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A Novel Sterol Regulatory Element-Binding Protein Gene (sreA) Identified in Penicilliumdigitatum Is Required for Prochloraz Resistance, Full Virulence and erg11 (cyp51) Regulation

Identifieur interne : 000125 ( Pmc/Curation ); précédent : 000124; suivant : 000126

A Novel Sterol Regulatory Element-Binding Protein Gene (sreA) Identified in Penicilliumdigitatum Is Required for Prochloraz Resistance, Full Virulence and erg11 (cyp51) Regulation

Auteurs : Jing Liu ; Yongze Yuan ; Zhi Wu ; Na Li ; Yuanlei Chen ; Tingting Qin ; Hui Geng ; Li Xiong ; Deli Liu

Source :

RBID : PMC:4336317

Abstract

Penicilliumdigitatum is the most destructive postharvest pathogen of citrus fruits, causing fruit decay and economic loss. Additionally, control of the disease is further complicated by the emergence of drug-resistant strains due to the extensive use of triazole antifungal drugs. In this work, an orthologus gene encoding a putative sterol regulatory element-binding protein (SREBP) was identified in the genome of P. digitatum and named sreA. The putative SreA protein contains a conserved domain of unknown function (DUF2014) at its carboxyl terminus and a helix-loop-helix (HLH) leucine zipper DNA binding domain at its amino terminus, domains that are functionally associated with SREBP transcription factors. The deletion of sreA (ΔsreA) in a prochloraz-resistant strain (PdHS-F6) by Agrobacteriumtumefaciens-mediated transformation led to increased susceptibility to prochloraz and a significantly lower EC50 value compared with the HS-F6 wild-type or complementation strain (COsreA). A virulence assay showed that the ΔsreA strain was defective in virulence towards citrus fruits, while the complementation of sreA could restore the virulence to a large extent. Further analysis by quantitative real-time PCR demonstrated that prochloraz-induced expression of cyp51A and cyp51B in PdHS-F6 was completely abolished in the ΔsreA strain. These results demonstrate that sreA is a critical transcription factor gene required for prochloraz resistance and full virulence in P. digitatum and is involved in the regulation of cyp51 expression.


