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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 lead...

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Autores principales: Iosip, Anda L., Böhm, Jennifer, Scherzer, Sönke, Al-Rasheid, Khaled A. S., Dreyer, Ingo, Schultz, Jörg, Becker, Dirk, Kreuzer, Ines, Hedrich, Rainer
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7725304/
https://www.ncbi.nlm.nih.gov/pubmed/33296375
http://dx.doi.org/10.1371/journal.pbio.3000964
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author Iosip, Anda L.
Böhm, Jennifer
Scherzer, Sönke
Al-Rasheid, Khaled A. S.
Dreyer, Ingo
Schultz, Jörg
Becker, Dirk
Kreuzer, Ines
Hedrich, Rainer
author_facet Iosip, Anda L.
Böhm, Jennifer
Scherzer, Sönke
Al-Rasheid, Khaled A. S.
Dreyer, Ingo
Schultz, Jörg
Becker, Dirk
Kreuzer, Ines
Hedrich, Rainer
author_sort Iosip, Anda L.
collection PubMed
description 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.
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spelling pubmed-77253042020-12-16 The Venus flytrap trigger hair–specific potassium channel KDM1 can reestablish the K(+) gradient required for hapto-electric signaling Iosip, Anda L. Böhm, Jennifer Scherzer, Sönke Al-Rasheid, Khaled A. S. Dreyer, Ingo Schultz, Jörg Becker, Dirk Kreuzer, Ines Hedrich, Rainer PLoS Biol Research Article 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. Public Library of Science 2020-12-09 /pmc/articles/PMC7725304/ /pubmed/33296375 http://dx.doi.org/10.1371/journal.pbio.3000964 Text en © 2020 Iosip et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Iosip, Anda L.
Böhm, Jennifer
Scherzer, Sönke
Al-Rasheid, Khaled A. S.
Dreyer, Ingo
Schultz, Jörg
Becker, Dirk
Kreuzer, Ines
Hedrich, Rainer
The Venus flytrap trigger hair–specific potassium channel KDM1 can reestablish the K(+) gradient required for hapto-electric signaling
title The Venus flytrap trigger hair–specific potassium channel KDM1 can reestablish the K(+) gradient required for hapto-electric signaling
title_full The Venus flytrap trigger hair–specific potassium channel KDM1 can reestablish the K(+) gradient required for hapto-electric signaling
title_fullStr The Venus flytrap trigger hair–specific potassium channel KDM1 can reestablish the K(+) gradient required for hapto-electric signaling
title_full_unstemmed The Venus flytrap trigger hair–specific potassium channel KDM1 can reestablish the K(+) gradient required for hapto-electric signaling
title_short The Venus flytrap trigger hair–specific potassium channel KDM1 can reestablish the K(+) gradient required for hapto-electric signaling
title_sort venus flytrap trigger hair–specific potassium channel kdm1 can reestablish the k(+) gradient required for hapto-electric signaling
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7725304/
https://www.ncbi.nlm.nih.gov/pubmed/33296375
http://dx.doi.org/10.1371/journal.pbio.3000964
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