A «Repertoire for Repertoire» Hypothesis: Repertoires of Type Three Effectors are Candidate Determinants of Host Specificity in Xanthomonas
Identifieur interne : 000A35 ( Ncbi/Merge ); précédent : 000A34; suivant : 000A36A «Repertoire for Repertoire» Hypothesis: Repertoires of Type Three Effectors are Candidate Determinants of Host Specificity in Xanthomonas
Auteurs : Ahmed Hajri [France] ; Chrystelle Brin [France] ; Gilles Hunault [France] ; Frédéric Lardeux [France] ; Christophe Lemaire [France] ; Charles Manceau [France] ; Tristan Boureau [France] ; Stéphane Poussier [France]Source :
- PLoS ONE [ 1932-6203 ] ; 2009.
Abstract
The genetic basis of host specificity for animal and plant pathogenic bacteria remains poorly understood. For plant pathogenic bacteria, host range is restricted to one or a few host plant species reflecting a tight adaptation to specific hosts.
Two hypotheses can be formulated to explain host specificity: either it can be explained by the phylogenetic position of the strains, or by the association of virulence genes enabling a pathological convergence of phylogenically distant strains. In this latter hypothesis, host specificity would result from the interaction between repertoires of bacterial virulence genes and repertoires of genes involved in host defences. To challenge these two hypotheses, we selected 132
These data provide insight into the potential role played by T3E genes for pathogenic bacteria and support a “repertoire for repertoire” hypothesis that may explain host specificity. Our work provides resources for functional and evolutionary studies aiming at understanding host specificity of pathogenic bacteria, functional redundancy between T3Es and the driving forces shaping T3E repertoires.
Url:
DOI: 10.1371/journal.pone.0006632
PubMed: 19680562
PubMed Central: 2722093
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<front><div type="abstract" xml:lang="en"><sec><title>Background</title>
<p>The genetic basis of host specificity for animal and plant pathogenic bacteria remains poorly understood. For plant pathogenic bacteria, host range is restricted to one or a few host plant species reflecting a tight adaptation to specific hosts.</p>
</sec>
<sec><title>Methodology/Principal Findings</title>
<p>Two hypotheses can be formulated to explain host specificity: either it can be explained by the phylogenetic position of the strains, or by the association of virulence genes enabling a pathological convergence of phylogenically distant strains. In this latter hypothesis, host specificity would result from the interaction between repertoires of bacterial virulence genes and repertoires of genes involved in host defences. To challenge these two hypotheses, we selected 132 <italic>Xanthomonas axonopodis</italic>
strains representative of 18 different pathovars which display different host range. First, the phylogenetic position of each strain was determined by sequencing the housekeeping gene <italic>rpoD</italic>
. This study showed that many pathovars of <italic>Xanthomonas axonopodis</italic>
are polyphyletic. Second, we investigated the distribution of 35 type III effector genes (T3Es) in these strains by both PCR and hybridization methods. Indeed, for pathogenic bacteria T3Es were shown to trigger and to subvert host defences. Our study revealed that T3E repertoires comprise core and variable gene suites that likely have distinct roles in pathogenicity and different evolutionary histories. Our results showed a correspondence between composition of T3E repertoires and pathovars of <italic>Xanthomonas axonopodis</italic>
. For polyphyletic pathovars, this suggests that T3E genes might explain a pathological convergence of phylogenetically distant strains. We also identified several DNA rearrangements within T3E genes, some of which correlate with host specificity of strains.</p>
</sec>
<sec><title>Conclusions/Significance</title>
<p>These data provide insight into the potential role played by T3E genes for pathogenic bacteria and support a “repertoire for repertoire” hypothesis that may explain host specificity. Our work provides resources for functional and evolutionary studies aiming at understanding host specificity of pathogenic bacteria, functional redundancy between T3Es and the driving forces shaping T3E repertoires.</p>
</sec>
</div>
</front>
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<author><name sortKey="Bonfield, Jk" uniqKey="Bonfield J">JK Bonfield</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Swofford, Dl" uniqKey="Swofford D">DL Swofford</name>
</author>
</analytic>
</biblStruct>
</listBibl>
</div1>
</back>
</TEI>
<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plosone</journal-id>
<journal-title-group><journal-title>PLoS ONE</journal-title>
</journal-title-group>
<issn pub-type="epub">1932-6203</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">19680562</article-id>
<article-id pub-id-type="pmc">2722093</article-id>
<article-id pub-id-type="publisher-id">09-PONE-RA-09855R1</article-id>
<article-id pub-id-type="doi">10.1371/journal.pone.0006632</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
<subj-group subj-group-type="Discipline"><subject>Evolutionary Biology</subject>
<subject>Evolutionary Biology/Microbial Evolution and Genomics</subject>
<subject>Microbiology/Plant-Biotic Interactions</subject>
</subj-group>
</article-categories>
<title-group><article-title>A «Repertoire for Repertoire» Hypothesis: Repertoires of Type Three Effectors are Candidate Determinants of Host Specificity in <italic>Xanthomonas</italic>
</article-title>
<alt-title alt-title-type="running-head"><italic>Xanthomonas</italic>
Host Specificity</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Hajri</surname>
<given-names>Ahmed</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Brin</surname>
<given-names>Chrystelle</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hunault</surname>
<given-names>Gilles</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lardeux</surname>
<given-names>Frédéric</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lemaire</surname>
<given-names>Christophe</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Manceau</surname>