Url:
DOI: 10.1371/journal.pone.0117115
PubMed: 25699519
PubMed Central: 4336317

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<title xml:lang="en">A Novel Sterol Regulatory Element-Binding Protein Gene (
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<italic>digitatum</italic>
Is Required for Prochloraz Resistance, Full Virulence and
<italic>erg11</italic>
(
<italic>cyp51</italic>
) Regulation</title>
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<name sortKey="Liu, Jing" sort="Liu, Jing" uniqKey="Liu J" first="Jing" last="Liu">Jing Liu</name>
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<title xml:lang="en" level="a" type="main">A Novel Sterol Regulatory Element-Binding Protein Gene (
<italic>sreA</italic>
) Identified in
<italic>Penicillium</italic>
<italic>digitatum</italic>
Is Required for Prochloraz Resistance, Full Virulence and
<italic>erg11</italic>
(
<italic>cyp51</italic>
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<name sortKey="Liu, Jing" sort="Liu, Jing" uniqKey="Liu J" first="Jing" last="Liu">Jing Liu</name>
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<p>
<italic>Penicillium</italic>
<italic>digitatum</italic>
is the most destructive postharvest pathogen of citrus fruits, causing fruit decay and economic loss. Additionally, control of the disease is further complicated by the emergence of drug-resistant strains due to the extensive use of triazole antifungal drugs. In this work, an orthologus gene encoding a putative sterol regulatory element-binding protein (SREBP) was identified in the genome of
<italic>P</italic>
.
<italic>digitatum</italic>
and named
<italic>sreA</italic>
. The putative SreA protein contains a conserved domain of unknown function (DUF2014) at its carboxyl terminus and a helix-loop-helix (HLH) leucine zipper DNA binding domain at its amino terminus, domains that are functionally associated with SREBP transcription factors. The deletion of
<italic>sreA</italic>
(ΔsreA) in a prochloraz-resistant strain (PdHS-F6) by
<italic>Agrobacterium</italic>
<italic>tumefaciens</italic>
-mediated transformation led to increased susceptibility to prochloraz and a significantly lower EC
<sub>50</sub>
value compared with the HS-F6 wild-type or complementation strain (CO
<italic>sreA</italic>
). A virulence assay showed that the Δ
<italic>sreA</italic>
strain was defective in virulence towards citrus fruits, while the complementation of
<italic>sreA</italic>
could restore the virulence to a large extent. Further analysis by quantitative real-time PCR demonstrated that prochloraz-induced expression of
<italic>cyp51A</italic>
and
<italic>cyp51B</italic>
in PdHS-F6 was completely abolished in the Δ
<italic>sreA</italic>
strain. These results demonstrate that
<italic>sreA</italic>
is a critical transcription factor gene required for prochloraz resistance and full virulence in
<italic>P</italic>
.
<italic>digitatum</italic>
and is involved in the regulation of
<italic>cyp51</italic>
expression.</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">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, CA USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">25699519</article-id>
<article-id pub-id-type="pmc">4336317</article-id>
<article-id pub-id-type="doi">10.1371/journal.pone.0117115</article-id>
<article-id pub-id-type="publisher-id">PONE-D-14-31804</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>A Novel Sterol Regulatory Element-Binding Protein Gene (
<italic>sreA</italic>
) Identified in
<italic>Penicillium</italic>
<italic>digitatum</italic>
Is Required for Prochloraz Resistance, Full Virulence and
<italic>erg11</italic>
(
<italic>cyp51</italic>
) Regulation</article-title>
<alt-title alt-title-type="running-head">Characterization of an SREBP in
<italic>P. digitatum</italic>
</alt-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Liu</surname>
<given-names>Jing</given-names>
</name>
<xref ref-type="author-notes" rid="econtrib001">
<sup></sup>
</xref>
<xref ref-type="aff" rid="aff001"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Yuan</surname>
<given-names>Yongze</given-names>
</name>
<xref ref-type="author-notes" rid="econtrib001">
<sup></sup>
</xref>
<xref ref-type="aff" rid="aff001"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Wu</surname>
<given-names>Zhi</given-names>
</name>
<xref ref-type="aff" rid="aff001"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Li</surname>
<given-names>Na</given-names>
</name>
<xref ref-type="aff" rid="aff001"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Chen</surname>
<given-names>Yuanlei</given-names>
</name>
<xref ref-type="aff" rid="aff001"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Qin</surname>
<given-names>Tingting</given-names>
</name>
<xref ref-type="aff" rid="aff001"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Geng</surname>
<given-names>Hui</given-names>
</name>
<xref ref-type="aff" rid="aff001"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Xiong</surname>
<given-names>Li</given-names>
</name>
<xref ref-type="aff" rid="aff001"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Liu</surname>
<given-names>Deli</given-names>
</name>
<xref rid="cor001" ref-type="corresp">*</xref>
<xref ref-type="aff" rid="aff001"></xref>
</contrib>
</contrib-group>
<aff id="aff001">
<addr-line>Hubei Key Laboratory of Genetic Regulation and Integrative Biology, School of Life Science, Central China Normal University, Wuhan, 430079, China</addr-line>
</aff>
<contrib-group>
<contrib contrib-type="editor">
<name>
<surname>Cramer</surname>
<given-names>Robert A.</given-names>
</name>
<role>Academic Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1">
<addr-line>Geisel School of Medicine at Dartmouth, UNITED STATES</addr-line>
</aff>
<author-notes>
<fn fn-type="conflict" id="coi001">
<p>
<bold>Competing Interests: </bold>
The authors have declared that no competing interests exist.</p>
</fn>
<fn fn-type="con" id="contrib001">
<p>Conceived and designed the experiments: DLL. Performed the experiments: JL YZY NL YLC TTQ. Analyzed the data: JL ZW. Contributed reagents/materials/analysis tools: HG LX. Wrote the paper: DLL JL.</p>
</fn>
<fn fn-type="other" id="econtrib001">
<p>‡ These authors contributed equally to this work.</p>
</fn>
<corresp id="cor001">* E-mail:
<email>ldl@mail.ccnu.edu.cn</email>
</corresp>
</author-notes>
<pub-date pub-type="epub">
<day>20</day>
<month>2</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="collection">
<year>2015</year>
</pub-date>
<volume>10</volume>
<issue>2</issue>
<elocation-id>e0117115</elocation-id>
<history>
<date date-type="received">
<day>4</day>
<month>8</month>
<year>2014</year>
</date>
<date date-type="accepted">
<day>17</day>
<month>12</month>
<year>2014</year>
</date>
</history>
<permissions>
<copyright-year>2015</copyright-year>
<copyright-holder>Liu et al</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/">
<license-p>This is an open access article distributed under the terms of the
<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>
, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:type="simple" xlink:href="pone.0117115.pdf"></self-uri>
<abstract>
<p>
<italic>Penicillium</italic>
<italic>digitatum</italic>
is the most destructive postharvest pathogen of citrus fruits, causing fruit decay and economic loss. Additionally, control of the disease is further complicated by the emergence of drug-resistant strains due to the extensive use of triazole antifungal drugs. In this work, an orthologus gene encoding a putative sterol regulatory element-binding protein (SREBP) was identified in the genome of
<italic>P</italic>
.
<italic>digitatum</italic>
and named
<italic>sreA</italic>
. The putative SreA protein contains a conserved domain of unknown function (DUF2014) at its carboxyl terminus and a helix-loop-helix (HLH) leucine zipper DNA binding domain at its amino terminus, domains that are functionally associated with SREBP transcription factors. The deletion of
<italic>sreA</italic>
(ΔsreA) in a prochloraz-resistant strain (PdHS-F6) by
<italic>Agrobacterium</italic>
<italic>tumefaciens</italic>
-mediated transformation led to increased susceptibility to prochloraz and a significantly lower EC
<sub>50</sub>
value compared with the HS-F6 wild-type or complementation strain (CO
<italic>sreA</italic>
). A virulence assay showed that the Δ
<italic>sreA</italic>
strain was defective in virulence towards citrus fruits, while the complementation of
<italic>sreA</italic>
could restore the virulence to a large extent. Further analysis by quantitative real-time PCR demonstrated that prochloraz-induced expression of
<italic>cyp51A</italic>
and
<italic>cyp51B</italic>
in PdHS-F6 was completely abolished in the Δ
<italic>sreA</italic>
strain. These results demonstrate that
<italic>sreA</italic>
is a critical transcription factor gene required for prochloraz resistance and full virulence in
<italic>P</italic>
.
<italic>digitatum</italic>
and is involved in the regulation of
<italic>cyp51</italic>
expression.</p>
</abstract>
<funding-group>
<funding-statement>This work was supported by the National Natural Science Foundations of China (NO. 31371893, 31071653, 31101595). 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="6"></fig-count>
<table-count count="1"></table-count>
<page-count count="17"></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.</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
<notes>
<title>Data Availability</title>
<p>All relevant data are within the paper.</p>
</notes>
</front>
</pmc>
</record>

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