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What Do Plants Need Action Potentials For?

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In: Action Potential ISBN 978-1-61668-833-2 Editor: Marc L. DuBois, pp. 1-26 © 2010 Nova Science Publishers, Inc. Chapter 1 WHAT DO PLANTS NEED ACTION POTENTIALS FOR? Elżbieta Król, Halina Dziubińska, and Kazimierz Trębacz Department of Biophysics, Institute of Biology, Maria Curie-Skłodowska University, Akademicka 19, 20–033 Lublin, Poland ABSTRACT For many years the physiological significance of electrical signalling in plants has been neglected, even though the very first action potentials (APs) were recorded in insectivorous plants in 1873 (1). Still many aspects of plant excitability are not sufficiently well elaborated. However, nowadays it is common knowledge that in animals as well as in plants: (i) ion fluxes through plasma membrane provide AP biophysical bases; (ii) AP transmission is electrotonic, without a decrement and is followed by a refractory period; (iii) there is an ―all-or-nothing‖ principle fulfilled, with an exponential dependency of threshold stimulus strength on stimulus duration; (iv) APs are initiated and propagated by excitable tissues to control a plethora of responses indispensable for growth, nutrient winning, reproduction, and defence against biotic and abiotic challenges. AP can be viewed as a burst of electrical activity that is dependent on a depolarizing current. In plants the depolarization phase of AP consists of Cl-- and Ca2+-fluxes. The following phase—a repolarization—relies in turn on K+ fluxes and active H+ flows that both drive membrane potential back to more negative values. Thus, the AP mechanism is electrochemically governed by the selective properties of the plasma membrane with ion selective conduits as key players. A more detailed understanding of how these membrane proteins work hand in hand during excitation and signal transduction is eagerly awaited. The existence of ion channels was first hypothesized by Alan Hodgkin and Andrew Huxley (2-8), and next confirmed with a patch-clamp technique by Erwin Neher and Bert Sakmann (9). These experiments though conducted on neurons and muscles, respectively, prompted plant electrophysiology as well. Since then substantial evidence for APs in a wide array of plants has been emerging and consequently growing in number. 2 Elżbieta Król, Halina Dziubińska and Kazimierz Trębacz INTRODUCTION Electrical sensitivity of living organisms originates from selective membranes that surround each cell. Thanks to active transport of ions by pumps and transporters (mainly K+, Na+, H+ and Ca2+ but also Cl-) and selective properties of the channels embedded in membranes, a transmembrane potential difference is generated (10-13). This membrane voltage (= membrane potential, transmembrane potential) is the difference between the inside and the outside (by convention set to 0) potential. The magnitude of the membrane potential directly depends on the membrane selective properties and hence on concentration of ions facing both sides of the membrane (12). There is a negative membrane resting potential (difference at rest) in most living cells. At rest, the net flow of ions through a selective membrane equals zero, which means that outflows and inflows of ions transported are counterbalanced. Any unbalanced movement of ions results in changes in the resting potential. Such imbalances can be triggered by stimuli as different as: electric current, light, pressure (mechanical or osmotic) and chemical substances of various derivation. The above- listed stimuli are either directly or indirectly responsible for ion channel, transporter or pump activation/inhibition, which transiently changes membrane permeability for corresponding ions and thus make the resting potential change (14). Evoked membrane potential changes hold (i) various shapes, (ii) kinetics, (iii) duration, (iv) properties and (v) functions and accordingly can be classified as: i. hyperpolarization / depolarization (if it drives the potential to more negative / less negative values); ii. graded / of constant amplitude (with an amplitude depending on / independent of stimulus strength); iii. transient / long-lasting; iv. propagable / non-propagable v. systemic / local (spreading within the whole organ or organism / appearing locally). Among them the best studied and characterized are action potentials (APs), which are a transient membrane depolarization with all-or-nothing characteristics (14-17), propagating systemically (18-20) with a cell-specific velocity (14,21) and without a decrement (an amplitude decrease). As for the AP amplitude that is cell-specific, too, it cannot be increased by an increase in stimulus strength. The physical depiction of the latter statement is reflected in the above-specified ―all-or-nothing characteristics‖. In