The Citrus transcription factor, CitERF13, regulates citric acid accumulation via a protein-protein interaction with the vacuolar proton pump, CitVHA-c4
Identifieur interne : 001E94 ( Ncbi/Merge ); précédent : 001E93; suivant : 001E95The Citrus transcription factor, CitERF13, regulates citric acid accumulation via a protein-protein interaction with the vacuolar proton pump, CitVHA-c4
Auteurs : Shao-Jia Li ; Xue-Ren Yin ; Xiu-Lan Xie ; Andrew C. Allan [Nouvelle-Zélande] ; Hang Ge ; Shu-Ling Shen ; Kun-Song ChenSource :
- Scientific Reports [ 2045-2322 ] ; 2016.
Abstract
Organic acids are essential to fruit flavor. The vacuolar H+ transporting adenosine triphosphatase (V-ATPase) plays an important role in organic acid transport and accumulation. However, less is known of V-ATPase interacting proteins and their relationship with organic acid accumulation. The relationship between V-ATPase and citric acid was investigated, using the citrus tangerine varieties ‘Ordinary Ponkan (OPK)’ and an early maturing mutant ‘Zaoshu Ponkan (ZPK)’. Five V-ATPase genes (
Url:
DOI: 10.1038/srep20151
PubMed: 26837571
PubMed Central: 4738278
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China</wicri:noCountry></affiliation><affiliation><nlm:aff id="a3"><institution>The State Agriculture Ministry Laboratory of Horticultural Plant Growth, Development and Quality Improvement, Zhejiang University, Zijingang Campus</institution>, Hangzhou 310058,<country>P.R. China</country></nlm:aff><wicri:noCountry code="nlm country">P.R. China</wicri:noCountry></affiliation></author><author><name sortKey="Yin, Xue Ren" sort="Yin, Xue Ren" uniqKey="Yin X" first="Xue-Ren" last="Yin">Xue-Ren Yin</name><affiliation><nlm:aff id="a1"><institution>College of Agriculture & Biotechnology, Zhejiang University, Zijingang Campus</institution>, Hangzhou 310058,<country>P.R. China</country></nlm:aff><wicri:noCountry code="nlm country">P.R. China</wicri:noCountry></affiliation><affiliation><nlm:aff id="a2"><institution>Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Zhejiang University, Zijingang Campus</institution>, Hangzhou 310058,<country>P.R. China</country></nlm:aff><wicri:noCountry code="nlm country">P.R. China</wicri:noCountry></affiliation><affiliation><nlm:aff id="a3"><institution>The State Agriculture Ministry Laboratory of Horticultural Plant Growth, Development and Quality Improvement, Zhejiang University, Zijingang Campus</institution>, Hangzhou 310058,<country>P.R. China</country></nlm:aff><wicri:noCountry code="nlm country">P.R. China</wicri:noCountry></affiliation></author><author><name sortKey="Xie, Xiu Lan" sort="Xie, Xiu Lan" uniqKey="Xie X" first="Xiu-Lan" last="Xie">Xiu-Lan Xie</name><affiliation><nlm:aff id="a1"><institution>College of Agriculture & Biotechnology, Zhejiang University, Zijingang Campus</institution>, Hangzhou 310058,<country>P.R. China</country></nlm:aff><wicri:noCountry code="nlm country">P.R. China</wicri:noCountry></affiliation></author><author><name sortKey="Allan, Andrew C" sort="Allan, Andrew C" uniqKey="Allan A" first="Andrew C." last="Allan">Andrew C. 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China</wicri:noCountry></affiliation></author><author><name sortKey="Shen, Shu Ling" sort="Shen, Shu Ling" uniqKey="Shen S" first="Shu-Ling" last="Shen">Shu-Ling Shen</name><affiliation><nlm:aff id="a1"><institution>College of Agriculture & Biotechnology, Zhejiang University, Zijingang Campus</institution>, Hangzhou 310058,<country>P.R. China</country></nlm:aff><wicri:noCountry code="nlm country">P.R. China</wicri:noCountry></affiliation></author><author><name sortKey="Chen, Kun Song" sort="Chen, Kun Song" uniqKey="Chen K" first="Kun-Song" last="Chen">Kun-Song Chen</name><affiliation><nlm:aff id="a1"><institution>College of Agriculture & Biotechnology, Zhejiang University, Zijingang Campus</institution>, Hangzhou 310058,<country>P.R. China</country></nlm:aff><wicri:noCountry code="nlm country">P.R. China</wicri:noCountry></affiliation><affiliation><nlm:aff id="a2"><institution>Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Zhejiang University, Zijingang Campus</institution>, Hangzhou 310058,<country>P.R. China</country></nlm:aff><wicri:noCountry code="nlm country">P.R. China</wicri:noCountry></affiliation><affiliation><nlm:aff id="a3"><institution>The State Agriculture Ministry Laboratory of Horticultural Plant Growth, Development and Quality Improvement, Zhejiang University, Zijingang Campus</institution>, Hangzhou 310058,<country>P.R. China</country></nlm:aff><wicri:noCountry code="nlm country">P.R. China</wicri:noCountry></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">26837571</idno><idno