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Disease interactions in a shared host plant: effects of pre-existing viral infection on cucurbit plant defense responses and resistance to bacterial wilt disease

Both biotic and abiotic stressors can elicit broad-spectrum plant resistance against subsequent pathogen challenges. However, we currently have little understanding of how such effects influence broader aspects of disease ecology and epidemiology in natural environments where plants interact with mu...

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Published in:PloS one 2013-10, Vol.8 (10), p.e77393
Main Authors: Shapiro, Lori R, Salvaudon, Lucie, Mauck, Kerry E, Pulido, Hannier, De Moraes, Consuelo M, Stephenson, Andrew G, Mescher, Mark C
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Salvaudon, Lucie
Mauck, Kerry E
Pulido, Hannier
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Mescher, Mark C
description Both biotic and abiotic stressors can elicit broad-spectrum plant resistance against subsequent pathogen challenges. However, we currently have little understanding of how such effects influence broader aspects of disease ecology and epidemiology in natural environments where plants interact with multiple antagonists simultaneously. In previous work, we have shown that healthy wild gourd plants (Cucurbita pepo ssp. texana) contract a fatal bacterial wilt infection (caused by Erwinia tracheiphila) at significantly higher rates than plants infected with Zucchini yellow mosaic virus (ZYMV). We recently reported evidence that this pattern is explained, at least in part, by reduced visitation of ZYMV-infected plants by the cucumber beetle vectors of E. tracheiphila. Here we examine whether ZYMV-infection may also directly elicit plant resistance to subsequent E. tracheiphila infection. In laboratory studies, we assayed the induction of key phytohormones (SA and JA) in single and mixed infections of these pathogens, as well as in response to the feeding of A. vittatum cucumber beetles on healthy and infected plants. We also tracked the incidence and progression of wilt disease symptoms in plants with prior ZYMV infections. Our results indicate that ZYMV-infection slightly delays the progression of wilt symptoms, but does not significantly reduce E. tracheiphila infection success. This observation supports the hypothesis that reduced rates of wilt disease in ZYMV-infected plants reflect reduced visitation by beetle vectors. We also documented consistently strong SA responses to ZYMV infection, but limited responses to E. tracheiphila in the absence of ZYMV, suggesting that the latter pathogen may effectively evade or suppress plant defenses, although we observed no evidence of antagonistic cross-talk between SA and JA signaling pathways. We did, however, document effects of E. tracheiphila on induced responses to herbivory that may influence host-plant quality for (and hence pathogen acquisition by) cucumber beetles.
doi_str_mv 10.1371/journal.pone.0077393
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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>Agriculture Science Database</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>ProQuest Biological Science Journals</collection><collection>Engineering Database</collection><collection>Nursing &amp; Allied Health Premium</collection><collection>ProQuest advanced technologies &amp; aerospace journals</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>Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Shapiro, Lori R</au><au>Salvaudon, Lucie</au><au>Mauck, Kerry E</au><au>Pulido, Hannier</au><au>De Moraes, Consuelo M</au><au>Stephenson, Andrew G</au><au>Mescher, Mark C</au><au>Desneux, Nicolas</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Disease interactions in a shared host plant: effects of pre-existing viral infection on cucurbit plant defense responses and resistance to bacterial wilt disease</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2013-10-14</date><risdate>2013</risdate><volume>8</volume><issue>10</issue><spage>e77393</spage><pages>e77393-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Both biotic and abiotic stressors can elicit broad-spectrum plant resistance against subsequent pathogen challenges. However, we currently have little understanding of how such effects influence broader aspects of disease ecology and epidemiology in natural environments where plants interact with multiple antagonists simultaneously. In previous work, we have shown that healthy wild gourd plants (Cucurbita pepo ssp. texana) contract a fatal bacterial wilt infection (caused by Erwinia tracheiphila) at significantly higher rates than plants infected with Zucchini yellow mosaic virus (ZYMV). We recently reported evidence that this pattern is explained, at least in part, by reduced visitation of ZYMV-infected plants by the cucumber beetle vectors of E. tracheiphila. Here we examine whether ZYMV-infection may also directly elicit plant resistance to subsequent E. tracheiphila infection. In laboratory studies, we assayed the induction of key phytohormones (SA and JA) in single and mixed infections of these pathogens, as well as in response to the feeding of A. vittatum cucumber beetles on healthy and infected plants. We also tracked the incidence and progression of wilt disease symptoms in plants with prior ZYMV infections. Our results indicate that ZYMV-infection slightly delays the progression of wilt symptoms, but does not significantly reduce E. tracheiphila infection success. This observation supports the hypothesis that reduced rates of wilt disease in ZYMV-infected plants reflect reduced visitation by beetle vectors. We also documented consistently strong SA responses to ZYMV infection, but limited responses to E. tracheiphila in the absence of ZYMV, suggesting that the latter pathogen may effectively evade or suppress plant defenses, although we observed no evidence of antagonistic cross-talk between SA and JA signaling pathways. We did, however, document effects of E. tracheiphila on induced responses to herbivory that may influence host-plant quality for (and hence pathogen acquisition by) cucumber beetles.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24155951</pmid><doi>10.1371/journal.pone.0077393</doi><tpages>e77393</tpages><oa>free_for_read</oa></addata></record>
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identifier ISSN: 1932-6203
ispartof PloS one, 2013-10, Vol.8 (10), p.e77393
issn 1932-6203
1932-6203
language eng
recordid cdi_plos_journals_1441866288
source PubMed (Medline); Publicly Available Content Database
subjects Acalymma vittatum
Analysis
Analysis of Variance
Animals
Antagonists
Arthropoda
Beetles
Coleoptera
Coleoptera - physiology
Crosstalk
Cucumis
Cucurbita - drug effects
Cucurbita - immunology
Cucurbita - microbiology
Cucurbita - virology
Cucurbita foetidissima
Cucurbita pepo texana
Cucurbitaceae
Defense industry
Disease resistance
Disease Resistance - drug effects
Disease Resistance - immunology
Disease Susceptibility
Ecological effects
Ecology
Epidemiology
Erwinia - drug effects
Erwinia - physiology
Erwinia amylovora
Erwinia tracheiphila
Flowers & plants
Gibberellins
Health aspects
Herbivores
Herbivory
Herbivory - drug effects
Host plants
Host-Pathogen Interactions - drug effects
Host-Pathogen Interactions - immunology
Infection
Infections
Microbial drug resistance
Natural environment
Pathogens
Plant bacterial diseases
Plant diseases
Plant Diseases - immunology
Plant Diseases - microbiology
Plant Diseases - virology
Plant Growth Regulators - pharmacology
Plant hormones
Plant resistance
Plant virus diseases
Potyvirus - drug effects
Potyvirus - physiology
Pseudomonas syringae
Salicylic Acid - pharmacology
Time Factors
Vectors
Vegetables
Viruses
Wilt
title Disease interactions in a shared host plant: effects of pre-existing viral infection on cucurbit plant defense responses and resistance to bacterial wilt disease
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