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Anaesthetics stop diverse plant organ movements, affect endocytic vesicle recycling and ROS homeostasis, and block action potentials in Venus flytraps

Abstract Background and Aims Anaesthesia for medical purposes was introduced in the 19th century. However, the physiological mode of anaesthetic drug actions on the nervous system remains unclear. One of the remaining questions is how these different compounds, with no structural similarities and ev...

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Published in:Annals of botany 2018-11, Vol.122 (5), p.747-756
Main Authors: Yokawa, K, Kagenishi, T, Pavlovič, A, Gall, S, Weiland, M, Mancuso, S, Baluška, F
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container_title Annals of botany
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creator Yokawa, K
Kagenishi, T
Pavlovič, A
Gall, S
Weiland, M
Mancuso, S
Baluška, F
description Abstract Background and Aims Anaesthesia for medical purposes was introduced in the 19th century. However, the physiological mode of anaesthetic drug actions on the nervous system remains unclear. One of the remaining questions is how these different compounds, with no structural similarities and even chemically inert elements such as the noble gas xenon, act as anaesthetic agents inducing loss of consciousness. The main goal here was to determine if anaesthetics affect the same or similar processes in plants as in animals and humans. Methods A single-lens reflex camera was used to follow organ movements in plants before, during and after recovery from exposure to diverse anaesthetics. Confocal microscopy was used to analyse endocytic vesicle trafficking. Electrical signals were recorded using a surface AgCl electrode. Key Results Mimosa leaves, pea tendrils, Venus flytraps and sundew traps all lost both their autonomous and touch-induced movements after exposure to anaesthetics. In Venus flytrap, this was shown to be due to the loss of action potentials under diethyl ether anaesthesia. The same concentration of diethyl ether immobilized pea tendrils. Anaesthetics also impeded seed germination and chlorophyll accumulation in cress seedlings. Endocytic vesicle recycling and reactive oxygen species (ROS) balance, as observed in intact Arabidopsis root apex cells, were also affected by all anaesthetics tested. Conclusions Plants are sensitive to several anaesthetics that have no structural similarities. As in animals and humans, anaesthetics used at appropriate concentrations block action potentials and immobilize organs via effects on action potentials, endocytic vesicle recycling and ROS homeostasis. Plants emerge as ideal model objects to study general questions related to anaesthesia, as well as to serve as a suitable test system for human anaesthesia.
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However, the physiological mode of anaesthetic drug actions on the nervous system remains unclear. One of the remaining questions is how these different compounds, with no structural similarities and even chemically inert elements such as the noble gas xenon, act as anaesthetic agents inducing loss of consciousness. The main goal here was to determine if anaesthetics affect the same or similar processes in plants as in animals and humans. Methods A single-lens reflex camera was used to follow organ movements in plants before, during and after recovery from exposure to diverse anaesthetics. Confocal microscopy was used to analyse endocytic vesicle trafficking. Electrical signals were recorded using a surface AgCl electrode. Key Results Mimosa leaves, pea tendrils, Venus flytraps and sundew traps all lost both their autonomous and touch-induced movements after exposure to anaesthetics. In Venus flytrap, this was shown to be due to the loss of action potentials under diethyl ether anaesthesia. The same concentration of diethyl ether immobilized pea tendrils. Anaesthetics also impeded seed germination and chlorophyll accumulation in cress seedlings. Endocytic vesicle recycling and reactive oxygen species (ROS) balance, as observed in intact Arabidopsis root apex cells, were also affected by all anaesthetics tested. Conclusions Plants are sensitive to several anaesthetics that have no structural similarities. As in animals and humans, anaesthetics used at appropriate concentrations block action potentials and immobilize organs via effects on action potentials, endocytic vesicle recycling and ROS homeostasis. Plants emerge as ideal model objects to study general questions related to anaesthesia, as well as to serve as a suitable test system for human anaesthesia.