type="pmc">4738278</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4738278</idno><idno type="RBID">PMC:4738278</idno><idno type="doi">10.1038/srep20151</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">000455</idno><idno type="wicri:Area/Pmc/Curation">000454</idno><idno type="wicri:Area/Pmc/Checkpoint">000026</idno><idno type="wicri:Area/Ncbi/Merge">001E94</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">The Citrus transcription factor, CitERF13, regulates citric acid accumulation via a protein-protein interaction with the vacuolar proton pump, CitVHA-c4</title><author><name sortKey="Li, Shao Jia" sort="Li, Shao Jia" uniqKey="Li S" first="Shao-Jia" last="Li">Shao-Jia Li</name><affiliation><nlm:aff id="a1"><institution>College of Agriculture & Biotechnology, Zhejiang University, Zijingang Campus</institution>, Hangzhou 310058,<country>P.R. China</country></nlm:aff><wicri:noCountry code="nlm country">P.R. China</wicri:noCountry></affiliation><affiliation><nlm:aff id="a2"><institution>Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Zhejiang University, Zijingang Campus</institution>, Hangzhou 310058,<country>P.R. China</country></nlm:aff><wicri:noCountry code="nlm country">P.R. China</wicri:noCountry></affiliation><affiliation><nlm:aff id="a3"><institution>The State Agriculture Ministry Laboratory of Horticultural Plant Growth, Development and Quality Improvement, Zhejiang University, Zijingang Campus</institution>, Hangzhou 310058,<country>P.R. China</country></nlm:aff><wicri:noCountry code="nlm country">P.R. China</wicri:noCountry></affiliation></author><author><name sortKey="Yin, Xue Ren" sort="Yin, Xue Ren" uniqKey="Yin X" first="Xue-Ren" last="Yin">Xue-Ren Yin</name><affiliation><nlm:aff id="a1"><institution>College of Agriculture & Biotechnology, Zhejiang University, Zijingang Campus</institution>, Hangzhou 310058,<country>P.R. China</country></nlm:aff><wicri:noCountry code="nlm country">P.R. China</wicri:noCountry></affiliation><affiliation><nlm:aff id="a2"><institution>Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Zhejiang University, Zijingang Campus</institution>, Hangzhou 310058,<country>P.R. China</country></nlm:aff><wicri:noCountry code="nlm country">P.R. China</wicri:noCountry></affiliation><affiliation><nlm:aff id="a3"><institution>The State Agriculture Ministry Laboratory of Horticultural Plant Growth, Development and Quality Improvement, Zhejiang University, Zijingang Campus</institution>, Hangzhou 310058,<country>P.R. China</country></nlm:aff><wicri:noCountry code="nlm country">P.R. China</wicri:noCountry></affiliation></author><author><name sortKey="Xie, Xiu Lan" sort="Xie, Xiu Lan" uniqKey="Xie X" first="Xiu-Lan" last="Xie">Xiu-Lan Xie</name><affiliation><nlm:aff id="a1"><institution>College of Agriculture & Biotechnology, Zhejiang University, Zijingang Campus</institution>, Hangzhou 310058,<country>P.R. China</country></nlm:aff><wicri:noCountry code="nlm country">P.R. China</wicri:noCountry></affiliation></author><author><name sortKey="Allan, Andrew C" sort="Allan, Andrew C" uniqKey="Allan A" first="Andrew C." last="Allan">Andrew C. Allan</name><affiliation wicri:level="1"><nlm:aff id="a4"><institution>New Zealand Institute for Plant & Food Research Limited</institution>, Private Bag 92169, Auckland,<country>New Zealand</country></nlm:aff><country xml:lang="fr">Nouvelle-Zélande</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="a5"><institution>School of Biological Sciences, University of Auckland</institution>, Auckland,<country>New Zealand</country></nlm:aff><country xml:lang="fr">Nouvelle-Zélande</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Ge, Hang" sort="Ge, Hang" uniqKey="Ge H" first="Hang" last="Ge">Hang Ge</name><affiliation><nlm:aff id="a1"><institution>College of Agriculture & Biotechnology, Zhejiang University, Zijingang Campus</institution>, Hangzhou 310058,<country>P.R. China</country></nlm:aff><wicri:noCountry code="nlm country">P.R. China</wicri:noCountry></affiliation></author><author><name sortKey="Shen, Shu Ling" sort="Shen, Shu Ling" uniqKey="Shen S" first="Shu-Ling" last="Shen">Shu-Ling Shen</name><affiliation><nlm:aff id="a1"><institution>College of Agriculture & Biotechnology, Zhejiang University, Zijingang Campus</institution>, Hangzhou 310058,<country>P.R. China</country></nlm:aff><wicri:noCountry code="nlm country">P.R. China</wicri:noCountry></affiliation></author><author><name sortKey="Chen, Kun Song" sort="Chen, Kun Song" uniqKey="Chen K" first="Kun-Song" last="Chen">Kun-Song Chen</name><affiliation><nlm:aff id="a1"><institution>College of Agriculture & Biotechnology, Zhejiang University, Zijingang Campus</institution>, Hangzhou 310058,<country>P.R. China</country></nlm:aff><wicri:noCountry