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Genomes of three tomato pathogens within the Ralstonia solanacearum species complex reveal significant evolutionary divergence

Identifieur interne : 000811 ( Ncbi/Checkpoint ); précédent : 000810; suivant : 000812

Genomes of three tomato pathogens within the Ralstonia solanacearum species complex reveal significant evolutionary divergence

Auteurs : Benoît Remenant [France] ; Bénédicte Coupat-Goutaland [France] ; Alice Guidot [France] ; Gilles Cellier [France] ; Emmanuel Wicker [France] ; Caitilyn Allen [États-Unis] ; Mark Fegan [Australie] ; Olivier Pruvost [France] ; Mounira Elbaz [France] ; Alexandra Calteau [France] ; Gregory Salvignol [France] ; Damien Mornico [France] ; Sophie Mangenot [France] ; Valérie Barbe [France] ; Claudine Médigue [France] ; Philippe Prior [France]

Source :

RBID : PMC:2900269

Abstract

Background

The Ralstonia solanacearum species complex includes thousands of strains pathogenic to an unusually wide range of plant species. These globally dispersed and heterogeneous strains cause bacterial wilt diseases, which have major socio-economic impacts. Pathogenicity is an ancestral trait in R. solanacearum and strains with high genetic variation can be subdivided into four phylotypes, correlating to isolates from Asia (phylotype I), the Americas (phylotype IIA and IIB), Africa (phylotype III) and Indonesia (phylotype IV). Comparison of genome sequences strains representative of this phylogenetic diversity can help determine which traits allow this bacterium to be such a pathogen of so many different plant species and how the bacteria survive in many different habitats.

Results

The genomes of three tomato bacterial wilt pathogens, CFBP2957 (phy. IIA), CMR15 (phy. III) and PSI07 (phy. IV) were sequenced and manually annotated. These genomes were compared with those of three previously sequenced R. solanacearum strains: GMI1000 (tomato, phy. I), IPO1609 (potato, phy. IIB), and Molk2 (banana, phy. IIB). The major genomic features (size, G+C content, number of genes) were conserved across all of the six sequenced strains. Despite relatively high genetic distances (calculated from average nucleotide identity) and many genomic rearrangements, more than 60% of the genes of the megaplasmid and 70% of those on the chromosome are syntenic. The three new genomic sequences revealed the presence of several previously unknown traits, probably acquired by horizontal transfers, within the genomes of R. solanacearum, including a type IV secretion system, a rhi-type anti-mitotic toxin and two small plasmids. Genes involved in virulence appear to be evolving at a faster rate than the genome as a whole.

Conclusions

Comparative analysis of genome sequences and gene content confirmed the differentiation of R. solanacearum species complex strains into four phylotypes. Genetic distances between strains, in conjunction with CGH analysis of a larger set of strains, revealed differences great enough to consider reclassification of the R. solanacearum species complex into three species. The data are still too fragmentary to link genomic classification and phenotypes, but these new genome sequences identify a pan-genome more representative of the diversity in the R. solanancearum species complex.


Url:
DOI: 10.1186/1471-2164-11-379
PubMed: 20550686
PubMed Central: 2900269


Affiliations:


