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Induced Release of a Plant-Defense Volatile ‘Deceptively’ Attracts Insect Vectors to Plants Infected with a Bacterial Pathogen

Identifieur interne : 000C81 ( Pmc/Checkpoint ); précédent : 000C80; suivant : 000C82

Induced Release of a Plant-Defense Volatile ‘Deceptively’ Attracts Insect Vectors to Plants Infected with a Bacterial Pathogen

Auteurs : Rajinder S. Mann [États-Unis] ; Jared G. Ali [États-Unis] ; Sara L. Hermann [États-Unis] ; Siddharth Tiwari [États-Unis] ; Kirsten S. Pelz-Stelinski [États-Unis] ; Hans T. Alborn [États-Unis] ; Lukasz L. Stelinski [États-Unis]

Source :

RBID : PMC:3310815

Abstract

Transmission of plant pathogens by insect vectors is a complex biological process involving interactions between the plant, insect, and pathogen. Pathogen-induced plant responses can include changes in volatile and nonvolatile secondary metabolites as well as major plant nutrients. Experiments were conducted to understand how a plant pathogenic bacterium, Candidatus Liberibacter asiaticus (Las), affects host preference behavior of its psyllid (Diaphorina citri Kuwayama) vector. D. citri were attracted to volatiles from pathogen-infected plants more than to those from non-infected counterparts. Las-infected plants were more attractive to D. citri adults than non-infected plants initially; however after feeding, psyllids subsequently dispersed to non-infected rather than infected plants as their preferred settling point. Experiments with Las-infected and non-infected plants under complete darkness yielded similar results to those recorded under light. The behavior of psyllids in response to infected versus non-infected plants was not influenced by whether or not they were carriers of the pathogen. Quantification of volatile release from non-infected and infected plants supported the hypothesis that odorants mediate psyllid preference. Significantly more methyl salicylate, yet less methyl anthranilate and D-limonene, was released by infected than non-infected plants. Methyl salicylate was attractive to psyllids, while methyl anthranilate did not affect their behavior. Feeding on citrus by D. citri adults also induced release of methyl salicylate, suggesting that it may be a cue revealing location of conspecifics on host plants. Infected plants were characterized by lower levels of nitrogen, phosphorus, sulfur, zinc, and iron, as well as, higher levels of potassium and boron than non-infected plants. Collectively, our results suggest that host selection behavior of D. citri may be modified by bacterial infection of plants, which alters release of specific headspace volatiles and plant nutritional contents. Furthermore, we show in a laboratory setting that this apparent pathogen-mediated manipulation of vector behavior may facilitate pathogen spread.


Url:
DOI: 10.1371/journal.ppat.1002610
PubMed: 22457628
PubMed Central: 3310815


Affiliations:


