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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Allelic barley MLA immune receptors recognize sequence-unrelated avirulence effectors of the powdery mildew pathogen</title><author><name sortKey="Lu, Xunli" sort="Lu, Xunli" uniqKey="Lu X" first="Xunli" last="Lu">Xunli Lu</name><affiliation><nlm:aff id="aff1">Department of Plant-Microbe Interactions,<institution>Max Planck Institute for Plant Breeding Research</institution>, Cologne D-50829,<country>Germany</country>;</nlm:aff></affiliation></author><author><name sortKey="Kracher, Barbara" sort="Kracher, Barbara" uniqKey="Kracher B" first="Barbara" last="Kracher">Barbara Kracher</name><affiliation><nlm:aff id="aff1">Department of Plant-Microbe Interactions,<institution>Max Planck Institute for Plant Breeding Research</institution>, Cologne D-50829,<country>Germany</country>;</nlm:aff></affiliation></author><author><name sortKey="Saur, Isabel M L" sort="Saur, Isabel M L" uniqKey="Saur I" first="Isabel M. L." last="Saur">Isabel M. L. Saur</name><affiliation><nlm:aff id="aff1">Department of Plant-Microbe Interactions,<institution>Max Planck Institute for Plant Breeding Research</institution>, Cologne D-50829,<country>Germany</country>;</nlm:aff></affiliation></author><author><name sortKey="Bauer, Saskia" sort="Bauer, Saskia" uniqKey="Bauer S" first="Saskia" last="Bauer">Saskia Bauer</name><affiliation><nlm:aff id="aff1">Department of Plant-Microbe Interactions,<institution>Max Planck Institute for Plant Breeding Research</institution>, Cologne D-50829,<country>Germany</country>;</nlm:aff></affiliation></author><author><name sortKey="Ellwood, Simon R" sort="Ellwood, Simon R" uniqKey="Ellwood S" first="Simon R." last="Ellwood">Simon R. Ellwood</name><affiliation><nlm:aff id="aff2">Centre for Crop and Disease Management, Department of Environment and Agriculture,<institution>Curtin University</institution>, Bentley, Perth, WA 6102,<country>Australia</country>;</nlm:aff></affiliation></author><author><name sortKey="Wise, Roger" sort="Wise, Roger" uniqKey="Wise R" first="Roger" last="Wise">Roger Wise</name><affiliation><nlm:aff id="aff3">Corn Insects and Crop Genetics Research, Agricultural Research Service,<institution>US Department of Agriculture</institution>, Ames,<addr-line>IA</addr-line> 50011-1020;</nlm:aff></affiliation><affiliation><nlm:aff id="aff4">Department of Plant Pathology and Microbiology, Center for Plant Responses to Environmental Stresses,<institution>Iowa State University</institution>, Ames,<addr-line>IA</addr-line> 50011-1020;</nlm:aff></affiliation></author><author><name sortKey="Yaeno, Takashi" sort="Yaeno, Takashi" uniqKey="Yaeno T" first="Takashi" last="Yaeno">Takashi Yaeno</name><affiliation><nlm:aff id="aff5">Faculty of Agriculture,<institution>Ehime University</institution>, Matsuyama, Ehime 790-8566,<country>Japan</country></nlm:aff></affiliation></author><author><name sortKey="Maekawa, Takaki" sort="Maekawa, Takaki" uniqKey="Maekawa T" first="Takaki" last="Maekawa">Takaki Maekawa</name><affiliation><nlm:aff id="aff1">Department of Plant-Microbe Interactions,<institution>Max Planck Institute for Plant Breeding Research</institution>, Cologne D-50829,<country>Germany</country>;</nlm:aff></affiliation></author><author><name sortKey="Schulze Lefert, Paul" sort="Schulze Lefert, Paul" uniqKey="Schulze Lefert P" first="Paul" last="Schulze-Lefert">Paul Schulze-Lefert</name><affiliation><nlm:aff id="aff1">Department of Plant-Microbe Interactions,<institution>Max Planck Institute for Plant Breeding Research</institution>, Cologne D-50829,<country>Germany</country>;</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">27702901</idno><idno type="pmc">5081590</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5081590</idno><idno type="RBID">PMC:5081590</idno><idno type="doi">10.1073/pnas.1612947113</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">000520</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000520</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Allelic barley MLA immune receptors recognize sequence-unrelated avirulence effectors of the powdery mildew pathogen</title><author><name sortKey="Lu, Xunli" sort="Lu, Xunli" uniqKey="Lu X" first="Xunli" last="Lu">Xunli Lu</name><affiliation><nlm:aff id="aff1">Department of Plant-Microbe Interactions,<institution>Max Planck Institute for Plant Breeding Research</institution>, Cologne D-50829,<country>Germany</country>;</nlm:aff></affiliation></author><author><name sortKey="Kracher, Barbara" sort="Kracher, Barbara" uniqKey="Kracher B" first="Barbara" last="Kracher">Barbara Kracher</name><affiliation><nlm:aff id="aff1">Department of Plant-Microbe Interactions,<institution>Max