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

PLoS Biol. 2020 Dec 9;18(12):e3000964. doi: 10.1371/journal.pbio.3000964. eCollection 2020 Dec.

Abstract

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / physiology
  • Biological Transport
  • Droseraceae / genetics*
  • Droseraceae / metabolism*
  • Electrophysiological Phenomena
  • Gene Expression / genetics
  • Gene Expression Regulation, Plant / genetics
  • Ions
  • Mechanoreceptors / metabolism
  • Mechanoreceptors / physiology
  • Plant Leaves / physiology
  • Potassium / metabolism
  • Potassium Channels / metabolism*
  • Potassium Channels / physiology
  • Signal Transduction
  • Transcriptome / genetics

Substances

  • Ions
  • Potassium Channels
  • Potassium

Grants and funding

This work was supported by a DFG Reinhart Koselleck grant (no. 415282803; https://www.dfg.de) to R.H. It was also supported by the Researchers Supporting Program (project no. RSP-2020/10), King Saud University, Saudi Arabia (https://ksu.edu.sa/en/) to R.H. and K.Al-R.. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.