Physiology
Electrotonic and action potentials in the Venus flytrap

https://doi.org/10.1016/j.jplph.2013.01.009Get rights and content

Abstract

The electrical phenomena and morphing structures in the Venus flytrap have attracted researchers since the nineteenth century. We have observed that mechanical stimulation of trigger hairs on the lobes of the Venus flytrap induces electrotonic potentials in the lower leaf. Electrostimulation of electrical circuits in the Venus flytrap can induce electrotonic potentials propagating along the upper and lower leaves. The instantaneous increase or decrease in voltage of stimulating potential generates a nonlinear electrical response in plant tissues. Any electrostimulation that is not instantaneous, such as sinusoidal or triangular functions, results in linear responses in the form of small electrotonic potentials. The amplitude and sign of electrotonic potentials depend on the polarity and the amplitude of the applied voltage. Electrical stimulation of the lower leaf induces electrical signals, which resemble action potentials, in the trap between the lobes and the midrib. The trap closes if the stimulating voltage is above the threshold level of 4.4 V. Electrical responses in the Venus flytrap were analyzed and reproduced in the discrete electrical circuit. The information gained from this study can be used to elucidate the coupling of intracellular and intercellular communications in the form of electrical signals within plants.

Introduction

Bioelectrical circuits (Nordenstrom, 1983) operate over large distances in biological tissues. The activation of electrical circuits in biological tissues can lead to various physiological and biochemical responses. The cells of many biological organs generate electrical potentials that can result in the flow of electric currents (Volkov et al., 1998). Electrical impulses, as a result of stimulation, can propagate to adjacent excitable cells. The change in transmembrane potential can create a wave of depolarization, which affects the adjoining resting membranes. While the plasma membrane is stimulated at any point, the action potential can propagate over the entire length of the cell membrane and along the conductive bundles of tissue with constant amplitude, duration, and speed (Volkov, 2006, Volkov, 2012a, Volkov, 2012b). Characteristic length of action potentials is defined as the propagation speed multiplied by the duration of the action potential. To detect the real action potentials, the distance between electrodes should exceed the characteristic length of an action potential. Graded and electrotonic potentials propagate with decreasing amplitude. A graded potential is a wave of electrical excitation that corresponds to the size of the stimulus. Electrical signals can propagate along the plasma membrane on short distances in plasmodesmata, and on long distances in conductive bundles. Action potentials in higher plants hold promise as the information carriers in intracellular and intercellular communication during environmental changes.

Touching trigger hairs protruding from the upper epidermal layer of the Venus flytrap's leaves activates mechanosensitive ion channels. As a result, receptor potentials are generated which in turn induce a propagating action potential throughout the upper leaf of the Venus flytrap (Benolken and Jacobson, 1970, Burdon-Sanderson, 1873, Burdon-Sanderson, 1874, Burdon-Sanderson, 1882, Escalante-Pérez et al., 2011, Jacobson, 1965, Volkov et al., 2008a). A receptor potential always precedes an action potential and couples the mechanical stimulation step to the action potential step of the preying sequence (Jacobson, 1965). A possible pathway of action potential propagation from lobes to the midrib includes vascular bundles and plasmodesmata in the upper leaf (Buchen et al., 1983, Ksenzhek and Volkov, 1998). Action potentials in the Venus flytrap do not propagate from the upper leaf, or the trap, to lower leaf of the Venus flytrap (Hodick and Sievers, 1986, Sibaoka, 1966, Volkov et al., 2007).

The main goal of this work is to detect propagation and interaction of electrotonic and action potentials in the Venus flytrap.

Section snippets

Plants

The Dionaea muscipula Ellis (Venus flytrap) were purchased from Fly-Trap Farm Supply (North Carolina, USA) and grown in well drained peat moss in plastic pots at 22 °C with 12:12 h light: dark photoperiod. The humidity averaged 45–50%. Irradiance was 700–800 μmol photons/m2/s. The soil was treated with distilled water. All experiments were performed on healthy adult specimens from the one hundred bulbs purchased.

Data acquisition

All measurements were conducted in the laboratory at constant room temperature of 22°С

Mechanical stimulation

Mechanical stimulation of a trigger hair in the trap induces action potential propagating between the trigger hairs in a lobe and the midrib (Hodick and Sievers, 1986, Sibaoka, 1966, Volkov et al., 2007). Action potentials do not penetrate to the lower leaf, but we did find small electrical potentials in the lower leaf of the Venus flytrap, which look similar to graded potentials or electrotonic potentials (Volkov et al., 2007, Volkov et al., 2008a). To understand the nature of these electrical

Discussion

The Venus flytrap can be closed by mechanical stimulation of trigger hairs using a cotton thread or wooden stick by gently touching two of the six trigger hairs inside the upper leaf of the Venus flytrap. The Venus flytrap can also be closed by an electrical pulse with amplitude of 1.5 V between the midrib and the lobe of the upper leaf without mechanical stimulation. The closing was achieved by electrical stimulation with a positive electrode connected to the midrib and a negative electrode

Acknowledgements

This article is based upon work supported in part by the National Science Foundation under Grant No. CBET-1064160 and in part by the U. S. Army Research Office under contract Grant No. W911NF-11-1-0132.

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