The CC-NB-LRR-Type Rdg2a Resistance Gene Confers Immunity to the Seed-Borne Barley Leaf Stripe Pathogen in the Absence of Hypersensitive Cell Death
Identifieur interne : 000A42 ( Pmc/Checkpoint ); précédent : 000A41; suivant : 000A43The CC-NB-LRR-Type Rdg2a Resistance Gene Confers Immunity to the Seed-Borne Barley Leaf Stripe Pathogen in the Absence of Hypersensitive Cell Death
Auteurs : Davide Bulgarelli [Italie, Allemagne] ; Chiara Biselli [Italie] ; Nicholas C. Collins [Australie] ; Gabriella Consonni [Italie] ; Antonio M. Stanca [Italie] ; Paul Schulze-Lefert [Allemagne] ; Giampiero Valè [Italie]Source :
- PLoS ONE [ 1932-6203 ] ; 2010.
Abstract
Leaf stripe disease on barley (
We describe here the positional cloning and functional characterization of the leaf stripe resistance gene
This work reports about the cloning of a resistance gene effective against a seed borne disease. We observed that
Url:
DOI: 10.1371/journal.pone.0012599
PubMed: 20844752
PubMed Central: 2937021
Affiliations:
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PMC:2937021Le document en format XML
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Resistance Gene Confers Immunity to the Seed-Borne Barley Leaf Stripe Pathogen in the Absence of Hypersensitive Cell Death</title>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">The CC-NB-LRR-Type <italic>Rdg2a</italic>
Resistance Gene Confers Immunity to the Seed-Borne Barley Leaf Stripe Pathogen in the Absence of Hypersensitive Cell Death</title>
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<author><name sortKey="Stanca, Antonio M" sort="Stanca, Antonio M" uniqKey="Stanca A" first="Antonio M." last="Stanca">Antonio M. Stanca</name>
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<author><name sortKey="Vale, Giampiero" sort="Vale, Giampiero" uniqKey="Vale G" first="Giampiero" last="Valè">Giampiero Valè</name>
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<series><title level="j">PLoS ONE</title>
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<front><div type="abstract" xml:lang="en"><sec><title>Background</title>
<p>Leaf stripe disease on barley (<italic>Hordeum vulgare</italic>
) is caused by the seed-transmitted hemi-biotrophic fungus <italic>Pyrenophora graminea</italic>
. Race-specific resistance to leaf stripe is controlled by two known <italic>Rdg</italic>
(<italic><underline>R</underline>
</italic>
esistance to <italic><underline>D</underline>
rechslera <underline>g</underline>
raminea</italic>
) genes: the <italic>H. spontaneum</italic>
-derived <italic>Rdg1a</italic>
and <italic>Rdg2a</italic>
, identified in <italic>H. vulgare</italic>
. The aim of the present work was to isolate the <italic>Rdg2a</italic>
leaf stripe resistance gene, to characterize the <italic>Rdg2a</italic>
locus organization and evolution and to elucidate the histological bases of <italic>Rdg2a</italic>
-based leaf stripe resistance.</p>
</sec>
<sec><title>Principal Findings</title>
<p>We describe here the positional cloning and functional characterization of the leaf stripe resistance gene <italic>Rdg2a</italic>
. At the <italic>Rdg2a</italic>
locus, three sequence-related coiled-coil, nucleotide-binding site, and leucine-rich repeat (CC-NB-LRR) encoding genes were identified. Sequence comparisons suggested that paralogs of this resistance locus evolved through recent gene duplication, and were subjected to frequent sequence exchange. Transformation of the leaf stripe susceptible cv. Golden Promise with two <italic>Rdg2a</italic>
-candidates under the control of their native 5′ regulatory sequences identified a member of the CC-NB-LRR gene family that conferred resistance against the Dg2 leaf stripe isolate, against which the <italic>Rdg2a</italic>
-gene is effective. Histological analysis demonstrated that <italic>Rdg2a</italic>
-mediated leaf stripe resistance involves autofluorescing cells and prevents pathogen colonization in the embryos without any detectable hypersensitive cell death response, supporting a cell wall reinforcement-based resistance mechanism.</p>
</sec>
<sec><title>Conclusions</title>
<p>This work reports about the cloning of a resistance gene effective against a seed borne disease. We observed that <italic>Rdg2a</italic>
was subjected to diversifying selection which is consistent with a model in which the <italic>R</italic>