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PMC:2900269

Le document en format XML

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<name sortKey="Barbe, Valerie" sort="Barbe, Valerie" uniqKey="Barbe V" first="Valérie" last="Barbe">Valérie Barbe</name>
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<name sortKey="Prior, Philippe" sort="Prior, Philippe" uniqKey="Prior P" first="Philippe" last="Prior">Philippe Prior</name>
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<title xml:lang="en" level="a" type="main">Genomes of three tomato pathogens within the
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<name sortKey="Guidot, Alice" sort="Guidot, Alice" uniqKey="Guidot A" first="Alice" last="Guidot">Alice Guidot</name>
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<name sortKey="Cellier, Gilles" sort="Cellier, Gilles" uniqKey="Cellier G" first="Gilles" last="Cellier">Gilles Cellier</name>
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<name sortKey="Wicker, Emmanuel" sort="Wicker, Emmanuel" uniqKey="Wicker E" first="Emmanuel" last="Wicker">Emmanuel Wicker</name>
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<nlm:aff id="I1">CIRAD, UMR Peuplements Végétaux et Bioagresseurs en Milieu Tropical, Saint Pierre F-97410, La Réunion, France</nlm:aff>
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<name sortKey="Allen, Caitilyn" sort="Allen, Caitilyn" uniqKey="Allen C" first="Caitilyn" last="Allen">Caitilyn Allen</name>
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<nlm:aff id="I5">University of Wisconsin-Madison, Department of Plant Pathology, 1630 Linden Drive, Madison, WI 53706, USA</nlm:aff>
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<name sortKey="Fegan, Mark" sort="Fegan, Mark" uniqKey="Fegan M" first="Mark" last="Fegan">Mark Fegan</name>
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<nlm:aff id="I6">Biosciences Research Division, Department of Primary Industries, 475 Mickleham Rd, Attwood, VIC, 3049, Australia</nlm:aff>
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<wicri:regionArea>Biosciences Research Division, Department of Primary Industries, 475 Mickleham Rd, Attwood, VIC, 3049</wicri:regionArea>
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<name sortKey="Pruvost, Olivier" sort="Pruvost, Olivier" uniqKey="Pruvost O" first="Olivier" last="Pruvost">Olivier Pruvost</name>
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<nlm:aff id="I1">CIRAD, UMR Peuplements Végétaux et Bioagresseurs en Milieu Tropical, Saint Pierre F-97410, La Réunion, France</nlm:aff>
<country xml:lang="fr">France</country>
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<name sortKey="Elbaz, Mounira" sort="Elbaz, Mounira" uniqKey="Elbaz M" first="Mounira" last="Elbaz">Mounira Elbaz</name>
<affiliation wicri:level="1">
<nlm:aff id="I3">CNRS-INRA, Laboratoire Interactions Plantes-Microorganismes, UMR2594, BP52627, Castanet-Tolosan F-31326, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>CNRS-INRA, Laboratoire Interactions Plantes-Microorganismes, UMR2594, BP52627, Castanet-Tolosan F-31326</wicri:regionArea>
<wicri:noRegion>31326</wicri:noRegion>
<wicri:noRegion>31326</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Calteau, Alexandra" sort="Calteau, Alexandra" uniqKey="Calteau A" first="Alexandra" last="Calteau">Alexandra Calteau</name>
<affiliation wicri:level="1">
<nlm:aff id="I7">CNRS-UMR 8030, Laboratoire d'Analyse Bioinformatique en Génomique et Métabolisme, Commissariat à l'Energie Atomique (CEA), Direction des Sciences du Vivant, Institut de Génomique, Genoscope, 2 rue Gaston Crémieux, 91057 Evry Cedex, Evry cedex F-91006, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>CNRS-UMR 8030, Laboratoire d'Analyse Bioinformatique en Génomique et Métabolisme, Commissariat à l'Energie Atomique (CEA), Direction des Sciences du Vivant, Institut de Génomique, Genoscope, 2 rue Gaston Crémieux, 91057 Evry Cedex, Evry cedex F-91006</wicri:regionArea>
<wicri:noRegion>91006</wicri:noRegion>
<wicri:noRegion>91006</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Salvignol, Gregory" sort="Salvignol, Gregory" uniqKey="Salvignol G" first="Gregory" last="Salvignol">Gregory Salvignol</name>
<affiliation wicri:level="1">
