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Electrophysiology of Plant Gravitropism

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Electrophysiology of Plant Gravitropism Electrophysiology of plant gravitropism Bratislav Stanković Brinks Hofer Gilson & Lione, 455 N. Cityfront Plaza Drive, Chicago, Illinois 60611, U.S.A. Introduction Earth’s gravitational field influences plant growth, morphology, and development. The vector of the gravity force is powerful enough to largely dominate the other directional tropic stimuli to which plants respond. Both roots and shoots respond to gravistimulation with differential, directional growth, through processes known as positive and negative gravitropism, respectively (Darwin, 1986). Some of the cellular events that underlie gravitropic responses are known (recently reviewed by Morita and Tasaka, 2004); the completion of a mechanistic model of plant gravity responses remains an elusive objective. In roots, the gravity-sensing cells are the columella cells located in the root cap. These cells, known as stacocytes, contain starch-filled amyloplasts that sediment in the direction of gravity (Masson, 1995). In shoots, the gravity-perceptive tissue is the endodermis, which contains sedimentable amyloplasts (Tasaka et al., 1999). In both roots and shoots, the perceived gravitropic stimulus is transduced to cells that start exhibiting differential growth, resulting in organ bending and reorientation. Little is known about the signaling pathway linking gravity perception to differential growth responses, either in the root, or in the shoot. Plant cells exhibit a spectrum of bioelectric characteristic including electrical potentials, conductance, impedance, and permeability. Plant physiological functions are closely intertwined with cells’ electric properties, through processes that involve energy maintenance and ion exchange with the environment. Steady-state electrical potentials can be measured across the plasma membrane, using microelectrodes and patch-clamping techniques. On the external plant surface, electrical potentials and ion fluxes are monitored using surface-contact electrodes and vibrating probes. A variety of abiotic stimuli induce electrical activity in plants. The best- characterized electrical signals in plants are the action potentials and the variation potentials (“slow waves”). Voltage-gated, mechanosensitive, and ligand-activated ion channels, as well as proton pumps, are involved in generation and maintenance of these bioelectric potentials. Action potentials and variation potentials are both local and intercellularly propagated electrical signals. Transmitted to distant regions, these signals trigger an array of systemic molecular and cellular responses (reviewed by Davies and Stanković, 2005). The information that the electrical signals carry and the responses that they evoke depend on either the ions traversing the membrane, the change in membrane potential, or both. Despite the long-documented existence of gravity-induced electrical activity in plants, this field is marked with a surprising dearth of investigation. Discovered a century ago in the petioles of Tropaeolum as a differential change in extracellular electric potential (Bose, 1907), the phenomenon of gravielectricity has been rarely studied by either electrophysiologists or by researchers studying gravitropism. Therefore, coming forth with a hypothesis to describe gravielectrical responses in plants is a speculative endeavor. This review summarizes the state of knowledge related to the role of extra- and intra-cellular electrical activity in gravistimulated higher plants. The seminal studies concerning the electrophysiology of plant gravitropism are highlighted. A few ideas on the correlation of electrical activity with responses to gravity are presented. In conclusion, a prospect for future research on the electrophysiology of gravitropism is suggested. Extracellular gravielectric potentials The early studies on involvement of electrical potentials in plant gravitropism involved measurements of extracellular electric potentials. In the heroic age of discovery of plant electrical activity, measurements were done using extracellular, surface contact electrodes, using ionic bridges typically consisting of diluted potassium chloride. Following the studies of Bose (1907), pioneering investigations in the field were conducted by Brauner (1927), Clark (1937), and Schrank (1947). These studies provided evidence that reorientation of plants induces transient electrical activity, a phenomenon that was dubbed “geolectric effect”. Decades had to pass before that phenomenon received further attention from plant biologists. Shoots Plants are electrically active. They generate characteristic steady-state transmembrane potential differences and extracellular ionic current patterns. Bioelectricity may be involved in the