2012) Natural elicitors, effectors and modulators of plant responses. Nat Prod Rep 29(11):1288–1303CrossRefPubMedGoogle Scholar
  41. Maischak H, Grigoriev PA, Vogel H, Boland W, Mithöfer A (2007) Oral secretions from herbivorous lepidopteran larvae exhibit ion channel-forming activities. FEBS Lett 581(5):898–904CrossRefPubMedGoogle Scholar
  42. Mattiacci L, Dicke M, Posthumus MA (1995) Beta-glucosidase—an elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps. Proc Natl Acad Sci USA 92(6):2036–2040CrossRefPubMedPubMedCentralGoogle Scholar
  43. Mithöfer A, Mazars C, Maffei ME (2009) Probing spatio-temporal intracellular calcium variations in plants. In: Pfannschmidt T (ed) Plant signal transduction, vol 479, Methods in molecular biology. Humana Press, New York, NY, pp 79–92CrossRefGoogle Scholar
  44. Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H, Shibuya N (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci USA 104(49):19613–19618CrossRefPubMedPubMedCentralGoogle Scholar
  45. Mohanta TK, Occhipinti A, Zebelo SA, Foti M, Fliegmann J, Bossi S, Maffei ME, Bertea CM (2012) Ginkgo biloba responds to herbivory by activating early signaling and direct defenses. PLoS One 7(3):e32822CrossRefPubMedPubMedCentralGoogle Scholar
  46. Nastuk WL, Hodgkin AL (1950) The electrical activity of single muscle fibers. J Cell Comp Physiol 35(1):39–73CrossRefGoogle Scholar
  47. Nuhse TS, Bottrill AR, Jones AME, Peck SC (2007) Quantitative phosphoproteomic analysis of plasma membrane proteins reveals regulatory mechanisms of plant innate immune responses. Plant J 51(5):931–940CrossRefPubMedPubMedCentralGoogle Scholar
  48. Nurnberger T, Scheel D (2001) Signal transmission in the plant immune response. Trends Plant Sci 6(8):372–379CrossRefPubMedGoogle Scholar
  49. Pike SM, Zhang XC, Gassmann W (2005) Electrophysiological characterization of the Arabidopsis avrRpt2-specific hypersensitive response in the absence of other bacterial signals. Plant Physiol 138(2):1009–1017CrossRefPubMedPubMedCentralGoogle Scholar
  50. Pyatygin SS, Opritov VA, Vodeneev VA (2008) Signaling role of action potential in higher plants. Russ J Plant Physiol 55(2):285–291CrossRefGoogle Scholar
  51. Reymond P, Bodenhausen N, Van Poecke RMP, Krishnamurthy V, Dicke M, Farmer EE (2004) A conserved transcript pattern in response to a specialist and a generalist herbivore. Plant Cell 16(11):3132–3147CrossRefPubMedPubMedCentralGoogle Scholar
  52. Romeis T, Ludwig AA, Martin R, Jones JDG (2001) Calcium-dependent protein kinases play an essential role in a plant defence response. EMBO J 20(20):5556–5567CrossRefPubMedPubMedCentralGoogle Scholar
  53. Roshchina VV (2001) Molecular–cellular mechanisms in pollen allelopathy. Allelopath J 8(1):11–28Google Scholar
  54. Sacco S, Maffei M (1997) The effect of isosakuranetin (5,7-dihydroxy 4′-methoxy flavanone) on potassium uptake in wheat root segments. Phytochemistry 46(2):245–248CrossRefGoogle Scholar
  55. Schaller A, Oecking C (1999) Modulation of plasma membrane H+-ATPase activity differentially activates wound and pathogen defense responses in tomato plants. Plant Cell 11(2):263–272PubMedPubMedCentralGoogle Scholar
  56. Schmelz EA, Carroll MJ, LeClere S, Phipps SM, Meredith J, Chourey PS, Alborn HT, Teal PEA (2006) Fragments of ATP synthase mediate plant perception of insect attack. Proc Natl Acad Sci USA 103(23):8894–8899CrossRefPubMedPubMedCentralGoogle Scholar
