CsPAO4 of Citrus sinensis functions in polyamine terminal catabolism and inhibits plant growth under salt stress
Identifieur interne : 000291 ( Pmc/Checkpoint ); précédent : 000290; suivant : 000292CsPAO4 of Citrus sinensis functions in polyamine terminal catabolism and inhibits plant growth under salt stress
Auteurs : Wei Wang [République populaire de Chine] ; Ji-Hong Liu [République populaire de Chine]Source :
- Scientific Reports [ 2045-2322 ] ; 2016.
Abstract
Polyamine oxidase (PAO) is a key enzyme catalyzing polyamine catabolism leading to H2O2 production. We previously demonstrated that
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DOI: 10.1038/srep31384
PubMed: 27535697
PubMed Central: 4989168
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en"><italic>CsPAO4</italic> of <italic>Citrus sinensis</italic> functions in polyamine terminal catabolism and inhibits plant growth under salt stress</title><author><name sortKey="Wang, Wei" sort="Wang, Wei" uniqKey="Wang W" first="Wei" last="Wang">Wei Wang</name><affiliation wicri:level="1"><nlm:aff id="a1"><institution>Key Laboratory of Horticultural Plant Biology, MOE, College of Horticulture and Forestry Sciences, Huazhong Agricultural University</institution>, Wuhan 430070,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Liu, Ji Hong" sort="Liu, Ji Hong" uniqKey="Liu J" first="Ji-Hong" last="Liu">Ji-Hong Liu</name><affiliation wicri:level="1"><nlm:aff id="a1"><institution>Key Laboratory of Horticultural Plant Biology, MOE, College of Horticulture and Forestry Sciences, Huazhong Agricultural University</institution>, Wuhan 430070,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">27535697</idno><idno type="pmc">4989168</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4989168</idno><idno type="RBID">PMC:4989168</idno><idno type="doi">10.1038/srep31384</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">000473</idno><idno type="wicri:Area/Pmc/Curation">000472</idno><idno type="wicri:Area/Pmc/Checkpoint">000291</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main"><italic>CsPAO4</italic> of <italic>Citrus sinensis</italic> functions in polyamine terminal catabolism and inhibits plant growth under salt stress</title><author><name sortKey="Wang, Wei" sort="Wang, Wei" uniqKey="Wang W" first="Wei" last="Wang">Wei Wang</name><affiliation wicri:level="1"><nlm:aff id="a1"><institution>Key Laboratory of Horticultural Plant Biology, MOE, College of Horticulture and Forestry Sciences, Huazhong Agricultural University</institution>, Wuhan 430070,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Liu, Ji Hong" sort="Liu, Ji Hong" uniqKey="Liu J" first="Ji-Hong" last="Liu">Ji-Hong Liu</name><affiliation wicri:level="1"><nlm:aff id="a1"><institution>Key Laboratory of Horticultural Plant Biology, MOE, College of Horticulture and Forestry Sciences, Huazhong Agricultural University</institution>, Wuhan 430070,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></analytic><series><title level="j">Scientific Reports</title><idno type="eISSN">2045-2322</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Polyamine oxidase (PAO) is a key enzyme catalyzing polyamine catabolism leading to H<sub>2</sub>O<sub>2</sub> production. We previously demonstrated that <italic>Citrus sinensis</italic> contains six putative <italic>PAO</italic> genes, but their functions are not well understood. In this work, we reported functional elucidation of <italic>CsPAO4</italic> in polyamine catabolism and salt stress response. CsPAO4 was localized to the apoplast and used both spermidine (Spd) and spermine (Spm) as substrates for terminal catabolism. Transgenic plants overexpressing <italic>CsPAO4</italic> displayed prominent increase in PAO activity, concurrent with marked decrease of Spm and Spd and elevation of H<sub>2</sub>O<sub>2</sub>. Seeds of transgenic lines displayed better germination when compared with wild type (WT) under salt stress. However, both vegetative growth and root elongation of the