A unique inventory of ion transporters poises the Venus flytrap to fast-propagating action potentials and calcium waves.

Since the 19th century, it has been known that the carnivorous Venus flytrap is electrically excitable. Nevertheless, the mechanism and the molecular entities of the flytrap action potential (AP) remain unknown. When entering the electrically excitable stage, the trap expressed a characteristic inventory of ion transporters, among which the increase in glutamate receptor GLR3.6 RNA was most pronounced. Trigger hair stimulation or glutamate application evoked an AP and a cytoplasmic Ca2+ transient that both propagated at the same speed from the site of induction along the entire trap lobe surface. A priming Ca2+ moiety entering the cytoplasm in the context of the AP was further potentiated by an organelle-localized calcium-induced calcium release (CICR)-like system prolonging the Ca2+ signal. While the Ca2+ transient persisted, SKOR K+ channels and AHA H+-ATPases repolarized the AP already. By counting the number of APs and long-lasting Ca2+ transients, the trap directs the different steps in the carnivorous plant's hunting cycle. VIDEO ABSTRACT.

The Venus flytrap trigger hair-specific potassium channel KDM1 can reestablish the K+ gradient required for hapto-electric signaling.

The carnivorous plant Dionaea muscipula harbors multicellular trigger hairs designed to sense mechanical stimuli upon contact with animal prey. At the base of the trigger hair, mechanosensation is transduced into an all-or-nothing action potential (AP) that spreads all over the trap, ultimately leading to trap closure and prey capture. To reveal the molecular basis for the unique functional repertoire of this mechanoresponsive plant structure, we determined the transcriptome of D. muscipula's trigger hair. Among the genes that were found to be highly specific to the trigger hair, the Shaker-type channel KDM1 was electrophysiologically characterized as a hyperpolarization- and acid-activated K+-selective channel, thus allowing the reuptake of K+ ions into the trigger hair's sensory cells during the hyperpolarization phase of the AP. During trap development, the increased electrical excitability of the trigger hair is associated with the transcriptional induction of KDM1. Conversely, when KDM1 is blocked by Cs+ in adult traps, the initiation of APs in response to trigger hair deflection is reduced, and trap closure is suppressed. KDM1 thus plays a dominant role in K+ homeostasis in the context of AP and turgor formation underlying the mechanosensation of trigger hair cells and thus D. muscipula's hapto-electric signaling.