A trio of viral proteins tunes aphid-plant interactions in Arabidopsis thaliana
Virus-induced deterrence to aphid feeding is believed to promote plant virus transmission by encouraging migration of virus-bearing insects away from infected plants. We investigated the effects of infection by an aphid-transmitted virus, cucumber mosaic virus (CMV), on the interaction of Arabidopsi...
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creator | Westwood, Jack H Groen, Simon C Du, Zhiyou Murphy, Alex M Anggoro, Damar Tri Tungadi, Trisna Luang-In, Vijitra Lewsey, Mathew G Rossiter, John T Powell, Glen Smith, Alison G Carr, John P |
description | Virus-induced deterrence to aphid feeding is believed to promote plant virus transmission by encouraging migration of virus-bearing insects away from infected plants. We investigated the effects of infection by an aphid-transmitted virus, cucumber mosaic virus (CMV), on the interaction of Arabidopsis thaliana, one of the natural hosts for CMV, with Myzus persicae (common names: 'peach-potato aphid', 'green peach aphid').
Infection of Arabidopsis (ecotype Col-0) with CMV strain Fny (Fny-CMV) induced biosynthesis of the aphid feeding-deterrent 4-methoxy-indol-3-yl-methylglucosinolate (4MI3M). 4MI3M inhibited phloem ingestion by aphids and consequently discouraged aphid settling. The CMV 2b protein is a suppressor of antiviral RNA silencing, which has previously been implicated in altering plant-aphid interactions. Its presence in infected hosts enhances the accumulation of CMV and the other four viral proteins. Another viral gene product, the 2a protein (an RNA-dependent RNA polymerase), triggers defensive signaling, leading to increased 4MI3M accumulation. The 2b protein can inhibit ARGONAUTE1 (AGO1), a host factor that both positively-regulates 4MI3M biosynthesis and negatively-regulates accumulation of substance(s) toxic to aphids. However, the 1a replicase protein moderated 2b-mediated inhibition of AGO1, ensuring that aphids were deterred from feeding but not poisoned. The LS strain of CMV did not induce feeding deterrence in Arabidopsis ecotype Col-0.
Inhibition of AGO1 by the 2b protein could act as a booby trap since this will trigger antibiosis against aphids. However, for Fny-CMV the interplay of three viral proteins (1a, 2a and 2b) appears to balance the need of the virus to inhibit antiviral silencing, while inducing a mild resistance (antixenosis) that is thought to promote transmission. The strain-specific effects of CMV on Arabidopsis-aphid interactions, and differences between the effects of Fny-CMV on this plant and those seen previously in tobacco (inhibition of resistance to aphids) may have important epidemiological consequences. |
doi_str_mv | 10.1371/journal.pone.0083066 |
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Infection of Arabidopsis (ecotype Col-0) with CMV strain Fny (Fny-CMV) induced biosynthesis of the aphid feeding-deterrent 4-methoxy-indol-3-yl-methylglucosinolate (4MI3M). 4MI3M inhibited phloem ingestion by aphids and consequently discouraged aphid settling. The CMV 2b protein is a suppressor of antiviral RNA silencing, which has previously been implicated in altering plant-aphid interactions. Its presence in infected hosts enhances the accumulation of CMV and the other four viral proteins. Another viral gene product, the 2a protein (an RNA-dependent RNA polymerase), triggers defensive signaling, leading to increased 4MI3M accumulation. The 2b protein can inhibit ARGONAUTE1 (AGO1), a host factor that both positively-regulates 4MI3M biosynthesis and negatively-regulates accumulation of substance(s) toxic to aphids. However, the 1a replicase protein moderated 2b-mediated inhibition of AGO1, ensuring that aphids were deterred from feeding but not poisoned. The LS strain of CMV did not induce feeding deterrence in Arabidopsis ecotype Col-0.
