Systemic Induction of NO-, Redox-, and cGMP Signaling in the Pumpkin Extrafascicular Phloem upon Local Leaf Wounding
Identifieur interne : 000302 ( Pmc/Curation ); précédent : 000301; suivant : 000303Systemic Induction of NO-, Redox-, and cGMP Signaling in the Pumpkin Extrafascicular Phloem upon Local Leaf Wounding
Auteurs : Frank Gaupels [Allemagne] ; Alexandra C. U. Furch [Allemagne] ; Matthias R. Zimmermann [Allemagne] ; Faxing Chen [République populaire de Chine] ; Volkhard Kaever [Allemagne] ; Anja Buhtz [Allemagne] ; Julia Kehr [Allemagne] ; Hakan Sarioglu [Allemagne] ; Karl-Heinz Kogel [Allemagne] ; Jörg Durner [Allemagne]Source :
- Frontiers in Plant Science [ 1664-462X ] ; 2016.
Abstract
Cucurbits developed the unique extrafascicular phloem (EFP) as a defensive structure against herbivorous animals. Mechanical leaf injury was previously shown to induce a systemic wound response in the EFP of pumpkin (
Url:
DOI: 10.3389/fpls.2016.00154
PubMed: 26904092
PubMed Central: 4751408
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<front><div type="abstract" xml:lang="en"><p>Cucurbits developed the unique extrafascicular phloem (EFP) as a defensive structure against herbivorous animals. Mechanical leaf injury was previously shown to induce a systemic wound response in the EFP of pumpkin (<italic>Cucurbita maxima</italic>
). Here, we demonstrate that the phloem antioxidant system and protein modifications by NO are strongly regulated during this process. Activities of the central antioxidant enzymes dehydroascorbate reductase, glutathione reductase and ascorbate reductase were rapidly down-regulated at 30 min with a second minimum at 24 h after wounding. As a consequence levels of total ascorbate and glutathione also decreased with similar bi-phasic kinetics. These results hint toward a wound-induced shift in the redox status of the EFP. Nitric oxide (NO) is another important player in stress-induced redox signaling in plants. Therefore, we analyzed NO-dependent protein modifications in the EFP. Six to forty eight hours after leaf damage total S-nitrosothiol content and protein S-nitrosylation were clearly reduced, which was contrasted by a pronounced increase in protein tyrosine nitration. Collectively, these findings suggest that NO-dependent S-nitrosylation turned into peroxynitrite-mediated protein nitration upon a stress-induced redox shift probably involving the accumulation of reactive oxygen species within the EFP. Using the biotin switch assay and anti-nitrotyrosine antibodies we identified 9 candidate S-nitrosylated and 6 candidate tyrosine-nitrated phloem proteins. The wound-responsive Phloem Protein 16-1 (PP16-1) and Cyclophilin 18 (CYP18) as well as the 26.5 kD isoform of Phloem Protein 2 (PP2) were amenable to both NO modifications and could represent important redox-sensors within the cucurbit EFP. We also found that leaf injury triggered the systemic accumulation of cyclic guanosine monophosphate (cGMP) in the EFP and discuss the possible function of this second messenger in systemic NO and redox signaling within the EFP.</p>
</div>
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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">Front Plant Sci</journal-id>
<journal-id journal-id-type="iso-abbrev">Front Plant Sci</journal-id>
<journal-id journal-id-type="publisher-id">Front. Plant Sci.</journal-id>
<journal-title-group><journal-title>Frontiers in Plant Science</journal-title>
</journal-title-group>
<issn pub-type="epub">1664-462X</issn>
<publisher><publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">26904092</article-id>
<article-id pub-id-type="pmc">4751408</article-id>
<article-id pub-id-type="doi">10.3389/fpls.2016.00154</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Plant Science</subject>
<subj-group><subject>Original Research</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Systemic Induction of NO-, Redox-, and cGMP Signaling in the Pumpkin Extrafascicular Phloem upon Local Leaf Wounding</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Gaupels</surname>
<given-names>Frank</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn001"><sup>*</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/69406/overview"></uri>
</contrib>
<contrib contrib-type="author"><name><surname>Furch</surname>
<given-names>Alexandra C. U.</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/107547/overview"></uri>
</contrib>
<contrib contrib-type="author"><name><surname>Zimmermann</surname>
<given-names>Matthias R.</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/293269/overview"></uri>
</contrib>
<contrib contrib-type="author"><name><surname>Chen</surname>
<given-names>Faxing</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/300056/overview"></uri>
</contrib>
<contrib contrib-type="author"><name><surname>Kaever</surname>
<given-names>Volkhard</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/266857/overview"></uri>
</contrib>
<contrib contrib-type="author"><name><surname>Buhtz</surname>
<given-names>Anja</given-names>
</name>
<xref ref-type="aff" rid="aff5"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kehr</surname>
<given-names>Julia</given-names>
</name>
<xref ref-type="aff" rid="aff6"><sup>6</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/45438/overview"></uri>
</contrib>
<contrib contrib-type="author"><name><surname>Sarioglu</surname>
<given-names>Hakan</given-names>
</name>
<xref ref-type="aff" rid="aff7"><sup>7</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/310681/overview"></uri>
</contrib>
<contrib contrib-type="author"><name><surname>Kogel</surname>
<given-names>Karl-Heinz</given-names>
</name>