<given-names>Charles</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author" equal-contrib="yes"><name><surname>Boureau</surname>
<given-names>Tristan</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>*</sup>
</xref>
</contrib>
<contrib contrib-type="author" equal-contrib="yes"><name><surname>Poussier</surname>
<given-names>Stéphane</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>*</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>1</label>
<addr-line>Département Santé des Plantes et Environnement, Institut National de la Recherche Agronomique (INRA), Beaucouzé, France</addr-line>
</aff>
<aff id="aff2"><label>2</label>
<addr-line>Département d'Informatique, Université d'Angers, Angers, France</addr-line>
</aff>
<aff id="aff3"><label>3</label>
<addr-line>Département de Biologie, Université d'Angers, Angers, Beaucouzé, France</addr-line>
</aff>
<aff id="aff4"><label>4</label>
<addr-line>Département de Sciences Biologiques, Agrocampus Ouest centre d'Angers, Institut National d'Horticulture et de Paysage (INHP), Beaucouzé, France</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Yang</surname>
<given-names>Ching-Hong</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1">University of Wisconsin-Milwaukee, United States of America</aff>
<author-notes><corresp id="cor1">* E-mail: <email>tristan.boureau@univ-angers.fr</email>
(TB); <email>stephane.poussier@agrocampus-ouest.fr</email>
(SP)</corresp>
<fn fn-type="con"><p>Conceived and designed the experiments: AH CM TB SPP. Performed the experiments: AH CB. Analyzed the data: AH GH FL CL CM TB SPP. Contributed reagents/materials/analysis tools: AH GH FL CL CM TB SPP. Wrote the paper: AH CL TB SPP.</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><year>2009</year>
</pub-date>
<pub-date pub-type="epub"><day>14</day>
<month>8</month>
<year>2009</year>
</pub-date>
<volume>4</volume>
<issue>8</issue>
<elocation-id>e6632</elocation-id>
<history><date date-type="received"><day>20</day>
<month>4</month>
<year>2009</year>
</date>
<date date-type="accepted"><day>9</day>
<month>7</month>
<year>2009</year>
</date>
</history>
<permissions><copyright-statement>Hajri et al. 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 credited.</copyright-statement>
</permissions>
<abstract><sec><title>Background</title>
<p>The genetic basis of host specificity for animal and plant pathogenic bacteria remains poorly understood. For plant pathogenic bacteria, host range is restricted to one or a few host plant species reflecting a tight adaptation to specific hosts.</p>
</sec>
<sec><title>Methodology/Principal Findings</title>
<p>Two hypotheses can be formulated to explain host specificity: either it can be explained by the phylogenetic position of the strains, or by the association of virulence genes enabling a pathological convergence of phylogenically distant strains. In this latter hypothesis, host specificity would result from the interaction between repertoires of bacterial virulence genes and repertoires of genes involved in host defences. To challenge these two hypotheses, we selected 132 <italic>Xanthomonas axonopodis</italic>
strains representative of 18 different pathovars which display different host range. First, the phylogenetic position of each strain was determined by sequencing the housekeeping gene <italic>rpoD</italic>
. This study showed that many pathovars of <italic>Xanthomonas axonopodis</italic>
are polyphyletic. Second, we investigated the distribution of 35 type III effector genes (T3Es) in these strains by both PCR and hybridization methods. Indeed, for pathogenic bacteria T3Es were shown to trigger and to subvert host defences. Our study revealed that T3E repertoires comprise core and variable gene suites that likely have distinct roles in pathogenicity and different evolutionary histories. Our results showed a correspondence between composition of T3E repertoires and pathovars of <italic>Xanthomonas axonopodis</italic>
. For polyphyletic pathovars, this suggests that T3E genes might explain a pathological convergence of phylogenetically distant strains. We also identified several DNA rearrangements within T3E genes, some of which correlate with host specificity of strains.</p>
</sec>
<sec><title>Conclusions/Significance</title>
<p>These data provide insight into the potential role played by T3E genes for pathogenic bacteria and support a “repertoire for repertoire” hypothesis that may explain host specificity. Our work provides resources for functional and evolutionary studies aiming at understanding host specificity of pathogenic bacteria, functional redundancy between T3Es and the driving forces shaping T3E repertoires.</p>
</sec>
</abstract>
<counts><page-count count="21"></page-count>
</counts>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>France</li>
</country>
<region><li>Pays de la Loire</li>
</region>
<settlement><li>Angers</li>
</settlement>
<orgName><li>Université d'Angers</li>
</orgName>
</list>
<tree><country name="France"><noRegion><name sortKey="Hajri, Ahmed" sort="Hajri, Ahmed" uniqKey="Hajri A" first="Ahmed" last="Hajri">Ahmed Hajri</name>
</noRegion>
<name sortKey="Boureau, Tristan" sort="Boureau, Tristan" uniqKey="Boureau T" first="Tristan" last="Boureau">Tristan Boureau</name>
<name sortKey="Brin, Chrystelle" sort="Brin, Chrystelle" uniqKey="Brin C" first="Chrystelle" last="Brin">Chrystelle Brin</name>
<name sortKey="Hunault, Gilles" sort="Hunault, Gilles" uniqKey="Hunault G" first="Gilles" last="Hunault">Gilles Hunault</name>
<name sortKey="Lardeux, Frederic" sort="Lardeux, Frederic" uniqKey="Lardeux F" first="Frédéric" last="Lardeux">Frédéric Lardeux</name>
<name sortKey="Lemaire, Christophe" sort="Lemaire, Christophe" uniqKey="Lemaire C" first="Christophe" last="Lemaire">Christophe Lemaire</name>
<name sortKey="Manceau, Charles" sort="Manceau, Charles" uniqKey="Manceau C" first="Charles" last="Manceau">Charles Manceau</name>
<name sortKey="Poussier, Stephane" sort="Poussier, Stephane" uniqKey="Poussier S" first="Stéphane" last="Poussier">Stéphane Poussier</name>
</country>
</tree>
</affiliations>
</record>
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