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A Small Cysteine-Rich Protein from the Asian Soybean Rust Fungus, Phakopsora pachyrhizi, Suppresses Plant Immunity

Identifieur interne : 000653 ( Pmc/Checkpoint ); précédent : 000652; suivant : 000654

A Small Cysteine-Rich Protein from the Asian Soybean Rust Fungus, Phakopsora pachyrhizi, Suppresses Plant Immunity

Auteurs : Mingsheng Qi [États-Unis] ; Tobias I. Link [Allemagne] ; Manuel Müller [Allemagne] ; Daniela Hirschburger [Allemagne] ; Ramesh N. Pudake [Inde] ; Kerry F. Pedley [États-Unis] ; Edward Braun [États-Unis] ; Ralf T. Voegele [Allemagne] ; Thomas J. Baum [États-Unis] ; Steven A. Whitham [États-Unis]

Source :

RBID : PMC:5038961

Abstract

The Asian soybean rust fungus, Phakopsora pachyrhizi, is an obligate biotrophic pathogen causing severe soybean disease epidemics. Molecular mechanisms by which P. pachyrhizi and other rust fungi interact with their host plants are poorly understood. The genomes of all rust fungi encode many small, secreted cysteine-rich proteins (SSCRP). While these proteins are thought to function within the host, their roles are completely unknown. Here, we present the characterization of P. pachyrhizi effector candidate 23 (PpEC23), a SSCRP that we show to suppress plant immunity. Furthermore, we show that PpEC23 interacts with soybean transcription factor GmSPL12l and that soybean plants in which GmSPL12l is silenced have constitutively active immunity, thereby identifying GmSPL12l as a negative regulator of soybean defenses. Collectively, our data present evidence for a virulence function of a rust SSCRP and suggest that PpEC23 is able to suppress soybean immune responses and physically interact with soybean transcription factor GmSPL12l, a negative immune regulator.


Url:
DOI: 10.1371/journal.ppat.1005827
PubMed: 27676173
PubMed Central: 5038961


Affiliations:


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PMC:5038961

Le document en format XML

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<p>The Asian soybean rust fungus,
<italic>Phakopsora pachyrhizi</italic>
, is an obligate biotrophic pathogen causing severe soybean disease epidemics. Molecular mechanisms by which
<italic>P</italic>
.
<italic>pachyrhizi</italic>
and other rust fungi interact with their host plants are poorly understood. The genomes of all rust fungi encode many small, secreted cysteine-rich proteins (SSCRP). While these proteins are thought to function within the host, their roles are completely unknown. Here, we present the characterization of
<italic>P</italic>
.
<italic>pachyrhizi</italic>
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EC23), a SSCRP that we show to suppress plant immunity. Furthermore, we show that
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SPL12l as a negative regulator of soybean defenses. Collectively, our data present evidence for a virulence function of a rust SSCRP and suggest that
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EC23 is able to suppress soybean immune responses and physically interact with soybean transcription factor
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SPL12l, a negative immune regulator.</p>
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<title-group>
<article-title>A Small Cysteine-Rich Protein from the Asian Soybean Rust Fungus,
<italic>Phakopsora pachyrhizi</italic>
, Suppresses Plant Immunity</article-title>
<alt-title alt-title-type="running-head">A Small Cysteine-Rich Rust Protein Suppresses Plant Immunity</alt-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Qi</surname>
<given-names>Mingsheng</given-names>
</name>
<xref ref-type="aff" rid="aff001">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Link</surname>
<given-names>Tobias I.</given-names>
</name>
<xref ref-type="aff" rid="aff002">
<sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Müller</surname>
<given-names>Manuel</given-names>
</name>
<xref ref-type="aff" rid="aff002">
<sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Hirschburger</surname>
<given-names>Daniela</given-names>
</name>
<xref ref-type="aff" rid="aff002">
<sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Pudake</surname>
<given-names>Ramesh N.</given-names>
</name>
<xref ref-type="aff" rid="aff003">
<sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Pedley</surname>
<given-names>Kerry F.</given-names>
</name>
<xref ref-type="aff" rid="aff004">
<sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Braun</surname>
<given-names>Edward</given-names>
</name>
<xref ref-type="aff" rid="aff001">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Voegele</surname>
<given-names>Ralf T.</given-names>
</name>
<xref ref-type="aff" rid="aff002">
<sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Baum</surname>
<given-names>Thomas J.</given-names>
</name>
<xref ref-type="aff" rid="aff001">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0003-3542-3188</contrib-id>
<name>
<surname>Whitham</surname>
<given-names>Steven A.</given-names>
</name>
<xref ref-type="aff" rid="aff001">
<sup>1</sup>
</xref>
<xref ref-type="corresp" rid="cor001">*</xref>
</contrib>
</contrib-group>
<aff id="aff001">
<label>1</label>
<addr-line>Department of Plant Pathology and Microbiology, Iowa State University, Ames, Iowa, United States of America</addr-line>
</aff>
<aff id="aff002">
<label>2</label>
<addr-line>Institut für Phytomedizin, Universität Hohenheim, Stuttgart, Germany</addr-line>
</aff>
<aff id="aff003">
<label>3</label>
<addr-line>Amity Institute of Nanotechnology, Amity University Uttar Pradesh, Noida, India</addr-line>
</aff>
<aff id="aff004">
<label>4</label>
<addr-line>Foreign Disease-Weed Science Research Unit, United States Department of Agriculture–Agricultural Research Service, Ft. Detrick, Maryland, United States of America</addr-line>
</aff>
<contrib-group>
<contrib contrib-type="editor">
<name>
<surname>Dodds</surname>
<given-names>Peter N</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1">
<addr-line>CSIRO, AUSTRALIA</addr-line>
</aff>
<author-notes>
<fn fn-type="COI-statement" id="coi001">
<p>The authors have declared that no competing interests exist.</p>
</fn>
<fn fn-type="con">
<p>
<list list-type="simple">
<list-item>
<p>
<bold>Conceived and designed the experiments:</bold>
MQ TIL KFP RTV TJB SAW.</p>
</list-item>
<list-item>
<p>
<bold>Performed the experiments:</bold>
MQ TIL MM DH KFP EB.</p>
</list-item>
<list-item>
<p>
<bold>Analyzed the data:</bold>
MQ TIL MM DH KFP EB SAW.</p>
</list-item>
<list-item>
<p>
<bold>Contributed reagents/materials/analysis tools:</bold>
TIL RNP KFP EB SAW.</p>
</list-item>
<list-item>
<p>
<bold>Wrote the paper:</bold>
MQ TIL KFP RTV TJB SAW.</p>
</list-item>
</list>
</p>
</fn>
<corresp id="cor001">* E-mail:
<email>swhitham@iastate.edu</email>
</corresp>
</author-notes>
<pub-date pub-type="epub">
<day>27</day>
<month>9</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="collection">
<month>9</month>
<year>2016</year>
</pub-date>
<volume>12</volume>
<issue>9</issue>
<elocation-id>e1005827</elocation-id>
<history>
<date date-type="received">
<day>19</day>
<month>7</month>
<year>2015</year>
</date>
<date date-type="accepted">
<day>26</day>
<month>7</month>
<year>2016</year>
</date>
</history>
<permissions>
<license xlink:href="https://creativecommons.org/publicdomain/zero/1.0/">
<license-p>This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration, which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:href="ppat.1005827.pdf"></self-uri>
<abstract>
<p>The Asian soybean rust fungus,
<italic>Phakopsora pachyrhizi</italic>
, is an obligate biotrophic pathogen causing severe soybean disease epidemics. Molecular mechanisms by which
<italic>P</italic>
.
<italic>pachyrhizi</italic>
and other rust fungi interact with their host plants are poorly understood. The genomes of all rust fungi encode many small, secreted cysteine-rich proteins (SSCRP). While these proteins are thought to function within the host, their roles are completely unknown. Here, we present the characterization of
<italic>P</italic>
.
