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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 |
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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. |
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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.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0077393</identifier><identifier>PMID: 24155951</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>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</subject><ispartof>PloS one, 2013-10, Vol.8 (10), p.e77393</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Shapiro et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://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. 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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.</description><subject>Acalymma vittatum</subject><subject>Analysis</subject><subject>Analysis of Variance</subject><subject>Animals</subject><subject>Antagonists</subject><subject>Arthropoda</subject><subject>Beetles</subject><subject>Coleoptera</subject><subject>Coleoptera - physiology</subject><subject>Crosstalk</subject><subject>Cucumis</subject><subject>Cucurbita - drug effects</subject><subject>Cucurbita - immunology</subject><subject>Cucurbita - microbiology</subject><subject>Cucurbita - virology</subject><subject>Cucurbita foetidissima</subject><subject>Cucurbita pepo texana</subject><subject>Cucurbitaceae</subject><subject>Defense industry</subject><subject>Disease resistance</subject><subject>Disease Resistance - drug effects</subject><subject>Disease Resistance - immunology</subject><subject>Disease Susceptibility</subject><subject>Ecological effects</subject><subject>Ecology</subject><subject>Epidemiology</subject><subject>Erwinia - drug effects</subject><subject>Erwinia - physiology</subject><subject>Erwinia amylovora</subject><subject>Erwinia tracheiphila</subject><subject>Flowers & plants</subject><subject>Gibberellins</subject><subject>Health aspects</subject><subject>Herbivores</subject><subject>Herbivory</subject><subject>Herbivory - drug effects</subject><subject>Host plants</subject><subject>Host-Pathogen Interactions - drug effects</subject><subject>Host-Pathogen Interactions - immunology</subject><subject>Infection</subject><subject>Infections</subject><subject>Microbial drug resistance</subject><subject>Natural environment</subject><subject>Pathogens</subject><subject>Plant bacterial diseases</subject><subject>Plant diseases</subject><subject>Plant Diseases - immunology</subject><subject>Plant Diseases - microbiology</subject><subject>Plant Diseases - virology</subject><subject>Plant Growth Regulators - pharmacology</subject><subject>Plant hormones</subject><subject>Plant resistance</subject><subject>Plant virus diseases</subject><subject>Potyvirus - drug effects</subject><subject>Potyvirus - physiology</subject><subject>Pseudomonas syringae</subject><subject>Salicylic Acid - pharmacology</subject><subject>Time Factors</subject><subject>Vectors</subject><subject>Vegetables</subject><subject>Viruses</subject><subject>Wilt</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNqNU1uL1DAULqK46-o_EA0Igg8zNkmbtD4Iy3obWFjw9hrS9GQmS6cZk3Rdf47_1NOd7jIFBWmhPcl3OXzJybKnNF9SLunrSz-EXnfLne9hmedS8prfy45pzdlCsJzfP_g_yh7FeJnnJa-EeJgdsYKWZV3S4-z3OxdBRyCuTxC0Sc73EQuiSdzoAC3Z-JjIrtN9ekPAWjApEm_JLsACrl1Mrl-TKxd0h6xxFwUIvmYwQ2jcRCUtWOjRJkDEhiNEovt2rFBB9wZI8qRBewgOlX66Din7zh5nD6zuIjyZvifZtw_vv559WpxffFydnZ4vjCyrtGBlDQA5Fa2spdAaa2PaumgZUNtYpq2pQVAjaK1Z3rZS08ogsBEWmGw4P8me73V3nY9qSjcqWhQUQ2NVhYjVHtF6fal2wW11-KW8dupmwYe10iE504FidPSSeACaFja3FS0xc87LBp1F0aDW28ltaLbQGugTRjgTne_0bqPW_kpxWYuiHJt5MQkE_2OAmP7R8oRaa-wKD8ijmNm6aNRpISsmmZAUUcu_oPBpYesM3i_rcH1GeDUjICbBdVrrIUa1-vL5_7EX3-fYlwfYDegubaLvhptbOQcWe6AJPsYA9i45mqtxPG7TUON4qGk8kPbsMPU70u088D8_fQ6T</recordid><startdate>20131014</startdate><enddate>20131014</enddate><creator>Shapiro, Lori R</creator><creator>Salvaudon, Lucie</creator><creator>Mauck, Kerry E</creator><creator>Pulido, Hannier</creator><creator>De Moraes, Consuelo M</creator><creator>Stephenson, Andrew G</creator><creator>Mescher, Mark C</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20131014</creationdate><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</title><author>Shapiro, Lori R ; Salvaudon, Lucie ; Mauck, Kerry E ; Pulido, Hannier ; De Moraes, Consuelo M ; Stephenson, Andrew G ; Mescher, Mark C</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c758t-259eee016d7976aa259ccd94d2e1fbf2afc9e61c619a20dd7a18c76ab6fe27b33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Acalymma vittatum</topic><topic>Analysis</topic><topic>Analysis of Variance</topic><topic>Animals</topic><topic>Antagonists</topic><topic>Arthropoda</topic><topic>Beetles</topic><topic>Coleoptera</topic><topic>Coleoptera - 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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> |
fulltext | fulltext |
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 |
url | http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-19T11%3A13%3A02IST&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=Disease%20interactions%20in%20a%20shared%20host%20plant:%20effects%20of%20pre-existing%20viral%20infection%20on%20cucurbit%20plant%20defense%20responses%20and%20resistance%20to%20bacterial%20wilt%20disease&rft.jtitle=PloS%20one&rft.au=Shapiro,%20Lori%20R&rft.date=2013-10-14&rft.volume=8&rft.issue=10&rft.spage=e77393&rft.pages=e77393-&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0077393&rft_dat=%3Cgale_plos_%3EA478272671%3C/gale_plos_%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c758t-259eee016d7976aa259ccd94d2e1fbf2afc9e61c619a20dd7a18c76ab6fe27b33%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=1441866288&rft_id=info:pmid/24155951&rft_galeid=A478272671&rfr_iscdi=true |