  57. Shabala S, Bose J (2012) Application of non-invasive microelectrode flux measurements in plant stress physiology. In: Volkov AG (ed) Plant electrophysiology. Springer, Berlin, Heidelberg, pp 91–126CrossRefGoogle Scholar
  58. Shabala S, Babourina O, Rengel Z, Nemchinov LG (2010) Non-invasive microelectrode potassium flux measurements as a potential tool for early recognition of virus-host compatibility in plants. Planta 232(4):807–815CrossRefPubMedGoogle Scholar
  59. Tasaki I (1952) Properties of myelinated fibers in sciatic nerve and in spinal cord (Frog) as examined with microelectrodes. Science 116(3020):529–530Google Scholar
  60. Veraestrella R, Barkla BJ, Higgins VJ, Blumwald E (1994) Plant defense response to fungal pathogens—activation of host-plasma membrane H+-ATpase by elicitor-induced enzyme dephosphorylation. Plant Physiol 104(1):209–215Google Scholar
  61. Volkov AG, Haack RA (1995) Insect-induced bioelectrochemical signals in potato plants. Bioelectrochem Bioenerg 37(1):55–60CrossRefGoogle Scholar
  62. Volkov A, Mwesigwa J (2000) Interfacial electrical phenomena in green plants: action potentials. In: Volkov AG (ed) Liquid interfaces in chemical, biological, and pharmaceutical applications. Dekker, New York, NYGoogle Scholar
  63. Wang Y (2012) Functional characterization of plant ion channels in heterologous expression systems. In: Volkov AG (ed) Plant electrophysiology. Springer, Berlin, Heidelberg, pp 301–321CrossRefGoogle Scholar
  64. Winterhalter M (2000) Black lipid membranes. Curr Opin Colloid Interface Sci 5(3–4):250–255CrossRefGoogle Scholar
  65. Zebelo SA, Maffei M (2012a) Signal transduction in plant–insect interactions: from membrane potential variations to metabolomics. In: Volkov AG (ed) Plant electrophysiology. Springer, Berlin, Heidelberg, pp 143–172CrossRefGoogle Scholar
  66. Zebelo SA, Maffei ME (2012b) The ventral eversible gland (VEG) of Spodoptera littoralis triggers early responses to herbivory in Arabidopsis thaliana. Arthropod Plant Interact 6(4):543–551CrossRefGoogle Scholar
  67. Zebelo AS, Maffei ME (2015) Role of early signalling events in plant–insect interactions. J Exp Bot 66:435–448CrossRefPubMedGoogle Scholar
  68. Zebelo SA, Matsui K, Ozawa R, Maffei ME (2012) Plasma membrane potential depolarization and cytosolic calcium flux are early events involved in tomato (Solanum lycopersicon) plant-to-plant communication. Plant Sci 196:93–100CrossRefPubMedGoogle Scholar
  69. Zhou FS, Andersen CH, Burhenne K, Fischer PH, Collinge DB, Thordal-Christensen H (2000) Proton extrusion is an essential signalling component in the HR of epidermal single cells in the barley–powdery mildew interaction. Plant J 23(2):245–254CrossRefPubMedGoogle Scholar
  70. Zimmermann MR, Maischak H, Mithofer A, Boland W, Felle HH (2009) System potentials, a novel electrical long-distance apoplastic signal in plants, induced by wounding. Plant Physiol 149(3):1593–1600CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Natural SciencesUniversity of Maryland Eastern ShorePrincess AnneUSA
  2. 2.Department of Life Sciences and Systems BiologyUniversity of TurinTurinItaly
  3. 3.Department of Agricultural, Food, and Resource EconomicsUniversity of Maryland Eastern ShorePrincess AnneUSA

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