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First published online July 22, 2005; 10.1104/pp.105.064196 Plant Physiology 138:2200-2209 (2005) © 2005 American Society of Plant Biologists Characteristics of Electrical Signals in Poplar and Responses in Photosynthesis1Fachgebiet Angewandte Holzbiologie, Technische Universität München, 80797 Munich, Germany (S.L., J.F.); and Lehrstuhl Ökophysiologie der Pflanze, Technische Universität München, 85354 Freising, Germany (T.E.E.G., R.M.)
To gain an understanding of the role of electrical signaling in trees, poplar (Populus trichocarpa, Populus tremula x P. tremuloides) shoots were stimulated by chilling as well as flaming. Two kinds of signal propagation were detected by microelectrode measurements (aphid technique) in the phloem of leaf veins: (1) basipetal, short-distance signaling that led to rapid membrane hyperpolarization caused by K+-efflux within the leaf lamina; and (2) acropetal, long-distance signaling that triggered depolarization of the membrane potential in the leaf phloem. In the latter, the depolarizing signals travel across the stem from the manipulated leaves to adjacent leaves where the net CO2 uptake rate is temporarily depressed toward compensation. With regard to photosystem II, both heat-induced long-distance and short-distance signaling were investigated using two-dimensional "imaging" analysis of chlorophyll fluorescence. Both types of signaling significantly reduced the quantum yield of electron transport through photosystem II. Imaging analysis revealed that the signal that causes yield reduction spreads through the leaf lamina. Coldblocking of the stem proved that the electrical signal transmission via the phloem becomes disrupted, causing the leaf gas exchange to remain unaffected. Calcium-deficient trees showed a marked contrast inasmuch as the amplitude of the electrical signal was distinctly reduced, concomitant with the absence of a significant response in leaf gas exchange upon flame wounding. In summary, the above results led us to conclude that calcium as well as potassium is involved in the propagation of phloem-transmitted electrical signals that evoke specific responses in the photosynthesis of leaves.
Electrical signaling in plants was first revealed in the 1870s in insectivorous plants by Burdon-Sanderson (1873)  and Darwin (1875). In the 20th century, evidence for the existence of action potentials was presented in a broad array of plant species, irrespective of the presence of rapid leaf movements (Bose, 1924; Pickard, 1973). Most of the research on electrical signaling dealt with responses evoked by wounding of aboveground organs, providing insights into various processes of plant physiology. Molecular tools made it possible to detect rapid changes in gene expression (Davies and Schuster, 1981; Stankovic and Davies, 1997) as well as activation of proteinase inhibitor genes within plants (Bowles, 1990; Ryan, 1990; Wildon et al., 1992) upon wounding, even across long distances. Wildon et al. (1992) showed the chemical signals evoked by wounding in the phloem to be significantly slower than the rapid changes in membrane potential. Electrical signals that were generated and transmitted from distant plant parts arrived at responding tissues well before the initiation of transcript accumulation. Vian et al. (1999) induced rapid and systemic accumulation of chloroplast mRNA-binding protein transcripts, in tomato (Lycopersicon esculentum), after flame stimulus. In addition to translation and transcription, evidence exists for a role of electrical signals in many processes of plant life, including respiration (Dziubinska et al., 1989; Filek and Koscielniak, 1997), water uptake (Davies et al., 1991), phloem unloading (Fromm, 1991), and phloem translocation (Fromm and Bauer, 1994) as well as fertilization (Fromm et al., 1995). Recently, this account was extended by a study on the inhibition of photosynthesis in Mimosa pudica (Koziolek et al., 2004) upon flame wounding, which demonstrated that electrical signals triggered transient changes in chlorophyll fluorescence (PSII electron quantum yield) and leaf gas exchange. Moreover, in this latter case, the transport of chemicals in the phloem was far too slow to account for the induced changes.