Inhibition of AGO1 by the 2b protein could act as a booby trap since this will trigger antibiosis against aphids. However, for Fny-CMV the interplay of three viral proteins (1a, 2a and 2b) appears to balance the need of the virus to inhibit antiviral silencing, while inducing a mild resistance (antixenosis) that is thought to promote transmission. The strain-specific effects of CMV on Arabidopsis-aphid interactions, and differences between the effects of Fny-CMV on this plant and those seen previously in tobacco (inhibition of resistance to aphids) may have important epidemiological consequences.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0083066</identifier><identifier>PMID: 24349433</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Accumulation ; Animals ; Antibiosis ; Antiviral agents ; Aphidoidea ; Aphids ; Aphids - physiology ; Aphids - virology ; Arabidopsis ; Arabidopsis - parasitology ; Arabidopsis - virology ; Arabidopsis thaliana ; Bioinformatics ; Biosynthesis ; Cucumovirus - metabolism ; Disease resistance ; Disease transmission ; DNA-directed RNA polymerase ; Epidemiology ; Feeding ; Feeding Behavior ; Flowers & plants ; Health aspects ; Host-Parasite Interactions ; Infection ; Infections ; Ingestion ; Inhibition ; Insects ; Migration ; Myzus persicae ; Physiological aspects ; Plant sciences ; Plant virus diseases ; Plant viruses ; Plants (botany) ; Plants (Organisms) ; Potatoes ; Process controls ; Proteins ; Replicase ; Ribonucleic acid ; RNA ; RNA-directed RNA polymerase ; RNA-mediated interference ; Signaling ; Studies ; Tobacco ; Viral proteins ; Viral Proteins - metabolism ; Virology ; Viruses</subject><ispartof>PloS one, 2013-12, Vol.8 (12), p.e83066</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Westwood et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2013 Westwood et al 2013 Westwood et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c6076-c16f978d985dc10d0e4a25afd61ebca4d76813c76b2be8bcbaa634f1763dbf593</citedby><cites>FETCH-LOGICAL-c6076-c16f978d985dc10d0e4a25afd61ebca4d76813c76b2be8bcbaa634f1763dbf593</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/PMC3859657/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3859657/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24349433$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Rao, A.L.N.</contributor><creatorcontrib>Westwood, Jack H</creatorcontrib><creatorcontrib>Groen, Simon C</creatorcontrib><creatorcontrib>Du, Zhiyou</creatorcontrib><creatorcontrib>Murphy, Alex M</creatorcontrib><creatorcontrib>Anggoro, Damar Tri</creatorcontrib><creatorcontrib>Tungadi, Trisna</creatorcontrib><creatorcontrib>Luang-In, Vijitra</creatorcontrib><creatorcontrib>Lewsey, Mathew G</creatorcontrib><creatorcontrib>Rossiter, John T</creatorcontrib><creatorcontrib>Powell, Glen</creatorcontrib><creatorcontrib>Smith, Alison G</creatorcontrib><creatorcontrib>Carr, John P</creatorcontrib><title>A trio of viral proteins tunes aphid-plant interactions in Arabidopsis thaliana</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Virus-induced deterrence to aphid feeding is believed to promote plant virus transmission by encouraging migration of virus-bearing insects away from infected plants. We investigated the effects of infection by an aphid-transmitted virus, cucumber mosaic virus (CMV), on the interaction of Arabidopsis thaliana, one of the natural hosts for CMV, with Myzus persicae (common names: 'peach-potato aphid', 'green peach aphid').
Infection of Arabidopsis (ecotype Col-0) with CMV strain Fny (Fny-CMV) induced biosynthesis of the aphid feeding-deterrent 4-methoxy-indol-3-yl-methylglucosinolate (4MI3M). 4MI3M inhibited phloem ingestion by aphids and consequently discouraged aphid settling. The CMV 2b protein is a suppressor of antiviral RNA silencing, which has previously been implicated in altering plant-aphid interactions. Its presence in infected hosts enhances the accumulation of CMV and the other four viral proteins. Another viral gene product, the 2a protein (an RNA-dependent RNA polymerase), triggers defensive signaling, leading to increased 4MI3M accumulation. The 2b protein can inhibit ARGONAUTE1 (AGO1), a host factor that both positively-regulates 4MI3M biosynthesis and negatively-regulates accumulation of substance(s) toxic to aphids. However, the 1a replicase protein moderated 2b-mediated inhibition of AGO1, ensuring that aphids were deterred from feeding but not poisoned. The LS strain of CMV did not induce feeding deterrence in Arabidopsis ecotype Col-0.
