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Contents lists available at ScienceDirect
Bioelectrochemistry
j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / b i o e l e c h e m
Electrical memory in Venus flytrap
Alexander G. Volkov a,⁎, Holly Carrell a, Andrew Baldwin a, Vladislav S. Markin b
a
b
Department of Chemistry and Biochemistry, Oakwood University, Huntsville, AL 35896, USA
Department of Neurology, University of Texas, Southwestern Medical Center, Dallas, TX 75390-9068, USA
a r t i c l e
i n f o
Article history:
Received 5 October 2008
Received in revised form 5 March 2009
Accepted 8 March 2009
Available online xxxx
Keywords:
Plant memory
Bioelectrochemistry
Electrophysiology
Electrical signaling
Venus flytrap
Dionaea muscipula Ellis
a b s t r a c t
Electrical signaling, memory and rapid closure of the carnivorous plant Dionaea muscipula Ellis (Venus
flytrap) have been attracting the attention of researchers since the XIX century. The electrical stimulus
between a midrib and a lobe closes the Venus flytrap upper leaf in 0.3 s without mechanical stimulation of
trigger hairs. Here we developed a new method for direct measurements of the exact electrical charge
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
between a lobe and midrib from the external capacitor, the trap starts to close at room temperature. At
temperatures 28–36 °C a smaller electrical charge of 4.1 µC is required to close the trap of the D. muscipula.
The cumulative character of electrical stimuli points to the existence of short-term electrical memory in the
Venus flytrap. We also found sensory memory in the Venus flytrap. When one sustained mechanical stimulus
was applied to only one trigger hair, the trap closed in a few seconds.
© 2009 Elsevier B.V. All rights reserved.
1. Introduction
Electrical signaling and memory play fundamental roles in plant
responses [1–8]. Examples of memory and learning have been observed in plants, including: storage and recall functions in seedlings
[9], chromatin remodelling in plant development [10,11], transgeneration memory of stress [12–14], immunological memory of tobacco
plants [15–16] and mountain birches [17], vernalization and epigenetic memory of winter [18–20], induced resistance and susceptibility
to herbivores [21], memory response in ABA-entrained plants [13],
phototropically and gravitotropically induced memory in maize
[22,23], ozone sensitivity of grapevine as a memory effect in a
perennial crop plant [24], memory of stimulus [3,4,25,26], systematic
acquired resistance in plants exposed to a pathogen [16], and electrical
memory in the Venus flytrap [3,4].
Rapid closure of the carnivorous plant Dionaea muscipula Ellis
(Venus flytrap) has been attracting the attention of researchers and as
a result its mechanism has been widely investigated [3,4,27–37].
When an insect touches the trigger hairs (Fig. 1), these mechanosensors trigger a receptor potential [38], which generate an electrical
signal that acts as an action potential. Two stimuli generate two action
potentials, which activate the trap closing at room temperature in a
fraction of a second [27]. At high temperatures of 28–36 °C, only one
mechanical stimulus is required for the trap closing [28,39–40].
Propagation of action potentials and the trap closing can be blocked by
⁎ Corresponding author. Tel./fax: +1 256 726 7113.
E-mail address: [email protected] (A.G. Volkov).
inhibitors of voltage gated channels [3,4,27,41]. The two mechanical
stimuli required for the trap closing should be applied within an
interval from 0.75 s to 40 s.
The inducement of non-excitability after excitation (refractory
period) and the summation of subthreshold irritations were developed in the vegetative and animal kingdoms in protoplasmic
structures prior to morphological differentiation of nervous tissues.
These protoplasmic structures merged into the organs of a nervous
system and adjusted the interfacing of the organism with the
environment. Some neuromotoric components include acetylcholine
neurotransmitters, cellular messenger calmodulin, cellular motors
actin and myosin, voltage-gated channels, and sensors for touch, light,
gravity and temperature [1,2,42]. Although this nerve-like cellular
equipment has not reached the same level of great complexity as in
animal nerves, a simple neural network has been formed within the
plasma membrane of a phloem or plasmodesmata enabling it to
communicate efficiently over long distances [1,2,5–7,43,44]. The
reason why plants have developed pathways for electrical signal
transmission most probably lies in the necessity to respond rapidly to
environmental stress factors [2,45,46]. Different environmental
stimuli evoke specific responses in living cells, which have the capacity to transmit a signal to the responding region. In contrast to
chemical signals such as hormones, electrical signals are able to
transmit information rapidly over long distances. Electrical potentials
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
potential) and the lobe (negative potential) causes Venus flytrap to
close the trap without any mechanical stimulation [27]. The average
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Fig. 1. Location of Ag/AgCl electrodes in the Dionaea muscipula. The three trigger hairs
in each lobe are seen.