gene co-evolves with a pathogen effector(s) gene. We propose that inducible responses giving rise to physical and chemical barriers to infection in the cell walls and intercellular spaces of the barley embryo tissues represent mechanisms by which the CC-NB-LRR-encoding <italic>Rdg2a</italic>
gene mediates resistance to leaf stripe in the absence of hypersensitive cell death.</p>
</sec>
</div>
</front>
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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">PLoS One</journal-id>
<journal-id journal-id-type="iso-abbrev">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">20844752</article-id>
<article-id pub-id-type="pmc">2937021</article-id>
<article-id pub-id-type="publisher-id">10-PONE-RA-19259R1</article-id>
<article-id pub-id-type="doi">10.1371/journal.pone.0012599</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
<subj-group subj-group-type="Discipline"><subject>Plant Biology/Plant Genetics and Gene Expression</subject>
<subject>Plant Biology/Plant Genomes and Evolution</subject>
<subject>Plant Biology/Plant-Biotic Interactions</subject>
</subj-group>
</article-categories>
<title-group><article-title>The CC-NB-LRR-Type <italic>Rdg2a</italic>
Resistance Gene Confers Immunity to the Seed-Borne Barley Leaf Stripe Pathogen in the Absence of Hypersensitive Cell Death</article-title>
<alt-title alt-title-type="running-head">Embryo Immunity to Leaf Stripe</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author" equal-contrib="yes"><name><surname>Bulgarelli</surname>
<given-names>Davide</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author" equal-contrib="yes"><name><surname>Biselli</surname>
<given-names>Chiara</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Collins</surname>
<given-names>Nicholas C.</given-names>
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<xref ref-type="aff" rid="aff3"><sup>3</sup>
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</contrib>
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<given-names>Gabriella</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
</contrib>
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<given-names>Antonio M.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
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</contrib>
<contrib contrib-type="author"><name><surname>Schulze-Lefert</surname>
<given-names>Paul</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
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<contrib contrib-type="author"><name><surname>Valè</surname>
<given-names>Giampiero</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
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<xref ref-type="corresp" rid="cor1"><sup>*</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>1</label>
<addr-line>Genomic Research Center, CRA-GPG, Fiorenzuola d'Arda, Italy</addr-line>
</aff>
<aff id="aff2"><label>2</label>
<addr-line>Department of Plant Microbe Interactions, Max Planck Institute für Züchtungsforschung, Köln, Germany</addr-line>
</aff>
<aff id="aff3"><label>3</label>
<addr-line>Australian Centre for Plant Functional Genomics, School of Agriculture Food and Wine, University of Adelaide, Glen Osmond, Australia</addr-line>
</aff>
<aff id="aff4"><label>4</label>
<addr-line>DiPROVE, University of Milan, Milano, Italy</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Bendahmane</surname>
<given-names>Mohammed</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1">Ecole Normale Superieure, France</aff>
<author-notes><corresp id="cor1">* E-mail: <email>giampiero.vale@entecra.it</email>
</corresp>
<fn fn-type="con"><p>Conceived and designed the experiments: DB CB NCC PSL GV. Performed the experiments: DB CB GC GV. Analyzed the data: DB CB GV. Wrote the paper: DB CB NCC AMS PSL GV.</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><year>2010</year>
</pub-date>
<pub-date pub-type="epub"><day>10</day>
<month>9</month>
<year>2010</year>
</pub-date>
<volume>5</volume>
<issue>9</issue>
<elocation-id>e12599</elocation-id>
<history><date date-type="received"><day>26</day>
<month>5</month>
<year>2010</year>
</date>
<date date-type="accepted"><day>12</day>
<month>8</month>
<year>2010</year>
</date>
</history>
<permissions><copyright-statement>Bulgarelli et al.</copyright-statement>
<copyright-year>2010</copyright-year>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>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 properly credited.</license-p>
