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Breaking dogmas: the plant vascular pathogen Xanthomonas albilineans is able to invade non-vascular tissues despite its reduced genome

Identifieur interne : 000889 ( Pmc/Checkpoint ); précédent : 000888; suivant : 000890

Breaking dogmas: the plant vascular pathogen Xanthomonas albilineans is able to invade non-vascular tissues despite its reduced genome

Auteurs : Imène Mensi [France] ; Marie-Stéphanie Vernerey [France] ; Daniel Gargani [France] ; Michel Nicole [France] ; Philippe Rott [France]

Source :

RBID : PMC:3938051

Abstract

Xanthomonas albilineans, the causal agent of sugarcane leaf scald, is missing the Hrp type III secretion system that is used by many Gram-negative bacteria to colonize their host. Until now, this pathogen was considered as strictly limited to the xylem of sugarcane. We used confocal laser scanning microscopy, immunocytochemistry and transmission electron microscopy (TEM) to investigate the localization of X. albilineans in diseased sugarcane. Sugarcane plants were inoculated with strains of the pathogen labelled with a green fluorescent protein. Confocal microscopy observations of symptomatic leaves confirmed the presence of the pathogen in the protoxylem and metaxylem; however, X. albilineans was also observed in phloem, parenchyma and bulliform cells of the infected leaves. Similarly, vascular bundles of infected sugarcane stalks were invaded by X. albilineans. Surprisingly, the pathogen was also observed in apparently intact storage cells of the stalk and in intercellular spaces between these cells. Most of these observations made by confocal microscopy were confirmed by TEM. The pathogen exits the xylem following cell wall and middle lamellae degradation, thus creating openings to reach parenchyma cells. This is the first description of a plant pathogenic vascular bacterium invading apparently intact non-vascular plant tissues and multiplying in parenchyma cells.


Url:
DOI: 10.1098/rsob.130116
PubMed: 24522883
PubMed Central: 3938051


Affiliations:


