Cargando…
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...
Autores principales: | , , , , , , , , |
---|---|
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 |
_version_ | 1783620677361729536 |
---|---|
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. |
format | Online Article Text |
id | pubmed-7725304 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
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 |
work_keys_str_mv | AT iosipandal thevenusflytraptriggerhairspecificpotassiumchannelkdm1canreestablishthekgradientrequiredforhaptoelectricsignaling AT bohmjennifer thevenusflytraptriggerhairspecificpotassiumchannelkdm1canreestablishthekgradientrequiredforhaptoelectricsignaling AT scherzersonke thevenusflytraptriggerhairspecificpotassiumchannelkdm1canreestablishthekgradientrequiredforhaptoelectricsignaling AT alrasheidkhaledas thevenusflytraptriggerhairspecificpotassiumchannelkdm1canreestablishthekgradientrequiredforhaptoelectricsignaling AT dreyeringo thevenusflytraptriggerhairspecificpotassiumchannelkdm1canreestablishthekgradientrequiredforhaptoelectricsignaling AT schultzjorg thevenusflytraptriggerhairspecificpotassiumchannelkdm1canreestablishthekgradientrequiredforhaptoelectricsignaling AT beckerdirk thevenusflytraptriggerhairspecificpotassiumchannelkdm1canreestablishthekgradientrequiredforhaptoelectricsignaling AT kreuzerines thevenusflytraptriggerhairspecificpotassiumchannelkdm1canreestablishthekgradientrequiredforhaptoelectricsignaling AT hedrichrainer thevenusflytraptriggerhairspecificpotassiumchannelkdm1canreestablishthekgradientrequiredforhaptoelectricsignaling AT iosipandal venusflytraptriggerhairspecificpotassiumchannelkdm1canreestablishthekgradientrequiredforhaptoelectricsignaling AT bohmjennifer venusflytraptriggerhairspecificpotassiumchannelkdm1canreestablishthekgradientrequiredforhaptoelectricsignaling AT scherzersonke venusflytraptriggerhairspecificpotassiumchannelkdm1canreestablishthekgradientrequiredforhaptoelectricsignaling AT alrasheidkhaledas venusflytraptriggerhairspecificpotassiumchannelkdm1canreestablishthekgradientrequiredforhaptoelectricsignaling AT dreyeringo venusflytraptriggerhairspecificpotassiumchannelkdm1canreestablishthekgradientrequiredforhaptoelectricsignaling AT schultzjorg venusflytraptriggerhairspecificpotassiumchannelkdm1canreestablishthekgradientrequiredforhaptoelectricsignaling AT beckerdirk venusflytraptriggerhairspecificpotassiumchannelkdm1canreestablishthekgradientrequiredforhaptoelectricsignaling AT kreuzerines venusflytraptriggerhairspecificpotassiumchannelkdm1canreestablishthekgradientrequiredforhaptoelectricsignaling AT hedrichrainer venusflytraptriggerhairspecificpotassiumchannelkdm1canreestablishthekgradientrequiredforhaptoelectricsignaling |