In trees, electrically induced action potentials were measured in willow (Salix viminalis) shoots, showing that calcium influx as well as potassium and chloride efflux are involved in the propagation of signals within the phloem (Fromm and Spanswick, 1993
Long-Distance Electrical Signaling
To detect electrical signals in poplar shoots, the membrane potential was measured either in the leaf mesophyll or in the phloem via severed aphid stylets, at a point in the upper stem (Fig. 1, electrode B) or at the first mature leaf (electrode A). The resting potential of the measured phloem cells ranged between –116 mV to –165 mV in 10 experiments with different plants and was similar to the sieve tube potentials in M. pudica (Fromm, 1991
Flame stimulation of the tip of leaf 1 evoked a propagating electrical signal with a hyperpolarizing amplitude of approximately 25 mV as measured in the phloem by electrodes A and B as well as in the mesophyll of the flame-wounded leaf, after electrode A had been inserted into the leaf mesophyll (Fig. 3, top graph). Signal transmission velocity in basipetal direction was 1 to 2 mm s–1. Following flame stimulation of the base of leaf 4, either electrode recorded an irregularly shaped propagating electrical signal with an amplitude of over +50 mV in the phloem as well as in the mesophyll of leaf 1 (Fig. 3, central graph). In contrast to the action potentials evoked by stem chilling (Fig. 2, bottom graph), the flame-induced signals reflected failure in reestablishing the original resting potential, indicating that the voltage changes are different from action potentials. The transmission velocity was 1 to 2 mm s–1 in acropetal direction and, hence, similar to that in basipetally propagating flame-induced signals. To disrupt the propagation of electrical signals, a coldblock of 4°C was applied to the stem between the second and third mature leaf underneath the apex. In contrast to the unchilled plants, the resting potential of the phloem depolarized only slightly at either electrode (Fig. 3, bottom graph), indicating a strong decrease in signal amplitudes.
It is remarkable that, independent of the type of stimulation (chilling, heating), signals moving in basipetal direction change toward the negative direction, which contrasts with the opposite response in acropetally traveling signals. The Ca2+-influx/Cl–-efflux/K+-efflux sequence in signal generation may explain the depolarizing direction, but different fluxes are needed to explain signals of the negative sign, such as K+-efflux preceding Cl–-efflux. The latter was proved by blocking K+ channels with 1 mM tetraethylammoniumchloride (TEA+), acting on both sides of the membranes (Wong and Adler, 1986 ) and applied to the artificial pond water (APW) medium of the stem (Fig. 1). After 1 d, the inhibitor had been distributed within the plant. When these plants were flame stimulated at the tip of leaf 1, no hyperpolarizing signal was measured in the phloem (Fig. 4, top graph). Obviously, transient hyperpolarization is caused by the transient opening of K+ channels in the plasma membrane.
As the ionic mechanism of excitation is based on the movement of potassium, chloride, and calcium (Tazawa et al., 1987 ; Fromm and Spanswick, 1993), the objective of experiments involving the stimulation of calcium-deficient plants was to characterize the excitation mechanism in poplar. The Ca-deficient plants were distinctly smaller and their leaf size was reduced compared with that in nonlimited plants. Flame wounding of the tip of leaf 1 evoked no detectable electrical signals in the phloem at either electrode position (Fig. 4, central graph). However, signals with strongly reduced amplitudes were measured in acropetal direction after flame stimulation of leaf 4 (Fig. 4, bottom graph), perhaps reflecting the physiological significance of the upwards transmission of electrical signals in plant life.
No photosynthetic response was found upon stimulation of leaves or stem with ice water. However, flaming of the tip of leaf 1 caused a substantial decrease in the electron quantum yield of PSII (Fig. 5A). This effect occurred 80 s after flame stimulation in the intercostal regions of the central part of the lamina, at a distance of 3 cm from the leaf tip. The inhibitory response spread basipetally throughout the leaf, showing a delay in the arrival of the electrical signal at electrode B (approximately 60 s after flame wounding of the leaf tip) in relation to electrode A (after only 2 s; Fig. 3, top graph). In the flame-stimulated leaf, the fluorescence response reached a minimum after about 300 s, prior to incipient recovery.
Flaming of leaf 4 caused a decrease in the electron quantum yield of PSII in leaf 1, evidence of which was found in the leaf veins 240 s of the latter after flame stimulation, and indicating that the signal spreads via the veins into the mesophyll (arrival after 300 s; Fig. 5B). The inhibitory response propagated acropetally throughout the leaf and was delayed in relation to the electrical signal that arrived in leaf 1 only 80 s after flaming of leaf 4 (Fig. 3, central graph). A minimum in the time course of the fluorescence response was reached in the left half of the lamina of leaf 1 after about 420 s (Fig. 5B, white arrow) prior to incipient recovery. However, it took about 600 s in the right half of the leaf for the minimum to occur (black arrow). The highly resolved time course of the fluorescence response shows the decrease in PSII quantum yield to occur simultaneously in both the veins and the intercostal regions of leaf 1 taking 160 s from the time of flame stimulation of the leaf tip (distance approximately 5 cm; Fig. 6A). By contrast, a distinct two-step response was observed in leaf 1 during acropetal signaling when leaf 4 was flame stimulated, as the response in veins was faster and stronger than in the intercostal regions (Fig. 6B). In these latter areas, the transient response was delayed by about 60 s compared with the occurrence in the veins. The differences in the response between long-distance signaling along the shoot (Fig. 6B) and short-distance signaling within the same leaf (Fig. 6A) reveal, in the first case, that the signals spread into the mesophyll via the veins, whereas in the latter case, signals travel across veins and mesophyll at similar velocities.