<nlm:aff id="I7">CNRS-UMR 8030, Laboratoire d'Analyse Bioinformatique en Génomique et Métabolisme, Commissariat à l'Energie Atomique (CEA), Direction des Sciences du Vivant, Institut de Génomique, Genoscope, 2 rue Gaston Crémieux, 91057 Evry Cedex, Evry cedex F-91006, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>CNRS-UMR 8030, Laboratoire d'Analyse Bioinformatique en Génomique et Métabolisme, Commissariat à l'Energie Atomique (CEA), Direction des Sciences du Vivant, Institut de Génomique, Genoscope, 2 rue Gaston Crémieux, 91057 Evry Cedex, Evry cedex F-91006</wicri:regionArea>
<wicri:noRegion>91006</wicri:noRegion>
<wicri:noRegion>91006</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Mornico, Damien" sort="Mornico, Damien" uniqKey="Mornico D" first="Damien" last="Mornico">Damien Mornico</name>
<affiliation wicri:level="1">
<nlm:aff id="I7">CNRS-UMR 8030, Laboratoire d'Analyse Bioinformatique en Génomique et Métabolisme, Commissariat à l'Energie Atomique (CEA), Direction des Sciences du Vivant, Institut de Génomique, Genoscope, 2 rue Gaston Crémieux, 91057 Evry Cedex, Evry cedex F-91006, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>CNRS-UMR 8030, Laboratoire d'Analyse Bioinformatique en Génomique et Métabolisme, Commissariat à l'Energie Atomique (CEA), Direction des Sciences du Vivant, Institut de Génomique, Genoscope, 2 rue Gaston Crémieux, 91057 Evry Cedex, Evry cedex F-91006</wicri:regionArea>
<wicri:noRegion>91006</wicri:noRegion>
<wicri:noRegion>91006</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Mangenot, Sophie" sort="Mangenot, Sophie" uniqKey="Mangenot S" first="Sophie" last="Mangenot">Sophie Mangenot</name>
<affiliation wicri:level="1">
<nlm:aff id="I8">Commissariat à l'Energie Atomique (CEA), Direction des Sciences du Vivant, Institut de Génomique, Genoscope, 2 rue Gaston Crémieux, 91057 Evry Cedex, Evry cedex F-91006, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Commissariat à l'Energie Atomique (CEA), Direction des Sciences du Vivant, Institut de Génomique, Genoscope, 2 rue Gaston Crémieux, 91057 Evry Cedex, Evry cedex F-91006</wicri:regionArea>
<wicri:noRegion>91006</wicri:noRegion>
<wicri:noRegion>91006</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Barbe, Valerie" sort="Barbe, Valerie" uniqKey="Barbe V" first="Valérie" last="Barbe">Valérie Barbe</name>
<affiliation wicri:level="1">
<nlm:aff id="I8">Commissariat à l'Energie Atomique (CEA), Direction des Sciences du Vivant, Institut de Génomique, Genoscope, 2 rue Gaston Crémieux, 91057 Evry Cedex, Evry cedex F-91006, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Commissariat à l'Energie Atomique (CEA), Direction des Sciences du Vivant, Institut de Génomique, Genoscope, 2 rue Gaston Crémieux, 91057 Evry Cedex, Evry cedex F-91006</wicri:regionArea>
<wicri:noRegion>91006</wicri:noRegion>
<wicri:noRegion>91006</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Medigue, Claudine" sort="Medigue, Claudine" uniqKey="Medigue C" first="Claudine" last="Médigue">Claudine Médigue</name>
<affiliation wicri:level="1">
<nlm:aff id="I7">CNRS-UMR 8030, Laboratoire d'Analyse Bioinformatique en Génomique et Métabolisme, Commissariat à l'Energie Atomique (CEA), Direction des Sciences du Vivant, Institut de Génomique, Genoscope, 2 rue Gaston Crémieux, 91057 Evry Cedex, Evry cedex F-91006, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>CNRS-UMR 8030, Laboratoire d'Analyse Bioinformatique en Génomique et Métabolisme, Commissariat à l'Energie Atomique (CEA), Direction des Sciences du Vivant, Institut de Génomique, Genoscope, 2 rue Gaston Crémieux, 91057 Evry Cedex, Evry cedex F-91006</wicri:regionArea>
<wicri:noRegion>91006</wicri:noRegion>
<wicri:noRegion>91006</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Prior, Philippe" sort="Prior, Philippe" uniqKey="Prior P" first="Philippe" last="Prior">Philippe Prior</name>
<affiliation wicri:level="1">
<nlm:aff id="I9">INRA-CIRAD, UMR Peuplements Végétaux et Bioagresseurs en Milieu Tropical, Saint Pierre F-97410, La Réunion, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>INRA-CIRAD, UMR Peuplements Végétaux et Bioagresseurs en Milieu Tropical, Saint Pierre F-97410, La Réunion</wicri:regionArea>
<wicri:noRegion>97410, La Réunion</wicri:noRegion>
<wicri:noRegion>97410, La Réunion</wicri:noRegion>
</affiliation>