<xref ref-type="aff" rid="aff8"><sup>8</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/37942/overview"></uri>
</contrib>
<contrib contrib-type="author"><name><surname>Durner</surname>
<given-names>Jörg</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/13418/overview"></uri>
</contrib>
</contrib-group>
<aff id="aff1"><sup>1</sup>
<institution>Institute of Biochemical Plant Pathology, Helmholtz Zentrum München, German Research Center for Environmental Health</institution>
<country>Neuherberg, Germany</country>
</aff>
<aff id="aff2"><sup>2</sup>
<institution>Institute of General Botany and Plant Physiology, Friedrich-Schiller-University</institution>
<country>Jena, Germany</country>
</aff>
<aff id="aff3"><sup>3</sup>
<institution>College of Horticulture, Fujian Agriculture and Forestry University</institution>
<country>Fuzhou, China</country>
</aff>
<aff id="aff4"><sup>4</sup>
<institution>Research Core Unit Metabolomics, Hannover Medical School</institution>
<country>Hannover, Germany</country>
</aff>
<aff id="aff5"><sup>5</sup>
<institution>Department Lothar Willmitzer, Max Planck Institute of Molecular Plant Physiology</institution>
<country>Potsdam, Germany</country>
</aff>
<aff id="aff6"><sup>6</sup>
<institution>Biocenter Klein Flottbek, University Hamburg</institution>
<country>Hamburg, Germany</country>
</aff>
<aff id="aff7"><sup>7</sup>
<institution>Department of Protein Science, Helmholtz Zentrum München, German Research Center for Environmental Health</institution>
<country>Neuherberg, Germany</country>
</aff>
<aff id="aff8"><sup>8</sup>
<institution>Research Center for BioSystems, Land Use and Nutrition, Institute of Phytopathology, Justus Liebig University Giessen</institution>
<country>Giessen, Germany</country>
</aff>
<author-notes><fn fn-type="edited-by"><p>Edited by: Irene Murgia, Università degli Studi di Milano, Italy</p>
</fn>
<fn fn-type="edited-by"><p>Reviewed by: María C. Romero-Puertas, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, Spain; Luisa M. Sandalio, Consejo Superior de Investigaciones Científicas, Spain</p>
</fn>
<corresp id="fn001">*Correspondence: Frank Gaupels <email xlink:type="simple">frank.gaupels@helmholtz-muenchen.de</email>
</corresp>
<fn fn-type="other" id="fn002"><p>This article was submitted to Plant Physiology, a section of the journal Frontiers in Plant Science</p>
</fn>
</author-notes>
<pub-date pub-type="epub"><day>12</day>
<month>2</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="collection"><year>2016</year>
</pub-date>
<volume>7</volume>
<elocation-id>154</elocation-id>
<history><date date-type="received"><day>04</day>
<month>12</month>
<year>2015</year>
</date>
<date date-type="accepted"><day>29</day>
<month>1</month>
<year>2016</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2016 Gaupels, Furch, Zimmermann, Chen, Kaever, Buhtz, Kehr, Sarioglu, Kogel and Durner.</copyright-statement>
<copyright-year>2016</copyright-year>
<copyright-holder>Gaupels, Furch, Zimmermann, Chen, Kaever, Buhtz, Kehr, Sarioglu, Kogel and Durner</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 Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</license-p>
</license>
</permissions>
<abstract><p>Cucurbits developed the unique extrafascicular phloem (EFP) as a defensive structure against herbivorous animals. Mechanical leaf injury was previously shown to induce a systemic wound response in the EFP of pumpkin (<italic>Cucurbita maxima</italic>
). Here, we demonstrate that the phloem antioxidant system and protein modifications by NO are strongly regulated during this process. Activities of the central antioxidant enzymes dehydroascorbate reductase, glutathione reductase and ascorbate reductase were rapidly down-regulated at 30 min with a second minimum at 24 h after wounding. As a consequence levels of total ascorbate and glutathione also decreased with similar bi-phasic kinetics. These results hint toward a wound-induced shift in the redox status of the EFP. Nitric oxide (NO) is another important player in stress-induced redox signaling in plants. Therefore, we analyzed NO-dependent protein modifications in the EFP. Six to forty eight hours after leaf damage total S-nitrosothiol content and protein S-nitrosylation were clearly reduced, which was contrasted by a pronounced increase in protein tyrosine nitration. Collectively, these findings suggest that NO-dependent S-nitrosylation turned into peroxynitrite-mediated protein nitration upon a stress-induced redox shift probably involving the accumulation of reactive oxygen species within the EFP. Using the biotin switch assay and anti-nitrotyrosine antibodies we identified 9 candidate S-nitrosylated and 6 candidate tyrosine-nitrated phloem proteins. The wound-responsive Phloem Protein 16-1 (PP16-1) and Cyclophilin 18 (CYP18) as well as the 26.5 kD isoform of Phloem Protein 2 (PP2) were amenable to both NO modifications and could represent important redox-sensors within the cucurbit EFP. We also found that leaf injury triggered the systemic accumulation of cyclic guanosine monophosphate (cGMP) in the EFP and discuss the possible function of this second messenger in systemic NO and redox signaling within the EFP.</p>
</abstract>
<kwd-group><kwd>phloem</kwd>
<kwd>systemic</kwd>
<kwd>wound response</kwd>
<kwd>signaling</kwd>
<kwd>NO</kwd>
<kwd>redox</kwd>
<kwd>antioxidant system</kwd>
<kwd>cGMP</kwd>
</kwd-group>
<counts><fig-count count="6"></fig-count>
<table-count count="0"></table-count>
<equation-count count="0"></equation-count>
<ref-count count="49"></ref-count>
<page-count count="11"></page-count>
<word-count count="8319"></word-count>
</counts>
</article-meta>
</front>
</pmc>
</record>
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