Inhibition of AGO1 by the 2b protein could act as a booby trap since this will trigger antibiosis against aphids. However, for Fny-CMV the interplay of three viral proteins (1a, 2a and 2b) appears to balance the need of the virus to inhibit antiviral silencing, while inducing a mild resistance (antixenosis) that is thought to promote transmission. The strain-specific effects of CMV on Arabidopsis-aphid interactions, and differences between the effects of Fny-CMV on this plant and those seen previously in tobacco (inhibition of resistance to aphids) may have important epidemiological consequences.</description><subject>Accumulation</subject><subject>Animals</subject><subject>Antibiosis</subject><subject>Antiviral agents</subject><subject>Aphidoidea</subject><subject>Aphids</subject><subject>Aphids - physiology</subject><subject>Aphids - virology</subject><subject>Arabidopsis</subject><subject>Arabidopsis - parasitology</subject><subject>Arabidopsis - virology</subject><subject>Arabidopsis thaliana</subject><subject>Bioinformatics</subject><subject>Biosynthesis</subject><subject>Cucumovirus - metabolism</subject><subject>Disease resistance</subject><subject>Disease transmission</subject><subject>DNA-directed RNA polymerase</subject><subject>Epidemiology</subject><subject>Feeding</subject><subject>Feeding Behavior</subject><subject>Flowers & plants</subject><subject>Health aspects</subject><subject>Host-Parasite Interactions</subject><subject>Infection</subject><subject>Infections</subject><subject>Ingestion</subject><subject>Inhibition</subject><subject>Insects</subject><subject>Migration</subject><subject>Myzus persicae</subject><subject>Physiological aspects</subject><subject>Plant sciences</subject><subject>Plant virus diseases</subject><subject>Plant viruses</subject><subject>Plants (botany)</subject><subject>Plants (Organisms)</subject><subject>Potatoes</subject><subject>Process controls</subject><subject>Proteins</subject><subject>Replicase</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA-directed RNA polymerase</subject><subject>RNA-mediated interference</subject><subject>Signaling</subject><subject>Studies</subject><subject>Tobacco</subject><subject>Viral proteins</subject><subject>Viral Proteins - 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physiology</topic><topic>Aphids - virology</topic><topic>Arabidopsis</topic><topic>Arabidopsis - parasitology</topic><topic>Arabidopsis - virology</topic><topic>Arabidopsis thaliana</topic><topic>Bioinformatics</topic><topic>Biosynthesis</topic><topic>Cucumovirus - metabolism</topic><topic>Disease resistance</topic><topic>Disease transmission</topic><topic>DNA-directed RNA polymerase</topic><topic>Epidemiology</topic><topic>Feeding</topic><topic>Feeding Behavior</topic><topic>Flowers & plants</topic><topic>Health aspects</topic><topic>Host-Parasite Interactions</topic><topic>Infection</topic><topic>Infections</topic><topic>Ingestion</topic><topic>Inhibition</topic><topic>Insects</topic><topic>Migration</topic><topic>Myzus persicae</topic><topic>Physiological aspects</topic><topic>Plant sciences</topic><topic>Plant virus diseases</topic><topic>Plant viruses</topic><topic>Plants (botany)</topic><topic>Plants (Organisms)</topic><topic>Potatoes</topic><topic>Process controls</topic><topic>Proteins</topic><topic>Replicase</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>RNA-directed RNA polymerase</topic><topic>RNA-mediated interference</topic><topic>Signaling</topic><topic>Studies</topic><topic>Tobacco</topic><topic>Viral proteins</topic><topic>Viral Proteins - 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We investigated the effects of infection by an aphid-transmitted virus, cucumber mosaic virus (CMV), on the interaction of Arabidopsis thaliana, one of the natural hosts for CMV, with Myzus persicae (common names: 'peach-potato aphid', 'green peach aphid').
