Reducing Cytoplasmic Polyamine Oxidase Activity in Arabidopsis Increases Salt and Drought Tolerance by Reducing Reactive Oxygen Species Production and Increasing Defense Gene Expression
Identifieur interne : 000047 ( Pmc/Checkpoint ); précédent : 000046; suivant : 000048Reducing Cytoplasmic Polyamine Oxidase Activity in Arabidopsis Increases Salt and Drought Tolerance by Reducing Reactive Oxygen Species Production and Increasing Defense Gene Expression
Auteurs : G. H. M. Sagor [Japon] ; Siyuan Zhang [Japon] ; Seiji Kojima [Japon] ; Stefan Simm [Allemagne] ; Thomas Berberich [Allemagne] ; Tomonobu Kusano [Japon]Source :
- Frontiers in Plant Science [ 1664-462X ] ; 2016.
Abstract
The link between polyamine oxidases (PAOs), which function in polyamine catabolism, and stress responses remains elusive. Here, we address this issue using
Url:
DOI: 10.3389/fpls.2016.00214
PubMed: 26973665
PubMed Central: 4770033
Affiliations:
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Increases Salt and Drought Tolerance by Reducing Reactive Oxygen Species Production and Increasing Defense Gene Expression</title>
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<author><name sortKey="Kusano, Tomonobu" sort="Kusano, Tomonobu" uniqKey="Kusano T" first="Tomonobu" last="Kusano">Tomonobu Kusano</name>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Reducing Cytoplasmic Polyamine Oxidase Activity in <italic>Arabidopsis</italic>
Increases Salt and Drought Tolerance by Reducing Reactive Oxygen Species Production and Increasing Defense Gene Expression</title>
<author><name sortKey="Sagor, G H M" sort="Sagor, G H M" uniqKey="Sagor G" first="G. H. M." last="Sagor">G. H. M. Sagor</name>
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<country>Sendai, Japan</country>
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<country xml:lang="fr">Japon</country>
<wicri:regionArea></wicri:regionArea>
</affiliation>
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<author><name sortKey="Zhang, Siyuan" sort="Zhang, Siyuan" uniqKey="Zhang S" first="Siyuan" last="Zhang">Siyuan Zhang</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Graduate School of Life Sciences, Tohoku University</institution>
<country>Sendai, Japan</country>
</nlm:aff>
<country xml:lang="fr">Japon</country>
<wicri:regionArea></wicri:regionArea>
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<author><name sortKey="Kojima, Seiji" sort="Kojima, Seiji" uniqKey="Kojima S" first="Seiji" last="Kojima">Seiji Kojima</name>
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<country>Sendai, Japan</country>
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<country xml:lang="fr">Japon</country>
<wicri:regionArea></wicri:regionArea>
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<country>Sendai, Japan</country>
</nlm:aff>
<country xml:lang="fr">Japon</country>
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<author><name sortKey="Simm, Stefan" sort="Simm, Stefan" uniqKey="Simm S" first="Stefan" last="Simm">Stefan Simm</name>
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<country>Frankfurt am Main, Germany</country>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea></wicri:regionArea>
</affiliation>
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<author><name sortKey="Berberich, Thomas" sort="Berberich, Thomas" uniqKey="Berberich T" first="Thomas" last="Berberich">Thomas Berberich</name>
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<country>Frankfurt am Main, Germany</country>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea></wicri:regionArea>
</affiliation>
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<author><name sortKey="Kusano, Tomonobu" sort="Kusano, Tomonobu" uniqKey="Kusano T" first="Tomonobu" last="Kusano">Tomonobu Kusano</name>
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<country>Sendai, Japan</country>
</nlm:aff>
<country xml:lang="fr">Japon</country>
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<series><title level="j">Frontiers in Plant Science</title>
<idno type="eISSN">1664-462X</idno>
<imprint><date when="2016">2016</date>