Planck Institute for Plant Breeding Research</institution>, Cologne D-50829,<country>Germany</country>;</nlm:aff></affiliation></author><author><name sortKey="Saur, Isabel M L" sort="Saur, Isabel M L" uniqKey="Saur I" first="Isabel M. L." last="Saur">Isabel M. L. Saur</name><affiliation><nlm:aff id="aff1">Department of Plant-Microbe Interactions,<institution>Max Planck Institute for Plant Breeding Research</institution>, Cologne D-50829,<country>Germany</country>;</nlm:aff></affiliation></author><author><name sortKey="Bauer, Saskia" sort="Bauer, Saskia" uniqKey="Bauer S" first="Saskia" last="Bauer">Saskia Bauer</name><affiliation><nlm:aff id="aff1">Department of Plant-Microbe Interactions,<institution>Max Planck Institute for Plant Breeding Research</institution>, Cologne D-50829,<country>Germany</country>;</nlm:aff></affiliation></author><author><name sortKey="Ellwood, Simon R" sort="Ellwood, Simon R" uniqKey="Ellwood S" first="Simon R." last="Ellwood">Simon R. Ellwood</name><affiliation><nlm:aff id="aff2">Centre for Crop and Disease Management, Department of Environment and Agriculture,<institution>Curtin University</institution>, Bentley, Perth, WA 6102,<country>Australia</country>;</nlm:aff></affiliation></author><author><name sortKey="Wise, Roger" sort="Wise, Roger" uniqKey="Wise R" first="Roger" last="Wise">Roger Wise</name><affiliation><nlm:aff id="aff3">Corn Insects and Crop Genetics Research, Agricultural Research Service,<institution>US Department of Agriculture</institution>, Ames,<addr-line>IA</addr-line> 50011-1020;</nlm:aff></affiliation><affiliation><nlm:aff id="aff4">Department of Plant Pathology and Microbiology, Center for Plant Responses to Environmental Stresses,<institution>Iowa State University</institution>, Ames,<addr-line>IA</addr-line> 50011-1020;</nlm:aff></affiliation></author><author><name sortKey="Yaeno, Takashi" sort="Yaeno, Takashi" uniqKey="Yaeno T" first="Takashi" last="Yaeno">Takashi Yaeno</name><affiliation><nlm:aff id="aff5">Faculty of Agriculture,<institution>Ehime University</institution>, Matsuyama, Ehime 790-8566,<country>Japan</country></nlm:aff></affiliation></author><author><name sortKey="Maekawa, Takaki" sort="Maekawa, Takaki" uniqKey="Maekawa T" first="Takaki" last="Maekawa">Takaki Maekawa</name><affiliation><nlm:aff id="aff1">Department of Plant-Microbe Interactions,<institution>Max Planck Institute for Plant Breeding Research</institution>, Cologne D-50829,<country>Germany</country>;</nlm:aff></affiliation></author><author><name sortKey="Schulze Lefert, Paul" sort="Schulze Lefert, Paul" uniqKey="Schulze Lefert P" first="Paul" last="Schulze-Lefert">Paul Schulze-Lefert</name><affiliation><nlm:aff id="aff1">Department of Plant-Microbe Interactions,<institution>Max Planck Institute for Plant Breeding Research</institution>, Cologne D-50829,<country>Germany</country>;</nlm:aff></affiliation></author></analytic><series><title level="j">Proceedings of the National Academy of Sciences of the United States of America</title><idno type="ISSN">0027-8424</idno><idno type="eISSN">1091-6490</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>Significance</title><p>Gene-for-gene immunity is frequently found in interactions between plants and host-adapted pathogens and reflects population-level diversification of immune receptors detecting matching pathogen effectors. We identified effector genes of a pathogenic powdery mildew fungus that are recognized by allelic variants of barley intracellular nucleotide-binding domain and leucine-rich repeat protein-type receptors. These pathogen effectors are phylogenetically unrelated, demonstrating that allelic immune receptors can evolve to recognize sequence-unrelated proteins. Conserved effector recognition in distantly related <italic>Arabidopsis</italic> indicates that the underlying mechanism is not restricted to monocotyledonous plants. Furthermore, our study reveals that the expression of a fungal avirulence effector alone is necessary and sufficient for allele-specific mildew resistance locus A receptor activation in planta<italic>.