Infection of Arabidopsis (ecotype Col-0) with CMV strain Fny (Fny-CMV) induced biosynthesis of the aphid feeding-deterrent 4-methoxy-indol-3-yl-methylglucosinolate (4MI3M). 4MI3M inhibited phloem ingestion by aphids and consequently discouraged aphid settling. The CMV 2b protein is a suppressor of antiviral RNA silencing, which has previously been implicated in altering plant-aphid interactions. Its presence in infected hosts enhances the accumulation of CMV and the other four viral proteins. Another viral gene product, the 2a protein (an RNA-dependent RNA polymerase), triggers defensive signaling, leading to increased 4MI3M accumulation. The 2b protein can inhibit ARGONAUTE1 (AGO1), a host factor that both positively-regulates 4MI3M biosynthesis and negatively-regulates accumulation of substance(s) toxic to aphids. However, the 1a replicase protein moderated 2b-mediated inhibition of AGO1, ensuring that aphids were deterred from feeding but not poisoned. The LS strain of CMV did not induce feeding deterrence in Arabidopsis ecotype Col-0.
Inhibition of AGO1 by the 2b protein could act as a booby trap since this will trigger antibiosis against aphids. However, for Fny-CMV the interplay of three viral proteins (1a, 2a and 2b) appears to balance the need of the virus to inhibit antiviral silencing, while inducing a mild resistance (antixenosis) that is thought to promote transmission. The strain-specific effects of CMV on Arabidopsis-aphid interactions, and differences between the effects of Fny-CMV on this plant and those seen previously in tobacco (inhibition of resistance to aphids) may have important epidemiological consequences.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24349433</pmid><doi>10.1371/journal.pone.0083066</doi><tpages>e83066</tpages><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 1932-6203 |
ispartof | PloS one, 2013-12, Vol.8 (12), p.e83066 |
issn | 1932-6203 1932-6203 |
language | eng |
recordid | cdi_plos_journals_1467274330 |
source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
subjects | Accumulation Animals Antibiosis Antiviral agents Aphidoidea Aphids Aphids - physiology Aphids - virology Arabidopsis Arabidopsis - parasitology Arabidopsis - virology Arabidopsis thaliana Bioinformatics Biosynthesis Cucumovirus - metabolism Disease resistance Disease transmission DNA-directed RNA polymerase Epidemiology Feeding Feeding Behavior Flowers & plants Health aspects Host-Parasite Interactions Infection Infections Ingestion Inhibition Insects Migration Myzus persicae Physiological aspects Plant sciences Plant virus diseases Plant viruses Plants (botany) Plants (Organisms) Potatoes Process controls Proteins Replicase Ribonucleic acid RNA RNA-directed RNA polymerase RNA-mediated interference Signaling Studies Tobacco Viral proteins Viral Proteins - metabolism Virology Viruses |
title | A trio of viral proteins tunes aphid-plant interactions in Arabidopsis thaliana |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-21T13%3A46%3A33IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=A%20trio%20of%20viral%20proteins%20tunes%20aphid-plant%20interactions%20in%20Arabidopsis%20thaliana&rft.jtitle=PloS%20one&rft.au=Westwood,%20Jack%20H&rft.date=2013-12-11&rft.volume=8&rft.issue=12&rft.spage=e83066&rft.pages=e83066-&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0083066&rft_dat=%3Cgale_plos_%3EA478330513%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1467274330&rft_id=info:pmid/24349433&rft_galeid=A478330513&rft_doaj_id=oai_doaj_org_article_ad1084b05b7c496cb8b89c80c29d260c&rfr_iscdi=true |