Abstract
In higher plants at least three different types of electrical long-distance signaling exist: action potential (AP), variation potential (VP), and system potential (SP), all of which have their own characteristics concerning their generation, duration, amplitude, velocity, and propagation. Whereas both AP and VP are due to a transient depolarization of the plasma membrane, the SP is based on hyperpolarization. For more than 100 years the AP is known and described for some specialized plants such as the Venus flytrap. Meanwhile, all three types of electrical signaling have been shown for many common plants, monocots as well as dicots, indicating that the capability to generate long-distance electrical signals is not the exception but a general physiological feature of plants. In spite of this, positive proofs for the involvement of these kinds of electrical signaling in the induction of many different plant responses to (a)biotic stresses or in developmental processes still wait to be established.
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1 Introduction
1.1 Electrical Long-Distance Signals: Brief History and Presence
The unequal separation of charged molecules and ions across the plasma membrane to generate a membrane potential is usually due to the activity of plasma membrane-located channels and pumps. The presence of a membrane potential is an essential feature for all kinds of living cells and necessary for the uptake of nutrients and minerals as well as to establish and regulate intracellular physiological processes. In addition, the interaction between different cells or different tissue and organs via an electrical signaling for communication over a long distance is a well-established phenomenon for animals and known for more than 200 years. Even for plants fast electrical signals were described about 140 years ago: In 1873, Burdon-Sanderson studied the leaf closing mechanism in the carnivorous Venus flytrap, Dionaea muscipula. In addition, Darwin (1875) investigated tentacle movements of sundew plants, Drosera spp. Some years later, Kunkel (1898) and Bose (1907) showed that in Mimosa pudica the fast leaf(let) movements depended on electrical signals. All those plants represent remarkable and very specialized species, which, thus, were highly attractive to the scientists. General studies on long-distance electrical signaling in other common plants were not very popular among physiologists for many decades although some studies suggested that upon wounding electrical signals may travel through phloem and/or xylem elements (Pickard 1973; Davies 1987; Rhodes et al. 1996). Fortunately, in recent years an increasing number of studies are published dealing with the phenomenon of electrical long-distance signaling in higher plants.
2 Electrical Signals in Plants
In animals only one genuine electrical signal is known, the action potential. In contrast, three different signal types have been identified in plants—(1) action potential, (2) variation potential, and (3) system potential; all of which will be described in the following.
2.1 Action Potential
The action potential (AP) is a transient depolarization of the plasma membrane with a very typical voltage signature that is interestingly found in animals as well as in plants. Plant- and animal-originated APs share fundamental characteristics: (1) the distinctive voltage signature, (2) the all-or-nothing law, (3) the ability of self-propagation, and (4) a refractory period, but they differ in (1) time frame and (2) molecular compounds involved (Pickard 1973; Beilby 2007; Pyatygin et al. 2008).
Most details about the complex and fine-adjusted molecular mechanism of APs were found for lower plants, e.g., Acetabularia spec. (Gradmann 1976), Chara spec. (Hope and Findlay 1964; Beilby 2007), Nitella spec. (Blatt 1974; Kikuyama 1987), and Conocephalum conicum (Dziubinska et al. 1983; Trebacz et al. 1989, 1994, 1997; Trebacz 1992). In higher plants, APs have been mainly examined in plants with motor activity, i.e., Mimosa pudica, Drosera spp., or Dionaea muscipula (Houwink 1935; Sibaoka 1969; Hodick and Sievers 1988; Volkov et al. 2010a, b). In addition, numerous studies with higher plant species without motor activities confirmed the general occurrence and characterized APs in plants (Table 1).
