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Electrical Memory in Venus Flytrap ARTICLE IN PRESS BIOJEC-06329; No of Pages 6 Bioelectrochemistry xxx (2009) xxx–xxx Contents lists available at ScienceDirect Bioelectrochemistry journal homepage: www.elsevier.com/locate/bioelechem Electrical memory in Venus flytrap Alexander G. Volkov a,⁎, Holly Carrell a, Andrew Baldwin a, Vladislav S. Markin b a Department of Chemistry and Biochemistry, Oakwood University, Huntsville, AL 35896, USA b Department of Neurology, University of Texas, Southwestern Medical Center, Dallas, TX 75390-9068, USA article info abstract Article history: Electrical signaling, memory and rapid closure of the carnivorous plant Dionaea muscipula Ellis (Venus Received 5 October 2008 flytrap) have been attracting the attention of researchers since the XIX century. The electrical stimulus Received in revised form 5 March 2009 between a midrib and a lobe closes the Venus flytrap upper leaf in 0.3 s without mechanical stimulation of Accepted 8 March 2009 trigger hairs. Here we developed a new method for direct measurements of the exact electrical charge Available online xxxx utilized by the D. muscipula Ellis to facilitate the trap closing and investigated electrical short memory in the Venus flytrap. As soon as the 8 µC charge for a small trap or a 9 µC charge for a large trap is transmitted Keywords: Plant memory between a lobe and midrib from the external capacitor, the trap starts to close at room temperature. At Bioelectrochemistry temperatures 28–36 °C a smaller electrical charge of 4.1 µC is required to close the trap of the D. muscipula. Electrophysiology The cumulative character of electrical stimuli points to the existence of short-term electrical memory in the Electrical signaling Venus flytrap. We also found sensory memory in the Venus flytrap. When one sustained mechanical stimulus Venus flytrap was applied to only one trigger hair, the trap closed in a few seconds. Dionaea muscipula Ellis © 2009 Elsevier B.V. All rights reserved. 1. Introduction inhibitors of voltage gated channels [3,4,27,41]. The two mechanical stimuli required for the trap closing should be applied within an Electrical signaling and memory play fundamental roles in plant interval from 0.75 s to 40 s. responses [1–8]. Examples of memory and learning have been ob- The inducement of non-excitability after excitation (refractory served in plants, including: storage and recall functions in seedlings period) and the summation of subthreshold irritations were devel- [9], chromatin remodelling in plant development [10,11], transgenera- oped in the vegetative and animal kingdoms in protoplasmic tion memory of stress [12–14], immunological memory of tobacco structures prior to morphological differentiation of nervous tissues. plants [15–16] and mountain birches [17], vernalization and epige- These protoplasmic structures merged into the organs of a nervous netic memory of winter [18–20], induced resistance and susceptibility system and adjusted the interfacing of the organism with the to herbivores [21], memory response in ABA-entrained plants [13], environment. Some neuromotoric components include acetylcholine phototropically and gravitotropically induced memory in maize neurotransmitters, cellular messenger calmodulin, cellular motors [22,23], ozone sensitivity of grapevine as a memory effect in a actin and myosin, voltage-gated channels, and sensors for touch, light, perennial crop plant [24], memory of stimulus [3,4,25,26], systematic gravity and temperature [1,2,42]. Although this nerve-like cellular acquired resistance in plants exposed to a pathogen [16], and electrical equipment has not reached the same level of great complexity as in memory in the Venus flytrap [3,4]. animal nerves, a simple neural network has been formed within the Rapid closure of the carnivorous plant Dionaea muscipula Ellis plasma membrane of a phloem or plasmodesmata enabling it to (Venus flytrap) has been attracting the attention of researchers and as communicate ef ficiently over long distances [1,2,5–7,43,44].The a result its mechanism has been widely investigated [3,4,27–37]. reason why plants have developed pathways for electrical signal When an insect touches the trigger hairs (Fig. 1), these mechan- transmission most probably lies in the necessity to respond rapidly to osensors trigger a receptor potential [38], which generate an electrical environmental stress factors [2,45,46]. Different environmental signal that acts as an action potential. Two stimuli generate two action stimuli evoke specific responses in living cells, which have the capa- potentials, which activate the trap closing at room temperature in a city to transmit a signal to the responding region. In contrast to fraction of a second [27]. At high temperatures of 28–36 °C, only one chemical signals such as hormones, electrical signals are able to mechanical stimulus is required for the trap closing [28,39–40]. transmit information rapidly over long