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Circadian Rhythms in Biologically Closed Electrical Circuits of Plants Plant Signaling & Behavior 7:2, 282–284; February 2012; G 2012 Landes Bioscience Circadian rhythms in biologically closed electrical circuits of plants Alexander G. Volkov,1,* Astian J. Waite,1 Joseph D. Wooten1 and Vladislav S. Markin2 1Department of Chemistry and Biochemistry; Oakwood University; Huntsville, AL USA; 2Department of Neurology, University of Texas, Southwestern Medical Center, Dallas, TX USA he circadian clock regulates a wide first attempt to resolve experimentally the T range of electrophysiological and origin of rhythm in the leaf movements developmental processes in plants. Here, of Mimosa pudica. We also investigated we discuss the direct influence of a the electrical activity of Mimosa pudica in circadian clock on biologically closed the day light, at night and in darkness the electrochemical circuits in vivo. The following day.2 biologically closed electrochemical cir- Isolated pulvinar protoplasts are res- cuits in the leaves of C. miniata (Kaffir ponsive to light signals in vitro.4-6 In the lily), Aloe vera and Mimosa pudica, dark period, the closed inward-directed K+ which regulate their physiology, were channels of extensor cells are opened analyzed using the charge stimulation within 3 min by blue light. Conversely, method. Plants are able to memorize the inward-directed K+ channels of flexor © 2012daytime Landes and nighttime. Even Bioscience. at continu- cells, which are open in the darkness, are ous light or darkness, plants recognize closed by blue light. In the light period, nighttime or daytime and change the however, the situation is more complex. Doinput resistance.not distribute. The circadian clock can Premature darkness alone is sufficient to be maintained endogenously and has close the open channels of extensor pro- electrochemical oscillators, which can toplasts, but both darkness and a preced- activate ion channels in biologically ing pulse of red light are required to closed electrochemical circuits. The open the closed channels in the flexor activation of voltage gated channels protoplasts.5,6 depends on the applied voltage, electrical The main goal of our experiments charge, and the speed of transmission of was to investigate circadian variation of Keywords: Clivia miniata, circadian electrical energy from the electrostimula- the C. miniata electrical properties.1 We rhythms, biological clock, plant tor to plants. investigated electrical responses of C. electrophysiology, electrostimulation, miniata to electrical stimulation during charge stimulation method the day in daylight, darkness at night, and In plants, circadian rhythms are linked to the following day in darkness with differ- Abbreviations: C, capacitance; D, diode; the light–dark cycle. Many of the circadian ent timing and voltages. Experimental R, resistance; U0, the initial voltage rhythmic responses to day and night setup is shown in Figure 1. of a capacitor continue in constant light or dark, at least The electrical discharge of 10 °F capaci- for a period of time.1,2 The circadian clock tor between two Ag/AgCl electrodes Submitted: 11/17/11 is an endogenous oscillator with a period in the leaf of C. miniata parallel to the Accepted: 11/17/11 of approximately 24 h; its rhythm is linked conductive bundles was studied. The dif- – http://dx.doi.org/10.4161/psb.18798 to the light dark cycle. The circadian ference between the two experiments is clock in plants is sensitive to light, which the polarity of the electrodes: the positive *Correspondence to: Alexander G. Volkov; Email: [email protected] resets the phase of the rhythm. Molecular pole is closer to the base of a leaf and the mechanism underlying circadian clock positive pole is closer to the apex. This Addendum to: Volkov AG, Wooten JD, Waite AJ, function is poorly understood, although presentation immediately shows if the Brown CR, Markin VS. Circadian rhythms in it is now widely accepted for both plants resistance of the leaf remains constant in electrical circuits of Clivia miniata. J Plant Physiol and animals that it is based on circadian time and how it varies with applied 2011; 168:1753–60; PMID:21546115; http://dx.doi. oscillators. The circadian clock was dis- voltage. One can see that with +/− position org/10.1016/j.jplph.2011.03.012 covered in 1729 by De Mairan3 in his of electrodes (“+” to the base and “−” to 282 Plant Signaling & Behavior Volume 7 Issue 2 ARTICLE ADDENDUM significantly slower. This means that leaf resistance strongly increases during the night time. The biological clock in the Clivia recognizes the daytime, even in darkness. The discharge during the following day and in darkness is very similar to the first day of the experiment. Input resistance in the initial moment of the capacitor discharge was the same as during the day light. During the third day when the lights are on, the results are the same as shown in the first