stimulation pulse voltage sufficient for rapid closure of the Venus
flytrap was 1.5 V (standard deviation is 0.01 V, n = 50) for 1 s. The
inverted polarity pulse with negative voltage applied to the midrib did
not close the plant [27]. Applying impulses in the same voltage range
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
ATP hydrolysis [48]. ATP is used for a fast transport of protons. The
amount of ATP drops from 950 µM per midrib before mechanical
stimulation to 650 µM per midrib after stimulation and closure [48].
However, it is not clear if electrical stimulation triggers the closing
process, or contributes energy to the closing action.
The action potential delivers the electrical signal to the midrib,
which can activate the trap closing. To check this hypothesis, we
measured the effects of transmitted electrical charge from the charged
capacitors between the lobe and the midrib of Venus flytrap.
Application of a single electrical charge initially stored on the
capacitor when it is connected to the electrodes inserted in the trap
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 propagating 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
and a lobe, even when the injected charge was increased from 14 µC to
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
Venus flytrap and analyzed the exact amount of submitted electrical
charge accumulated in the trap.
2. Materials and methods
2.1. Images
Digital video recorders Sony DCR-HC36 and Canon ZR300 were
used to monitor the Venus flytraps and to collect digital images, which
were analyzed frame by frame.
2.2. Electrodes
All measurements were conducted in the laboratory at a 21 °C and
some experiments at 30 °C inside a Faraday cage mounted on a
vibration-stabilized table. Ag/AgCl electrodes were prepared from
Teflon coated silver wires. Following insertion of the electrodes into
Fig. 2. Experimental setup.
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lobes and a midrib, the traps closed. We allowed plants to rest until
the traps were completely open.
2.3. Data acquisition
NI-PXI-4071 digital multimeter, NI-PXI-5124 oscilloscope (National
Instruments), data acquisition boards NI-PXI-6115 or NI-PCI-6115
(National Instruments) interfaced through a NI SCB-68 shielded
connector block to 0.1 mm thick nonpolarizable reversible Ag/AgCl
electrodes were used to record the digital data (Fig. 2). The results
were reproduced on a workstation with data acquisition board NI
6052E DAQ with input impedance of 100 GΩ interfaced through a NI
SC-2040 Simultaneous Sample and Hold. The system integrates
standard low-pass anti-aliasing filters at one half of the sampling
frequency. Measuring signals were recorded as ASCII files using LabView (National Instruments) software with low pass filters. The NI-PXI4071 high-resolution digital multimeter delivers fast voltage measurements from 10 nV to 1000 V, current measurements from 1 pA to 3 A,
and resistance measurements from 10 µΩ to 5 GΩ.
2.4. Plant electrostimulation
The Charge-Injection Method [3] has been used to precisely estimate
the amount of electrical energy necessary to cause trap closure. A double
pole, double throw (DPDT) switch was used to connect the known
capacitor to the 1.5 V battery during charging, and then to the plant
during plant stimulation. Since the charge of capacitor Q connected to
the voltage source U is Q =CU, we can precisely regulate the amount of
charge using different capacitors and applying various voltages. By
changing switch position, we can instantaneously connect the charged
capacitor to the plant and induce an evoked response. We used different
capacitors with a capacitance ranging from 1.0 to 9.4 µF.
3
2.5. Continuous single-touch stimulus
Using a small wooden probe, one trigger hair was gently held down
until the trap closed. The wooden probe was removed just before the
leaves closed.
2.6. Plants
Three hundred bulbs of D. muscipula (Venus flytrap) were purchased for this experimental work from Fly-Trap Farm (Supply, North
Carolina) and grown in well drained peat moss in plastic pots at 21 °C
with a 12:12 h light:dark photoperiod. The peat moss was treated with
distilled water. Humidity averaged 45–50%. Irradiance was 77 µE/m2 s.
All experiments were performed on healthy adult specimens.
