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<title xml:lang="en">Effector MiSSP7 of the mutualistic fungus
<italic>Laccaria bicolor</italic>
stabilizes the
<italic>Populus</italic>
JAZ6 protein and represses jasmonic acid (JA) responsive genes</title>
<author>
<name sortKey="Plett, Jonathan M" sort="Plett, Jonathan M" uniqKey="Plett J" first="Jonathan M." last="Plett">Jonathan M. Plett</name>
<affiliation>
<nlm:aff id="aff1">Laboratoire d’Excellence Advanced Research on the Biology of Tree and Forest Ecosystems, Unité Mixte de Recherche
<institution>Institut National de la Recherche Agronomique–Université de Lorraine</institution>
“Interactions Arbres/Micro-organismes,” Champenoux 54180,
<country>France</country>
;</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff wicri:cut="; and" id="aff2">Hawkesbury Institute for the Environment,
<institution>University of Western Sydney</institution>
, Richmond 2753, NSW,
<country>Australia</country>
</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Daguerre, Yohann" sort="Daguerre, Yohann" uniqKey="Daguerre Y" first="Yohann" last="Daguerre">Yohann Daguerre</name>
<affiliation>
<nlm:aff id="aff1">Laboratoire d’Excellence Advanced Research on the Biology of Tree and Forest Ecosystems, Unité Mixte de Recherche
<institution>Institut National de la Recherche Agronomique–Université de Lorraine</institution>
“Interactions Arbres/Micro-organismes,” Champenoux 54180,
<country>France</country>
;</nlm:aff>
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<author>
<name sortKey="Wittulsky, Sebastian" sort="Wittulsky, Sebastian" uniqKey="Wittulsky S" first="Sebastian" last="Wittulsky">Sebastian Wittulsky</name>
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<nlm:aff id="aff1">Laboratoire d’Excellence Advanced Research on the Biology of Tree and Forest Ecosystems, Unité Mixte de Recherche
<institution>Institut National de la Recherche Agronomique–Université de Lorraine</institution>
“Interactions Arbres/Micro-organismes,” Champenoux 54180,
<country>France</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Vayssieres, Alice" sort="Vayssieres, Alice" uniqKey="Vayssieres A" first="Alice" last="Vayssières">Alice Vayssières</name>
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<institution>Institut National de la Recherche Agronomique–Université de Lorraine</institution>
“Interactions Arbres/Micro-organismes,” Champenoux 54180,
<country>France</country>
;</nlm:aff>
</affiliation>
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<author>
<name sortKey="Deveau, Aurelie" sort="Deveau, Aurelie" uniqKey="Deveau A" first="Aurelie" last="Deveau">Aurelie Deveau</name>
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<nlm:aff id="aff1">Laboratoire d’Excellence Advanced Research on the Biology of Tree and Forest Ecosystems, Unité Mixte de Recherche
<institution>Institut National de la Recherche Agronomique–Université de Lorraine</institution>
“Interactions Arbres/Micro-organismes,” Champenoux 54180,
<country>France</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Melton, Sarah J" sort="Melton, Sarah J" uniqKey="Melton S" first="Sarah J." last="Melton">Sarah J. Melton</name>
<affiliation>
<nlm:aff id="aff3">Biological and Nanoscale Systems, BioSciences Division,
<institution>Oak Ridge National Laboratory</institution>
, Oak Ridge,
<addr-line>TN</addr-line>
37831-6445</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Kohler, Annegret" sort="Kohler, Annegret" uniqKey="Kohler A" first="Annegret" last="Kohler">Annegret Kohler</name>
<affiliation>
<nlm:aff id="aff1">Laboratoire d’Excellence Advanced Research on the Biology of Tree and Forest Ecosystems, Unité Mixte de Recherche
<institution>Institut National de la Recherche Agronomique–Université de Lorraine</institution>
“Interactions Arbres/Micro-organismes,” Champenoux 54180,