</description><identifier>ISSN: 0305-7364</identifier><identifier>ISSN: 1095-8290</identifier><identifier>EISSN: 1095-8290</identifier><identifier>DOI: 10.1093/aob/mcx155</identifier><identifier>PMID: 29236942</identifier><language>eng</language><publisher>US: Oxford University Press</publisher><subject>action potentials ; Action Potentials - drug effects ; Action Potentials - physiology ; anesthesia ; Anesthetics - adverse effects ; Arabidopsis ; Arabidopsis - drug effects ; Arabidopsis - physiology ; cameras ; chlorophyll ; Chlorophyll - metabolism ; confocal microscopy ; consciousness ; Dionaea muscipula ; Drosera ; Drosera - drug effects ; Drosera - physiology ; Droseraceae - drug effects ; Droseraceae - physiology ; electrodes ; Ether - adverse effects ; ethyl ether ; Germination - drug effects ; Homeostasis ; humans ; leaves ; Lepidium sativum - drug effects ; Lepidium sativum - physiology ; Magnoliopsida - drug effects ; Magnoliopsida - physiology ; Mimosa ; Mimosa - drug effects ; Mimosa - physiology ; Organelles - drug effects ; Organelles - physiology ; peas ; Pisum sativum - drug effects ; Pisum sativum - physiology ; Plant Leaves - drug effects ; Plant Leaves - physiology ; reactive oxygen species ; Reactive Oxygen Species - metabolism ; Research in Context ; seed germination ; seedlings ; silver chloride ; synaptic vesicles ; Transport Vesicles - drug effects ; Transport Vesicles - physiology ; xenon</subject><ispartof>Annals of botany, 2018-11, Vol.122 (5), p.747-756</ispartof><rights>The Author(s) 2017. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. 2017</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c485t-d54b50015bc32984b4b3604d28ad341fe05d3962ac4fab54a2b8eca86079c5ab3</citedby><cites>FETCH-LOGICAL-c485t-d54b50015bc32984b4b3604d28ad341fe05d3962ac4fab54a2b8eca86079c5ab3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6215046/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6215046/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,27903,27904,53769,53771</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29236942$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yokawa, K</creatorcontrib><creatorcontrib>Kagenishi, T</creatorcontrib><creatorcontrib>Pavlovič, A</creatorcontrib><creatorcontrib>Gall, S</creatorcontrib><creatorcontrib>Weiland, M</creatorcontrib><creatorcontrib>Mancuso, S</creatorcontrib><creatorcontrib>Baluška, F</creatorcontrib><title>Anaesthetics stop diverse plant organ movements, affect endocytic vesicle recycling and ROS homeostasis, and block action potentials in Venus flytraps</title><title>Annals of botany</title><addtitle>Ann Bot</addtitle><description>Abstract Background and Aims Anaesthesia for medical purposes was introduced in the 19th century. However, the physiological mode of anaesthetic drug actions on the nervous system remains unclear. One of the remaining questions is how these different compounds, with no structural similarities and even chemically inert elements such as the noble gas xenon, act as anaesthetic agents inducing loss of consciousness. The main goal here was to determine if anaesthetics affect the same or similar processes in plants as in animals and humans. Methods A single-lens reflex camera was used to follow organ movements in plants before, during and after recovery from exposure to diverse anaesthetics. Confocal microscopy was used to analyse endocytic vesicle trafficking. Electrical signals were recorded using a surface AgCl electrode. Key Results Mimosa leaves, pea tendrils, Venus flytraps and sundew traps all lost both their autonomous and touch-induced movements after exposure to anaesthetics. In Venus flytrap, this was shown to be due to the loss of action potentials under diethyl ether anaesthesia. The same concentration of diethyl ether immobilized pea tendrils. Anaesthetics also impeded seed germination and chlorophyll accumulation in cress seedlings. Endocytic vesicle recycling and reactive oxygen species (ROS) balance, as observed in intact Arabidopsis root apex cells, were also affected by all anaesthetics tested. Conclusions Plants are sensitive to several anaesthetics that have no structural similarities. As in animals and humans, anaesthetics used at appropriate concentrations block action potentials and immobilize organs via effects on action potentials, endocytic vesicle recycling and ROS homeostasis. Plants emerge as ideal model objects to study general questions related to anaesthesia, as well as to serve as a suitable test system for human anaesthesia.