3. Results
Touching of one sensitive hair twice or two different hairs with an
interval up to 40 s induces the trap closing. We found that one
sustained mechanical stimulus applied to only one trigger hair can
close the trap of D. muscipula in a few seconds (Fig. 3). Prolonged
pressing of the trigger hair generates two electrical signals similar
to action potentials reported in reference [27] within an interval
of about 2 s, which stimulate the trap closing. The Venus flytrap can
capture insects by any of these three ways of mechanical stimulation
of trigger hairs. Insects can touch a few trigger hairs for just 1 or 2 s. In
biology, this effect is referred to as molecular or sensory memory. It
was shown that sustained membrane depolarization induced a
“molecular” memory phenomenon and has profound implication on
the biophysical properties of voltage-gated ion channels [49].
Figs. 4 and 5 illustrate the short term memory in the Venus flytrap.
Recently we found that transmission of an electrical charge between
Fig. 3. Closing of the Dionaea muscipula trap by pressing of only one trigger hair at 21 °C. These results were reproduced 14 times on different Venus flytrap plants. Reproducibility of
the movement of the trap is ±33 ms.
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give the possibility of finding the exact electrical charge utilized by the
Venus flytrap to facilitate trap closing. We measured voltage between
two electrodes #1 and #2 (Fig. 1) inserted in the midrib and one of the
lobes connected to a charged capacitor (Fig. 2). Charge was estimated
as the voltage U between two Ag/AgCl electrodes multiplied by a
capacitance C of the capacitor: Q = UC. The trap closing charge was
estimated as the difference between the initial charge of a capacitor
and the final charge of a capacitor, when the trap begins to close. In the
experiments, when a few small charges were applied to close the trap,
the closing charge was estimated as the sum of all charges transmitted
from a capacitor. This shows that repeated application of smaller
charges demonstrates a summation of stimuli (Figs. 4 and 5).
We studied the capacitor discharge on small traps with a midrib
length of 1.0 cm and large traps with a midrib length of 3.5 cm. Fig. 4
shows that as soon as 8.05 µC charge (mean 8.05 µC, median 9.00 µC,
std. dev. 0.06 µC, n = 34) for small trap or 9.01 µC charge (mean
9.01 µC, median 8.00 µC, std. dev. 0.27 µC, n = 34) for large trap is
transmitted between a lobe and midrib from the capacitor, the trap
begins to close at room temperature. At temperatures of 28–36 °C a
smaller electrical charge of 4.1 µC (mean 4.1 µC, median 4.1 µC, std.
dev. 0.24 µC, n = 34) is required to close the trap of the D. muscipula
(Fig. 5). Probably, there is a phase transition at temperature between
25 °C and 28 °C and due to this reason only one mechanical stimulus
or a small electrical charge is required to close the trap.
Line 1 on Fig. 6a and b shows electrical discharge in the D.
muscipula trap at 30 °C between electrodes inserted in a lobe and
midrib and connected to a charged capacitor. Two other Ag/AgCl
Fig. 4. Closing of the Dionaea muscipula trap at 21 °C by electrical charge Q injected
between a lobe and a midrib: (a) small trap with the midrib length of 1.0 cm and
(b) large trap with the midrib length of 3.5 cm. Electrical discharge was measured using
NI-PXI-4071 digital multimeter.
electrodes #1 and #2 (Fig. 1) in a lobe and the midrib causes closure of
the trap [3,27]. If we apply two or more injections of electrical charges
within a period of less than 40 s, the Venus flytrap upper leaf closes as
soon as a 14 µC charge is applied. The capacitor slowly discharges with
time, so although a 14 µC charge was applied, not all of this charge was
accumulated during 20–40 s to assist in closing the trap. It is important
to measure the exact amount of electrical charge used by the Venus
flytrap to close. Figs. 4 and 5 show a new series of experiments, which
Fig. 5. Closing of the Dionaea muscipula trap at 30 °C by electrical charge Q injected
between a lobe and a midrib. The length of the midrib was 3.5 cm. Electrical discharge
was measured using NI-PXI-4071 digital multimeter. These results were reproduced 16
times on different Venus flytrap plants.
Fig. 6. Electrical discharge in the Dionaea muscipula trap at 30 °C between electrodes
located in a lobe and a midrib connected to charged capacitor and NI-PXI-4071 digital
multimeter (1) or between electrodes located in another lobe and a midrib connected
to NI-PXI-6115 data acquisition system (2). Panels (a) and (b) show both curves but at
different time scales. The length of the midrib was 3.5 cm. These results were
reproduced 16 times on different Venus flytrap plants.
