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

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Deciphering Chemical Language of Plant Communication

Part of the book series: Signaling and Communication in Plants ((SIGCOMM))

Abstract

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 (V m), which is the first event preceding the regulation of signal transduction pathways and gene expression. Change in the V m 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 V m depolarization and plant signal transduction pathways leading to changes in gene expression.

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References

  • 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):12976–12981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arimura G, Maffei ME (2010) Calcium and secondary CPK signaling in plants in response to herbivore attack. Biochem Biophys Res Commun 400(4):455–460

    Article  CAS  PubMed  Google Scholar 

  • 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):375–387

    Article  CAS  PubMed  Google Scholar 

  • 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):661–671

    Article  CAS  PubMed  Google Scholar 

  • 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):1425–1440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 60:379–406

    Article  CAS  PubMed  Google Scholar 

  • 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):2177–2187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):719–729

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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):14–25

    Article  CAS  PubMed  Google Scholar 

  • Cao J, Cole IB, Murch SJ (2006) Neurotransmitters, neuroregulators and neurotoxins in the life of plants. Can J Plant Sci 86(4):1183–1188

    Article  CAS  Google Scholar 

  • 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):727–737

    Article  CAS  PubMed  Google Scholar 

  • Duclohier H, Alder G, Kociolek K, Leplawy MT (2003) Channel properties of template assembled alamethicin tetramers. J Pept Sci 9(11–12):776–783

    Article  CAS  PubMed  Google Scholar 

  • Elmore JM, Coaker G (2011) The role of the plasma membrane H+-ATPase in plant–microbe interactions. Mol Plant 4(3):416–427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH (2004) Airborne signals prime plants against insect herbivore attack. Proc Natl Acad Sci USA 101(6):1781–1785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Felle HH, Zimmermann MR (2007) Systemic signalling in barley through action potentials. Planta 226(1):203–214

    Article  CAS  PubMed  Google Scholar 

  • Felton G (2008) Caterpillar secretions and induced plant responses. In: Schaller A (ed) Induced plant resistance to herbivory. Springer, Dordrecht, pp 369–387

    Chapter  Google Scholar 

  • 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):456–459

    Article  CAS  PubMed  Google Scholar 

  • Fromm J, Bauer T (1994) Action-potentials in maize sieve tubes change phloem translocation. J Exp Bot 45(273):463–469

    Article  Google Scholar 

  • Fromm J, Lautner S (2007) Electrical signals and their physiological significance in plants. Plant Cell Environ 30(3):249–257

    Article  CAS  PubMed  Google Scholar 

  • 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):21288–21295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gelli A, Higgins VJ, Blumwald E (1997) Activation of plant plasma membrane Ca2+-permeable channels by race-specific fungal elicitors. Plant Physiol 113(1):269–279

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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):711–717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):5467–5472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):15–22

    Article  CAS  Google Scholar 

  • 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):367–378

    Article  CAS  PubMed  Google Scholar 

  • 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):439–445

    CAS  PubMed  Google Scholar 

  • 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):39140–39149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knogge W (1996) Fungal infection of plants. Plant Cell 8(10):1711–1722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lebaudy A, Very AA, Sentenac H (2007) K+ channel activity in plants: genes, regulations and functions. FEBS Lett 581(12):2357–2366

    Article  CAS  PubMed  Google Scholar 

  • 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):527–538

    Article  CAS  PubMed  Google Scholar 

  • Luhring H, Nguyen VD, Schmidt L, Rose USR (2007) Caterpillar regurgitant induces pore formation in plant membranes. FEBS Lett 581(28):5361–5370

    Article  PubMed  Google Scholar 

  • Maathuis JM, Ichida AM, Sanders D, Schroeder JI (1997) Roles of higher plant K+ channels. Plant Physiol 114(4):1141–1149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maffei M, Bossi S (2006) Electrophysiology and plant responses to biotic stress. In: Volkov A (ed) Plant electrophysiology. Springer, Berlin, Heidelberg, pp 461–481

    Chapter  Google Scholar 

  • Maffei M, Camusso W, Sacco S (2001) Effect of Mentha x piperita essential oil and monoterpenes on cucumber root membrane potential. Phytochemistry 58(5):703–707

