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Positive selection is the main driving force for evolution of citrus canker-causing Xanthomonas

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Positive selection is the main driving force for evolution of citrus canker-causing Xanthomonas

Auteurs : Yunzeng Zhang [États-Unis] ; Neha Jalan [États-Unis] ; Xiaofeng Zhou [États-Unis] ; Erica Goss [États-Unis] ; Jeffrey B. Jones [États-Unis] ; João C. Setubal [Brésil] ; Xiaoling Deng [République populaire de Chine] ; Nian Wang [États-Unis]

Source :

The ISME Journal [ 1751-7362 ] ; 2015.

RBID : PMC:4579464

Abstract

Understanding the evolutionary history and potential of bacterial pathogens is critical to prevent the emergence of new infectious bacterial diseases. Xanthomonas axonopodis subsp. citri (Xac) (synonym X. citri subsp. citri), which causes citrus canker, is one of the hardest-fought plant bacterial pathogens in US history. Here, we sequenced 21 Xac strains (14 XacA, 3 XacA* and 4 XacA^w) with different host ranges from North America and Asia and conducted comparative genomic and evolutionary analyses. Our analyses suggest that acquisition of beneficial genes and loss of detrimental genes most likely allowed XacA to infect a broader range of hosts as compared with XacA^w and XacA*. Recombination was found to have occurred frequently on the relative ancient branches, but rarely on the young branches of the clonal genealogy. The ratio of recombination/mutation ρ/θ was 0.0790±0.0005, implying that the Xac population was clonal in structure. Positive selection has affected 14% (395 out of 2822) of core genes of the citrus canker-causing Xanthomonas. The genes affected are enriched in ‘carbohydrate transport and metabolism' and ‘DNA replication, recombination and repair' genes (P<0.05). Many genes related to virulence, especially genes involved in the type III secretion system and effectors, are affected by positive selection, further highlighting the contribution of positive selection to the evolution of citrus canker-causing Xanthomonas. Our results suggest that both metabolism and virulence genes provide advantages to endow XacA with higher virulence and a wider host range. Our analysis advances our understanding of the genomic basis of specialization by positive selection in bacterial evolution.

Url:

