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The dual nature of trehalose in citrus canker disease: a virulence factor for Xanthomonas citri subsp. citri and a trigger for plant defence responses

Identifieur interne : 000324 ( Pmc/Checkpoint ); précédent : 000323; suivant : 000325

The dual nature of trehalose in citrus canker disease: a virulence factor for Xanthomonas citri subsp. citri and a trigger for plant defence responses

Auteurs : Ainelén Piazza [Argentine] ; Tamara Zimaro [Argentine] ; Betiana S. Garavaglia [Argentine] ; Florencia A. Ficarra [Argentine] ; Ludivine Thomas [Arabie saoudite] ; Claudius Marondedze [Arabie saoudite] ; Regina Feil [Allemagne] ; John E. Lunn [Allemagne] ; Chris Gehring [Arabie saoudite] ; Jorgelina Ottado [Argentine] ; Natalia Gottig [Argentine]

Source :

RBID : PMC:4986880

Abstract

Highlight:

Trehalose is a double-edged sword for both partners in the citrus–Xanthomonas interaction, as it is necessary for bacterial survival but also triggers citrus defence responses.


Url:
DOI: 10.1093/jxb/erv095
PubMed: 25770587
PubMed Central: 4986880


Affiliations:


Links toward previous steps (curation, corpus...)