Leaf Gas Exchange In leaf 1, the net CO2 uptake rate (JCO2) sharply dropped to about compensation 30 s after flame stimulation of the leaf tip and stayed there for about 90 s before subsequent recovery (Fig. 7A). At the same time, the stomatal conductance (gH2O) remained stable, indicating the absence of stomatal movements. The finding of a photosynthetic reaction not showing any reaction in the gH2O is astonishing. However, the internal CO2 concentration increased transiently (data not shown), indicating that the relationship between JCO2 and gH2O is correct. A similar response occurred in leaf 1, when leaf 4 was flame stimulated at a distance of over 10 cm. At 120 s after stimulation, the JCO2 decreased immediately to compensation, staying there for 100 s and then recovering almost completely (Fig. 7B). Chilling the stem slowly down to a temperature of +4°C (coldblock) between leaves 2 and 3 showed that the gas exchange of leaf 1 remained unaltered (Fig. 7C), concomitant with the suppression of the long-distance electrical signal (Fig. 3, bottom graph). This coincidence indicates that the electrical signal has a modifying impact on CO2 uptake. Experimentation with calcium-deficient plants did not result in any significant response in gas exchange after flame stimulation of leaf 4 (Fig. 7D), which is consistent with the distinctly reduced amplitude of the recorded electrical signal (Fig. 4, bottom graph).
To determine the velocity of chemical signaling, the petioles of excised leaves were fed with 14C-labeled Suc. After a 600-s translocation, macroautoradiography showed that the primary vein became labeled and 14C-Suc extended from the vein across the entire lamina (data not shown). Since the velocity of electrical signal transmission following flame stimulation was 1 to 2 mm s–1 in both acropetal and basipetal direction, autoradiography proved chemical signaling to be much too slow to account for the photosynthetic response after flame stimulation.
The results presented here show that electrical signals propagated over long distances as well as short distances are capable of modifying photosynthesis in trees. Previous studies had reported on the capacity of many plant species to generate and transmit action potentials as well as variation potentials (Pickard, 1973 ; Davies, 1987). In ecophysiology, electrical signals play a key role in the communication of environmental stimuli within plants, apparently acting within and across cells, tissues, and organs (Volkov and Mwesigwa, 2001). For instance, the pesticide 2,4-dinitrophenol, considered an environmental problem in agriculture as well as a human health hazard, induced fast action potentials and decreased the variation potential in soybean (Glycine max; Mwesigwa et al., 2000). Pentachlorophenol too, a known pollutant and uncoupler of oxidative phosphorylation, induced action potentials in soybean (Volkov et al., 2000). Recent experiments on signal transmission in M. pudica demonstrated that a link exists between flame-induced electrical signals and photosynthetic responses, as inferred from two-dimensional imaging analysis of chlorophyll fluorescence in combination with gas exchange assessment (Koziolek et al., 2004).
This study on poplar confirms the latter findings for trees. Moreover, our results demonstrate that different stimulation types and positions incite characteristic electrical signals, each with a specific influence on photosynthesis. We used the aphid technique to measure electrical signals in phloem cells that share fundamental properties with nerve cells in animals, i.e. the existence of excitable membranes by which electrical excitations can be transmitted from cell to cell. In poplar, the nature of the signal depends on the traveling direction. Basipetally propagating signals (induced by chilling as well as flaming) showed negative voltage changes, whereas acropetally moving signals were characterized by transient membrane depolarization (Figs. 2 and 3). The ionic mechanism of action potentials in plants, i.e. depolarizing signals with positive sign, is based on calcium influx as well as initial chloride efflux followed by potassium efflux (Beilby and Coster, 1979
In the poplars of this study, electrical signals were induced by chilling as well as by flame wounding. As regards chilling, amplitudes and dynamics of the acropetally transmitted signals were typical of plant action potentials, as previously demonstrated in maize (Fromm and Fei, 1998 In poplar, hydraulic signals may play a role in the generation of electrical excitation. Since we managed to measure flame-induced signals in the phloem, the question arises whether pressure or chemical changes in the xylem can activate ion channels in the phloem, making it appear as if a hydraulically induced variation potential were passing through the phloem. However, as the electric signal transmission was disrupted after applying a coldblock to the stem and gas exchange did not respond to flame wounding, it is thought unlikely that hydraulic events play any role in long-distance signaling in poplar. Moreover, variation potentials certainly depend on the prevailing water status of the plant. When shoot water status is saturated, as in the case of the well-watered plants used in this study, xylem tension becomes negligible and variation potentials should not travel at all. We are therefore convinced that the phloem-transmitted flame-induced signals in poplar are self-propagating signals, independent of chemicals traveling through the xylem.