<country>France</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Morrell Falvey, Jennifer L" sort="Morrell Falvey, Jennifer L" uniqKey="Morrell Falvey J" first="Jennifer L." last="Morrell-Falvey">Jennifer L. Morrell-Falvey</name>
<affiliation>
<nlm:aff id="aff3">Biological and Nanoscale Systems, BioSciences Division,
<institution>Oak Ridge National Laboratory</institution>
, Oak Ridge,
<addr-line>TN</addr-line>
37831-6445</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Brun, Annick" sort="Brun, Annick" uniqKey="Brun A" first="Annick" last="Brun">Annick Brun</name>
<affiliation>
<nlm:aff id="aff1">Laboratoire d’Excellence Advanced Research on the Biology of Tree and Forest Ecosystems, Unité Mixte de Recherche
<institution>Institut National de la Recherche Agronomique–Université de Lorraine</institution>
“Interactions Arbres/Micro-organismes,” Champenoux 54180,
<country>France</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Veneault Fourrey, Claire" sort="Veneault Fourrey, Claire" uniqKey="Veneault Fourrey C" first="Claire" last="Veneault-Fourrey">Claire Veneault-Fourrey</name>
<affiliation>
<nlm:aff id="aff1">Laboratoire d’Excellence Advanced Research on the Biology of Tree and Forest Ecosystems, Unité Mixte de Recherche
<institution>Institut National de la Recherche Agronomique–Université de Lorraine</institution>
“Interactions Arbres/Micro-organismes,” Champenoux 54180,
<country>France</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Martin, Francis" sort="Martin, Francis" uniqKey="Martin F" first="Francis" last="Martin">Francis Martin</name>
<affiliation>
<nlm:aff id="aff1">Laboratoire d’Excellence Advanced Research on the Biology of Tree and Forest Ecosystems, Unité Mixte de Recherche
<institution>Institut National de la Recherche Agronomique–Université de Lorraine</institution>
“Interactions Arbres/Micro-organismes,” Champenoux 54180,
<country>France</country>
;</nlm:aff>
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<title xml:lang="en" level="a" type="main">Effector MiSSP7 of the mutualistic fungus
<italic>Laccaria bicolor</italic>
stabilizes the
<italic>Populus</italic>
JAZ6 protein and represses jasmonic acid (JA) responsive genes</title>
<author>
<name sortKey="Plett, Jonathan M" sort="Plett, Jonathan M" uniqKey="Plett J" first="Jonathan M." last="Plett">Jonathan M. Plett</name>
<affiliation>
<nlm:aff id="aff1">Laboratoire d’Excellence Advanced Research on the Biology of Tree and Forest Ecosystems, Unité Mixte de Recherche
<institution>Institut National de la Recherche Agronomique–Université de Lorraine</institution>
“Interactions Arbres/Micro-organismes,” Champenoux 54180,
<country>France</country>
;</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff wicri:cut="; and" id="aff2">Hawkesbury Institute for the Environment,
<institution>University of Western Sydney</institution>
, Richmond 2753, NSW,
<country>Australia</country>
</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Daguerre, Yohann" sort="Daguerre, Yohann" uniqKey="Daguerre Y" first="Yohann" last="Daguerre">Yohann Daguerre</name>
<affiliation>
<nlm:aff id="aff1">Laboratoire d’Excellence Advanced Research on the Biology of Tree and Forest Ecosystems, Unité Mixte de Recherche
<institution>Institut National de la Recherche Agronomique–Université de Lorraine</institution>
“Interactions Arbres/Micro-organismes,” Champenoux 54180,
<country>France</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Wittulsky, Sebastian" sort="Wittulsky, Sebastian" uniqKey="Wittulsky S" first="Sebastian" last="Wittulsky">Sebastian Wittulsky</name>
<affiliation>
<nlm:aff id="aff1">Laboratoire d’Excellence Advanced Research on the Biology of Tree and Forest Ecosystems, Unité Mixte de Recherche
<institution>Institut National de la Recherche Agronomique–Université de Lorraine</institution>
“Interactions Arbres/Micro-organismes,” Champenoux 54180,
<country>France</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Vayssieres, Alice" sort="Vayssieres, Alice" uniqKey="Vayssieres A" first="Alice" last="Vayssières">Alice Vayssières</name>