Up to now, diverse stimuli (touch, heat, cold, KCl, CaCl2, glutamic acid, electrical current) have been identified to initiate the orchestrated molecular cascade of an AP (Fig. 1) via three different mechanisms: (1) a depolarization (KCl, electrical current), (2) an increase of apoplastic Ca2+ (CaCl2), or (3) a ligand-binding receptor (glutamic acid; Felle and Zimmermann 2007). In each case, the consequence is a Ca2+ influx from the apoplast into the cytoplasm. This increase of cytosolic Ca2+ causes the opening of anion channels in the plasma membrane and, subsequently, an efflux of anions (mainly Cl−) along the electrochemical gradient from the cytoplasm into the apoplast (Bradley and Williams 1966; Tarr et al. 1970; Lunevsky et al. 1983; Tsutsui et al. 1986; Felle and Zimmermann 2007). Interestingly, Mg2+ is not able to replace Ca2+ confirming the specific role of Ca2+ during an AP (Tarr et al. 1970). Only if a certain threshold is passed all anion channels will open and the characteristic rapid and strong depolarization (“break-through”) can be observed (Fig. 1). The massive loss of negative charges affects the membrane potential and the Nernstian potential of potassium. This results in a passively driven K+ efflux from the cytoplasm into the apoplast (Tsutsui et al. 1986; Felle and Zimmermann 2007). At the end of the depolarization phase when anion- and K+-efflux is balanced and the H+-ATPases start working, the peak of the depolarization is reached (Fig. 1). To some extent, the single phases are reflected in the voltage pattern of the depolarization phase with its typical kinetics (Fig. 1). The repolarization is based upon an active symport of H+/Cl− and a passively driven K+-influx from the apoplast into the cytoplasm (Felle and Zimmermann 2007).
The reported rate of transmission (velocity) ranges from 0.78 to 300 cm min−1 (Table 1) suggesting differences in the electrical coupling within diverse plant species. In general, the phloem is supposed to be the main responsible cellular translocation pathway for an AP within a plant (Eschrich et al. 1988; Fromm and Bauer 1994). Sieve elements and companion cells exhibit a relative high electrical coupling via abundant cell-to-cell contacts (plasmodesmata; van Bel and Ehlers 2005). Direct local and systemic measurements of APs within sieve elements supported the thesis (Eschrich et al. 1988). But also the apoplast was suggested to have a crucial role in long-distance transmission of APs (Herde et al. 1998; Felle and Zimmermann 2007). Without doubt, plants have to cope with the problem of a missing electrical shield around the phloem (vascular system). The consequence is a leakage current and, thus, a longitudinal loss of voltage (see also cable theory; Adam et al. 2009). In mammalian, a myelin sheath acts as an electrical shield. That handicap might be compensated in plants—at least in part—by an intensive interplay of the phloem and the corresponding apoplast.
Finally, any AP-originated disturbance of the membrane potential has to be reset to the original conditions. During this time frame, called (absolute/relative) refractory period, cells are restricted for a next excitation. The refractory period is characteristic of APs. In the literature, a time range from 50 s (Mimosa pudica) to 2 h is reported indicating the refractory period to be plant specific (Paszewski and Zawadzki 1976; Fromm and Spanswick 1993; Fromm and Bauer 1994).
2.2 Variation Potential
The variation potentials (VPs), also known as slow wave potentials (SWPs), are transient depolarizations of the plasma membrane with variable shape, amplitude, and time fame (Fig. 2; Table 2) (Houwink 1935; Sibaoka 1953; Roblin and Bonnemain 1985; Stahlberg and Cosgrove 1996). VPs have been reported for a wide range of herbaceous plants (Table 2) and have been detected solely or in combination with APs (Roblin 1985; Furch et al. 2007). Diverse mechanical/ physical stimuli such as heat, wounding (cutting, excision), and pressure as well as chemical factors (Ricca’s factor, cyanide, aziden 2,4-dinitrophenol, sodium cholate) have been identified as external stimuli (Table 2) (Ricca 1916; van Sambeek and Pickard 1976b; Stahlberg and Cosgrove 1997a; Stanković et al. 1997). The observed inconsistent but characteristic voltage pattern is a result of the underlying molecular mechanism.
