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A Trio of Viral Proteins Tunes Aphid-Plant Interactions in Arabidopsis thaliana
BACKGROUND: 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 o...
Autores principales: | , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2013
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3859657/ https://www.ncbi.nlm.nih.gov/pubmed/24349433 http://dx.doi.org/10.1371/journal.pone.0083066 |
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author | 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. |
author_facet | 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. |
author_sort | Westwood, Jack H. |
collection | PubMed |
description | BACKGROUND: 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’). METHODOLOGY/PRINCIPAL FINDINGS: 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. CONCLUSIONS/SIGNIFICANCE: 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. |
format | Online Article Text |
id | pubmed-3859657 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2013 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-38596572013-12-13 A Trio of Viral Proteins Tunes Aphid-Plant Interactions in Arabidopsis thaliana 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. PLoS One Research Article BACKGROUND: 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’). METHODOLOGY/PRINCIPAL FINDINGS: 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. CONCLUSIONS/SIGNIFICANCE: 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. Public Library of Science 2013-12-11 /pmc/articles/PMC3859657/ /pubmed/24349433 http://dx.doi.org/10.1371/journal.pone.0083066 Text en © 2013 Westwood 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, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited. |
spellingShingle | Research Article 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. A Trio of Viral Proteins Tunes Aphid-Plant Interactions in Arabidopsis thaliana |
title | A Trio of Viral Proteins Tunes Aphid-Plant Interactions in Arabidopsis thaliana
|
title_full | A Trio of Viral Proteins Tunes Aphid-Plant Interactions in Arabidopsis thaliana
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title_fullStr | A Trio of Viral Proteins Tunes Aphid-Plant Interactions in Arabidopsis thaliana
|
title_full_unstemmed | A Trio of Viral Proteins Tunes Aphid-Plant Interactions in Arabidopsis thaliana
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title_short | A Trio of Viral Proteins Tunes Aphid-Plant Interactions in Arabidopsis thaliana
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title_sort | trio of viral proteins tunes aphid-plant interactions in arabidopsis thaliana |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3859657/ https://www.ncbi.nlm.nih.gov/pubmed/24349433 http://dx.doi.org/10.1371/journal.pone.0083066 |
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