    Article  CAS  PubMed  Google Scholar 

  • 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):1752–1762

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):1022–1035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maffei ME, Mithöfer A, Boland W (2007a) Before gene expression: early events in plant–insect interaction. Trends Plant Sci 12(7):310–316

    Article  CAS  PubMed  Google Scholar 

  • 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):2946–2959

    Article  CAS  PubMed  Google Scholar 

  • Maffei ME, Arimura GI, Mithöfer A (2012) Natural elicitors, effectors and modulators of plant responses. Nat Prod Rep 29(11):1288–1303

    Article  CAS  PubMed  Google Scholar 

  • 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):898–904

    Article  CAS  PubMed  Google Scholar 

  • 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):2036–2040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 79–92

    Chapter  Google Scholar 

  • 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):19613–19618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):e32822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nastuk WL, Hodgkin AL (1950) The electrical activity of single muscle fibers. J Cell Comp Physiol 35(1):39–73

    Article  CAS  Google Scholar 

  • 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):931–940

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nurnberger T, Scheel D (2001) Signal transmission in the plant immune response. Trends Plant Sci 6(8):372–379

    Article  CAS  PubMed  Google Scholar 

  • 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):1009–1017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pyatygin SS, Opritov VA, Vodeneev VA (2008) Signaling role of action potential in higher plants. Russ J Plant Physiol 55(2):285–291

    Article  CAS  Google Scholar 

  • 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):3132–3147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):5556–5567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roshchina VV (2001) Molecular–cellular mechanisms in pollen allelopathy. Allelopath J 8(1):11–28

    Google Scholar 

  • 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):245–248

    Article  CAS  Google Scholar 

  • 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):263–272

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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):8894–8899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 91–126

    Chapter  Google Scholar 

  • 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):807–815

    Article  CAS  PubMed  Google Scholar 

  • Tasaki I (1952) Properties of myelinated fibers in sciatic nerve and in spinal cord (Frog) as examined with microelectrodes. Science 116(3020):529–530

    Google Scholar 

  • 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):209–215

    CAS  Google Scholar 

  • Volkov AG, Haack RA (1995) Insect-induced bioelectrochemical signals in potato plants. Bioelectrochem Bioenerg 37(1):55–60

    Article  CAS  Google Scholar 

  • 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, NY

    Google Scholar 

  • Wang Y (2012) Functional characterization of plant ion channels in heterologous expression systems. In: Volkov AG (ed) Plant electrophysiology. Springer, Berlin, Heidelberg, pp 301–321

    Chapter  Google Scholar 

  • Winterhalter M (2000) Black lipid membranes. Curr Opin Colloid Interface Sci 5(3–4):250–255

    Article  CAS  Google Scholar 

  • 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 143–172

    Chapter  Google Scholar 

  • 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):543–551

    Article  Google Scholar 

  • Zebelo AS, Maffei ME (2015) Role of early signalling events in plant–insect interactions. J Exp Bot 66:435–448

    Article  CAS  PubMed  Google Scholar 

  • 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 196:93–100

    Article  CAS  PubMed  Google Scholar 

  • 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):245–254

    Article  CAS  PubMed  Google Scholar 

  • 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):1593–1600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Natural Sciences, University of Maryland Eastern Shore, 1117 Trigg Hall, Princess Anne, 21853, MD, USA

    Simon A. Zebelo

  2. Department of Life Sciences and Systems Biology, University of Turin, Via Quarello 15/A, Turin, 10135, Italy

    Massimo E. Maffei

  3. Department of Agricultural, Food, and Resource Economics, University of Maryland Eastern Shore, 1117 Trigg Hall, Princess Anne, 21853, MD, USA

    Simon A. Zebelo

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  1. Simon A. Zebelo
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Correspondence to Massimo E. Maffei .

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Editors and Affiliations

  1. Department of Environmental and Bio. Sci, University of Eastern Finland, Kuopio, Finland

    James D. Blande

  2. Department of Crop Production Ecology, Swedish University of Agricultural Sci., Uppsala, Sweden

    Robert Glinwood

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Zebelo, S.A., Maffei, M.E. (2016). Plant Electrophysiology: Early Stages of the Plant Response to Chemical Signals. In: Blande, J., Glinwood, R. (eds) Deciphering Chemical Language of Plant Communication. Signaling and Communication in Plants. Springer, Cham. https://doi.org/10.1007/978-3-319-33498-1_12

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