experiment done in the daylight. There is a difference in kinetics of 10°F capacitor discharge during daytime depending on the polarity of electrodes. This difference is small at low applied voltage of 0.25 V and increases with the increase in the initial voltage of a capacitor. Figure 1. Experimental setup. There is a slight difference in kinetics of 10°F capacitor discharge during nighttime the apex), the traces are actually slightly gated channel, we reproduced experi- depending on polarity of electrodes. There curved lines and slope varies with initial mental dependencies of the capacitor is a difference in kinetics of 10°F capacitor 7 voltage U0. From here we calculated input discharge in plant tissue. Figure 2A shows discharge during daytime in darkness. The resistance. In both cases there© is2012 a a passive Landes RC equivalent electrical Bioscience. scheme, amplitude of variation is similar to the deviation in logarithmic coordinates from which is not sensitive to a polarity of same in the first day. In all three examples, the linear predictions in equation. The applied voltage. Figure 2B shows a simple kinetics of a capacitor discharge depends deviation is rather small with +/− polarity, Doactive circuit,not which distribute. is sensitive to polarity on polarity of electrodes in a leaf of but very pronounced with −/+ electrodes. of applied voltage. We model voltage gated C. miniata due to electrical anisotropy of This means that the conductance between ion channels by rectifying diodes, which the leaf. We were also able to illustrate the two electrodes cannot be presented by a have voltammetric characteristics similar to plant memory of a “sunset.” Normally, single constant resistance. Similar rectifica- current-voltage dependencies of voltage- the lights were switched off at 5:00 p.m., tion effects were found in Aloe vera, the gated ion channels. however in this experiment they were not Venus flytrap and the Mimosa pudica. The same electrical discharge was dis- switched off at that time. Any time from While using a silicon rectifier Schotky played in darkness during the nighttime. the morning and during a day until diode NTE583, as a model of a voltage The kinetics of the night discharge is 4:00 p.m., the time dependencies of a 10°F capacitor discharge coincide. At 5:00 p.m. resistance in leaves starts to increase and at 7:00 p.m. it reaches the same parameters as at night even at continuous light. The capacitor discharge is fast during a daytime, but speed of the capacitor discharge decreases after 4:00 p.m. even under continuous light and reaches minimal value at 7:00 p.m. as in the dark during nighttime. Circadian oscillators are components of the biological clocks that regulate the activities of plants in relation to environ- mental cycles and provide an internal temporal framework. Darwin8 found that leaves in Clivia move periodically: “A Figure 2. Electrical equivalent schemes of a capacitor discharge in plant tissue. Abbreviations: C1, long glass filament was fixed to a leaf, charged capacitor from voltage source U0;C2, capacitance; R , resistance; D1 and D2 are diodes as and the angle formed by it with the models of voltage gated ion channels. horizon was measured occasionally during www.landesbioscience.com Plant Signaling & Behavior 283 three successive days. It fell each morning of voltage gated channels. These results that the internal clock does change until between 3:00 and 4:00 p.m., and are very impressive: the biological clock electrical conductance, but alone, without rose at night. The smallest angle at any in C. miniata recognizes the approach- environmental clues (light), it cannot time above the horizon was 48°, and the ing of darkness after 4:00 p.m. even ideally generate the same values of day largest 50°; so that it rose only 2° at night; under constant light from 6.00 a.m. to and night conductance. The plant needs but as this was observed each day, and as 6.00 p.m. The circadian rhythm can be additional environmental information, similar observations were nightly made related to the difference in the membrane and then the properties of electrical on another leaf of a distinct plant, there potentials during the day and night circuits will be restored to the same can be no doubt that the leaves move time, which was found in pulvini of conditions. These results demonstrate that periodically. The position of the apex different plants.5,6,9 the circadian clock can be maintained when it stood highest was 0.8 of an While in darkness the following day, the endogenously, probably involving electro- inch above its lowest point.” The peri- plant remembers the time and the rate of chemical oscillators, which can activate odical movement of leaves in Clivia has discharge drastically increases approaching or deactivate ion channels in biologically the electrophysiological component. Two the rate of the first day. However, the closed electrochemical circuits.
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