The depolarization of VPs results primarily from an inhibition of the plasma membrane H+-ATPases. It was shown that during a VP, no changes in cell input resistance occurred, which actually is typical for APs, and a decreased activity of proton pumps was concluded (Julien et al. 1991; Stahlberg and Cosgrove 1992). Congruously, a study with diverse proton pump inhibitors showed voltage patterns (Stahlberg and Cosgrove 1996) that are comparable with those evoked by mechanical stimuli. In addition, heat, cutting, or exogenous pressure application induces an alteration of the hydraulic pressure conditions within the xylem/apoplast via an import of energy (heat, pressure) or an opening of the vascular system (cutting). Indeed, changes of turgor pressure could be measured locally and systemically following application of heat or exogenous pressure (Malone and Stanković 1991; Malone 1992). Moreover, a combined determination of stem length and leaf thickness via transducers as a sign of hydraulic pressure alteration and electrical recordings showed a temporal correlation (Malone 1992; Stanković et al. 1997). The change of hydraulic pressure propagates in terms of a diminished wave along the xylem vessels and affects the surrounding cells by an inhibition of the proton pumps in the plasma membrane causing a transient depolarization. An essential turgor sensitivity of proton pumps was reported earlier (ref. see Stahlberg and Cosgrove 1992, 1996). The decline of proton pump activity results in reduced H+-extrusion from the cytoplasm into the xylem/ apoplast. There, the consequent alkalization could be determined with a pH-sensitive fluorescent dye, for example, in Pisum sativum from pH 4.5 to 6.0 (Stahlberg and Cosgrove 1996); this is additionally supported by the observed pH dependence of VPs (Julien et al. 1991). So VPs reflect the local electrical consequence of a hydraulic pressure wave running along xylem/apoplast (Malone 1992; Stahlberg et al. 2005).
The variable strength (amplitude and duration, time frame) of a VP is positively correlated with the force of the locally affecting hydraulic pressure wave. It could be observed that an increasing exogenous pressure application (30–100 kPa) at the root of Pisum sativum provoked stronger shapes of VPs, and simultaneously, a negative regression analysis displayed a decline of VPs with an increase of distance to the given continuous stimulus (50 kPa). The related radial leak of xylem pressure was calculated to be approximately 4 kPa cm−1 and is in direct context to the strength of a VP (Stahlberg and Cosgrove 1997a).
Between the occurrence of a hydraulic pressure wave and the VP, a lag time was observed depending on the strength of hydraulic pressure (Malone and Stanković 1991; Malone 1992; Stanković et al. 1997; Stahlberg et al. 2005). A faster stimulation of a VP was measured with stronger hydraulic pressure explaining why a wide range of measured velocities can be found in the literature (Table 2) due to the fact that the rate of propagation depends on the distance between stimulus and recording site and declined with an increasing distance (Stanković et al. 1997; Hlavácková et al. 2006). Here, it has to be noticed that in contrast to APs, VPs are not able to self-propagate excluding them to be a genuine long-distance signal (Stahlberg and Cosgrove 1997a). That aspect is additionally supported by the results that chemically induced VPs via proton pump inhibitors could be merely measured at the site of application with the exception of Ricca’s factor and sodium cholate (Ricca 1916; Stahlberg and Cosgrove 1997a).
Concerning physical stimuli, it is likely that at least mechanosensitive channels are also influenced during a VP. Depolarization with various proton pump inhibitors did not evoke APs, thus indicating a participation of mechanosensitive Ca2+ channels during VPs only (Stahlberg and Cosgrove 1997b). The observed stronger Ca2+ release was arrestingly demonstrated by the Ca2+-dependent forisome dispersion within sieve elements of Vicia faba plants after a heat stimulus (Furch et al. 2007, 2009).
The transmission of VPs was demonstrated for both directions—acropetal and basipetal (van Sambeek and Pickard 1976a)—and is even able to pass dead tissue being in good accordance with the concept of a running hydraulic wave along xylem vessels (Roblin 1985; Roblin and Bonnemain 1985). However, a recent study observed discrimination between the acro- and basipetal pathway. Following a cut at a petiole of Cucurbita maxima plants, the recorded VPs were stronger at the basal side (basipetal direction) (Zimmermann et al. 2013). In addition, it could be shown that the electrical reaction after application of heat was strongest in phloem cells (sieve elements and companion cells) in comparison to other cell types, i.e., epidermal, cortical, and vascular parenchyma cells. This may be founded by the intensive interaction of xylem and phloem (Eschrich et al. 1988; Rhodes et al. 1996).
Heat is a favored stimulus to provoke electrical signals (see Tables 1 and 2). After a heat stimulus, a combined spatiotemporal appearance of APs and VPs has been reported (Roblin 1985; Furch et al. 2007, 2009). Typically, electrical recordings close to the stimulus site are characterized by an overlap of AP and VP. This phenomenon complicates an exact determination of the particular signaling type and is referred to as electropotential wave (EPW; Fig. 3) (Furch et al. 2007). Any increase of the distance between stimulus and recording site thus strongly decreases the part of VP and in many cases the AP remains. Consequently, systemic measurements in a distant leaf only showed an AP (Zimmermann and Felle 2009).