addition, the relation between threshold stimulus charge (strength) and stimulus duration can be represented by Weiss's experimental formula—the exponential dependence of threshold stimulus strength on its duration (22). The AP transmission along excitable membranes is achieved through electrotonic transmission. A local current flows between the just activated part and the adjacent yet unexcited part. After the passage of each single AP there is a refractory period—the period of transient unexcitability or, in other words, time needed for a cell to restore its excitability. Finally, one must keep in mind that excitability in electrophysiology nomenclature means the ability to generate and transmit APs. The cells on whose membranes the other potential changes but not APs occur are not considered excitable (23). What Do Plants Need Action Potentials for? 3 A PINCH OF HISTORY When in 1786 Luigi Galvani dissected a frog, touched its leg with a charged scalpel and saw the frog‘s leg kicking after the charge had jumped from the scalpel to the muscle tissue, he had no idea that the charge flow induced an AP and that the muscles contracted as a result of AP (excitation) spreading. However, his observation made Galvani the first investigator to appreciate the relationship between electricity and movement in living organisms. His associate and intellectual adversary Alessandro Volta went deeper into the nature of electrochemical processes (which allowed him invent the first battery—a galvanic cell). His intuition that ―animal electricity‖ has the same underpinnings as electrochemical reactions proved correct and widely contributed to our understanding of ion-pulling forces in living systems (24). Starting from 1830 till his death in 1865 another Italian scientist, the physician and neurophysiologist Carlo Matteucci pursued experiments on frog muscles, using them as a kind of electricity-detector (25). His work influenced directly the German physician Emil du Bois-Reymond, who, trying to duplicate Matteucci‘s results, ended up with the discovery of APs. At that time he termed them ―negative variations‖. The results of du Bois-Reymond‘s inquiries were being compiled systematically in his life-work Researches on Animal Electricity, the first part of which appeared in 1848, and the last in 1884. Though the story of bioelectricity began with a frog, its impact on plant biology was equally impressive. The very first APs recorded in plants were reported by the English physician-physiologist Sir John Scott Burdon-Sanderson, who—encouraged by Charles Darwin—was the first to recognize the electric phenomena in carnivorous plants (1). For his pioneering work in the field of electrophysiology and plant physiology, the Royal Society awarded Burdon-Sanderson a Royal Medal in 1872. Inspired by Burdon-Sanderson‘s work, another British scientist Walter Gardiner (a botanist) devoted himself to carnivorous spp. trying to find a link between excitation and histological changes in secretory glands (26). Next, the Austrian botanists and father of a plant cell totipotentiality theory, Gottlieb Johann Friedrich Haberlandt found non- carnivorous plants to move after electrical stimulation (27). At the same time in Bengal, Haberlandt‘s peer Sir Jagadish Chandra Bose (a polymath: physicist, biologist, archaeologist and writer) studied the correlation between plant development and environmental stimulants (wounds, chemical agents, light and temperature changes) with the help of his self-invented devices (a crescograph to measure plant growth; microamperemeter for current assessments; an electric probe for voltage recordings). On intact plants he measured electrical conduction and corresponding changes in the cell membrane potential in response to chemical and physical stimulation (28-29). Having generalized that all strong stimuli produced a transient diminution of growth rate, a negative mechanical response (cell shrinking) and an electric response of ―galvanometric negativity‖ (= AP), he was very close to discerning excitation as an endogenous form of cell signalling for stress/danger-sensing (29-30). He also worked on isolated vascular bundles to conclude that plants contain organs which are analogous to muscle and nerves in animals (30), just as Burdon-Sanderson had suspected (31). However, because of prevailing prejudices and general acceptance that plants should not be compared to animals, Bose‘s observations were not taken into serious consideration and neglected for over 70 years. Letting higher plants fall into oblivion, the first intracellular recordings (with a cell- inserted microelectrode) of APs were registered in lower plants (32-34). Varied 4 Elżbieta Król, Halina Dziubińska and Kazimierz Trębacz responsiveness of higher plants according to season, vigour, water status, temperature,
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