Signaling and transport processes related to the carnivorous lifestyle of plants living on nutrient-poor soil

Abstract

In Eukaryotes, long-distance and rapid signal transmission is required in order to be able to react fast and flexibly to external stimuli. This long-distance signal transmission cannot take place by diffusion of signal molecules from the site of perception to the target tissue, as their speed is insufficient. Therefore, for adequate stimulus transmission, plants as well as animals make use of electrical signal transmission, as this can quickly cover long distances. This update summarises the most important advances in plant electrical signal transduction with a focus on the carnivorous Venus flytrap. It highlights the different types of electrical signals, examines their underlying ion fluxes and summarises the carnivorous processes downstream of the electrical signals.

Figure 1

Schematic model of the signaling cascade from prey perception to digestion in Dionaea. Touching the TH (center) is converted into an AP. The predominant opinion on the ion fluxes involved, which lead to a plant AP, are shown in the upper left corner. An initial Ca²⁺ influx subsequently triggers Cl⁻ efflux-associated depolarization of the membrane potential. This depolarization is compensated by the activation of K⁺ efflux. The following repolarization is dominated by an H⁺ efflux. Finally, the original Ca²⁺, Cl⁻, and K⁺ concentrations have to be re-adjusted again. Besides showing different ion permeabilities, the involved transport proteins also exhibit diverse transport activities, kinetics, and voltage dependencies. Thus, the mediated ion fluxes show overlapping phases, which are important for the fine tuning of the AP. The touch-induced AP leads to a calcium wave in the trap and when two APs are triggered within a short time interval, the Ca²⁺ threshold value is exceeded, and the trap closes quickly. Furthermore, the electrical signal also causes an induction of the plant hormone JA. After continuous electrical stimulation, the JA signaling pathway is activated, resulting in the expression of digestive enzymes and finally in prey digestion.

Figure 2

Calcium wave and AP propagation go hand in hand. A, Model of the experimental setup used for parallel AP and Ca²⁺ measurements in the Venus flytrap. Ca²⁺ signal (indicated in red) originates at the stimulated TH and the propagation is monitored using calcium reporter GCaMP (cf. Suda et al., 2020) whose fluorescence is recorded with 50 frames per second. The AP propagation velocity is traced using two surface potential electrodes placed with a known distance at the trap surface and a reference electrode located in the soil. B, This cartoon illustrates simultaneous measurements of the Ca²⁺ wave (red) and the AP transmission (black) in the trap tissue. By bending a TH, both signals propagate from the point of origin (TH) to known positions (Δx) with measured time delays (Δt) resulting in the calculation of comparable velocities for signals of: Ca²⁺ velocity (2.06 ± 0.34 cm s⁻¹, n = 4) and AP velocity (1.91 ± 0.23 cm s⁻¹, n = 16, mean ± sd). C, AP propagation velocity is temperature-dependent. While at 10°C, the AP travels at a speed of only 1.3 cm s⁻¹, warming leads to an increase in velocity by a factor of 1.5 ± 0.2 (mean ± sd, n = 15) until at 40°C the AP reaches an average speed of 6.2 cm s⁻¹.

Figure 3

Gland cell activation by the JA and Ca²⁺ signaling pathways to enable prey digestion and nutrient uptake. The expression of transport proteins to acidify the formed stomach after trap closure as well as the expression of digestive enzymes, like hydrolases etc., are induced via the JA signaling pathway (blue). Although, the associated transport proteins are not known in detail, one could suggest the involvement of H⁺ ATPases and chloride selective channels, which lead to an efflux of HCl into the stomach (left gland). Together with early exocytotic vesicles loaded with proton and chloride ions (green and yellow), the stomach is acidified in order to enable digestive enzyme activity and prey decomposition. The digestive fluid, including a diversity of digestive enzymes, is secreted into the trap and the prey is degraded. Thereby, the fusion process of exocytotic vesicles is triggered by the second messenger calcium (red). The released nutrients (e.g. phosphate, nitrogen species, and potassium) as well as organic compounds and prey derived building blocks are taken up by the gland cells via channel-based transport processes or endocytosis (right gland). DmAMT1 displays an ammonium channel and therefore transports the nitrogen source into the cytosol of the gland cells. The macronutrient potassium is taken up with high capacity and low affinity by the K⁺ selective DmKT1 channel and the proton-driven, high-affine transporter DmHAK5. Both modules enable a consistent potassium uptake and are activated via the Ca²⁺-dependent sensor/kinase complex CBL/CIPK. The absorption of prey-derived sodium ions is mediated by the DmHKT1 channel and is further sequestered into the trap vacuole to prevent the toxification of photosynthetically active tissue. The nutrient uptake by transport proteins is furthermore supplemented by endocytosis (gray) that facilitates the absorption of whole proteins as well as the re-absorption of the secreted digestive enzymes. Endocytoses enables the Venus flytrap to finalize the uptake process and to prevent a loss of compounds during the following re-opening. ATP: adenosine triphosphate; expr: expression; CBL: Calcineurin B-like protein; CIPK: CBL-interacting protein kinase.