</italic></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">Proc Natl Acad Sci U S A</journal-id><journal-id journal-id-type="iso-abbrev">Proc. Natl. Acad. Sci. U.S.A</journal-id><journal-id journal-id-type="hwp">pnas</journal-id><journal-id journal-id-type="pmc">pnas</journal-id><journal-id journal-id-type="publisher-id">PNAS</journal-id><journal-title-group><journal-title>Proceedings of the National Academy of Sciences of the United States of America</journal-title></journal-title-group><issn pub-type="ppub">0027-8424</issn><issn pub-type="epub">1091-6490</issn><publisher><publisher-name>National Academy of Sciences</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">27702901</article-id><article-id pub-id-type="pmc">5081590</article-id><article-id pub-id-type="publisher-id">201612947</article-id><article-id pub-id-type="doi">10.1073/pnas.1612947113</article-id><article-categories><subj-group subj-group-type="heading"><subject>PNAS Plus</subject></subj-group><subj-group subj-group-type="heading"><subject>Biological Sciences</subject><subj-group><subject>Microbiology</subject></subj-group></subj-group><series-title>PNAS Plus</series-title></article-categories><title-group><article-title>Allelic barley MLA immune receptors recognize sequence-unrelated avirulence effectors of the powdery mildew pathogen</article-title><alt-title alt-title-type="short">Isolation of powdery mildew avirulence effectors</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Lu</surname><given-names>Xunli</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="author-notes" rid="fn1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Kracher</surname><given-names>Barbara</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="author-notes" rid="fn1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Saur</surname><given-names>Isabel M. L.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Bauer</surname><given-names>Saskia</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Ellwood</surname><given-names>Simon R.</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref></contrib><contrib contrib-type="author"><name><surname>Wise</surname><given-names>Roger</given-names></name><xref ref-type="aff" rid="aff3"><sup>c</sup></xref><xref ref-type="aff" rid="aff4"><sup>d</sup></xref></contrib><contrib contrib-type="author"><name><surname>Yaeno</surname><given-names>Takashi</given-names></name><xref ref-type="aff" rid="aff5"><sup>e</sup></xref></contrib><contrib contrib-type="author"><name><surname>Maekawa</surname><given-names>Takaki</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="corresp" rid="cor1"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Schulze-Lefert</surname><given-names>Paul</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="corresp" rid="cor1"><sup>2</sup></xref></contrib><aff id="aff1"><sup>a</sup>Department of Plant-Microbe Interactions,<institution>Max Planck Institute for Plant Breeding Research</institution>, Cologne D-50829,<country>Germany</country>;</aff><aff id="aff2"><sup>b</sup>Centre for Crop and Disease Management, Department of Environment and Agriculture,<institution>Curtin University</institution>, Bentley, Perth, WA 6102,<country>Australia</country>;</aff><aff id="aff3"><sup>c</sup>Corn Insects and Crop Genetics Research, Agricultural Research Service,<institution>US Department of Agriculture</institution>, Ames,<addr-line>IA</addr-line> 50011-1020;</aff><aff id="aff4"><sup>d</sup>Department of Plant Pathology and Microbiology, Center for Plant Responses to Environmental Stresses,<institution>Iowa State University</institution>, Ames,<addr-line>IA</addr-line> 50011-1020;</aff><aff id="aff5"><sup>e</sup>Faculty of Agriculture,<institution>Ehime University</institution>, Matsuyama, Ehime 790-8566,<country>Japan</country></aff></contrib-group><author-notes><corresp id="cor1"><sup>2</sup>To whom correspondence may be addressed. Email: <email>schlef@mpipz.mpg.de</email> or <email>maekawa@mpipz.mpg.de</email>.</corresp><fn fn-type="edited-by"><p>Contributed by Paul Schulze-Lefert, August 4, 2016 (sent for review June 20, 2016; reviewed by Sophien Kamoun, Beat Keller, and Brian J. Staskawicz)</p></fn><fn fn-type="con"><p>Author contributions: X.L., T.M., and P.S.-L. designed research; X.L., I.M.L.S., S.B., and T.M. performed research; S.R.E., R.W., and T.Y. contributed new reagents/analytic tools; B.K. analyzed data; and X.L., B.K., T.M., and P.S.-L. wrote the paper.</p></fn><fn fn-type="con"><p>Reviewers: S.K., The Sainsbury Laboratory; B.K., University of Zürich; and B.J.S., University of California Berkeley.</p></fn><fn fn-type="equal" id="fn1"><p><sup>1</sup>X.L. and B.K. contributed equally to this work.</p></fn><fn fn-type="COI-statement"><p>The authors declare no conflict of interest.</p></fn></author-notes><pub-date pub-type="ppub"><day>18</day><month>10</month><year>2016</year></pub-date><pub-date pub-type="epub"><day>4</day><month>10</month><year>2016</year></pub-date><pub-date pub-type="pmc-release"><day>4</day><month>10</month><year>2016</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was based on the