transgenic lines were prominently inhibited under salt stress, accompanied by higher level of H<sub>2</sub>O<sub>2</sub> and more conspicuous programmed cell death (PCD). Exogenous supply of catalase (CAT), a H<sub>2</sub>O<sub>2</sub> scavenger, partially recovered the vegetative growth and root elongation. In addition, spermine inhibited root growth of transgenic plants. Taken together, these data demonstrated that <italic>CsPAO4</italic> accounts for production of H<sub>2</sub>O<sub>2</sub> causing oxidative damages under salt stress and that down-regulation of a <italic>PAO</italic> gene involved in polyamine terminal catabolism may be an alternative approach for improving salt stress tolerance.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Miller, G" uniqKey="Miller G">G. Miller</name></author><author><name sortKey="Suzuki, N" uniqKey="Suzuki N">N. Suzuki</name></author><author><name sortKey="Ciftci Yilmaz, S" uniqKey="Ciftci Yilmaz S">S. Ciftci-Yilmaz</name></author><author><name sortKey="Mittler, R" uniqKey="Mittler R">R. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Sci Rep</journal-id><journal-id journal-id-type="iso-abbrev">Sci Rep</journal-id><journal-title-group><journal-title>Scientific Reports</journal-title></journal-title-group><issn pub-type="epub">2045-2322</issn><publisher><publisher-name>Nature Publishing Group</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">27535697</article-id><article-id pub-id-type="pmc">4989168</article-id><article-id pub-id-type="pii">srep31384</article-id><article-id pub-id-type="doi">10.1038/srep31384</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title><italic>CsPAO4</italic> of <italic>Citrus sinensis</italic> functions in polyamine terminal catabolism and inhibits plant growth under salt stress</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Wang</surname><given-names>Wei</given-names></name><xref ref-type="aff" rid="a1">1</xref></contrib><contrib contrib-type="author"><name><surname>Liu</surname><given-names>Ji-Hong</given-names></name><xref ref-type="corresp" rid="c1">a</xref><xref ref-type="aff" rid="a1">1</xref></contrib><aff id="a1"><label>1</label><institution>Key Laboratory of Horticultural Plant Biology, MOE, College of Horticulture and Forestry Sciences, Huazhong Agricultural University</institution>, Wuhan 430070,<country>China</country></aff></contrib-group><author-notes><corresp id="c1"><label>a</label><email>liujihong@mail.hzau.edu.cn</email></corresp></author-notes><pub-date pub-type="epub"><day>18</day><month>08</month><year>2016</year></pub-date><pub-date pub-type="collection"><year>2016</year></pub-date><volume>6</volume><elocation-id>31384</elocation-id><history><date date-type="received"><day>10</day><month>03</month><year>2016</year></date><date date-type="accepted"><day>11</day><month>07</month><year>2016</year></date></history><permissions><copyright-statement>Copyright © 2016, The Author(s)</copyright-statement><copyright-year>2016</copyright-year><copyright-holder>The Author(s)</copyright-holder><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/4.0/"><pmc-comment>author-paid</pmc-comment>
<license-p>This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link></license-p></license></permissions><abstract><p>Polyamine oxidase (PAO) is a key enzyme catalyzing polyamine catabolism leading to H<sub>2</sub>O<sub>2</sub> production. We previously demonstrated that <italic>Citrus sinensis</italic> contains six putative <italic>PAO</italic> genes, but their functions are not well understood. In this work, we reported functional elucidation of <italic>CsPAO4</italic> in polyamine catabolism and salt stress response. CsPAO4 was localized to the apoplast and used both spermidine (Spd) and spermine (Spm) as substrates for terminal catabolism. Transgenic plants overexpressing <italic>CsPAO4</italic> displayed prominent increase in PAO activity, concurrent with marked decrease of Spm and Spd and elevation of H<sub>2</sub>O<sub>2</sub>. Seeds of transgenic