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PMC:3938051

Le document en format XML

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<italic>X. albilineans</italic>
in diseased sugarcane. Sugarcane plants were inoculated with strains of the pathogen labelled with a green fluorescent protein. Confocal microscopy observations of symptomatic leaves confirmed the presence of the pathogen in the protoxylem and metaxylem; however,
<italic>X. albilineans</italic>
was also observed in phloem, parenchyma and bulliform cells of the infected leaves. Similarly, vascular bundles of infected sugarcane stalks were invaded by
<italic>X. albilineans</italic>
. Surprisingly, the pathogen was also observed in apparently intact storage cells of the stalk and in intercellular spaces between these cells. Most of these observations made by confocal microscopy were confirmed by TEM. The pathogen exits the xylem following cell wall and middle lamellae degradation, thus creating openings to reach parenchyma cells. This is the first description of a plant pathogenic vascular bacterium invading apparently intact non-vascular plant tissues and multiplying in parenchyma cells.</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">Open Biol</journal-id>
<journal-id journal-id-type="iso-abbrev">Open Biol</journal-id>
<journal-id journal-id-type="publisher-id">RSOB</journal-id>
<journal-id journal-id-type="hwp">royopenbio</journal-id>
<journal-title-group>
<journal-title>Open Biology</journal-title>
</journal-title-group>
<issn pub-type="epub">2046-2441</issn>
<publisher>
<publisher-name>The Royal Society</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">24522883</article-id>
<article-id pub-id-type="pmc">3938051</article-id>
<article-id pub-id-type="doi">10.1098/rsob.130116</article-id>
<article-id pub-id-type="publisher-id">rsob130116</article-id>
<article-categories>
<subj-group subj-group-type="hwp-journal-coll">
<subject>1001</subject>
<subject>200</subject>
</subj-group>
<subj-group subj-group-type="heading">
<subject>Research</subject>
</subj-group>
<subj-group subj-group-type="leader">
<subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>Breaking dogmas: the plant vascular pathogen
<italic>Xanthomonas albilineans</italic>
is able to invade non-vascular tissues despite its reduced genome</article-title>
<alt-title alt-title-type="short">Xanthomonas albilineans breaks dogmas</alt-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Mensi</surname>
<given-names>Imène</given-names>
</name>
<xref ref-type="aff" rid="af1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Vernerey</surname>
<given-names>Marie-Stéphanie</given-names>
</name>
<xref ref-type="aff" rid="af1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Gargani</surname>
<given-names>Daniel</given-names>
</name>
<xref ref-type="aff" rid="af1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Nicole</surname>
<given-names>Michel</given-names>
</name>
<xref ref-type="aff" rid="af2">2</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Rott</surname>
<given-names>Philippe</given-names>
</name>
<xref ref-type="aff" rid="af1">1</xref>
<xref ref-type="author-notes" rid="AN2"></xref>
<xref ref-type="corresp" rid="cor1"></xref>
</contrib>
</contrib-group>
<aff id="af1">
<label>1</label>
<institution>CIRAD, UMR BGPI, TA A-54/K</institution>
,
<addr-line>Montpellier Cedex 5 34398</addr-line>
,
<country>France</country>
</aff>
<aff id="af2">
<label>2</label>
<institution>IRD, UMR RPB, BP 64501</institution>
,
<addr-line>Montpellier Cedex 5 34394</addr-line>
,
<country>France</country>
</aff>
<author-notes>
<corresp id="cor1">e-mail:
<email>pcrott@ufl.edu</email>
</corresp>
<fn fn-type="present-address" id="AN2">
<label></label>
<p>Present address: Everglades Research and Education Center, University of Florida, 3200 East Palm Beach Road, Belle Glade, FL 33430, USA.</p>
</fn>
</author-notes>
<pub-date pub-type="collection">
<month>2</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="epub">
<day>12</day>
<month>2</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="pmc-release">
<day>12</day>
<month>2</month>
<year>2014</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on the . </pmc-comment>
<volume>4</volume>
<issue>2</issue>
<elocation-id>130116</elocation-id>
<history>
<date date-type="received">
<day>19</day>
<month>7</month>
<year>2013</year>
</date>
<date date-type="accepted">
<day>20</day>
<month>1</month>
<year>2014</year>
</date>
</history>
<permissions>
<copyright-statement></copyright-statement>
<copyright-year>2014</copyright-year>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/3.0/">
<license-p>© 2014 The Authors. Published by the Royal Society 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 use, provided the original author and source are credited.</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:type="simple" xlink:href="rsob-4-130116.pdf"></self-uri>
<abstract>
<p>
<italic>Xanthomonas albilineans</italic>
, the causal agent of sugarcane leaf scald, is missing the Hrp type III secretion system that is used by many Gram-negative bacteria to colonize their host. Until now, this pathogen was considered as strictly limited to the xylem of sugarcane. We used confocal laser scanning microscopy, immunocytochemistry and transmission electron microscopy (TEM) to investigate the localization of
<italic>X. albilineans</italic>
in diseased sugarcane. Sugarcane plants were inoculated with strains of the pathogen labelled with a green fluorescent protein. Confocal microscopy observations of symptomatic leaves confirmed the presence of the pathogen in the protoxylem and metaxylem; however,
<italic>X. albilineans</italic>
was also observed in phloem, parenchyma and bulliform cells of the infected leaves. Similarly, vascular bundles of infected sugarcane stalks were invaded by
<italic>X. albilineans</italic>
. Surprisingly, the pathogen was also observed in apparently intact storage cells of the stalk and in intercellular spaces between these cells. Most of these observations made by confocal microscopy were confirmed by TEM. The pathogen exits the xylem following cell wall and middle lamellae degradation, thus creating openings to reach parenchyma cells. This is the first description of a plant pathogenic vascular bacterium invading apparently intact non-vascular plant tissues and multiplying in parenchyma cells.</p>
</abstract>
<kwd-group>
<kwd>
<italic>Xanthomonas albilineans</italic>
</kwd>
<kwd>confocal laser scanning microscopy</kwd>
<kwd>cytochemistry</kwd>
<kwd>transmission electron microscopy</kwd>
<kwd>non-vascular plant tissue</kwd>
</kwd-group>
<custom-meta-group>
<custom-meta>
<meta-name>cover-date</meta-name>
<meta-value>February 2014</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
</front>
</pmc>
<affiliations>
<list>
<country>
<li>France</li>
</country>
</list>
<tree>
<country name="France">
<noRegion>
<name sortKey="Mensi, Imene" sort="Mensi, Imene" uniqKey="Mensi I" first="Imène" last="Mensi">Imène Mensi</name>
</noRegion>
<name sortKey="Gargani, Daniel" sort="Gargani, Daniel" uniqKey="Gargani D" first="Daniel" last="Gargani">Daniel Gargani</name>
<name sortKey="Nicole, Michel" sort="Nicole, Michel" uniqKey="Nicole M" first="Michel" last="Nicole">Michel Nicole</name>
<name sortKey="Rott, Philippe" sort="Rott, Philippe" uniqKey="Rott P" first="Philippe" last="Rott">Philippe Rott</name>
<name sortKey="Vernerey, Marie Stephanie" sort="Vernerey, Marie Stephanie" uniqKey="Vernerey M" first="Marie-Stéphanie" last="Vernerey">Marie-Stéphanie Vernerey</name>
</country>
</tree>
</affiliations>
</record>

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