<affiliation>
<nlm:aff id="aff1">Laboratoire d’Excellence Advanced Research on the Biology of Tree and Forest Ecosystems, Unité Mixte de Recherche
<institution>Institut National de la Recherche Agronomique–Université de Lorraine</institution>
“Interactions Arbres/Micro-organismes,” Champenoux 54180,
<country>France</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Deveau, Aurelie" sort="Deveau, Aurelie" uniqKey="Deveau A" first="Aurelie" last="Deveau">Aurelie Deveau</name>
<affiliation>
<nlm:aff id="aff1">Laboratoire d’Excellence Advanced Research on the Biology of Tree and Forest Ecosystems, Unité Mixte de Recherche
<institution>Institut National de la Recherche Agronomique–Université de Lorraine</institution>
“Interactions Arbres/Micro-organismes,” Champenoux 54180,
<country>France</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Melton, Sarah J" sort="Melton, Sarah J" uniqKey="Melton S" first="Sarah J." last="Melton">Sarah J. Melton</name>
<affiliation>
<nlm:aff id="aff3">Biological and Nanoscale Systems, BioSciences Division,
<institution>Oak Ridge National Laboratory</institution>
, Oak Ridge,
<addr-line>TN</addr-line>
37831-6445</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Kohler, Annegret" sort="Kohler, Annegret" uniqKey="Kohler A" first="Annegret" last="Kohler">Annegret Kohler</name>
<affiliation>
<nlm:aff id="aff1">Laboratoire d’Excellence Advanced Research on the Biology of Tree and Forest Ecosystems, Unité Mixte de Recherche
<institution>Institut National de la Recherche Agronomique–Université de Lorraine</institution>
“Interactions Arbres/Micro-organismes,” Champenoux 54180,
<country>France</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Morrell Falvey, Jennifer L" sort="Morrell Falvey, Jennifer L" uniqKey="Morrell Falvey J" first="Jennifer L." last="Morrell-Falvey">Jennifer L. Morrell-Falvey</name>
<affiliation>
<nlm:aff id="aff3">Biological and Nanoscale Systems, BioSciences Division,
<institution>Oak Ridge National Laboratory</institution>
, Oak Ridge,
<addr-line>TN</addr-line>
37831-6445</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Brun, Annick" sort="Brun, Annick" uniqKey="Brun A" first="Annick" last="Brun">Annick Brun</name>
<affiliation>
<nlm:aff id="aff1">Laboratoire d’Excellence Advanced Research on the Biology of Tree and Forest Ecosystems, Unité Mixte de Recherche
<institution>Institut National de la Recherche Agronomique–Université de Lorraine</institution>
“Interactions Arbres/Micro-organismes,” Champenoux 54180,
<country>France</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Veneault Fourrey, Claire" sort="Veneault Fourrey, Claire" uniqKey="Veneault Fourrey C" first="Claire" last="Veneault-Fourrey">Claire Veneault-Fourrey</name>
<affiliation>
<nlm:aff id="aff1">Laboratoire d’Excellence Advanced Research on the Biology of Tree and Forest Ecosystems, Unité Mixte de Recherche
<institution>Institut National de la Recherche Agronomique–Université de Lorraine</institution>
“Interactions Arbres/Micro-organismes,” Champenoux 54180,
<country>France</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Martin, Francis" sort="Martin, Francis" uniqKey="Martin F" first="Francis" last="Martin">Francis Martin</name>
<affiliation>
<nlm:aff id="aff1">Laboratoire d’Excellence Advanced Research on the Biology of Tree and Forest Ecosystems, Unité Mixte de Recherche
<institution>Institut National de la Recherche Agronomique–Université de Lorraine</institution>
“Interactions Arbres/Micro-organismes,” Champenoux 54180,
<country>France</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="2014">2014</date>
</imprint>
</series>
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<front>
<div type="abstract" xml:lang="en">
<title>Significance</title>