lines displayed better germination when compared with wild type (WT) under salt stress. However, both vegetative growth and root elongation of the transgenic lines were prominently inhibited under salt stress, accompanied by higher level of H<sub>2</sub>O<sub>2</sub> and more conspicuous programmed cell death (PCD). Exogenous supply of catalase (CAT), a H<sub>2</sub>O<sub>2</sub> scavenger, partially recovered the vegetative growth and root elongation. In addition, spermine inhibited root growth of transgenic plants. Taken together, these data demonstrated that <italic>CsPAO4</italic> accounts for production of H<sub>2</sub>O<sub>2</sub> causing oxidative damages under salt stress and that down-regulation of a <italic>PAO</italic> gene involved in polyamine terminal catabolism may be an alternative approach for improving salt stress tolerance.</p></abstract></article-meta></front><floats-group><fig id="f1"><label>Figure 1</label><caption><title>Subcellular localization of CsPAO4.</title><p>(<bold>a</bold>) Fluorescence signals derived from GFP. (<bold>b</bold>) Fluorescence signals derived from GFP-CsPAO4 fusion protein. (<bold>c</bold>) Fluorescence signals derived from GFP-CsPAO4 fusion protein after plasmolysis. The images are taken under bright (left) and fluorescence (middle) field, respectively, and the merged ones are shown on the right.</p></caption><graphic xlink:href="srep31384-f1"></graphic></fig><fig id="f2"><label>Figure 2</label><caption><title>Characterization of recombinant CsPAO4.</title><p>(<bold>a</bold>) Purification of CsPAO4. M, protein size marker; lane 1, <italic>E. coli</italic> whole-cell lysate without IPTG induction; lane 2, <italic>E. coli</italic> whole-cell lysate with IPTG induction; lane 3, purified CsPAO4. (<bold>b</bold>) Absorbance spectrum of the purified CsPAO4, ranging from 300 to 540 nm. (<bold>c</bold>) Optimum pH for measuring CsPAO4 activity using Spd as a substrate. The buffers used include the following: pH 4.0–5.0, 100 mM MES buffer, pH 5.5–9.0, 100 mM phosphate buffer. (<bold>d</bold>) Optimum pH for measuring CsPAO4 activity using Spm as a substrate. (<bold>e</bold>) Optimum temperature for measuring CsPAO4 activity using Spd as a substrate at pH 7.0. (<bold>f</bold>) Optimum temperature for measuring CsPAO4 activity using Spm as substrate at pH 8.0.</p></caption><graphic xlink:href="srep31384-f2"></graphic></fig><fig id="f3"><label>Figure 3</label><caption><title>PAs substrate specificity of recombinant CsPAO4 and analysis of the CsPAO4-catalyzed reaction products of Spd and Spm.</title><p>(<bold>a</bold>) The enzymatic activity of recombinant CsPAO4 was determined in 100 mM phosphate buffer at pH 7.0 and 37 °C. (<bold>b</bold>) The enzymatic activity of recombinant CsPAO4 was determined in 100 mM phosphate buffer at pH 8.0 and 30 °C. (<bold>c,d</bold>) HPLC analysis of reaction products from Spd (<bold>c</bold>) and Spm (<bold>d</bold>), respectively. The top row shows the Put, Dap, Spd and Spm standard; the second and bottom rows show products analysis after incubation with CsPAO4 for 0, 30 and 60 min, respectively.</p></caption><graphic xlink:href="srep31384-f3"></graphic></fig><fig id="f4"><label>Figure 4</label><caption><title>Analysis of PAO activity, free polyamines and ROS levels in wild type (WT) and transgenic plants (#25 and #27).</title><p>(<bold>a</bold>) PAO activities in the wild type (WT) and transgenic lines (#25 and #27). (<bold>b</bold>) Levels of free putrescine (Put), spermidine (Spd), spermine (Spm) and 1, 3-Diaminopropane (Dap) in WT and transgenic lines. (<bold>c</bold>) H<sub>2</sub>O<sub>2</sub> and O<sub>2</sub><sup>•−</sup> contents in WT and transgenic lines. Error bars represent standard deviations (n = 3). Asterisks indicate significant difference between transgenic lines and WT (*<italic>P</italic> < 0.05, **<italic>P</italic> < 0.01, ***<italic>P</italic> < 0.001).