</description><subject>action potentials</subject><subject>Action Potentials - drug effects</subject><subject>Action Potentials - physiology</subject><subject>anesthesia</subject><subject>Anesthetics - adverse effects</subject><subject>Arabidopsis</subject><subject>Arabidopsis - drug effects</subject><subject>Arabidopsis - physiology</subject><subject>cameras</subject><subject>chlorophyll</subject><subject>Chlorophyll - metabolism</subject><subject>confocal microscopy</subject><subject>consciousness</subject><subject>Dionaea muscipula</subject><subject>Drosera</subject><subject>Drosera - drug effects</subject><subject>Drosera - physiology</subject><subject>Droseraceae - drug effects</subject><subject>Droseraceae - physiology</subject><subject>electrodes</subject><subject>Ether - adverse effects</subject><subject>ethyl ether</subject><subject>Germination - drug effects</subject><subject>Homeostasis</subject><subject>humans</subject><subject>leaves</subject><subject>Lepidium sativum - drug effects</subject><subject>Lepidium sativum - physiology</subject><subject>Magnoliopsida - drug effects</subject><subject>Magnoliopsida - physiology</subject><subject>Mimosa</subject><subject>Mimosa - drug effects</subject><subject>Mimosa - physiology</subject><subject>Organelles - drug effects</subject><subject>Organelles - physiology</subject><subject>peas</subject><subject>Pisum sativum - drug effects</subject><subject>Pisum sativum - physiology</subject><subject>Plant Leaves - drug effects</subject><subject>Plant Leaves - physiology</subject><subject>reactive oxygen species</subject><subject>Reactive Oxygen Species - metabolism</subject><subject>Research in Context</subject><subject>seed germination</subject><subject>seedlings</subject><subject>silver chloride</subject><subject>synaptic vesicles</subject><subject>Transport Vesicles - drug effects</subject><subject>Transport Vesicles - physiology</subject><subject>xenon</subject><issn>0305-7364</issn><issn>1095-8290</issn><issn>1095-8290</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><recordid>eNp9kdtq3DAQhkVpabZpb_oARTeFUupE1sFr3xRC6CEQCPR0K0byeFetLTmSvHRfpM9bhU1Ce5Mrwcw3n4b5CXlZs5OadeIUgjmd7O9aqUdkVSqqannHHpMVE0xVa9HII_IspZ-MMd509VNyxDsumk7yFflz5gFT3mJ2NtGUw0x7t8OYkM4j-ExD3ICnU9jhhD6ndxSGAW2m6Ptg92WK7jA5OyKNaPd2dH5Dwff0y9VXug0ThpQhuZu5UjRjsL8o2OyCp3PIxehgTNR5-gP9kugw7nOEOT0nT4bSwBe37zH5_vHDt_PP1eXVp4vzs8vKylblqlfSKMZqZazgXSuNNKJhsuct9ELWAzLVi67hYOUARkngpkULbcPWnVVgxDF5f_DOi5mwt2WhCKOeo5sg7nUAp__veLfVm7DTDa8Vk00RvLkVxHC9lEvqySWLY7kdhiVpLtaSl0yatqBvD6iNIaWIw_03NdM3QeoSpD4EWeBX_y52j94lV4DXByAs80Oiv8jZq68</recordid><startdate>20181103</startdate><enddate>20181103</enddate><creator>Yokawa, K</creator><creator>Kagenishi, T</creator><creator>Pavlovič, A</creator><creator>Gall, S</creator><creator>Weiland, M</creator><creator>Mancuso, S</creator><creator>Baluška, F</creator><general>Oxford University Press</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope></search><sort><creationdate>20181103</creationdate><title>Anaesthetics stop diverse plant organ movements, affect endocytic vesicle recycling and ROS homeostasis, and block action potentials in Venus flytraps</title><author>Yokawa, K ; Kagenishi, T ; Pavlovič, A ; Gall, S ; Weiland, M ; Mancuso, S ; Baluška, F</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c485t-d54b50015bc32984b4b3604d28ad341fe05d3962ac4fab54a2b8eca86079c5ab3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>action potentials</topic><topic>Action Potentials - drug effects</topic><topic>Action Potentials - physiology</topic><topic>anesthesia</topic><topic>Anesthetics - adverse effects</topic><topic>Arabidopsis</topic><topic>Arabidopsis - drug effects</topic><topic>Arabidopsis - physiology</topic><topic>cameras</topic><topic>chlorophyll</topic><topic>Chlorophyll - metabolism</topic><topic>confocal microscopy</topic><topic>consciousness</topic><topic>Dionaea muscipula</topic><topic>Drosera</topic><topic>Drosera - drug effects</topic><topic>Drosera - physiology</topic><topic>Droseraceae - drug effects</topic><topic>Droseraceae - physiology</topic><topic>electrodes</topic><topic>Ether - adverse effects</topic><topic>ethyl ether</topic><topic>Germination - drug effects</topic><topic>Homeostasis</topic><topic>humans</topic><topic>leaves</topic><topic>Lepidium sativum - drug effects</topic><topic>Lepidium sativum - physiology</topic><topic>Magnoliopsida - drug effects</topic><topic>Magnoliopsida - physiology</topic><topic>Mimosa</topic><topic>Mimosa - drug effects</topic><topic>Mimosa - physiology</topic><topic>Organelles - drug effects</topic><topic>Organelles - physiology</topic><topic>peas</topic><topic>Pisum sativum - drug effects</topic><topic>Pisum sativum - physiology</topic><topic>Plant Leaves - drug effects</topic><topic>Plant Leaves - physiology</topic><topic>reactive oxygen species</topic><topic>Reactive Oxygen Species - metabolism</topic><topic>Research in