Excitability and propagation of the electrical impulse in Venus flytrap; a comparative electrophysiological study of unipolar electrograms with myocardial tissue.

Mammalian heart cells and cells of leaves of Dionaea muscipula share the ability to generate propagated action potentials, because the excitable cells are electrically coupled. In the heart the propagated action potential causes synchronized contraction of the heart muscle after automatic generation of the impulse in the sinus node. In Dionaea propagation results in closure of the trap after activation of trigger hairs by an insect. The electrical activity can be recorded in the extracellular space as an extracellular electrogram, resulting from transmembrane currents. Although the underlying physiological mechanism that causes the electrogram is similar for heart and Dionaea cells, the contribution of the various ions to the transmembrane current is different. We recorded extracellular electrograms from Dionaea leaves and compared the recorded signals with those known from the heart. The morphology of the electrograms differed considerably. In comparison to activation in mammalian myocardium, electrograms of Dionaea are more temporally and spatially variable. Whereas electrograms in healthy myocardium recorded at some distance from the site of activation reveal a simple biphasic pattern, Dionaea activation showed positive, negative or biphasic deflections. Comparison of patch clamp data from plant cells and cardiomyocytes suggests a role of temperature and ion concentrations in extracellular space for the diversity of morphologies of the Dionaea electrograms.

Kinematics Governing Mechanotransduction in the Sensory Hair of the Venus flytrap.

Insects fall prey to the Venus flytrap (Dionaea muscipula) when they touch the sensory hairs located on the flytrap lobes, causing sudden trap closure. The mechanical stimulus imparted by the touch produces an electrical response in the sensory cells of the trigger hair. These cells are found in a constriction near the hair base, where a notch appears around the hair's periphery. There are mechanosensitive ion channels (MSCs) in the sensory cells that open due to a change in membrane tension; however, the kinematics behind this process is unclear. In this study, we investigate how the stimulus acts on the sensory cells by building a multi-scale hair model, using morphometric data obtained from µ-CT scans. We simulated a single-touch stimulus and evaluated the resulting cell wall stretch. Interestingly, the model showed that high stretch values are diverted away from the notch periphery and, instead, localized in the interior regions of the cell wall. We repeated our simulations for different cell shape variants to elucidate how the morphology influences the location of these high-stretch regions. Our results suggest that there is likely a higher mechanotransduction activity in these 'hotspots', which may provide new insights into the arrangement and functioning of MSCs in the flytrap.

The carnivorous Venus flytrap uses prey-derived amino acid carbon to fuel respiration.

The present study was performed to elucidate the fate of carbon (C) and nitrogen (N) derived from protein of prey caught by carnivorous Dionaea muscipula. For this, traps were fed 13 C/15 N-glutamine (Gln). The release of 13 CO2 was continuously monitored by isotope ratio infrared spectrometry. After 46 h, the allocation of C and N label into different organs was determined and tissues were subjected to metabolome, proteome and transcriptome analyses. Nitrogen of Gln fed was already separated from its C skeleton in the decomposing fluid secreted by the traps. Most of the Gln-C and Gln-N recovered inside plants were localized in fed traps. Among nonfed organs, traps were a stronger sink for Gln-C compared to Gln-N, and roots were a stronger sink for Gln-N compared to Gln-C. A significant amount of the Gln-C was respired as indicated by 13 C-CO2 emission, enhanced levels of metabolites of respiratory Gln degradation and increased abundance of proteins of respiratory processes. Transcription analyses revealed constitutive expression of enzymes involved in Gln metabolism in traps. It appears that prey not only provides building blocks of cellular constituents of carnivorous Dionaea muscipula, but also is used for energy generation by respiratory amino acid degradation.

Venus flytrap carnivorous lifestyle builds on herbivore defense strategies.

Although the concept of botanical carnivory has been known since Darwin's time, the molecular mechanisms that allow animal feeding remain unknown, primarily due to a complete lack of genomic information. Here, we show that the transcriptomic landscape of the Dionaea trap is dramatically shifted toward signal transduction and nutrient transport upon insect feeding, with touch hormone signaling and protein secretion prevailing. At the same time, a massive induction of general defense responses is accompanied by the repression of cell death-related genes/processes. We hypothesize that the carnivory syndrome of Dionaea evolved by exaptation of ancient defense pathways, replacing cell death with nutrient acquisition.

Calcium sensor kinase activates potassium uptake systems in gland cells of Venus flytraps.

The Darwin plant Dionaea muscipula is able to grow on mineral-poor soil, because it gains essential nutrients from captured animal prey. Given that no nutrients remain in the trap when it opens after the consumption of an animal meal, we here asked the question of how Dionaea sequesters prey-derived potassium. We show that prey capture triggers expression of a K(+) uptake system in the Venus flytrap. In search of K(+) transporters endowed with adequate properties for this role, we screened a Dionaea expressed sequence tag (EST) database and identified DmKT1 and DmHAK5 as candidates. On insect and touch hormone stimulation, the number of transcripts of these transporters increased in flytraps. After cRNA injection of K(+)-transporter genes into Xenopus oocytes, however, both putative K(+) transporters remained silent. Assuming that calcium sensor kinases are regulating Arabidopsis K(+) transporter 1 (AKT1), we coexpressed the putative K(+) transporters with a large set of kinases and identified the CBL9-CIPK23 pair as the major activating complex for both transporters in Dionaea K(+) uptake. DmKT1 was found to be a K(+)-selective channel of voltage-dependent high capacity and low affinity, whereas DmHAK5 was identified as the first, to our knowledge, proton-driven, high-affinity potassium transporter with weak selectivity. When the Venus flytrap is processing its prey, the gland cell membrane potential is maintained around -120 mV, and the apoplast is acidified to pH 3. These conditions in the green stomach formed by the closed flytrap allow DmKT1 and DmHAK5 to acquire prey-derived K(+), reducing its concentration from millimolar levels down to trace levels.

Cytochemical and ultrastructural aspects of aquatic carnivorous plant turions.

Turions, which are modified shoot apices, are vegetative, dormant overwintering organs produced by perennial aquatic plants. In this study, the turion cytochemistry and ultrastructure of Aldrovanda vesiculosa, Utricularia vulgaris and U. stygia were compared with particular emphasis placed on storage substances. These three aquatic, rootless carnivorous plant species were studied at the end of their winter dormancy. At this stage, the turions of all species had starch as their main storage material. In contrast with A. vesiculosa, Utricularia turions were rich in protein storage vacuoles, and proteins were also accumulated as crystalline inclusions in the nuclei. All examined species accumulated lipid droplets in cells of epidermal glands.

Shape-changing shell-like structures.

Plants such as Dionaea muscipula (Venus Flytrap) can change the shape of their shell-like leaves by actively altering the cell pressures. These leaves are hydraulic actuators that do not require any complex controls and that possess an energy efficiency that is unmatched by natural or artificial muscles (Huber et al 1997 Proc. R. Soc. A 453 2185-205). We extend our previous work (Pagitz et al 2012 Bioinspir. Biomim. 7 016007) on pressure-actuated cellular structures by introducing a concept for shape-changing shell-like structures that can significantly alter their Gaussian curvature. The potential of this concept is demonstrated by a hemispherical shell that can reversibly change the sign of its Gaussian curvature. Furthermore, it is shown that a snap-through behaviour, similar to the one known from Dionaea muscipula, can be achieved by lowering the pressure in a single layer of cells.