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PMC:3310815

Le document en format XML

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<p>Transmission of plant pathogens by insect vectors is a complex biological process involving interactions between the plant, insect, and pathogen. Pathogen-induced plant responses can include changes in volatile and nonvolatile secondary metabolites as well as major plant nutrients. Experiments were conducted to understand how a plant pathogenic bacterium,
<italic>Candidatus</italic>
Liberibacter asiaticus (Las), affects host preference behavior of its psyllid (
<italic>Diaphorina citri</italic>
Kuwayama) vector.
<italic>D. citri</italic>
were attracted to volatiles from pathogen-infected plants more than to those from non-infected counterparts. Las-infected plants were more attractive to
<italic>D. citri</italic>
adults than non-infected plants initially; however after feeding, psyllids subsequently dispersed to non-infected rather than infected plants as their preferred settling point. Experiments with Las-infected and non-infected plants under complete darkness yielded similar results to those recorded under light. The behavior of psyllids in response to infected versus non-infected plants was not influenced by whether or not they were carriers of the pathogen. Quantification of volatile release from non-infected and infected plants supported the hypothesis that odorants mediate psyllid preference. Significantly more methyl salicylate, yet less methyl anthranilate and D-limonene, was released by infected than non-infected plants. Methyl salicylate was attractive to psyllids, while methyl anthranilate did not affect their behavior. Feeding on citrus by
<italic>D. citri</italic>
adults also induced release of methyl salicylate, suggesting that it may be a cue revealing location of conspecifics on host plants. Infected plants were characterized by lower levels of nitrogen, phosphorus, sulfur, zinc, and iron, as well as, higher levels of potassium and boron than non-infected plants. Collectively, our results suggest that host selection behavior of
<italic>D. citri</italic>
may be modified by bacterial infection of plants, which alters release of specific headspace volatiles and plant nutritional contents. Furthermore, we show in a laboratory setting that this apparent pathogen-mediated manipulation of vector behavior may facilitate pathogen spread.</p>
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<pmc article-type="research-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">PLoS Pathog</journal-id>
<journal-id journal-id-type="iso-abbrev">PLoS Pathog</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plospath</journal-id>
<journal-title-group>
<journal-title>PLoS Pathogens</journal-title>
</journal-title-group>
<issn pub-type="ppub">1553-7366</issn>
<issn pub-type="epub">1553-7374</issn>
<publisher>
<publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">22457628</article-id>
<article-id pub-id-type="pmc">3310815</article-id>
<article-id pub-id-type="publisher-id">PPATHOGENS-D-11-02137</article-id>
<article-id pub-id-type="doi">10.1371/journal.ppat.1002610</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Research Article</subject>
</subj-group>
<subj-group subj-group-type="Discipline-v2">
<subject>Agriculture</subject>
<subj-group>
<subject>Crops</subject>
</subj-group>
<subj-group>
<subject>Pest Control</subject>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v2">
<subject>Biology</subject>
<subj-group>
<subject>Ecology</subject>
</subj-group>
<subj-group>
<subject>Plant Science</subject>
</subj-group>
<subj-group>
<subject>Zoology</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Induced Release of a Plant-Defense Volatile ‘Deceptively’ Attracts Insect Vectors to Plants Infected with a Bacterial Pathogen</article-title>
<alt-title alt-title-type="running-head">Attraction of Vectors to Induced Plant Volatile</alt-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Mann</surname>
<given-names>Rajinder S.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Ali</surname>
<given-names>Jared G.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Hermann</surname>
<given-names>Sara L.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Tiwari</surname>
<given-names>Siddharth</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Pelz-Stelinski</surname>
<given-names>Kirsten S.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Alborn</surname>
<given-names>Hans T.</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Stelinski</surname>
<given-names>Lukasz L.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="corresp" rid="cor1">
<sup>*</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1">
<label>1</label>
<addr-line>University of Florida, Entomology and Nematology Department, Citrus Research and Education Center, Lake Alfred, Florida, United States of America</addr-line>
</aff>
<aff id="aff2">
<label>2</label>
<addr-line>Center for Medical, Agricultural, and Veterinary Entomology, Agricultural Research Service, U.S. Department of Agriculture, Gainesville, Florida, United States of America</addr-line>
</aff>
<contrib-group>
<contrib contrib-type="editor">
<name>
<surname>Eigenbrode</surname>
<given-names>Sanford</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1">University of Idaho, United States of America</aff>
<author-notes>
<corresp id="cor1">* E-mail:
<email>stelinski@ufl.edu</email>
</corresp>
<fn fn-type="con">
<p>Conceived and designed the experiments: LLS RSM JGA. Performed the experiments: RSM JGA SLH. Analyzed the data: RSM JGA KSPS LLS. Contributed reagents/materials/analysis tools: RSM KSPS ST HTA LLS. Wrote the paper: RSM LLS KSPS JGA.</p>
</fn>
</author-notes>
<pub-date pub-type="collection">
<month>3</month>
<year>2012</year>