2.3 System Potential
System potentials (SPs), in contrast to APs and VPs, reflect a systemic self-propagating hyperpolarization of the plasma membrane or depolarization of apoplastic voltage, respectively (Fig. 4) (Zimmermann et al. 2009). The term SP considers the striking fact this electrical signals can be reliably recorded on systemically, in contrast to APs and VPs. An occurrence of SPs was demonstrated for monocots as well as for dicots indicating a general ability of higher plants to transmit hyperpolarizations systemically (Zimmermann et al. 2009; Zimmermann 2010).
The combined application of wounding (cutting) and different chemical substances (e.g., glutamic acid, LiCl2, CuCl2, aspartic acid, glutamate) as well as stimulation with heat (scorching) evoked SPs (Zimmermann 2010). However, closer analysis was executed with diverse salt solutions (KCl, NaCl, MgCl2, and CaCl2). SPs were systemically recorded with a noninvasive approach of substomatal-placed microelectrodes (Felle et al. 2000; Zimmermann et al. 2009) by giving a stimulus at one leaf and recording of the electrical reaction at a distant leaf. A constant propagation rate of SPs was detected with 5–6 cm min−1 for both directions acropetal and basipetal. The determined range of velocity indicates rather an electrotonic propagation of SPs than a possible induction of wound-allocated electrogenic substances, which has been mentioned for VPs and was determined to be approximately 0.8–1.7 cm min−1 (Canny 1975).
Studies with various chemical stimuli (KCl, NaCl, MgCl2, and CaCl2) at different concentrations (10–100 mM) showed that (1) cations rather than anion trigger SPs, (2) shapes of SPs are adapted to the mode of the stimulus, and (3) strength (in terms of concentration) of the stimulus; all of which indicate the possibility of encoding more sophisticated information (Zimmermann et al. 2009).
An analysis of diverse ion activities (Ca2+, K+, H+, Cl−) within the apoplast of substomatal cavity during a SP again indicated the participation of proton pumps. This hypothesis was proven with the application of fusicoccin, a toxin of the phytopathogenic fungus Fusicoccum amygdali, causing an activation of proton pumps (Marrè 1979; Hager 2003). Besides the induction of SPs by fusicoccin, the transmission of the electrical signal could be prevented with the application of the proton pump inhibitor vanadate (Zimmermann et al. 2009). Hence, these results suggest that the activated status of proton pumps may be relayed from cell to cell reasoning the self-propagation of SPs. Although the same applied stimuli are well known to provoke APs (i.e., glutamic acid, KCl, CaCl2) or VPs (heat), SPs were systemically recorded in the most cases, indicating a higher probability of long-distance transmission for SPs in comparison to APs and VPs (Zimmermann 2010). However, it seems contradictory that the same stimuli evoke different electrical signaling types; but the depolarizations of APs and VPs can be seen as “regulated” disturbances of the membrane potential that has to be recovered with the activation of proton pumps; the latter, on the other hand, possess a sufficient electrical coupling for long-distance transmission. Without a doubt, the diverse stimuli trigger APs and/ or VPs at the site of application but the depolarization gets “lost” on the systemic spreading due to the pronounced decrement of VPs and/or the obvious suboptimal electrical coupling of plant cells for APs (Zimmermann et al. 2009).
Hence, SPs represent the first affirmation of previously proposed concept of propagating signals basing upon fast changes of active pumps (refs. see Stahlberg and Cosgrove 1992) and support previous results of systemically recorded hyperpolarizations (Lautner et al. 2005).
3 Downstream Signaling and Physiological Responses
The evidence of electrical signals in plant tissues per se, generated upon artificial treatments such as heat or high salt concentrations, does not necessarily mean that those signals are of physiological relevance. However, up to now various studies demonstrated an involvement of electrical signals in various physiological reactions in higher plants (Table 3). Numerous indications were given for a proper role of electrical signals within intra- and distant intercellular communication and for the regulation of physiological processes at the molecular, cellular, and the organism level (Davies 1987; Fromm and Bauer 1994; Fromm and Lautner 2007). The most obvious results were obtained for plants with motor activity, i.e., tentacle bending in Drosera spp., or leaf movements in Mimosa pudica or Dionaea muscipula. The necessity of mechanically triggered action potentials for the induction of rapid, thigmonastic leaf movement has been well established (Braam 2004; Volkov et al. 2007, 2009, 2010b). All these motor activities depend on the generation of an AP (Sibaoka 1969; Williams and Pickard 1972; Fromm and Eschrich 1988).