establishment of plant cell and organ polarity (Nechitailo and Gordeev, 2001). For example, electrical current flows along the surface of upright-growing epicotyls (Toko et al., 1989, 1990). On the physically lower end of the organ, the plasma membrane is hyperpolarized by 1-2 mV. This hyperpolarization is presumably correlated to spatial information (Etherton and Dedolph, 1972). Horizontal reorientation induces electrical activity in both lower and higher plants (reviewed by Weisenseel and Meyer, 1997). Gravistimulation alters the patterns of extracellular ionic currents, causing current asymmetry. Gravistimulation also changes the patterns of electrical potential along roots and shoots. For example, within minutes of horizontal reorientation of maize coleoptiles, the electrical potential became more positive on the lower side than on the upper side. The maximal change in potential was 20-25 mV, and it was reversible when the coleoptiles were rotated back to vertical (Grahm and Hertz, 1962). In soybean hypocotyls, directional change in the gravity vector induced fast electrical field changes (Tanada and Vinten-Johansen, 1980). These changes were 2 reflected as increase in positive electrical potential in the lower side of the hypocotyl, occurring rapidly, approximately one minute after horizontal placement. The increase in positive electrical potential was maximal in the region undergoing gravity-induced curvature, in a zone 1-2 cm below the hook. The maximal amplitude of the transient change in electrical potential was about 17 mV (Tanada and Vinten-Johansen, 1980). Similarly, in bean epicotyls, electrical potential on the lower side increased, whereas the potential on the upper side decreased for about one hour after gravistimulation (Imagawa et al., 1991). The electrical activity was monitored as soon as the plants were rotated. The amplitudes of the electrical potential changes were 10-25 mV, and were dependent on the position of the electrodes attached to the epicotyls (Imagawa et al., 1991). More recently, Shigematsu et al. (1994) monitored rapid surface potential changes in gravistimulated bean epicotyls. In a limited region on the upper side of the epicotyl, surface electrical potential decreased soon after gravistimulation. The magnitude of the transient potential change was about 10 mV, and it occurred 30-120 seconds following gravistimulation. At the same time, the surface potentials on the lower side of the epicotyls scarcely changed. The rapid change in potential on the upper side was highly correlated to the early downward curvature (transient positive gravitropic response) that was simultaneously monitored (Shigematsu et al., 1994). It has been suggested that the electrical asymmetry across the epicotyl is related to asymmetric auxin distribution and contributes to induction of H+ secretion, which is thought to initiate differential growth in shoot gravitropism (Wright and David, 1983). Indeed, because the electrical changes occur prior to the plausible movement of auxin, it was postulated that the signals mediate the asymmetric auxin distribution or asymmetric Ca2+ distribution during gravitropism (Imagawa et al., 1991). 20 Upper side 15 Lower side 10 5 0 -5 -10 Electrical potential (mV) -15 -20 -5 0 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75 80 85 90 Time (min) 3 Figure 1. Changes in extracellular potentials in gravistimulated shoots (approximate data are redrawn from Imagawa et al., 1991). Kinetics of the change in surface electrical potential in the upper and lower sides of gravistimulated adzuki bean (Phaseolus angularis) epicotyl is shown. The measured area was approximately 20 mm from the base of the first leaves. At zero time, the epicotyl was rotated to horizontal position. Roots The growing root tip also exhibits strong electrical activity. Detailed measurements of endogenous currents surrounding roots were reported over 40 years ago (Scott and Martin, 1962). Since then, several related studies have indicated that the pattern of endogenous ionic currents around vertically growing roots is consistent across species. Ionic currents typically enter the meristem and the younger parts of the elongation zone, and leave the remainder of the elongation zone and the more mature parts of the root (Behrens et al., 1982; Weisenseel et al., 1992). An area of variable current exists around the root cap; an area of large inward current is present around the meristem and apical part of the elongation zone; and an area of moderate outward current is present in the remainder of the elongation zone and the mature root tissue (Collings et al., 1992). Horizontal reorientation of plants induces changes in the current pattern around the root. The change in current pattern is rapid, and is initiated at the root cap; it also appears at the meristem and the elongation
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