</license>
</permissions>
<abstract><sec><title>Background</title>
<p>Leaf stripe disease on barley (<italic>Hordeum vulgare</italic>
) is caused by the seed-transmitted hemi-biotrophic fungus <italic>Pyrenophora graminea</italic>
. Race-specific resistance to leaf stripe is controlled by two known <italic>Rdg</italic>
(<italic><underline>R</underline>
</italic>
esistance to <italic><underline>D</underline>
rechslera <underline>g</underline>
raminea</italic>
) genes: the <italic>H. spontaneum</italic>
-derived <italic>Rdg1a</italic>
and <italic>Rdg2a</italic>
, identified in <italic>H. vulgare</italic>
. The aim of the present work was to isolate the <italic>Rdg2a</italic>
leaf stripe resistance gene, to characterize the <italic>Rdg2a</italic>
locus organization and evolution and to elucidate the histological bases of <italic>Rdg2a</italic>
-based leaf stripe resistance.</p>
</sec>
<sec><title>Principal Findings</title>
<p>We describe here the positional cloning and functional characterization of the leaf stripe resistance gene <italic>Rdg2a</italic>
. At the <italic>Rdg2a</italic>
locus, three sequence-related coiled-coil, nucleotide-binding site, and leucine-rich repeat (CC-NB-LRR) encoding genes were identified. Sequence comparisons suggested that paralogs of this resistance locus evolved through recent gene duplication, and were subjected to frequent sequence exchange. Transformation of the leaf stripe susceptible cv. Golden Promise with two <italic>Rdg2a</italic>
-candidates under the control of their native 5′ regulatory sequences identified a member of the CC-NB-LRR gene family that conferred resistance against the Dg2 leaf stripe isolate, against which the <italic>Rdg2a</italic>
-gene is effective. Histological analysis demonstrated that <italic>Rdg2a</italic>
-mediated leaf stripe resistance involves autofluorescing cells and prevents pathogen colonization in the embryos without any detectable hypersensitive cell death response, supporting a cell wall reinforcement-based resistance mechanism.</p>
</sec>
<sec><title>Conclusions</title>
<p>This work reports about the cloning of a resistance gene effective against a seed borne disease. We observed that <italic>Rdg2a</italic>
was subjected to diversifying selection which is consistent with a model in which the <italic>R</italic>
gene co-evolves with a pathogen effector(s) gene. We propose that inducible responses giving rise to physical and chemical barriers to infection in the cell walls and intercellular spaces of the barley embryo tissues represent mechanisms by which the CC-NB-LRR-encoding <italic>Rdg2a</italic>
gene mediates resistance to leaf stripe in the absence of hypersensitive cell death.</p>
</sec>
</abstract>
<counts><page-count count="14"></page-count>
</counts>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>Allemagne</li>
<li>Australie</li>
<li>Italie</li>
</country>
<region><li>District de Cologne</li>
<li>Rhénanie-du-Nord-Westphalie</li>
</region>
<settlement><li>Cologne</li>
</settlement>
</list>
<tree><country name="Italie"><noRegion><name sortKey="Bulgarelli, Davide" sort="Bulgarelli, Davide" uniqKey="Bulgarelli D" first="Davide" last="Bulgarelli">Davide Bulgarelli</name>
</noRegion>
<name sortKey="Biselli, Chiara" sort="Biselli, Chiara" uniqKey="Biselli C" first="Chiara" last="Biselli">Chiara Biselli</name>
<name sortKey="Consonni, Gabriella" sort="Consonni, Gabriella" uniqKey="Consonni G" first="Gabriella" last="Consonni">Gabriella Consonni</name>
<name sortKey="Stanca, Antonio M" sort="Stanca, Antonio M" uniqKey="Stanca A" first="Antonio M." last="Stanca">Antonio M. Stanca</name>
<name sortKey="Vale, Giampiero" sort="Vale, Giampiero" uniqKey="Vale G" first="Giampiero" last="Valè">Giampiero Valè</name>
</country>
<country name="Allemagne"><region name="Rhénanie-du-Nord-Westphalie"><name sortKey="Bulgarelli, Davide" sort="Bulgarelli, Davide" uniqKey="Bulgarelli D" first="Davide" last="Bulgarelli">Davide Bulgarelli</name>
</region>
<name sortKey="Schulze Lefert, Paul" sort="Schulze Lefert, Paul" uniqKey="Schulze Lefert P" first="Paul" last="Schulze-Lefert">Paul Schulze-Lefert</name>
</country>
<country name="Australie"><noRegion><name sortKey="Collins, Nicholas C" sort="Collins, Nicholas C" uniqKey="Collins N" first="Nicholas C." last="Collins">Nicholas C. Collins</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>
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