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electrodes were located in another lobe and midrib, and connected to
a data acquisition system. Electrical discharge at two electrodes
connected to the capacitor takes place within many seconds (Fig. 6,
line 1), but also induces a fast electrical signal between another lobe
and midrib, which completely disappears in 70 ms (Fig. 6, line 2). It
merely demonstrates that injecting charge into one leaf elicits also a
short electrical signal in another leaf. The upper leaf of the Venus
flytrap has very dense network of plasmodesmata and vascular
bundles with highly conductive plasma membrane.
4. Discussion
4.1. Plant memory
The general classification of memory in plants is based on the
duration of memory retention, and identifies three distinct types of
memory: sensory memory, short term memory and long term memory.
Sensory memory corresponds approximately to the initial 0.2–3.0 s after
an item is perceived. Some information in sensory memory can be
transferred then to short-term memory. Short-term memory allows one
to recall something from several second to as long as a minute without
rehearsal. The storage in sensory memory and short-term memory
generally has a strictly limited capacity and duration, which means
information is available for a certain period of time, but is not retained
indefinitely. Long-term memory can store much larger quantities of
information for potentially unlimited duration up to a whole life span of
the plant. The Venus flytrap can accumulate small subthreshold charges,
and when the threshold value is reached, the trap closes. The cumulative
character of electrical stimuli points to the existence of short-term
electrical memory in the Venus flytrap.
Fig. 8. Scheme of a trap closure.
4.2. Biologically closed electrical circuits
If a capacitor of capacitance C is discharged through a parallel
resistor R, the dependence of the capacitor voltage Uc on time is
t
;
UC ðt Þ = U0 × exp −
τ
ð1Þ
where
τ ¼ RC
ð2Þ
and U0 is initial voltage. The circuit time constant τ governs the
discharging process. With increasing capacitance, the time of the
capacitor discharge increases according to Eqs. (1) and (2).
Fig. 7. Dependence of voltage on a capacitor (2 µF in experiments at 30 °C and 4.7 µF at
21 °C) during discharge in the Dionaea muscipula on time. Small traps were used with
the midrib length of 1.0 cm and large trap were with the midrib length of 3.5 cm. These
results were reproduced 16 times on different Venus flytrap plants.
Fig. 7 shows that the experimental time dependencies at different
temperatures look like they are predicted by Eq. (1) for t b τ/2, but
deviate increasingly from Eq. (1) for t N τ/2, because the equivalent
electrical circuit of the Venus flytrap is more complicated than just a
resistor. The capacitive time constant τ depends on the size of the trap
and decreases with increasing trap size.
The trap can be closed by applying a voltage (or action potentials)
or by electrical charge. Probably, both ways of electrostimulation
activated the ion pump in the midrib.
4.3. Chain of events in the trap closing
Fig. 8 shows schematically the possible mechanism of a trap
closure. When a mechanical stimuli is received by the trigger hairs in
an open trap, a receptor potential is generated [35,36]. After the
receptor potential, action potentials are generated, which are
propagated to the midrib of the plant through the plasmodesmata
[27]. Action potential can be inhibited by uncouplers and blockers of
fast anion and potassium channels [3,27,33,34]. The Venus flytrap
memorizes first electrical signal for short period of time and as soon as
second action potential propagates to the midrib in 1 to 40 s, electrical
signals activate the ATP hydrolysis [48], starting fast proton transport
[50,51] and initiating aquaporin opening [41]. Fast proton transport
induces transport of water and a change in turgor [41]. It is common
knowledge that the leaves of the Venus flytrap actively employ turgor
pressure and hydrodynamic flow for fast movement and catching
insects. In these processes the upper and lower surfaces of the leaf
behave quite differently. During the trap closing, the loss of turgor by
parenchyma lying beneath the upper epidermis, accompanied by the
active expansion of the tissues of the lower layers of parenchyma near
the under epidermis, closes the trap. The cells on the inner face of the
trap jettison their cargo of water, shrink, and allow the trap lobe to
fold over. The cells of the lower epidermis expand rapidly, folding the
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trap lobe over. The minimum elastic energy of the leaf, including mean
and Gaussian curvature, corresponds to the closed state. These anatomical features constitute the basis of the new hydroelastic curvature
model [37].
References
[1] A.G. Volkov (Ed.), Plant Electrophysiology, Springer-Verlag, Berlin, 2006.
[2] A.G. Volkov, Electrophysiology and phototropism, in: F. Balushka, S. Manusco, D.