distances. Electrical potentials Propagation of action potentials and the trap closing can be blocked by have been measured at the tissue and whole plant levels [8,43–47]. We found that Venus flytrap has a short term electrical memory [3,4]. Using our new charge injection method, it was evident that the application of an electrical stimulus between the midrib (positive fl ⁎ Corresponding author. Tel./fax: +1 256 726 7113. potential) and the lobe (negative potential) causes Venus ytrap to E-mail address: [email protected] (A.G. Volkov). close the trap without any mechanical stimulation [27]. The average 1567-5394/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.bioelechem.2009.03.005 Please cite this article as: A.G. Volkov, et al., Electrical memory in Venus flytrap, Bioelectrochemistry (2009), doi:10.1016/j.bioelechem.2009.03.005 ARTICLE IN PRESS 2 A.G. Volkov et al. / Bioelectrochemistry xxx (2009) xxx–xxx of D. muscipula (mean 13.63 µC, median 14.00 µC, std. dev. 1.51 µC, n=41) causes trap closure and induces an electrical signal propagat- ing between the lobes and the midrib [3,37]. Not all of the applied “initial” charge was accumulated during 20–40 s and new series of experiments is necessary to determine the exact electrical charge accumulated by the closing trap. The electrical signal in the lobes was not an action potential, because its amplitude depended on the applied voltage from the charged capacitor. Charge induced closing of a trap plant can be repeated 2–3 times on the same Venus flytrap plant after complete reopening of the trap. The Venus flytrap can accumulate small charges, and when the threshold value is reached, the trap closes [3,37]. A summation of stimuli is demonstrated through the repetitive application of smaller charges [3]. Previous work by Brown and Sharp [39] indicated that strong electrical shock between lower and upper leaves can cause the Venus flytrap to close, but in their article, the amplitude and polarity of applied voltage, charge, and electrical current were not reported. The trap did not close when we applied the same electrostimulation between the upper and lower leaves as we applied between a midrib Fig. 1. Location of Ag/AgCl electrodes in the Dionaea muscipula. The three trigger hairs and a lobe, even when the injected charge was increased from 14 µC to in each lobe are seen. 750 µC [3]. It is probable that the electroshock induced by Brown and Sharp [39] had a very high voltage or electrical current. In the present work we investigated electrical memory in the stimulation pulse voltage sufficient for rapid closure of the Venus Venus flytrap and analyzed the exact amount of submitted electrical flytrap was 1.5 V (standard deviation is 0.01 V, n=50) for 1 s. The charge accumulated in the trap. inverted polarity pulse with negative voltage applied to the midrib did not close the plant [27]. Applying impulses in the same voltage range 2. Materials and methods with inverted polarity did not open the trap, even with pulses of up to 100 s [3,27]. It was found that energy for trap closure is generated by 2.1. Images ATP hydrolysis [48]. ATP is used for a fast transport of protons. The amount of ATP drops from 950 µM per midrib before mechanical Digital video recorders Sony DCR-HC36 and Canon ZR300 were stimulation to 650 µM per midrib after stimulation and closure [48]. used to monitor the Venus flytraps and to collect digital images, which However, it is not clear if electrical stimulation triggers the closing were analyzed frame by frame. process, or contributes energy to the closing action. The action potential delivers the electrical signal to the midrib, 2.2. Electrodes which can activate the trap closing. To check this hypothesis, we measured the effects of transmitted electrical charge from the charged All measurements were conducted in the laboratory at a 21 °C and capacitors between the lobe and the midrib of Venus flytrap. some experiments at 30 °C inside a Faraday cage mounted on a Application of a single electrical charge initially stored on the vibration-stabilized table. Ag/AgCl electrodes were prepared from capacitor when it is connected to the electrodes inserted in the trap Teflon coated silver wires. Following insertion of the electrodes into Fig. 2. Experimental setup. Please cite this article as: A.G. Volkov, et al., Electrical memory in Venus flytrap, Bioelectrochemistry (2009), doi:10.1016/j.bioelechem.2009.03.005 ARTICLE IN PRESS A.G. Volkov et al. / Bioelectrochemistry xxx (2009) xxx–xxx 3 lobes and a midrib, the traps closed. We allowed plants to rest until 2.5. Continuous single-touch stimulus the traps were completely open. Using a small wooden probe, one trigger hair was gently held down 2.3. Data acquisition until the trap closed. The wooden probe was removed just before the leaves closed. NI-PXI-4071 digital multimeter, NI-PXI-5124 oscilloscope (National Instruments), data acquisition boards NI-PXI-6115 or NI-PCI-6115 2.6.
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