<p>Plants use the hormone jasmonic acid (JA) to modulate plant:microbe interactions. Disease-causing microbes use proteins to alter host JA signaling to aid their growth in plant tissues. Beneficial symbiotic fungi, which colonize plant tissues and provide essential ecosystem services such as carbon sequestration and plant fertilization, can also alter JA signaling in plant cells to promote colonization. Here, we demonstrate that the MiSSP7 (Mycorrhiza-induced small secreted protein-7) protein of the beneficial fungus
<italic>Laccaria bicolor</italic>
interacts with host plant JA signaling repressors and, in contrast to biotrophic pathogens, promotes symbiosis by blocking JA action. These results shed new light on how beneficial and pathogenic microbes have evolutionarily diverged in the mechanisms by which they overcome plant defenses.</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">24847068</article-id>
<article-id pub-id-type="pmc">4050555</article-id>
<article-id pub-id-type="publisher-id">201322671</article-id>
<article-id pub-id-type="doi">10.1073/pnas.1322671111</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Biological Sciences</subject>
<subj-group>
<subject>Plant Biology</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Effector MiSSP7 of the mutualistic fungus
<italic>Laccaria bicolor</italic>
stabilizes the
<italic>Populus</italic>
JAZ6 protein and represses jasmonic acid (JA) responsive genes</article-title>
<alt-title alt-title-type="short">Effector MiSSP7 interacts with JAZ proteins</alt-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Plett</surname>
<given-names>Jonathan M.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
<xref ref-type="author-notes" rid="fn1">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Daguerre</surname>
<given-names>Yohann</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>Wittulsky</surname>
<given-names>Sebastian</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>Vayssières</surname>
<given-names>Alice</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Deveau</surname>
<given-names>Aurelie</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Melton</surname>
<given-names>Sarah J.</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>c</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Kohler</surname>
<given-names>Annegret</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Morrell-Falvey</surname>
<given-names>Jennifer L.</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>c</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Brun</surname>
<given-names>Annick</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Veneault-Fourrey</surname>
<given-names>Claire</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>Martin</surname>
<given-names>Francis</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
<xref ref-type="author-notes" rid="fn1">
<sup>1</sup>
</xref>
<xref ref-type="corresp" rid="cor1">
<sup>2</sup>
</xref>
</contrib>
<aff id="aff1">
<sup>a</sup>
Laboratoire d’Excellence Advanced Research on the Biology of Tree and Forest Ecosystems, Unité Mixte de Recherche
<institution>Institut National de la Recherche Agronomique–Université de Lorraine</institution>
“Interactions Arbres/Micro-organismes,” Champenoux 54180,
<country>France</country>
;</aff>
<aff id="aff2">
<sup>b</sup>
Hawkesbury Institute for the Environment,
<institution>University of Western Sydney</institution>
, Richmond 2753, NSW,
<country>Australia</country>
; and</aff>
<aff id="aff3">
<sup>c</sup>
Biological and Nanoscale Systems, BioSciences Division,
<institution>Oak Ridge National Laboratory</institution>
, Oak Ridge,
<addr-line>TN</addr-line>
37831-6445</aff>
</contrib-group>
<author-notes>
<corresp id="cor1">
<sup>2</sup>
To whom correspondence should be addressed. E-mail:
<email>fmartin@nancy.inra.fr</email>
.</corresp>
<fn fn-type="edited-by">
<p>Edited by Jeffery L. Dangl, Howard Hughes Medical Institute and The University of North Carolina at Chapel Hill, Chapel Hill, NC, and approved April 8, 2014 (received for review December 8, 2013)</p>