Heat induces both AP and VP that accompany the enhancement of systemic ethylene emission, for example, in leaves of Vicia faba seedlings (Dziubinska et al. 2003). Other studies focused on general metabolic processes (photosynthesis respiration, gas exchange, stomata movements) following diverse abiotic stimuli (Table 3).
Encouraging results have been published in the field of plant defense supporting the idea of electrical signaling as an integral signaling event in the initiation of defensive reactions (Stahlberg and Cosgrove 1994; Favre et al. 2001). Electrical signals have been shown to cause effects in systemic leaves, for example, the regulation of various genes (Graham et al. 1986; Wildon et al. 1992; Stanković and Davies 1997; Herde et al. 1998). In tomato (Lycopersicon esculentum), the first results described that proteinase inhibitor (pin) as well as calmodulin genes were upregulated due to wounding and heat stimuli. Consequentially, plants that generated no electrical signal could not accumulate pin mRNA (Stanković and Davies 1997). Moreover, a heat-induced and VP-mediated accumulation of proteinase inhibitor genes (pin II) and jasmonic acid was described in potato (Solanum tuberosum) plants (Fisahn et al. 2004). Proteinase inhibitors negatively affect the digestion of herbivores and jasmonic acid is a well-established regulator within herbivory-induced plant defense responses (Mithöfer and Boland 2012). A previous report of a general decline of phloem content translocation (Fromm and Bauer 1994) has been specified in recent studies where a distinct relationship of transmitted electrical signals and the release of Ca2+ into sieve elements were shown. The consequence was the occlusion of sieve elements via Ca2+-dependent forisome dispersion in Vicia faba plants or protein plugs in Cucurbita maxima (Furch et al. 2007, 2009, 2010). Sealing of sieve elements can be seen as an early response to pathogen and/or herbivore attack to prevent transmission of attacker-released toxins and loss of valuable phloem sap.
The biological significance of SPs as a common signal asks for a natural trigger and an involvement within distinct physiological processes. First indications were found following feeding of herbivorous lepidopteran caterpillars (Spodoptera littoralis). Various hyperpolarizations could be recorded in distant leaves indicating SPs. Moreover, preliminary results suggest a systemic decrease of jasmonic acid accumulation after induction of SPs (Zimmermann 2010).
4 Conclusions and Outlook
For higher plants, the existence of electrical long-distance signals is well established and accepted. The three types of electrical signaling, AP, VP, and SP, have been demonstrated for various plants, monocots as well as dicots. Regardless of how the different types of electrical signals are generated, realized, and propagated, this indicates that this kind of signaling is widespread and a general feature in plants, though the best-noticed studies have been done with specialized plants such as the carnivorous Dionaea muscipula or touch-sensitive Mimosa pudica.
Although there is a growing body of evidence strongly suggesting that electrical signals in plants are indeed constituents of abiotic and biotic stress-induced signaling cascades, a final proof is still missing. Unfortunately, still very often the applied stimuli used to induce electrical signals are artificial and far from being physiological. There is no question that such experiments clearly showed the ability of plants to generate electrical signals, but it is difficult to generally conclude that these signals are naturally occurring and involved in plant’s physiology, particularly in the communication between distant cells or organs. Thus, in order to understand electrical long-distance signaling in plants, the elucidation of a signaling cascade that includes or depends on an electrical signal and leads to the initiation of a defined physiological response is still a task that urgently needs to be addressed. For sure, this will remain a major scientific challenge for plant physiologists in the future.