Context</topic><topic>seed germination</topic><topic>seedlings</topic><topic>silver chloride</topic><topic>synaptic vesicles</topic><topic>Transport Vesicles - drug effects</topic><topic>Transport Vesicles - physiology</topic><topic>xenon</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yokawa, K</creatorcontrib><creatorcontrib>Kagenishi, T</creatorcontrib><creatorcontrib>Pavlovič, A</creatorcontrib><creatorcontrib>Gall, S</creatorcontrib><creatorcontrib>Weiland, M</creatorcontrib><creatorcontrib>Mancuso, S</creatorcontrib><creatorcontrib>Baluška, F</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Annals of botany</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yokawa, K</au><au>Kagenishi, T</au><au>Pavlovič, A</au><au>Gall, S</au><au>Weiland, M</au><au>Mancuso, S</au><au>Baluška, F</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Anaesthetics stop diverse plant organ movements, affect endocytic vesicle recycling and ROS homeostasis, and block action potentials in Venus flytraps</atitle><jtitle>Annals of botany</jtitle><addtitle>Ann Bot</addtitle><date>2018-11-03</date><risdate>2018</risdate><volume>122</volume><issue>5</issue><spage>747</spage><epage>756</epage><pages>747-756</pages><issn>0305-7364</issn><issn>1095-8290</issn><eissn>1095-8290</eissn><abstract>Abstract Background and Aims Anaesthesia for medical purposes was introduced in the 19th century. However, the physiological mode of anaesthetic drug actions on the nervous system remains unclear. One of the remaining questions is how these different compounds, with no structural similarities and even chemically inert elements such as the noble gas xenon, act as anaesthetic agents inducing loss of consciousness. The main goal here was to determine if anaesthetics affect the same or similar processes in plants as in animals and humans. Methods A single-lens reflex camera was used to follow organ movements in plants before, during and after recovery from exposure to diverse anaesthetics. Confocal microscopy was used to analyse endocytic vesicle trafficking. Electrical signals were recorded using a surface AgCl electrode. Key Results Mimosa leaves, pea tendrils, Venus flytraps and sundew traps all lost both their autonomous and touch-induced movements after exposure to anaesthetics. In Venus flytrap, this was shown to be due to the loss of action potentials under diethyl ether anaesthesia. The same concentration of diethyl ether immobilized pea tendrils. Anaesthetics also impeded seed germination and chlorophyll accumulation in cress seedlings. Endocytic vesicle recycling and reactive oxygen species (ROS) balance, as observed in intact Arabidopsis root apex cells, were also affected by all anaesthetics tested. Conclusions Plants are sensitive to several anaesthetics that have no structural similarities. As in animals and humans, anaesthetics used at appropriate concentrations block action potentials and immobilize organs via effects on action potentials, endocytic vesicle recycling and ROS homeostasis. Plants emerge as ideal model objects to study general questions related to anaesthesia, as well as to serve as a suitable test system for human anaesthesia.</abstract><cop>US</cop><pub>Oxford University Press</pub><pmid>29236942</pmid><doi>10.1093/aob/mcx155</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record>
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source Oxford Journals Online; JSTOR Archival Journals; PubMed Central
subjects action potentials
Action Potentials - drug effects
Action Potentials - physiology
anesthesia
Anesthetics - adverse effects
Arabidopsis
Arabidopsis - drug effects
Arabidopsis - physiology
cameras
chlorophyll
Chlorophyll - metabolism
confocal microscopy
consciousness
Dionaea muscipula
Drosera
Drosera - drug effects
Drosera - physiology
Droseraceae - drug effects
Droseraceae - physiology
electrodes
Ether - adverse effects
ethyl ether
Germination - drug effects
Homeostasis
humans
leaves
Lepidium sativum - drug effects
Lepidium sativum - physiology
Magnoliopsida - drug effects
Magnoliopsida - physiology
Mimosa
Mimosa - drug effects
Mimosa - physiology
Organelles - drug effects
Organelles - physiology
peas
Pisum sativum - drug effects
Pisum sativum - physiology
Plant Leaves - drug effects
Plant Leaves - physiology
reactive oxygen species
Reactive Oxygen Species - metabolism
Research in Context
seed germination
seedlings
silver chloride
synaptic vesicles
Transport Vesicles - drug effects
Transport Vesicles - physiology
xenon
title Anaesthetics stop diverse plant organ movements, affect endocytic vesicle recycling and ROS homeostasis, and block action potentials in Venus flytraps
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