Volkman (Eds.), Communication in Plants. Neuronal Aspects of Plant Life, SpringerVerlag, Berlin, 2006, pp. 351–367.
[3] A.G. Volkov, T. Adesina, V.S. Markin, E. Jovanov, Kinetics and mechanism of Dionaea
muscipula trap closing, Plant Physiol. 146 (2008) 694–702.
[4] A.G. Volkov, H. Carrell, T. Adesina, V.S. Markin, E. Jovanov, Plant electrical memory,
Plant Signal. Behav. 3 (2008) 490–492.
[5] P.W. Barlow, Reflections on “plant neurobiology”, Biosystems 92 (2008) 132–147.
[6] F. Baluška, S. Mancuso, D. Volkman (Eds.), Communication in Plants. Neuronal
Aspects of Plant Life, Springer Verlag, Berlin, 2006.
[7] A. Trewavas, Aspects of plant intelligence, Ann. Bot. 92 (2003) 1–20.
[8] J. Demongeot, R. Thomas, M. Thellier, A mathematical model for storage and recall
functions in plants, C. R. Acad. Sci. 323 (2000) 93–97.
[9] M. Thellier, L.L. Sceller, V. Norris, M.C. Verdus, C. Ripoll, Long-distance transport,
storage and recall of morphogenetic information in plants. The existence of a sort
of primitive plant “memory”, C.R. Acad. Sci. Paris 323 (2000) 81–91.
[10] J. Goodrich, S. Tweedie, Remembrance of things past: chromatin remodeling in
plant development, Ann. Rev. Cell Dev. Biol. 18 (2002) 707–746.
[11] J.C. Reyes, L. Hennig, W. Gruissem, Chromatin-remodeling and memory factors.
New regulators of plant development, Plant Physiol. 130 (2002) 1090–1101.
[12] T.J.A. Bruce, M.C. Matthes, J. Napier, J.A. Pickett, Stressful “memories” of plants:
evidence and possible mechanisms, Plant Sci. 173 (2007) 603–608.
[13] C.H. Goh, H.G. Nam, Y.S. Park, Stress memory in plants: a negative regulation of
stomatal response and transient induction of rd22 gene to light in abscisic acidentrained Arabidopsis plants, Plant J. 36 (2003) 240–255.
[14] J. Molinier, G. Ries, C. Zipfel, B. Hohn, Transgeneration memory of stress in plants,
Nature 442 (2006) 1046–1049.
[15] I.T. Baldwin, E.A. Schmelz, Immunological “memory” in the induced accumulation
of nicotine in wild tobacco, Ecology 77 (1996) 236–246.
[16] U. Conrath, Systemic acquired resistance, Plant Signal Behav 1 (2006) 179–184.
[17] T. Ruuhola, J.P. Salminen, S. Haviola, S. Yang, M.J. Rantala, Immunological memory
of mountain birches: effects of phenolics on performance of the autumnal moth
depend on herbivory history of trees, J. Chem. Ecology 33 (2007) 1160–1176.
[18] R. Amasino, Vernalization, competence, and the epigenic memory of winter, Plant
Cell 16 (2004) 2553–2559.
[19] S. Sung, R.M. Amasino, Molecular genetic study of the memory of winter, J. Exper.
Bot. 57 (2006) 3369–3377.
[20] S. Sung, R.M. Amasino, Vernalisation and epigenetics: how plants remember
winter, Curr. Opin. Plant Biol. 7 (2004) 4–10.
[21] R. Karban, C. Niiho, Induced resistance and susceptibility to herbivory: plant
memory and altered plant development, Ecology 76 (1995) 1220–1225.
[22] P. Nick, K. Sailer, E. Schafer, On the relation between photo- and gravitropically
induced spatial memory in maize coleoptiles, Planta 181 (1990) 385–392.
[23] P. Nick, E. Schafer, Spatial memory during the tropism of maize (Zea mays L.)
coleoptiles, Planta 175 (1988) 380–388.
[24] G. Soja, M. Eid, H. Gangl, H. Redl, Ozone sensitivity of grapevine (Vitis vinifera L.):
evidence for a memory effect in a perennial crop plant? Phyton Ann. Rev. Bot. 37
(1997) 265–270.
[25] M. Ueda, Y. Nakamura, M. Okada, Endogeneous factors involved in the regulation
of movement and “memory” in plants, Pure Appl. Chem. 79 (2007) 519–527.