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<front><div type="abstract" xml:lang="en"><p>The link between polyamine oxidases (PAOs), which function in polyamine catabolism, and stress responses remains elusive. Here, we address this issue using <italic>Arabidopsis pao</italic>
mutants in which the expression of the five <italic>PAO</italic>
genes is knocked-out or knocked-down. As the five single <italic>pao</italic>
mutants and wild type (WT) showed similar response to salt stress, we tried to generate the mutants that have either the cytoplasmic PAO pathway (<italic>pao1 pao5</italic>
) or the peroxisomal PAO pathway (<italic>pao2 pao3 pao4</italic>
) silenced. However, the latter triple mutant was not obtained. Thus, in this study, we used two double mutants, <italic>pao1 pao5</italic>
and <italic>pao2 pao4</italic>
. Of interest, <italic>pao1 pao5</italic>
mutant was NaCl- and drought-tolerant, whereas <italic>pao2 pao4</italic>
showed similar sensitivity to those stresses as WT. To reveal the underlying mechanism of salt tolerance, further analyses were performed. Na uptake of the mutant (<italic>pao1 pao5</italic>
) decreased to 75% of WT. PAO activity of the mutant was reduced to 62% of WT. The content of reactive oxygen species (ROS) such as hydrogen peroxide, a reaction product of PAO action, and superoxide anion in the mutant became 81 and 72% of the levels in WT upon salt treatment. The mutant contained 2.8-fold higher thermospermine compared to WT. Moreover, the mutant induced the genes of salt overly sensitive-, abscisic acid (ABA)-dependent- and ABA-independent- pathways more strongly than WT upon salt treatment. The results suggest that the <italic>Arabidopsis</italic>
plant silencing cytoplasmic <italic>PAO</italic>
s shows salinity tolerance by reducing ROS production and strongly inducing subsets of stress-responsive genes under stress conditions.</p>
</div>
</front>
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<journal-id journal-id-type="iso-abbrev">Front Plant Sci</journal-id>
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<article-id pub-id-type="pmc">4770033</article-id>
<article-id pub-id-type="doi">10.3389/fpls.2016.00214</article-id>
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<title-group><article-title>Reducing Cytoplasmic Polyamine Oxidase Activity in <italic>Arabidopsis</italic>
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<given-names>Thomas</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/264461/overview"></uri>
</contrib>
<contrib contrib-type="author"><name><surname>Kusano</surname>
<given-names>Tomonobu</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/140212/overview"></uri>
</contrib>
</contrib-group>
<aff id="aff1"><sup>1</sup>
<institution>Graduate School of Life Sciences, Tohoku University</institution>
<country>Sendai, Japan</country>
</aff>
<aff id="aff2"><sup>2</sup>
<institution>Frontier Research Institute for Interdisciplinary Sciences, Tohoku University</institution>
<country>Sendai, Japan</country>
</aff>
<aff id="aff3"><sup>3</sup>
<institution>Department of Biosciences, Molecular Cell Biology of Plants, Goethe University</institution>
<country>Frankfurt am Main, Germany</country>
</aff>
<aff id="aff4"><sup>4</sup>
<institution>Biodiversity and Climate Research Center, Laboratory Center</institution>
<country>Frankfurt am Main, Germany</country>
</aff>
<author-notes><fn fn-type="edited-by"><p>Edited by: <italic>Taku Takahashi, Okayama University, Japan</italic>
</p>
</fn>
<fn fn-type="edited-by"><p>Reviewed by: <italic>Subhash C. Minocha, University of New Hampshire, USA; Ji-Hong Liu, Huazhong Agricultural University, China; Ma Zhiying, Hebei Agricultural University, China</italic>
</p>
</fn>
<corresp id="fn001">*Correspondence: <italic>Tomonobu Kusano, <email xlink:type="simple">kusano@ige.tohoku.ac.jp</email>
</italic>
</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>29</day>
<month>2</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="collection"><year>2016</year>
</pub-date>
<volume>7</volume>
<elocation-id>214</elocation-id>
<history><date date-type="received"><day>30</day>
