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.Plants can react to mechanical stimuli (Ksenzhek and Volkov, 1998;Braam, 2005) with the use of mechanosensitive channels. These channels are found in different types of cells-animal, plant, fungal, and bacterial. The omnipresence of these channels indicates their important physiological function in the regulation of osmolarity, cell volume, and growth (Markin and Sachs, 2004). They are ideal transducers of physiologically relevant mechanical forces (Benolken and Jacobson, 1970). Mechanosensory ion channels in plants are activated by mechanical stress and transduce the sensed information into electrical signals (Volkov and Haack, 1995). In higher plants, these channels are involved in the response to environmental stress (Volkov et al

Actuation systems in plants as prototypes for bioinspired devices

“…(Haupt 1977;Hart 1990). Some of the systems are associated with a rapid response to external stimuli, as well described for the leaf folding of Venus flytrap or mimosa (Weintraub 1952;Findlay 1984;Hodick & Sievers 1988;Braam 2005;Forterre et al 2005;Volkov et al 2008). Others perform very slow movements to adjust the spatial orientation of organs, as known for leaning stems and branches in trees (Wardrop 1965;Okuyama et al 1994;Burgert et al 2007;Coutand et al 2007;Goswami et al 2008) or to specifically deform organs, as analysed for pine cones and wheat awns, respectively (Dawson et al 1997;Elbaum et al 2007Elbaum et al , 2008.…”

Plants on the move: Towards common mechanisms governing mechanically-induced plant movements

“…48 As in legume pulvini, the movement of the Venus flytrap lobes is caused by changes in cell volume of opposing tissue groups by differential water flow linked to ion fluxes. 45 Nevertheless, despite the fact that researchers have investigated the mechanisms by which the trap closes so fast, only in the past 6 y, the dynamic of the movement started to become more clear, notably thanks to Forterre et al and Volkov et al 43,44,46,[50][51][52][53] Forterre et al divided the Venus flytrap movement into two components: an active biochemical component, pertinent to the mechanisms causing microscopic changes, and a passive elastic component, which is the macroscopic closing process determined by the doubly-curved leaf. A difference in turgor pressure constantly maintained between the upper and the lower cell layers of the leaf provides elastic curvature energy storage locked in the leaves.…”

“…43,49 The rapid changes in the curvature of each lobe, rather than the movement of the leaf as a whole, are responsible for the closing movement. 43 More recently, the total hunting cycle of the Venus flytrap was defined as consisting of five different states: open, closed, locked, constriction/ digestion and semi-open. 46 When opened, the trap has a convex shape and in the other phases, the trap changes its curvature to a concave format.…”

“…A difference in turgor pressure constantly maintained between the upper and the lower cell layers of the leaf provides elastic curvature energy storage locked in the leaves. 43,54 The transference of fluid from the upper to the lower cell layer after a stimulus in the sensitive trigger hairs, induces the trap to close due to the return to an equilibrium state of the leaf. 43,49 The rapid changes in the curvature of each lobe, rather than the movement of the leaf as a whole, are responsible for the closing movement.…”

“…43,54 The transference of fluid from the upper to the lower cell layer after a stimulus in the sensitive trigger hairs, induces the trap to close due to the return to an equilibrium state of the leaf. 43,49 The rapid changes in the curvature of each lobe, rather than the movement of the leaf as a whole, are responsible for the closing movement. 43 More recently, the total hunting cycle of the Venus flytrap was defined as consisting of five different states: open, closed, locked, constriction/ digestion and semi-open.…”