[26] M. Ueda, Y. Nakamura, Metabolites involved in plant movement and “memory”:
nyctinasy of legumes and trap movement in the Venus flytrap, Nat. Prod. Rep. 23
(2006) 548–557.
[27] A.G. Volkov, T. Adesina, E. Jovanov, Closing of Venus flytrap by electrical
stimulation of motor cells, Plant Signal Behav. 2 (2007) 139–144.
[28] W.H. Brown, The mechanism of movement and the duration of the effect of
stimulation in the leaves of Dionaea, Am. J. Bot. 3 (1916) 68–90.
[29] J. Burdon-Sanderson, Venus fly-trap (Dionaea muscipula), Nature 10 (1874) 105–107;
127–128.
[30] J. Burdon-Sanderson, On the electromotive properties of the leaf of Dionaea in the
excited and unexcited states, Philos. Trans. R. Soc. Lond. 173 (1882) 1–55.
[31] J. Burdon-Sanderson, Note on the electrical phenomena which accompany
stimulation of the leaf of Dionaea muscipula Ellis, Philos. Proc. R. Soc. Lond. 21
(1873) 495–496.
[32] C. Darwin, Insectivorous Plants, Murray, London, 1875.
[33] D. Hodick, A. Sievers, The action potential of Dionaea muscipula Ellis, Planta 174
(1988) 8–18.
[34] D. Hodick, A. Sievers, On the mechanism of trap closure of Venus flytrap (Dionaea
muscipula Ellis), Planta 179 (1989) 32–42.
[35] S.L. Jacobson, Receptor response in Venus's flytrap, J. Gen. Physiol. 49 (1965)
117–129.
[36] S.L. Jacobson, The effect of ionic environment on the response of the sensory hair
of Venus's flytrap, Can. J. Bot. 52 (1974) 1293–1302.
[37] V.S. Markin, A.G. Volkov, E. Jovanov, Active movements in plants: mechanism of
trap closure by Dionaea muscipula Ellis, Plant Signal Behav. 3 (2008) 778–783.
[38] R.M. Benolken, S.L. Jacobson, Response properties of a sensory hair excised from
Venus's flytrap, J. Gen. Physiol. 56 (1970) 64–82.
[39] W.H. Brown, L.W. Sharp, The closing response in Dionaea, Bot. Gaz. 49 (1910)
290–302.
[40] F.E. Lloyd, The Carnivorous Plants, Ronald Press, New York, 1942.
[41] A.G. Volkov, K.J. Coopwood, V.S. Markin, Inhibition of the Dionaea muscipula Ellis
trap closure by ion and water channels blockers and uncouplers, Plant Sci. 175
(2008) 642–649.
[42] V.V. Roshchina, Neurotransmitters in Plant Life, Science Publ., Enfield, 2001.
[43] A.G. Volkov, C.L. Brown, Electrochemistry of plant life, in: A.G. Volkov (Ed.), Plant
Electrophysiology—Theory & Methods, Springer, Berlin, 2006, pp. 437–459.
[44] A.G. Volkov, J. Mwesigwa, A. Labady, S. Kelly, D'J. Thomas, K. Lewis, T. Shvetsova,
Soybean electrophysiology: effects of acid rain, Plant Sci. 162 (2002) 723–731.
[45] A.G. Volkov, Green plants: electrochemical interfaces, J. Electroanal. Chem. 483
(2000) 150–156.
[46] A.G. Volkov, R.A. Haack, Insect induces bioelectrochemical signals in potato plants,
Bioelectrochem. Bioenerg. 35 (1995) 55–60.
[47] O.S. Ksenzhek, A.G. Volkov, Plant Energetics, Academic Press, San Diego, 1998.
[48] M.J. Jaffe, The role of ATP in mechanically stimulated rapid closure of the Venus's
flytrap, Plant Physiol. 51 (1973) 17–18.
[49] T.K. Nayak, S.K. Sikdar, Time-dependent molecular memory in single voltage-gated
sodium channel, J. Membr. Biol. 219 (2007) 19–36.
[50] P.A. Rea, The dynamics of H+ efflux from the trap lobes of Dionaea muscipula Ellis
(Venus's flytrap), Plant Cell Environ. 6 (1983) 125–134.
[51] S.E. Williams, A.B. Bennet, Leaf closure in the Venus flytrap: an acid growth
response, Science 218 (1982) 1120–1121.
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