Kinetics and mechanism of Dionaea muscipula trap closing

Abstract

The Venus flytrap (Dionaea muscipula) possesses an active trapping mechanism to capture insects with one of the most rapid movements in the plant kingdom, as described by Darwin. This article presents a detailed experimental investigation of trap closure by mechanical and electrical stimuli and the mechanism of this process. Trap closure consists of three distinctive phases: a silent phase with no observable movement; an accelerated movement of the lobes; and the relaxation of the lobes in their closed state, resulting in a new equilibrium. Uncouplers and blockers of membrane channels were used to investigate the mechanisms of different phases of closing. Uncouplers increased trap closure delay and significantly decreased the speed of trap closure. Ion channel blockers and aquaporin inhibitors increased time of closing. Transmission of a single electrical charge between a lobe and the midrib causes closure of the trap and induces an electrical signal propagating between both lobes and midrib. The Venus flytrap can accumulate small subthreshold charges, and when the threshold value is reached, the trap closes. Repeated application of smaller charges demonstrates the summation of stimuli. The cumulative character of electrical stimuli points to the existence of electrical memory in the Venus flytrap. The observed fast movement can be explained by the hydroelastic curvature model without invoking buckling instability. The new hydroelastic curvature mechanism provides an accurate description of the authors' experimental data.

Figure 1.

Experimental setup. [See online article for color version of this figure.]

Figure 2.

Closing of the trap with a 14-μC electrical stimulus.

Figure 3.

Kinetics of trap closure at 20°C (1) and 36°C (2) applying a 14-μC charge injection to the midrib; y is the distance between the edges of the lobes. A, Dependencies of distances between the edges of the lobes at 20°C (1) and 36°C (2) on time after electrical stimulation. B, Dependencies of the speed of trap closure on time after electrical stimulation at 20°C (solid line) and 36°C (dashed line). [See online article for color version of this figure.]

Figure 4.

The effect of anion channel blockers on charge-induced stimulation using two Ag/AgCl electrodes located in the midrib (+) and in one of the two lobes (−). The soil was treated by 25 mL of 10 mm 9-AC 24 h before experiments. A, Photos of the trap closing by different charge stimulations. B, Dependencies of the distance between the edges of the lobes (y) on injected charges. An additional electrical charge was injected to the plant every 5 s. The soil was treated by 25 mL of 10 mm 9-AC 4 h (2) or 24 h (3) before experiments. The capacitor was charged by a 1.5-V battery. [See online article for color version of this figure.]

Figure 5.

Kinetics of trap closing at 20°C by a 42-μC charge injection to the midrib; y is the distance between rims of lobes. A, Variation of distance between the edges of the lobes at 20°C after electrical stimulation. B, Variation of trap closure speed with time after electrical stimulation at 20°C. The soil was treated by 25 mL of 10 mm 9-AC 4 h before experiments. The capacitor was charged by a 1.5-V battery.

Figure 6.

Kinetics of a trap closing after 70 μC electrical stimulation (1). Fifty milliliters of 10 μm CCCP was added to the soil 4.5 h before experiments. The soil around the Venus flytrap was washed with distilled water to decrease CCCP concentration (2).

Figure 7.

The kinetics of trap closure after stimulation of the trigger hairs by a small piece of gelatin (2) or by 28 μC electrical stimulation (1). Fifty milliliters of 10 mm ZnCl₂ was added to the soil 4.5 h before experiments. A, Dependencies of distances between the edges of the lobes on time at 20°C after electrical stimulation. B, Dependencies of trap closure speed on time after electrical stimulation at 20°C.

Figure 8.

The mechanism of trap closure based on experimental and theoretical analysis of this work and experimental data from Volkov et al. (2007).