</author>
</analytic>
<series>
<title level="j">BMC Genomics</title>
<idno type="eISSN">1471-2164</idno>
<imprint>
<date when="2010">2010</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc>
<textClass></textClass>
</profileDesc>
</teiHeader>
<front>
<div type="abstract" xml:lang="en">
<sec>
<title>Background</title>
<p>The
<italic>Ralstonia solanacearum </italic>
species complex includes thousands of strains pathogenic to an unusually wide range of plant species. These globally dispersed and heterogeneous strains cause bacterial wilt diseases, which have major socio-economic impacts. Pathogenicity is an ancestral trait in
<italic>R. solanacearum </italic>
and strains with high genetic variation can be subdivided into four phylotypes, correlating to isolates from Asia (phylotype I), the Americas (phylotype IIA and IIB), Africa (phylotype III) and Indonesia (phylotype IV). Comparison of genome sequences strains representative of this phylogenetic diversity can help determine which traits allow this bacterium to be such a pathogen of so many different plant species and how the bacteria survive in many different habitats.</p>
</sec>
<sec>
<title>Results</title>
<p>The genomes of three tomato bacterial wilt pathogens, CFBP2957 (phy. IIA), CMR15 (phy. III) and PSI07 (phy. IV) were sequenced and manually annotated. These genomes were compared with those of three previously sequenced
<italic>R. solanacearum </italic>
strains: GMI1000 (tomato, phy. I), IPO1609 (potato, phy. IIB), and Molk2 (banana, phy. IIB). The major genomic features (size, G+C content, number of genes) were conserved across all of the six sequenced strains. Despite relatively high genetic distances (calculated from average nucleotide identity) and many genomic rearrangements, more than 60% of the genes of the megaplasmid and 70% of those on the chromosome are syntenic. The three new genomic sequences revealed the presence of several previously unknown traits, probably acquired by horizontal transfers, within the genomes of
<italic>R. solanacearum</italic>
, including a type IV secretion system, a rhi-type anti-mitotic toxin and two small plasmids. Genes involved in virulence appear to be evolving at a faster rate than the genome as a whole.</p>
</sec>
<sec>
<title>Conclusions</title>
<p>Comparative analysis of genome sequences and gene content confirmed the differentiation of
<italic>R. solanacearum </italic>
species complex strains into four phylotypes. Genetic distances between strains, in conjunction with CGH analysis of a larger set of strains, revealed differences great enough to consider reclassification of the
<italic>R. solanacearum </italic>
species complex into three species. The data are still too fragmentary to link genomic classification and phenotypes, but these new genome sequences identify a pan-genome more representative of the diversity in the
<italic>R. solanancearum </italic>
species complex.</p>
</sec>
</div>
</front>
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<name sortKey="Kaipa, P" uniqKey="Kaipa P">P Kaipa</name>
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<name sortKey="Krummenacker, M" uniqKey="Krummenacker M">M Krummenacker</name>
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<li>Île-de-France</li>
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<name sortKey="Coupat Goutaland, Benedicte" sort="Coupat Goutaland, Benedicte" uniqKey="Coupat Goutaland B" first="Bénédicte" last="Coupat-Goutaland">Bénédicte Coupat-Goutaland</name>
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<name sortKey="Medigue, Claudine" sort="Medigue, Claudine" uniqKey="Medigue C" first="Claudine" last="Médigue">Claudine Médigue</name>
<name sortKey="Mornico, Damien" sort="Mornico, Damien" uniqKey="Mornico D" first="Damien" last="Mornico">Damien Mornico</name>
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<name sortKey="Allen, Caitilyn" sort="Allen, Caitilyn" uniqKey="Allen C" first="Caitilyn" last="Allen">Caitilyn Allen</name>
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<country name="Australie">
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<name sortKey="Fegan, Mark" sort="Fegan, Mark" uniqKey="Fegan M" first="Mark" last="Fegan">Mark Fegan</name>
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