<month>10</month>
<year>2015</year>
</date>
<date date-type="accepted"><day>08</day>
<month>2</month>
<year>2016</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2016 Sagor, Zhang, Kojima, Simm, Berberich and Kusano.</copyright-statement>
<copyright-year>2016</copyright-year>
<copyright-holder>Sagor, Zhang, Kojima, Simm, Berberich and Kusano</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>The link between polyamine oxidases (PAOs), which function in polyamine catabolism, and stress responses remains elusive. Here, we address this issue using <italic>Arabidopsis pao</italic>
mutants in which the expression of the five <italic>PAO</italic>
genes is knocked-out or knocked-down. As the five single <italic>pao</italic>
mutants and wild type (WT) showed similar response to salt stress, we tried to generate the mutants that have either the cytoplasmic PAO pathway (<italic>pao1 pao5</italic>
) or the peroxisomal PAO pathway (<italic>pao2 pao3 pao4</italic>
) silenced. However, the latter triple mutant was not obtained. Thus, in this study, we used two double mutants, <italic>pao1 pao5</italic>
and <italic>pao2 pao4</italic>
. Of interest, <italic>pao1 pao5</italic>
mutant was NaCl- and drought-tolerant, whereas <italic>pao2 pao4</italic>
showed similar sensitivity to those stresses as WT. To reveal the underlying mechanism of salt tolerance, further analyses were performed. Na uptake of the mutant (<italic>pao1 pao5</italic>
) decreased to 75% of WT. PAO activity of the mutant was reduced to 62% of WT. The content of reactive oxygen species (ROS) such as hydrogen peroxide, a reaction product of PAO action, and superoxide anion in the mutant became 81 and 72% of the levels in WT upon salt treatment. The mutant contained 2.8-fold higher thermospermine compared to WT. Moreover, the mutant induced the genes of salt overly sensitive-, abscisic acid (ABA)-dependent- and ABA-independent- pathways more strongly than WT upon salt treatment. The results suggest that the <italic>Arabidopsis</italic>
plant silencing cytoplasmic <italic>PAO</italic>
s shows salinity tolerance by reducing ROS production and strongly inducing subsets of stress-responsive genes under stress conditions.</p>
</abstract>
<kwd-group><kwd><italic>Arabidopsis thaliana</italic>
</kwd>
<kwd>drought stress</kwd>
<kwd>loss-of-function mutant</kwd>
<kwd>polyamine oxidase</kwd>
<kwd>reactive oxygen species</kwd>
<kwd>salinity stress</kwd>
</kwd-group>
<funding-group><award-group><funding-source id="cn001">Japan Society for the Promotion of Science<named-content content-type="fundref-id">10.13039/501100001691</named-content>
</funding-source>
<award-id rid="cn001">15K14705, 2604081</award-id>
</award-group>
</funding-group>
<counts><fig-count count="9"></fig-count>
<table-count count="0"></table-count>
<equation-count count="0"></equation-count>
<ref-count count="69"></ref-count>
<page-count count="16"></page-count>
<word-count count="0"></word-count>
</counts>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>Allemagne</li>
<li>Japon</li>
</country>
</list>
<tree><country name="Japon"><noRegion><name sortKey="Sagor, G H M" sort="Sagor, G H M" uniqKey="Sagor G" first="G. H. M." last="Sagor">G. H. M. Sagor</name>
</noRegion>
<name sortKey="Kojima, Seiji" sort="Kojima, Seiji" uniqKey="Kojima S" first="Seiji" last="Kojima">Seiji Kojima</name>
<name sortKey="Kojima, Seiji" sort="Kojima, Seiji" uniqKey="Kojima S" first="Seiji" last="Kojima">Seiji Kojima</name>
<name sortKey="Kusano, Tomonobu" sort="Kusano, Tomonobu" uniqKey="Kusano T" first="Tomonobu" last="Kusano">Tomonobu Kusano</name>
<name sortKey="Zhang, Siyuan" sort="Zhang, Siyuan" uniqKey="Zhang S" first="Siyuan" last="Zhang">Siyuan Zhang</name>
</country>
<country name="Allemagne"><noRegion><name sortKey="Simm, Stefan" sort="Simm, Stefan" uniqKey="Simm S" first="Stefan" last="Simm">Stefan Simm</name>
</noRegion>
<name sortKey="Berberich, Thomas" sort="Berberich, Thomas" uniqKey="Berberich T" first="Thomas" last="Berberich">Thomas Berberich</name>
</country>
</tree>
</affiliations>
</record>
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