<volume>113</volume><issue>42</issue><fpage>E6486</fpage><lpage>E6495</lpage><permissions><license license-type="open-access"><license-p>Freely available online through the PNAS open access option.</license-p></license></permissions><self-uri xlink:title="pdf" xlink:href="pnas.201612947.pdf"></self-uri><abstract abstract-type="executive-summary"><title>Significance</title><p>Gene-for-gene immunity is frequently found in interactions between plants and host-adapted pathogens and reflects population-level diversification of immune receptors detecting matching pathogen effectors. We identified effector genes of a pathogenic powdery mildew fungus that are recognized by allelic variants of barley intracellular nucleotide-binding domain and leucine-rich repeat protein-type receptors. These pathogen effectors are phylogenetically unrelated, demonstrating that allelic immune receptors can evolve to recognize sequence-unrelated proteins. Conserved effector recognition in distantly related <italic>Arabidopsis</italic> indicates that the underlying mechanism is not restricted to monocotyledonous plants. Furthermore, our study reveals that the expression of a fungal avirulence effector alone is necessary and sufficient for allele-specific mildew resistance locus A receptor activation in planta<italic>.</italic></p></abstract><abstract><p>Disease-resistance genes encoding intracellular nucleotide-binding domain and leucine-rich repeat proteins (NLRs) are key components of the plant innate immune system and typically detect the presence of isolate-specific avirulence (AVR) effectors from pathogens. <italic>NLR</italic> genes define the fastest-evolving gene family of flowering plants and are often arranged in gene clusters containing multiple paralogs, contributing to copy number and allele-specific <italic>NLR</italic> variation within a host species. Barley <italic>mildew resistance locus a</italic> (<italic>Mla</italic>) has been subject to extensive functional diversification, resulting in allelic resistance specificities each recognizing a cognate, but largely unidentified, <italic>AVR</italic><sub><italic>a</italic></sub> gene of the powdery mildew fungus, <italic>Blumeria graminis</italic> f. sp. <italic>hordei</italic> (<italic>Bgh</italic>). We applied a transcriptome-wide association study among 17 <italic>Bgh</italic> isolates containing different <italic>AVR</italic><sub><italic>a</italic></sub> genes and identified <italic>AVR</italic><sub><italic>a1</italic></sub> and <italic>AVR</italic><sub><italic>a13</italic></sub>, encoding candidate-secreted effectors recognized by <italic>Mla1</italic> and <italic>Mla13</italic> alleles, respectively. Transient expression of the effector genes in barley leaves or protoplasts was sufficient to trigger <italic>Mla1</italic> or <italic>Mla13</italic> allele-specific cell death, a hallmark of NLR receptor-mediated immunity. <italic>AVR</italic><sub><italic>a1</italic></sub> and <italic>AVR</italic><sub><italic>a13</italic></sub> are phylogenetically unrelated, demonstrating that certain allelic MLA receptors evolved to recognize sequence-unrelated effectors. They are ancient effectors because corresponding loci are present in wheat powdery mildew. AVR<sub>A1</sub> recognition by barley MLA1 is retained in transgenic <italic>Arabidopsis</italic>, indicating that AVR<sub>A1</sub> directly binds MLA1 or that its recognition involves an evolutionarily conserved host target of AVR<sub>A1</sub>. Furthermore, analysis of transcriptome-wide sequence variation among the <italic>Bgh</italic> isolates provides evidence for <italic>Bgh</italic> population structure that is partially linked to geographic isolation.</p></abstract><kwd-group><kwd>avirulence effectors</kwd><kwd>association analysis</kwd><kwd>R genes</kwd><kwd>plant-microbe interactions</kwd><kwd>powdery mildew</kwd></kwd-group><funding-group><award-group id="gs1"><funding-source id="sp1">Max-Planck-Gesellschaft (Max Planck Society)<named-content content-type="funder-id">501100004189</named-content></funding-source><award-id rid="sp1">N/A</award-id></award-group><award-group id="gs2"><funding-source id="sp2">Deutsche Forschungsgemeinschaft (DFG)<named-content content-type="funder-id">501100001659</named-content></funding-source><award-id rid="sp2">SFB670</award-id></award-group><award-group id="gs3"><funding-source id="sp3">Grains Research and Development Corporation (GRDC)<named-content content-type="funder-id">501100000980</named-content></funding-source><award-id rid="sp3">CUR00017</award-id><award-id rid="sp3">CUR00023 P8</award-id></award-group><award-group id="gs4"><funding-source id="sp4">Inamori Foundation<named-content content-type="funder-id">501100003844</named-content></funding-source><award-id rid="sp4">JP16K07618</award-id></award-group></funding-group><counts><page-count count="10"></page-count></counts></article-meta></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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