Concerning chemical signaling in the phloem that spreads from the stimulation site through the sieve tubes, the thought cannot be dismissed that photosynthesis is affected by chemical signals. Canny (1975)
With regard to the photosynthetic response, only flame-evoked signals caused photosynthetic changes, whereas chill-induced signals had no impact on photosynthesis. Interestingly, the noninvasive imaging analysis of chlorophyll fluorescence revealed that short-distance signals within leaves after flame stimulation at the tip cause a simultaneous decrease in electron quantum yield of PSII in both veins and intercostal regions (compare with Fig. 6A). By contrast, long-distance signals, again generated by flame wounding of leaves but arriving after having traveled across the plant, reduce the electron quantum yield of PSII in the veins first and in the intercostal regions afterward (Fig. 6B), hence suggesting that the signal spreads via the veins into the mesophyll. Reduction in photosynthesis upon impact by electrical signals is also known for M. pudica (Koziolek et al., 2004
Plant Material and Growth Conditions
One-year-old plants of Populus trichocarpa cv Trichobel were grown in the summer from cuttings under standard greenhouse conditions, at 25°C and 85% relative humidity, in sandy culture medium. In addition, 8-week-old plants of Populus tremula x P. tremuloides Michx. were grown hydroponically but under otherwise identical greenhouse conditions. The latter plants were provided with macro- and micronutrients in a modified Hoagland solution (Hoagland and Arnon, 1950
When about six leaves had developed, plants were cut from their roots and transferred to a Faraday cage for experimentation. They had to be cut from their roots in order to detect the membrane potential by measurements from two sides of the membrane. Microelectrode tips were either inserted into the leaf mesophyll or brought into contact with the exudate droplet on a severed aphid stylet. In the latter case, contact was made at two different positions, either at some point in the upper stem (electrode B) or at the lower side of the first mature leaf underneath the apex (electrode A, Fig. 1). The reference electrode (Ag/AgCl) was immersed into the APW where the cut cross section of the excised stem had also been submerged. The APW was composed of 1.0 mM NaCl, 0.1 mM KCl, 0.1 mM CaCl2, and 1.0 mM MES, adjusted with Tris to a pH value of 6.0.
The electrical potential of the phloem was measured via severed aphid stylets. This involved introducing aphids to a leaf or the stem and allowing them to settle overnight. On the following day, they were severed from their stylets by shots from a laser beam generator (Beck, Neu-Isenburg, Germany), connected to a Zeiss microscope. Electric potential changes were measured through glass microelectrodes with tip diameters of less than 1 µm, back-filled with 3 M KCl. The microelectrode was clamped in an Ag/AgCl pellet holder (WPI) and connected to a microelectrode preamplifier (input impedance >1012 ohms) to which a WPI amplifier (model 750, WPI, Sarasota, FL) was attached. The response time of the microelectrodes is about 1 s, which is fast enough to measure electrical responses induced by heat and cold stimulation. The electrodes were inserted into the leaf mesophyll or attached to the stylet stump by micromanipulators: electrode A in leaf 1 at a mean distance of 30 to 40 mm to the stimulated tip; electrode B at some point in the stem (Fig. 1). The resistance for an electric current inside the aphid stylet is relatively low (around 109
The two-dimensional imaging approach described by Koziolek et al. (2004
The gas exchange in the attached leaves was measured using a steady-state CO2/water diffusion porometer (CQP130, Walz, Effeltrich, Germany) at ambient CO2 concentration of about 360 µL L–1 and a relative humidity of approx. 60%, leaf temperature of about 27°C, and PPFD of about 100 µmol m–2 s–1. Leaf 1 was attached to the porometer and its leaf tip or leaf 4 (compare with Fig. 1) were stimulated by flaming. Leaf net-CO2 exchange was calculated based on single leaf area and expressed as JCO2.
For autoradiographic demonstration of assimilate transport the petiole of a mature leaf was placed into a 5 M 14C-Suc solution. Macroautoradiographs were prepared according to Fromm and Eschrich (1988)
We are grateful to FOR Randolf Schirmer (Bayerisches Amt für Forstliche Saat- und Pflanzenzucht Teisendorf) for providing the poplar plants. Received April 13, 2005; returned for revision May 11, 2005; accepted May 11, 2005.
1 This work was supported by the Deutsche Forschungsgemeinschaft (FR 955/10–1,2).  Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.064196. * Corresponding author; e-mail fromm{at}wzw.tum.de; fax 0049–(0)89–2180–6429.
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F/F'm assessed by chlorophyll fluorescence imaging. The imaged area (l, 22 mm; w, 17 mm) covers the center of leaf 1. A, The tip of leaf 1 was flame stimulated at a distance of 3 cm. Times are given in relation to the instant of injury (at time 0). Changes in 
according to Wright and Fisher, 1981