References
Adam G, Läuger P, Stark G (2009) Physikalische Chemie und Biophysik. Springer, Heidelberg
Beilby MJ (2007) Action potential in charophytes. Int Rev Cytol 257:43–82
Blatt FJ (1974) Temperature dependence of the action potential in Nitella flexilis. Biochim Biophys Acta 339:382–389
Bose JCH (1907) Plant response as a means of physiological investigation. Longman, Green & Co, London
Braam J (2004) In touch: plant responses to mechanical stimuli. New Phytol 165:373–389
Bradley J, Williams EJ (1966) Chloride electrochemical potentials and membrane resistances in Nitella translucens. J Exp Bot 18:241–253
Burdon-Sanderson J (1873) Note on the electrical phenomena which accompany irritation of the leaf of Dionaea muscipula. Proc R Soc Lond 21:495–496
Canny MJP (1975) Mass transfer. In: Zimmermann HM, Milburn JA (eds) Encyclopedia of plant physiology. Springer, Berlin, pp 139–153
Darwin CR (1875) Insectivorous plants. John Murray, London
Davies E (1987) Action potentials as multifunctional signals in plants: a unifying hypothesis to explain apparently disparate wound responses. Plant Cell Environ 10:623–631
Dziubinska H, Paszewski A, Trebacz K, Zawadzki T (1983) Electrical activity of the liverwort Conocephalum conicum: The all-or-nothing law, strength-duration relation, refractory periods and intracellular potentials. Physiol Plantarum 57:279–284
Dziubinska H, Trebacz K, Zawadzki T (2001) Transmission route for action potentials and variation potentials in Helianthus annuus L. J Plant Physiol 158:1167–1172
Dziubinska H, Filek M, Koscielniak J, Trebacz K (2003) Variation and action potentials evoked by thermal stimuli accompany enhancement of ethylene emission in distant non-stimulated leaves of Vicia faba minor seedlings. J Plant Physiol 160:1203–1210
Eschrich W, Fromm J, Evert RF (1988) Transmission of electric signals in sieve tubes of zucchini plants. Bot Acta 101:327–331
Favre P, Greppin H, Agosti RD (2001) Repetitive action potentials induced in Arabidopsis thaliana leaves by wounding and potassium chloride application. Plant Physiol 39:961–969
Felle HH, Zimmermann MR (2007) Systemic signalling in barley through action potentials. Planta 226:203–214
Felle HH, Hanstein S, Steinmeyer R, Hedrich R (2000) Dynamics of ionic activities in the apoplast of the sub-stomatal cavity of intact Vicia faba leaves during stomatal closure evoked by ABA and darkness. Plant J 24:297–304
Fisahn J, Herde O, Willmitzer L, Peña-Cortés 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 45:456–459
Fromm J, Bauer T (1994) Action potentials in maize sieve tubes change phloem translocation. J Exp Bot 45:463–469
Fromm J, Eschrich W (1988) Transport processes in stimulated and non-stimulated leaves of Mimosa pudica. Trees 2:18–24
Fromm J, Eschrich W (1993) Electric signals released from roots of willow Salix viminalis L. change transpiration and photosynthesis. J Plant Physiol 141:673–680
Fromm J, Fei HM (1998) Electrical signaling and gas exchange in maize plants of drying soil. Plant Sci 132:203–213
Fromm J, Lautner S (2007) Electrical signals and their physiological significance in plants. Plant Cell Environ 30:249–257
Fromm J, Spanswick R (1993) Characteristics of action potentials in willow (Salix viminalis L.). J Exp Bot 44:1119–1125
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 61:3697–3708
Furch ACU, van Bel AJE, Fricker MD, Felle HH, Fuchs M, Hafke JB (2009) Sieve element Ca2+ channels as relay stations between remote stimuli and sieve tube occlusion in Vicia faba. Plant Cell 21:2118–2132
Furch ACU, Zimmermann MR, Will T, Hafke JB, van Bel AJE (2010) Remote-controlled stop of phloem mass flow by biphasic occlusion in Cucurbita maxima. J Exp Bot 61:3697–3708
Gradmann D (1976) “Metabolic” action potentials in Acetabularia. J Membr Biol 29:23–45
Graham JS, Hall G, Pearce G, Ryan CA (1986) Regulation of proteinase inhibitors I and II mRNAs in leaves of wounded tomato plants. Planta 169:399–405
Hager A (2003) Role of the plasma membrane H+-ATPase in auxin-induced elongation growth: historical and new aspects. J Plant Res 116:483–505