<italic>pachyrhizi</italic>
effector candidate 23 (
<italic>Pp</italic>
EC23), a SSCRP that we show to suppress plant immunity. Furthermore, we show that
<italic>Pp</italic>
EC23 interacts with soybean transcription factor
<italic>Gm</italic>
SPL12l and that soybean plants in which
<italic>GmSPL12l</italic>
is silenced have constitutively active immunity, thereby identifying
<italic>Gm</italic>
SPL12l as a negative regulator of soybean defenses. Collectively, our data present evidence for a virulence function of a rust SSCRP and suggest that
<italic>Pp</italic>
EC23 is able to suppress soybean immune responses and physically interact with soybean transcription factor
<italic>Gm</italic>
SPL12l, a negative immune regulator.</p>
</abstract>
<abstract abstract-type="summary">
<title>Author Summary</title>
<p>Asian soybean rust is a disease caused by the rust fungus,
<italic>Phakopsora pachyrhizi</italic>
, which was first described in Japan in 1902 and eventually reached North and South America in the early 2000s. Like other rust fungi,
<italic>P</italic>
.
<italic>pachyrhizi</italic>
, is capable of causing disease epidemics that severely reduce crop yields. Rust fungi require living host tissue in order to complete their life cycles, and thus, we expect that they produce and secrete effector proteins that are transferred into plant cells to interfere with immune responses. Small proteins that are rich in the amino acid cysteine and predicted to be secreted have been proposed to be likely candidates for effector proteins. Here, we report that a secreted, small cysteine-rich protein from
<italic>P</italic>
.
<italic>pachyrhizi</italic>
suppresses plant immunity, and furthermore, it interacts with a soybean transcription factor protein. Interestingly, silencing of this transcription factor results in plants that have increased expression of defense marker genes and enhanced disease resistance, which demonstrates that it is a negative regulator of soybean immune responses. Our work shows that, indeed, a small cysteine-rich protein from a rust fungus can suppress plant immunity, and furthermore, it identifies a new function for SQUAMOSA PROMOTER BINDING-LIKE (SPL) transcription factors as components of the defense regulatory networks that holds immune responses in check.</p>
</abstract>
<funding-group>
<award-group id="award001">
<funding-source>
<institution>Iowa Soybean Association</institution>
</funding-source>
<principal-award-recipient>
<contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0003-3542-3188</contrib-id>
<name>
<surname>Whitham</surname>
<given-names>Steven A</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group id="award002">
<funding-source>
<institution-wrap>
<institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/501100001659</institution-id>
<institution>Deutsche Forschungsgemeinschaft</institution>
</institution-wrap>
</funding-source>
<award-id>VO595/3-1</award-id>
<principal-award-recipient>
<name>
<surname>Voegele</surname>
<given-names>Ralf T.</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group id="award003">
<funding-source>
<institution-wrap>
<institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/501100001659</institution-id>
<institution>Deutsche Forschungsgemeinschaft</institution>
</institution-wrap>
</funding-source>
<award-id>VO595/3-2</award-id>
<principal-award-recipient>
<name>
<surname>Voegele</surname>
<given-names>Ralf T.</given-names>
</name>
</principal-award-recipient>
</award-group>
<funding-statement>This work was supported by the Iowa Soybean Association (SAW TJB), USDA National Institute of Food and Agriculture Hatch project 3708, and the Deutsche Forschungsgemeinschaft (VO595/3-1 and VO595/3-2 to RTV). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement>
</funding-group>
<counts>
<fig-count count="7"></fig-count>
<table-count count="2"></table-count>
<page-count count="29"></page-count>
</counts>
<custom-meta-group>
<custom-meta id="data-availability">
<meta-name>Data Availability</meta-name>
<meta-value>All relevant data are within the paper and its Supporting Information files.</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
<notes>
<title>Data Availability</title>
<p>All relevant data are within the paper and its Supporting Information files.</p>
</notes>
</front>
</pmc>
<affiliations>
<list>
<country>
<li>Allemagne</li>
<li>Inde</li>
<li>États-Unis</li>
</country>
<region>
<li>Bade-Wurtemberg</li>
<li>District de Stuttgart</li>
<li>Iowa</li>
<li>Maryland</li>
</region>
<settlement>
<li>Ames (Iowa)</li>
<li>Stuttgart</li>
</settlement>
<orgName>
<li>Université d'État de l'Iowa</li>
</orgName>
</list>
<tree>
<country name="États-Unis">
<region name="Iowa">
<name sortKey="Qi, Mingsheng" sort="Qi, Mingsheng" uniqKey="Qi M" first="Mingsheng" last="Qi">Mingsheng Qi</name>
</region>
<name sortKey="Baum, Thomas J" sort="Baum, Thomas J" uniqKey="Baum T" first="Thomas J." last="Baum">Thomas J. Baum</name>
<name sortKey="Braun, Edward" sort="Braun, Edward" uniqKey="Braun E" first="Edward" last="Braun">Edward Braun</name>
<name sortKey="Pedley, Kerry F" sort="Pedley, Kerry F" uniqKey="Pedley K" first="Kerry F." last="Pedley">Kerry F. Pedley</name>
<name sortKey="Whitham, Steven A" sort="Whitham, Steven A" uniqKey="Whitham S" first="Steven A." last="Whitham">Steven A. Whitham</name>
</country>
<country name="Allemagne">
<region name="Bade-Wurtemberg">
<name sortKey="Link, Tobias I" sort="Link, Tobias I" uniqKey="Link T" first="Tobias I." last="Link">Tobias I. Link</name>
</region>
<name sortKey="Hirschburger, Daniela" sort="Hirschburger, Daniela" uniqKey="Hirschburger D" first="Daniela" last="Hirschburger">Daniela Hirschburger</name>
<name sortKey="Muller, Manuel" sort="Muller, Manuel" uniqKey="Muller M" first="Manuel" last="Müller">Manuel Müller</name>
<name sortKey="Voegele, Ralf T" sort="Voegele, Ralf T" uniqKey="Voegele R" first="Ralf T." last="Voegele">Ralf T. Voegele</name>
</country>
<country name="Inde">
<noRegion>
<name sortKey="Pudake, Ramesh N" sort="Pudake, Ramesh N" uniqKey="Pudake R" first="Ramesh N." last="Pudake">Ramesh N. Pudake</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>

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