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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 |
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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. |
doi_str_mv | 10.1093/aob/mcx155 |
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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><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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