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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Veröffentlicht in:PloS one 2013-12, Vol.8 (12), p.e83066
Hauptverfasser: 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
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container_title PloS one
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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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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><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 &amp; 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. 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Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing &amp; Allied Health Database (Alumni Edition)</collection><collection>Meteorological &amp; Geoastrophysical Abstracts - Academic</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Nursing &amp; Allied Health Premium</collection><collection>Advanced Technologies &amp; Aerospace Database</collection><collection>ProQuest Advanced Technologies &amp; Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Westwood, Jack H</au><au>Groen, Simon C</au><au>Du, Zhiyou</au><au>Murphy, Alex M</au><au>Anggoro, Damar Tri</au><au>Tungadi, Trisna</au><au>Luang-In, Vijitra</au><au>Lewsey, Mathew G</au><au>Rossiter, John T</au><au>Powell, Glen</au><au>Smith, Alison G</au><au>Carr, John P</au><au>Rao, A.L.N.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A trio of viral proteins tunes aphid-plant interactions in Arabidopsis thaliana</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2013-12-11</date><risdate>2013</risdate><volume>8</volume><issue>12</issue><spage>e83066</spage><pages>e83066-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>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.</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>
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1932-6203
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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
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