Characteristics of Electrical Signals in Poplar and Responses in Photosynthesis

Abstract

To gain an understanding of the role of electrical signaling in trees, poplar (Populus trichocarpa, Populus tremula 3 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 1 -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 CO 2 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, evid...

Variation potential in higher plants: Mechanisms of generation and propagation

“…VP amplitude decrease or full suppression of these electrical signals under the action of ion channel blockers were also shown. 46,86 Potentiometric analysis showed that VP generation was accompanied by an increase in external concentrations of Cl ¡ . 37,46 What seems apparently contradictory in these different studies may be explained by differences in ion mechanisms among different VP components.…”

Electrophysiology of Woody Plants

“…Additional studies made considerable progress in linking electrical signals with respiration and photosynthesis (Lautner et al, 2005;Koziolek et al 2003), phloem transport (Fromm & Eschrich, 1988;Fromm & Bauer, 1994) and the rapid, plant-wide deployment of plant defenses (Wildon et al 1992;Malone et al 1994;Herde et al 1995Herde et al , 1996Volkov & Haak 1995;Stankovic & Davies, 1996Volkov, 2000). The significant development of plant neurobiology in the last decade is mostly related to electrophysiology based research, as an integrated view of plant signaling and behavior (Brenner et al, 2006;Baluška & Mancuso 2008;Barlow, 2008).…”

“…Research on plant electrophysiology specifically focused on woody plants like poplar and willow trees, have been seldom reported (Fromm & Spanswick, 1993;Lautner et al, 2005;Gibert et al, 2006). In fruit bearing deciduous and perennial plant species, electrophysiology studies are very limited as well, although it is in such plants that the need for rapid and efficient signals other than chemical and hydraulic signaling becomes more obvious Nadler et al 2008;Gurovich & Hermosilla, 2009;Oyarce & Gurovich, 2011).…”

“…The existence of electrophysiological mechanisms for information perception, transmission and processing between different plant organs and tissues, allowing the expression of fast and accurate physiological reactions to specific biotic or abiotic stimuli, is expressed by means of real-time detectable action (APs) and variation (VPs) potentials (Datta & Palit, 2004;Lautner et al, 2005;Oyarce & Gurovich, 2010;Volkov et al, 2009;Wang et al, 2009). An additional type of electric potential in plants has been proposed by Zimmermann et al (2009), to be called system potential.…”

A testimony of inter-plant communication through electrophysiological signal analysis

“…The AP propagates with constant amplitude along the length of cell membrane when phloem is stimulated. (Davies and Murray 2004, Fromm and Lautner 2005, Fromm 2006). The Variation Potential is quite similar to the concept of event related potentials in humans.…”