http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4579464

DOI: 10.1038/ismej.2015.15
PubMed: 25689023
PubMed Central: 4579464

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<country xml:lang="fr">États-Unis</country>
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<front><div type="abstract" xml:lang="en"><p>Understanding the evolutionary history and potential of bacterial pathogens is critical to prevent the emergence of new infectious bacterial diseases. <italic>Xanthomonas axonopodis</italic>
 subsp. <italic>citri</italic>
 (Xac) (synonym <italic>X. citri</italic>
 subsp. <italic>citri</italic>
), which causes citrus canker, is one of the hardest-fought plant bacterial pathogens in US history. Here, we sequenced 21 Xac strains (14 XacA, 3 XacA* and 4 XacA<sup>w</sup>
) with different host ranges from North America and Asia and conducted comparative genomic and evolutionary analyses. Our analyses suggest that acquisition of beneficial genes and loss of detrimental genes most likely allowed XacA to infect a broader range of hosts as compared with XacA<sup>w</sup>
 and XacA*. Recombination was found to have occurred frequently on the relative ancient branches, but rarely on the young branches of the clonal genealogy. The ratio of recombination/mutation ρ/θ was 0.0790±0.0005, implying that the Xac population was clonal in structure. Positive selection has affected 14% (395 out of 2822) of core genes of the citrus canker-causing <italic>Xanthomonas</italic>
. The genes affected are enriched in ‘carbohydrate transport and metabolism' and ‘DNA replication, recombination and repair' genes (<italic>P</italic>
<0.05). Many genes related to virulence, especially genes involved in the type III secretion system and effectors, are affected by positive selection, further highlighting the contribution of positive selection to the evolution of citrus canker-causing <italic>Xanthomonas</italic>
. Our results suggest that both metabolism and virulence genes provide advantages to endow XacA with higher virulence and a wider host range. Our analysis advances our understanding of the genomic basis of specialization by positive selection in bacterial evolution.</p>
</div>
</front>
</TEI>
<pmc article-type="research-article"><pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
  <front><journal-meta><journal-id journal-id-type="nlm-ta">ISME J</journal-id>
<journal-id journal-id-type="iso-abbrev">ISME J</journal-id>
<journal-title-group><journal-title>The ISME Journal</journal-title>
</journal-title-group>
<issn pub-type="ppub">1751-7362</issn>
<issn pub-type="epub">1751-7370</issn>
<publisher><publisher-name>Nature Publishing Group</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">25689023</article-id>
<article-id pub-id-type="pmc">4579464</article-id>
<article-id pub-id-type="pii">ismej201515</article-id>
<article-id pub-id-type="doi">10.1038/ismej.2015.15</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Original Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Positive selection is the main driving force for evolution of citrus canker-causing <italic>Xanthomonas</italic>
</article-title>
<alt-title alt-title-type="running">Positive selection for evolution of Xac</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Zhang</surname>
<given-names>Yunzeng</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="author-notes" rid="note1"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Jalan</surname>
<given-names>Neha</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="author-notes" rid="note1"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Zhou</surname>
<given-names>Xiaofeng</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Goss</surname>
<given-names>Erica</given-names>
</name>
<xref ref-type="aff" rid="aff2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Jones</surname>
<given-names>Jeffrey B</given-names>
</name>
<xref ref-type="aff" rid="aff2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Setubal</surname>
<given-names>João C</given-names>
</name>
<xref ref-type="aff" rid="aff3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Deng</surname>
<given-names>Xiaoling</given-names>
</name>
<xref ref-type="aff" rid="aff4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wang</surname>
<given-names>Nian</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="corresp" rid="caf1">*</xref>
</contrib>
<aff id="aff1"><label>1</label>
<institution>Citrus Research and Education Center, Department of Microbiology and Cell Science, University of Florida</institution>
, Lake Alfred, FL,<country>USA</country>
</aff>
<aff id="aff2"><label>2</label>
<institution>Department of Plant Pathology, University of Florida</institution>
, Gainesville, FL,<country>USA</country>
</aff>
<aff id="aff3"><label>3</label>
<institution>Departamento de Bioquímica, Instituto de Química, Universidade de São Paulo</institution>
, São Paulo,<country>Brazil</country>
</aff>
<aff id="aff4"><label>4</label>
<institution>Department of Plant Pathology, South China Agricultural University</institution>
, Guangzhou, Guangdong,<country>China</country>
</aff>
</contrib-group>
<author-notes><corresp id="caf1"><label>*</label>
<institution>Citrus Research and Education Center, Department of Microbiology and Cell Science, University of Florida</institution>
, 700 Experiment Station Road, Lake Alfred, FL 33850, <country>USA</country>
. E-mail: <email>nianwang@ufl.edu</email>
</corresp>
<fn fn-type="present-address" id="note1"><label>5</label>
<p>These two authors contributed equally to this work.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><month>10</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="epub"><day>17</day>
<month>02</month>
<year>2015</year>
</pub-date>
<volume>9</volume>
<issue>10</issue>
<fpage>2128</fpage>
<lpage>2138</lpage>
<history><date date-type="received"><day>03</day>
<month>10</month>
<year>2014</year>
</date>
<date date-type="rev-recd"><day>29</day>
<month>12</month>
<year>2014</year>
</date>
<date date-type="accepted"><day>06</day>
<month>01</month>
<year>2015</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2015 International Society for Microbial Ecology</copyright-statement>
<copyright-year>2015</copyright-year>
<copyright-holder>International Society for Microbial Ecology</copyright-holder>
</permissions>
<abstract><p>Understanding the evolutionary history and potential of bacterial pathogens is critical to prevent the emergence of new infectious bacterial diseases. <italic>Xanthomonas axonopodis</italic>
 subsp. <italic>citri</italic>
 (Xac) (synonym <italic>X. citri</italic>
 subsp. <italic>citri</italic>
), which causes citrus canker, is one of the hardest-fought plant bacterial pathogens in US history. Here, we sequenced 21 Xac strains (14 XacA, 3 XacA* and 4 XacA<sup>w</sup>
) with different host ranges from North America and Asia and conducted comparative genomic and evolutionary analyses. Our analyses suggest that acquisition of beneficial genes and loss of detrimental genes most likely allowed XacA to infect a broader range of hosts as compared with XacA<sup>w</sup>
 and XacA*. Recombination was found to have occurred frequently on the relative ancient branches, but rarely on the young branches of the clonal genealogy. The ratio of recombination/mutation ρ/θ was 0.0790±0.0005, implying that the Xac population was clonal in structure. Positive selection has affected 14% (395 out of 2822) of core genes of the citrus canker-causing <italic>Xanthomonas</italic>
. The genes affected are enriched in ‘carbohydrate transport and metabolism' and ‘DNA replication, recombination and repair' genes (<italic>P</italic>
<0.05). Many genes related to virulence, especially genes involved in the type III secretion system and effectors, are affected by positive selection, further highlighting the contribution of positive selection to the evolution of citrus canker-causing <italic>Xanthomonas</italic>
. Our results suggest that both metabolism and virulence genes provide advantages to endow XacA with higher virulence and a wider host range. Our analysis advances our understanding of the genomic basis of specialization by positive selection in bacterial evolution.</p>
</abstract>
</article-meta>
</front>
</pmc>
</record>

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Positive selection is the main driving force for evolution of citrus canker-causing Xanthomonas

Positive selection is the main driving force for evolution of citrus canker-causing Xanthomonas

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