</p></caption><graphic xlink:href="srep31384-f4"></graphic></fig><fig id="f5"><label>Figure 5</label><caption><title>Analysis of H<sub>2</sub>O<sub>2</sub> in wild type (WT) and transgenic lines (#25 and #27), as revealed by histochemical staining with diaminobenzidine (DAB).</title><p>(<bold>a,b</bold>) <italic>In situ</italic> accumulation of H<sub>2</sub>O<sub>2</sub> in leaves treated without (Control, upper panel) or with 1.0 mM Spd (<bold>a</bold>) or Spm (<bold>b</bold>) (middle panel) and 1.0 mM Spd or Spm + 20 μM guazatine (bottom panel).</p></caption><graphic xlink:href="srep31384-f5"></graphic></fig><fig id="f6"><label>Figure 6</label><caption><title>Seed germination of wild type (WT) and transgenic lines (#25 and #27) under salt stress.</title><p>(<bold>a,b</bold>) Seed germination phenotype (<bold>a</bold>) or time-course change in seed germination rates (<bold>b</bold>) of WT and transgenic lines on MS medium supplemented with 0, 100 and 200 mM NaCl for 30 d. Error bars represent standard deviations for three plates. Asterisks indicate significant difference between WT and transgenic lines at the same time point (*<italic>P</italic> < 0.05, **<italic>P</italic> < 0.01, ***<italic>P</italic> < 0.001).</p></caption><graphic xlink:href="srep31384-f6"></graphic></fig><fig id="f7"><label>Figure 7</label><caption><title>Root growth and H<sub>2</sub>O<sub>2</sub> accumulation of wild type (WT) and transgenic lines (#25 and #27) under salt stress.</title><p>(<bold>a,b</bold>) Phenotype (<bold>a</bold>) and quantitative root length (<bold>b</bold>) of four-day-old seedlings of WT and transgenic plants grown on MS medium (Control, upper panel), MS + 100 mM NaCl (middle panel) and MS + 100 mM NaCl + 100 U/ml CAT (bottom panel). (<bold>c</bold>) Fluorescence of primary root tips from six-day-old seedlings of WT and transgenic lines grown in water (Control, upper panel), 200 mM NaCl (middle panel) and 200 mM NaCl + 100 U/ml CAT (bottom panel) for 4 h. (<bold>d</bold>) Quantitative analysis of fluorescence intensity in (<bold>c</bold>). AU, arbitrary units. Error bars represent standard deviations (n = 3). Asterisks indicate significant difference between WT and transgenic lines (*<italic>P</italic> < 0.05, **<italic>P</italic> < 0.01, ***<italic>P</italic> < 0.001).</p></caption><graphic xlink:href="srep31384-f7"></graphic></fig><fig id="f8"><label>Figure 8</label><caption><title>Growth of wild type (WT) and transgenic plants (#25 and #27) under salt stress treatment.</title><p>(<bold>a–c</bold>) Phenotype (<bold>a</bold>), fresh weight (<bold>b</bold>) and electrolyte leakage (<bold>c</bold>) of WT and transgenic plants grown for 30 days on MS medium (Control, upper panel), MS medium added with 200 mM NaCl (middle panel) or MS medium added with 200 mM NaCl and 100 U/ml CAT (bottom panel). (<bold>d–g</bold>) Chlorophyll content (<bold>d</bold>), MDA content (<bold>e</bold>), H<sub>2</sub>O<sub>2</sub> (<bold>f</bold>) and O<sub>2</sub><sup>•−</sup> (<bold>g</bold>) in WT and transgenic plants under control and salt stress conditions. (<bold>h–i)</bold> Analysis of cell death (<bold>h</bold>) and DNA laddering profiles (<bold>i</bold>) of the leaves sampled from WT and transgenic plants grown on MS (control), MS + 200 mM NaCl or MS + 200 mM NaCl + 100 U/ml CAT. Error bars represent standard deviations for three replicates. Asterisks indicate significant difference between WT and transgenic lines under the same growth conditions (*<italic>P</italic> < 0.05, **<italic>P</italic> < 0.01, ***<italic>P</italic> < 0.001).</p></caption><graphic xlink:href="srep31384-f8"></graphic></fig></floats-group></pmc><affiliations><list><country><li>République populaire de Chine</li></country></list><tree><country name="République populaire de Chine"><noRegion><name sortKey="Wang, Wei" sort="Wang, Wei" uniqKey="Wang W" first="Wei" last="Wang">Wei Wang</name></noRegion><name sortKey="Liu, Ji Hong" sort="Liu, Ji Hong" uniqKey="Liu J" first="Ji-Hong" last="Liu">Ji-Hong Liu</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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