</fn>
<fn fn-type="con">
<p>Author contributions: J.M.P., Y.D., S.W., A.V., A.D., J.M.-F., A.B., C.V.-F., and F.M. designed research; J.M.P., Y.D., S.W., A.V., A.D., S.J.M., A.K., J.M.-F., A.B., and C.V.-F. performed research; J.M.-F., A.B., C.V.-F., and F.M. contributed new reagents/analytic tools; J.M.P., Y.D., S.W., A.V., A.D., S.J.M., A.K., J.M.-F., A.B., C.V.-F., and F.M. analyzed data; and J.M.P., Y.D., J.M.-F., C.V.-F., and F.M. wrote the paper.</p>
</fn>
<fn fn-type="equal" id="fn1">
<p>
<sup>1</sup>
J.M.P., Y.D., S.W., C.V.-F., and F.M. contributed equally to this work.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub">
<day>3</day>
<month>6</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="epub">
<day>20</day>
<month>5</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="pmc-release">
<day>20</day>
<month>5</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>111</volume>
<issue>22</issue>
<fpage>8299</fpage>
<lpage>8304</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:type="simple" xlink:href="pnas.201322671.pdf"></self-uri>
<abstract abstract-type="executive-summary">
<title>Significance</title>
<p>Plants use the hormone jasmonic acid (JA) to modulate plant:microbe interactions. Disease-causing microbes use proteins to alter host JA signaling to aid their growth in plant tissues. Beneficial symbiotic fungi, which colonize plant tissues and provide essential ecosystem services such as carbon sequestration and plant fertilization, can also alter JA signaling in plant cells to promote colonization. Here, we demonstrate that the MiSSP7 (Mycorrhiza-induced small secreted protein-7) protein of the beneficial fungus
<italic>Laccaria bicolor</italic>
interacts with host plant JA signaling repressors and, in contrast to biotrophic pathogens, promotes symbiosis by blocking JA action. These results shed new light on how beneficial and pathogenic microbes have evolutionarily diverged in the mechanisms by which they overcome plant defenses.</p>
</abstract>
<abstract>
<p>Ectomycorrhizal fungi, such as
<italic>Laccaria bicolor</italic>
, support forest growth and sustainability by providing growth-limiting nutrients to their plant host through a mutualistic symbiotic relationship with host roots. We have previously shown that the effector protein MiSSP7 (Mycorrhiza-induced Small Secreted Protein 7) encoded by
<italic>L. bicolor</italic>
is necessary for the establishment of symbiosis with host trees, although the mechanistic reasoning behind this role was unknown. We demonstrate here that MiSSP7 interacts with the host protein PtJAZ6, a negative regulator of jasmonic acid (JA)-induced gene regulation in
<italic>Populus.</italic>
As with other characterized JASMONATE ZIM-DOMAIN (JAZ) proteins, PtJAZ6 interacts with PtCOI1 in the presence of the JA mimic coronatine, and PtJAZ6 is degraded in plant tissues after JA treatment. The association between MiSSP7 and PtJAZ6 is able to protect PtJAZ6 from this JA-induced degradation. Furthermore, MiSSP7 is able to block—or mitigate—the impact of JA on
<italic>L. bicolor</italic>
colonization of host roots. We show that the loss of MiSSP7 production by
<italic>L. bicolor</italic>
can be complemented by transgenically varying the transcription of
<italic>PtJAZ6</italic>
or through inhibition of JA-induced gene regulation. We conclude that
<italic>L. bicolor</italic>
, in contrast to arbuscular mycorrhizal fungi and biotrophic pathogens, promotes mutualism by blocking JA action through the interaction of MiSSP7 with PtJAZ6.</p>
</abstract>
<kwd-group>
<kwd>ectomycorrhizal fungus</kwd>
<kwd>defense</kwd>
<kwd>tree nutrition</kwd>
<kwd>host immunity</kwd>
<kwd>plant hormone</kwd>
</kwd-group>
<counts>
<page-count count="6"></page-count>
</counts>
</article-meta>
</front>
</pmc>
</record>

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