</pub-date>
<pmc-comment> Fake ppub added to accomodate plos workflow change from 03/2008 and 03/2009 </pmc-comment>
<pub-date pub-type="ppub">
<month>3</month>
<year>2012</year>
</pub-date>
<pub-date pub-type="epub">
<day>22</day>
<month>3</month>
<year>2012</year>
</pub-date>
<volume>8</volume>
<issue>3</issue>
<elocation-id>e1002610</elocation-id>
<history>
<date date-type="received">
<day>27</day>
<month>9</month>
<year>2011</year>
</date>
<date date-type="accepted">
<day>13</day>
<month>2</month>
<year>2012</year>
</date>
</history>
<permissions>
<copyright-statement>This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.</copyright-statement>
<copyright-year>2012</copyright-year>
</permissions>
<abstract>
<p>Transmission of plant pathogens by insect vectors is a complex biological process involving interactions between the plant, insect, and pathogen. Pathogen-induced plant responses can include changes in volatile and nonvolatile secondary metabolites as well as major plant nutrients. Experiments were conducted to understand how a plant pathogenic bacterium,
<italic>Candidatus</italic>
Liberibacter asiaticus (Las), affects host preference behavior of its psyllid (
<italic>Diaphorina citri</italic>
Kuwayama) vector.
<italic>D. citri</italic>
were attracted to volatiles from pathogen-infected plants more than to those from non-infected counterparts. Las-infected plants were more attractive to
<italic>D. citri</italic>
adults than non-infected plants initially; however after feeding, psyllids subsequently dispersed to non-infected rather than infected plants as their preferred settling point. Experiments with Las-infected and non-infected plants under complete darkness yielded similar results to those recorded under light. The behavior of psyllids in response to infected versus non-infected plants was not influenced by whether or not they were carriers of the pathogen. Quantification of volatile release from non-infected and infected plants supported the hypothesis that odorants mediate psyllid preference. Significantly more methyl salicylate, yet less methyl anthranilate and D-limonene, was released by infected than non-infected plants. Methyl salicylate was attractive to psyllids, while methyl anthranilate did not affect their behavior. Feeding on citrus by
<italic>D. citri</italic>
adults also induced release of methyl salicylate, suggesting that it may be a cue revealing location of conspecifics on host plants. Infected plants were characterized by lower levels of nitrogen, phosphorus, sulfur, zinc, and iron, as well as, higher levels of potassium and boron than non-infected plants. Collectively, our results suggest that host selection behavior of
<italic>D. citri</italic>
may be modified by bacterial infection of plants, which alters release of specific headspace volatiles and plant nutritional contents. Furthermore, we show in a laboratory setting that this apparent pathogen-mediated manipulation of vector behavior may facilitate pathogen spread.</p>
</abstract>
<abstract abstract-type="summary">
<title>Author Summary</title>
<p>In this investigation, we experimentally demonstrate specific mechanisms through which a bacterial plant pathogen induces plant responses that modify behavior of its insect vector.
<italic>Candidatus</italic>
Liberibacter asiaticus, a fastidious, phloem-limited bacterium responsible for causing huanglongbing disease of citrus, induced release of a specific volatile chemical, methyl salicylate, which increased attractiveness of infected plants to its insect vector,
<italic>Diaphorina citri</italic>
, and caused vectors to initially prefer infected plants. However, the insect vectors subsequently dispersed to non-infected plants as their preferred location of prolonged settling because of likely sub-optimal nutritional content of infected plants. The duration of initial feeding on infected plants was sufficiently long for the vectors to acquire the pathogen before they dispersed to non-infected plants, suggesting that the bacterial pathogen manipulates behavior of its insect vector to promote its own proliferation. The behavior of psyllids in response to infected versus non-infected plants was not influenced by whether or not they were carriers of the pathogen and was similar under both light and dark conditions. Feeding on citrus by
<italic>D. citri</italic>
adults also induced the release of methyl salicylate, suggesting that it may be a cue revealing location of conspecifics on host plants.</p>
</abstract>
<counts>
<page-count count="13"></page-count>
</counts>
</article-meta>
</front>
</pmc>
<affiliations>
<list>
<country>
<li>États-Unis</li>
</country>
<region>
<li>Floride</li>
</region>
</list>
<tree>
<country name="États-Unis">
<region name="Floride">
<name sortKey="Mann, Rajinder S" sort="Mann, Rajinder S" uniqKey="Mann R" first="Rajinder S." last="Mann">Rajinder S. Mann</name>
</region>
<name sortKey="Alborn, Hans T" sort="Alborn, Hans T" uniqKey="Alborn H" first="Hans T." last="Alborn">Hans T. Alborn</name>
<name sortKey="Ali, Jared G" sort="Ali, Jared G" uniqKey="Ali J" first="Jared G." last="Ali">Jared G. Ali</name>
<name sortKey="Hermann, Sara L" sort="Hermann, Sara L" uniqKey="Hermann S" first="Sara L." last="Hermann">Sara L. Hermann</name>
<name sortKey="Pelz Stelinski, Kirsten S" sort="Pelz Stelinski, Kirsten S" uniqKey="Pelz Stelinski K" first="Kirsten S." last="Pelz-Stelinski">Kirsten S. Pelz-Stelinski</name>
<name sortKey="Stelinski, Lukasz L" sort="Stelinski, Lukasz L" uniqKey="Stelinski L" first="Lukasz L." last="Stelinski">Lukasz L. Stelinski</name>
<name sortKey="Tiwari, Siddharth" sort="Tiwari, Siddharth" uniqKey="Tiwari S" first="Siddharth" last="Tiwari">Siddharth Tiwari</name>
</country>
</tree>
</affiliations>
</record>

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