Herde O, Peña-Cortés H, Willmitzer L, Fisahn J (1998) Remote stimulation by heat induces characteristic membrane-potential responses in the veins of wild-type and abscisic acid-deficient tomato plants. Planta 206:146–153
Hlavácková V, Krchnák P, Naus J, Novák O, Spundová M, Strnad M (2006) Electrical and chemical signals involved in short-term systemic photosynthetic responses of tobacco plants to local burning. Planta 225:235–244
Hodick D, Sievers A (1988) The action potential of Dionaea muscipula Ellis. Planta 174:8–18
Hope AB, Findlay GP (1964) The action potential in Chara. Plant Cell Physiol 5:377–379
Houwink AL (1935) The conduction of excitation in Mimosa pudica. Recueil des Travaux Botaniques Neerlandais 32:51–91
Julien JL, Desbiez MO, de Jeagher G, Frachisse JM (1991) Characteristics of the wave of depolarization induced by wounding in Bidens pilosa. J Exp Bot 42:131–137
Kikuyama M (1987) Ion efflux during a single action potential of Nitella axilliformis in medium lacking Ca2+. Plant Cell Physiol 28:179–186
Kunkel KAJ (1898) Über elektromotorische Wirkungen an unverletzten lebenden Pflanzenteilen. Arbeiten des Botanischen Instituts Würzburg 2:1–17
Lautner S, Grams EET, Matyssek R, Fromm J (2005) Characteristics of electrical signals in poplar and responses in photosynthesis. Plant Physiol 139:2200–2209
Lunevsky VZ, Zherelova OM, Yostrikov IY, Berestovsky GN (1983) Excitation of Characeae cell membranes as a result of activation of calcium and chloride channels. J Membr Biol 72:43–58
Malone M (1992) Kinetics of wound-induced hydraulic signals and variation potentials in wheat seedlings. Planta 187:505–510
Malone M, Stanković B (1991) Surface potentials and hydraulic signals in wheat leaves following localized wounding by heat. Plant Cell Environ 14:431–436
Marrè E (1979) Fusicoccin: a tool in plant physiology. Ann Rev Plant Physiol 30:273–288
Mithöfer A, Boland W (2012) Plant defense against herbivores: chemical aspects. Ann Rev Plant Biol 63:431–450
Opritov VA, Lobov SA, Pyatgin SS, Mysyagin SA (2005) Analysis of possible involvement of local bioelectric responses in chilling perception by higher plants exemplified by Cucurbita pepo. Russ J Plant Physiol 52:801–808
Paszewski A, Zawadzki T (1976) Action potentials in Lupinus angustifolius L. shoots. III. Determination of the refractory periods. J Exp Bot 27:369–374
Pickard BG (1973) Action potentials in higher plants. Bot Rev 39:172–201
Pyatygin SS, Opritov VA, Vodeneev VA (2008) Signaling role of action potentials in higher plants. Russ J Plant Physiol 55:285–291
Rhodes JD, Thain JF, Wildon DC (1996) The pathway for systemic electrical signal conduction in the wounded tomato plant. Planta 200:50–57
Ricca U (1916) Soluzione d´un problema di fisiologia: la propagazione di stimulo nella Mimosa. Nuovo Giornale Botanico Italiano 23:51–170
Roblin G (1985) Analysis of the variation potential induced by wounding in plants. Plant Cell Physiol 26:455–461
Roblin G, Bonnemain JL (1985) Propagation in Vicia faba stem of a potential variation induced by wounding. Plant Cell Physiol 26:1273–1283
Sibaoka T (1953) Some aspects on the slow conduction of stimuli in the leaf of Mimosa pudica. Sci Rep Tohoku Univ Biol 20:72–88
Sibaoka T (1969) Physiology of rapid movements in higher plants. Ann Rev Plant Physiol 20:165–184
Stahlberg R, Cosgrove DJ (1992) Rapid alterations in growth rate and electrical potentials upon stem excision in pea seedlings. Planta 187:523–531
Stahlberg R, Cosgrove DJ (1994) Comparison of electric and growth responses to excision in cucumber and pea seedlings. I. Short-distance effects are a result of wounding. Plant Cell Environ 17:1143–1151
Stahlberg R, Cosgrove DJ (1996) Induction and ionic basis of slow wave potentials in seedlings of Pisum sativum L. Planta 200:416–425
Stahlberg R, Cosgrove DJ (1997a) The propagation of slow wave potentials in pea epicotyls. Plant Physiol 113:209–217
Stahlberg R, Cosgrove DJ (1997b) Slow wave potentials in cucumber differ in form and growth effect from those in pea seedlings. Physiol Plantarum 101:379–388
Stahlberg R, Cleland RE, van Volkenburgh E (2005) Decrement and amplification of slow wave potentials during their propagation in Helianthus annuus L. shoots. Planta 220:550–558