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PMC:4986880

Le document en format XML

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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">J Exp Bot</journal-id>
<journal-id journal-id-type="iso-abbrev">J. Exp. Bot</journal-id>
<journal-id journal-id-type="hwp">jexbot</journal-id>
<journal-id journal-id-type="publisher-id">exbotj</journal-id>
<journal-title-group>
<journal-title>Journal of Experimental Botany</journal-title>
</journal-title-group>
<issn pub-type="ppub">0022-0957</issn>
<issn pub-type="epub">1460-2431</issn>
<publisher>
<publisher-name>Oxford University Press</publisher-name>
<publisher-loc>UK</publisher-loc>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">25770587</article-id>
<article-id pub-id-type="pmc">4986880</article-id>
<article-id pub-id-type="doi">10.1093/jxb/erv095</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Research Paper</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>The dual nature of trehalose in citrus canker disease: a virulence factor for
<italic>Xanthomonas citri</italic>
subsp.
<italic>citri</italic>
and a trigger for plant defence responses</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Piazza</surname>
<given-names>Ainelén</given-names>
</name>
<xref ref-type="aff" rid="AF0001">
<sup>1</sup>
</xref>
<xref ref-type="corresp" rid="c2">*</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Zimaro</surname>
<given-names>Tamara</given-names>
</name>
<xref ref-type="aff" rid="AF0001">
<sup>1</sup>
</xref>
<xref ref-type="corresp" rid="c2">*</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Garavaglia</surname>
<given-names>Betiana S.</given-names>
</name>
<xref ref-type="aff" rid="AF0001">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Ficarra</surname>
<given-names>Florencia A.</given-names>
</name>
<xref ref-type="aff" rid="AF0001">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Thomas</surname>
<given-names>Ludivine</given-names>
</name>
<xref ref-type="aff" rid="AF0002">
<sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Marondedze</surname>
<given-names>Claudius</given-names>
</name>
<xref ref-type="aff" rid="AF0002">
<sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Feil</surname>
<given-names>Regina</given-names>
</name>
<xref ref-type="aff" rid="AF0003">
<sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Lunn</surname>
<given-names>John E.</given-names>
</name>
<xref ref-type="aff" rid="AF0003">
<sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Gehring</surname>
<given-names>Chris</given-names>
</name>
<xref ref-type="aff" rid="AF0002">
<sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Ottado</surname>
<given-names>Jorgelina</given-names>
</name>
<xref ref-type="aff" rid="AF0001">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Gottig</surname>
<given-names>Natalia</given-names>
</name>
<xref ref-type="aff" rid="AF0001">
<sup>1</sup>
</xref>
<xref ref-type="corresp" rid="c1">
<sup></sup>
</xref>
</contrib>
<aff id="AF0001">
<sup>1</sup>
<institution>Instituto de Biología Molecular y Celular de Rosario, Consejo Nacional de Investigaciones Científicas y Técnicas (IBR-CONICET) and Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario</institution>
,
<addr-line>Ocampo y Esmeralda, Rosario 2000</addr-line>
,
<country>Argentina</country>
</aff>
<aff id="AF0002">
<sup>2</sup>
<institution>Biological and Environmental Science and Engineering Division, King Abdullah University of Science and Technology</institution>
,
<addr-line>Thuwal 23955-6900</addr-line>
,
<country>Saudi Arabia</country>
</aff>
<aff id="AF0003">
<sup>3</sup>
<institution>Max Planck Institute of Molecular Plant Physiology, Wissenschaftspark Golm</institution>
,
<addr-line>Am Mühlenberg 1, 14476 Potsdam (OT) Golm</addr-line>
,
<country>Germany</country>
</aff>
</contrib-group>
<author-notes>
<corresp id="c2">* These authors contributed equally to this work.</corresp>
<corresp id="c1">
<sup></sup>
To whom correspondence should be addressed. E-mail:
<email>gottig@ibr-conicet.gov.ar</email>
</corresp>
</author-notes>
<pub-date pub-type="ppub">
<month>5</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="epub">
<day>14</day>
<month>3</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="pmc-release">
<day>14</day>
<month>3</month>
<year>2015</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on the . </pmc-comment>
<volume>66</volume>
<issue>9</issue>
<fpage>2795</fpage>
<lpage>2811</lpage>
<permissions>
<copyright-statement>© The Author 2015. Published by Oxford University Press on behalf of the Society for Experimental Biology.</copyright-statement>
<copyright-year>2015</copyright-year>
<license license-type="creative-commons" xlink:href="http://creativecommons.org/licenses/by/3.0">
<license-p>This is an Open Access article distributed under the terms of the Creative Commons Attribution License (
<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/3.0/">http://creativecommons.org/licenses/by/3.0/</ext-link>
), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.</license-p>
</license>
</permissions>
<abstract abstract-type="precis">
<title>Highlight:</title>
<p>Trehalose is a double-edged sword for both partners in the citrus–
<italic>Xanthomonas</italic>
interaction, as it is necessary for bacterial survival but also triggers citrus defence responses.</p>
</abstract>
<abstract>
<p>
<italic>Xanthomonas citri</italic>
subsp.
<italic>citri</italic>
(Xcc) is a bacterial pathogen that causes citrus canker in susceptible
<italic>Citrus</italic>
spp. The Xcc genome contains genes encoding enzymes from three separate pathways of trehalose biosynthesis. Expression of genes encoding trehalose-6-phosphate synthase (
<italic>otsA</italic>
) and trehalose phosphatase (
<italic>otsB</italic>
) was highly induced during canker development, suggesting that the two-step pathway of trehalose biosynthesis via trehalose-6-phosphate has a function in pathogenesis. This pathway was eliminated from the bacterium by deletion of the
<italic>otsA</italic>
gene. The resulting XccΔotsA mutant produced less trehalose than the wild-type strain, was less resistant to salt and oxidative stresses, and was less able to colonize plant tissues. Gene expression and proteomic analyses of infected leaves showed that infection with XccΔotsA triggered only weak defence responses in the plant compared with infection with Xcc, and had less impact on the host plant’s metabolism than the wild-type strain. These results suggested that trehalose of bacterial origin, synthesized via the otsA–otsB pathway, in Xcc, plays a role in modifying the host plant’s metabolism to its own advantage but is also perceived by the plant as a sign of pathogen attack. Thus, trehalose biosynthesis has both positive and negative consequences for Xcc. On the one hand, it enables this bacterial pathogen to survive in the inhospitable environment of the leaf surface before infection and exploit the host plant’s resources after infection, but on the other hand, it is a tell-tale sign of the pathogen’s presence that triggers the plant to defend itself against infection.</p>
</abstract>
<kwd-group>
<title>Key words:</title>
<kwd>Canker</kwd>
<kwd>citrus</kwd>
<kwd>defence</kwd>
<kwd>
<italic>otsA</italic>
</kwd>
<kwd>trehalose</kwd>
<kwd>
<italic>Xanthomonas</italic>
.</kwd>
</kwd-group>
<counts>
<page-count count="17"></page-count>
</counts>
</article-meta>
</front>
</pmc>
<affiliations>
<list>
<country>
<li>Allemagne</li>
<li>Arabie saoudite</li>
<li>Argentine</li>
</country>
</list>
<tree>
<country name="Argentine">
<noRegion>
<name sortKey="Piazza, Ainelen" sort="Piazza, Ainelen" uniqKey="Piazza A" first="Ainelén" last="Piazza">Ainelén Piazza</name>
</noRegion>
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<name sortKey="Garavaglia, Betiana S" sort="Garavaglia, Betiana S" uniqKey="Garavaglia B" first="Betiana S." last="Garavaglia">Betiana S. Garavaglia</name>
<name sortKey="Gottig, Natalia" sort="Gottig, Natalia" uniqKey="Gottig N" first="Natalia" last="Gottig">Natalia Gottig</name>
<name sortKey="Ottado, Jorgelina" sort="Ottado, Jorgelina" uniqKey="Ottado J" first="Jorgelina" last="Ottado">Jorgelina Ottado</name>
<name sortKey="Zimaro, Tamara" sort="Zimaro, Tamara" uniqKey="Zimaro T" first="Tamara" last="Zimaro">Tamara Zimaro</name>
</country>
<country name="Arabie saoudite">
<noRegion>
<name sortKey="Thomas, Ludivine" sort="Thomas, Ludivine" uniqKey="Thomas L" first="Ludivine" last="Thomas">Ludivine Thomas</name>
</noRegion>
<name sortKey="Gehring, Chris" sort="Gehring, Chris" uniqKey="Gehring C" first="Chris" last="Gehring">Chris Gehring</name>
<name sortKey="Marondedze, Claudius" sort="Marondedze, Claudius" uniqKey="Marondedze C" first="Claudius" last="Marondedze">Claudius Marondedze</name>
</country>
<country name="Allemagne">
<noRegion>
<name sortKey="Feil, Regina" sort="Feil, Regina" uniqKey="Feil R" first="Regina" last="Feil">Regina Feil</name>
</noRegion>
<name sortKey="Lunn, John E" sort="Lunn, John E" uniqKey="Lunn J" first="John E." last="Lunn">John E. Lunn</name>
</country>
</tree>
</affiliations>
</record>

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