Stanković B, Davies E (1996) Both action potentials and variation potentials induce proteinase inhibitor gene expression in tomato. FEBS Lett 390:275–279
Stanković B, Davies E (1997) Intercellular communication in plants: electrical stimulation of proteinase inhibitor gene expression in tomato. Planta 202:402–406
Stanković B, Zawadzki T, Davies E (1997) Characterization of the variation potential in sunflower. Plant Physiol 115:1083–1088
Tarr SE, Lannoye RJ, Dainty J (1970) Changes of ionic and electrical properties of Chara australis when the external Ca is replaced by Mg. J Exp Bot 21:552–557
Trebacz K (1992) Measurements of intra- and extracellular pH in the liverwort Conocephalum conicum during action potentials. Physiol Plantarum 84:448–452
Trebacz K, Tarnecki R, Zawadzki T (1989) The effects of ionic channel inhibitors and factors modifying metabolism on the excitability of the liverwort Conocephalum conicum. Physiol Plantarum 75:24–30
Trebacz K, Simonis W, Schönknecht G (1994) Cytoplasmatic Ca2+, K+, Cl−, and NO3 − activities in the liverwort Conocephalum conicum L. at rest and during action potentials. Plant Physiol 106:1073–1084
Trebacz K, Simonis W, Schönknecht G (1997) Effects of anion channel inhibitors on light-induced potential changes in the liverwort Conocephalum conicum. Plant Cell Physiol 38:550–557
Tsutsui I, Taka-aki O, Kishimoto U (1986) Inhibition of Cl− channel activation in Chara corallina membrane by lanthanum ion. Plant Cell Physiol 27:1197–1200
van Bel AJE, Ehlers K (2005) Electrical signalling via plasmodesmata. In: Oparka KJ (ed) Plasmodesmata. Blackwell, Oxford, pp 263–278
van Sambeek JW, Pickard BG (1976a) 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 54:2642–2650
van Sambeek JW, Pickard BG (1976b) Mediation 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
Vian A, Vian-Henry C, Schantz R, Ledoigt G, Frachisse JM, Desbiez MO, Julien JL (1996) Is membrane potential involved in calmodulin gene expression after external stimulation in plants? FEBS Lett 380:93–96
Volkov AG, Adesina T, Markin VS, Jovanov E (2007) Kinetics and mechanism of Dionaea muscipula trap closing. Plant Physiol 146:694–702
Volkov AG, Carrell H, Markin VS (2009) Biologically closed electrical circuits in venus flytrap. Plant Physiol 149:1661–1667
Volkov AG, Foster JC, Ashby TA, Walker RK, Johnson JA, Markin VS (2010a) Mimosa pudica: Electrical and mechanical stimulation of plant movement. Plant Cell Environ 33:163–173
Volkov AG, Foster JC, Markin VS (2010b) Signal transduction in Mimosa pudica: biologically closed electrical circuits. Plant Cell Environ 33:816–827
Wildon DC, Thain JF, Minchin PEH, Gubb IR, Reilly AJ, Skipper YD, Doherty HM, O’Donnell PJ, Bowles DJ (1992) Electrical signalling and systemic proteinase inhibitor induction in the wounded plant. Nature 360:62–65
Williams SE, Pickard BG (1972) Properties of action potentials in Drosera tentacles. Planta 103:222–240
Zimmermann MR (2010) Analyse der (elektrophysiologisch vermittelten) systemischen Signalübertragung bei Hordeum vulgare L. und Vicia faba L. Doctoral thesis, Justus-Liebig-University Gießen, Germany
Zimmermann MR, Felle HH (2009) Dissection of heat-induced systemic signals: Superiority of ion fluxes to voltage changes in substomatal cavities. Planta 229:539–547
Zimmermann MR, Maischak H, Mithöfer A, Boland W, Felle HH (2009) System potentials, a novel electrical long-distance apoplastic signal in plants, induced by wounding. Plant Physiol 149:1593–1600
Zimmermann MR, Hafke JB, van Bel AJE, Furch ACU (2013) Interaction of xylem and phloem during exudation and wound occlusion in Cucurbita maxima. Plant Cell Environ 36:237–247. doi:10.1111/j.1365-3040.2012.02571.x
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Zimmermann, M.R., Mithöfer, A. (2013). Electrical Long-Distance Signaling in Plants. In: Baluška, F. (eds) Long-Distance Systemic Signaling and Communication in Plants. Signaling and Communication in Plants, vol 19. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-36470-9_15
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