code="nlm country">P.R. China</wicri:noCountry></affiliation><affiliation><nlm:aff id="a2"><institution>Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Zhejiang University, Zijingang Campus</institution>, Hangzhou 310058,<country>P.R. China</country></nlm:aff><wicri:noCountry code="nlm country">P.R. China</wicri:noCountry></affiliation><affiliation><nlm:aff id="a3"><institution>The State Agriculture Ministry Laboratory of Horticultural Plant Growth, Development and Quality Improvement, Zhejiang University, Zijingang Campus</institution>, Hangzhou 310058,<country>P.R. China</country></nlm:aff><wicri:noCountry code="nlm country">P.R. China</wicri:noCountry></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>Organic acids are essential to fruit flavor. The vacuolar H<sup>+</sup> transporting adenosine triphosphatase (V-ATPase) plays an important role in organic acid transport and accumulation. However, less is known of V-ATPase interacting proteins and their relationship with organic acid accumulation. The relationship between V-ATPase and citric acid was investigated, using the citrus tangerine varieties ‘Ordinary Ponkan (OPK)’ and an early maturing mutant ‘Zaoshu Ponkan (ZPK)’. Five V-ATPase genes (<italic>CitVHA</italic>) were predicted as important to citric acid accumulation. Among the genes, <italic>CitVHA-c4</italic> was observed, using a yeast two-hybrid screen, to interact at the protein level with an ethylene response factor, CitERF13. This was verified using bimolecular fluorescence complementation assays. A similar interaction was also observed between <italic>Arabidopsis</italic> AtERF017 (a CitERF13 homolog) and AtVHA-c4 (a CitVHA-c4 homolog). A synergistic effect on citric acid levels was observed between V-ATPase proteins and interacting ERFs when analyzed using transient over-expression in tobacco and <italic>Arabidopsis</italic> mutants. Furthermore, the transcript abundance of <italic>CitERF13</italic> was concomitant with <italic>CitVHA-c4. CitERF13</italic> or <italic>AtERF017</italic> over-expression leads to significant citric acid accumulation. This accumulation was abolished in an <italic>AtVHA-c4</italic> mutant background. ERF-VHA interactions appear to be involved in citric acid accumulation, which was observed in both citrus and <italic>Arabidopsis</italic>.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Hooks, M A" uniqKey="Hooks M">M. A. Hooks</name></author><author><name sortKey="Turner, J E" uniqKey="Turner J">J. E. Turner</name></author><author><name sortKey="Murphy, E C" uniqKey="Murphy E">E. C. Murphy</name></author><author><name sortKey="Graham, I A" uniqKey="Graham I">I. A. Graham</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ding, Z J" uniqKey="Ding Z">Z. J. Ding</name></author><author><name sortKey="Yan, J Y" uniqKey="Yan J">J. Y. Yan</name></author><author><name sortKey="Xu, X Y" uniqKey="Xu X">X. Y. Xu</name></author><author><name sortKey="Li, G X" uniqKey="Li G">G. X. Li</name></author><author><name sortKey="Zheng, S J" uniqKey="Zheng S">S. J. 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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">26837571</article-id><article-id pub-id-type="pmc">4738278</article-id><article-id pub-id-type="pii">srep20151</article-id><article-id pub-id-type="doi">10.1038/srep20151</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>The Citrus transcription factor, CitERF13, regulates citric acid accumulation via a protein-protein interaction with the vacuolar proton pump, CitVHA-c4</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Li</surname><given-names>Shao-jia</given-names></name><xref ref-type="aff" rid="a1">1</xref><xref ref-type="aff" rid="a2">2</xref><xref ref-type="aff" rid="a3">3</xref><xref ref-type="author-notes" rid="n1">*</xref></contrib><contrib contrib-type="author"><name><surname>Yin</surname><given-names>Xue-ren</given-names></name><xref ref-type="aff" rid="a1">1</xref><xref ref-type="aff" rid="a2">2</xref><xref ref-type="aff" rid="a3">3</xref><xref ref-type="author-notes" rid="n1">*</xref></contrib><contrib contrib-type="author"><name><surname>Xie</surname><given-names>Xiu-lan</given-names></name><xref ref-type="aff" rid="a1">1</xref></contrib><contrib contrib-type="author"><name><surname>Allan</surname><given-names>Andrew C.</given-names></name><xref ref-type="aff" rid="a4">4</xref><xref ref-type="aff" rid="a5">5</xref></contrib><contrib contrib-type="author"><name><surname>Ge</surname><given-names>Hang</given-names></name><xref ref-type="aff" rid="a1">1</xref></contrib><contrib contrib-type="author"><name><surname>Shen</surname><given-names>Shu-ling</given-names></name><xref ref-type="aff" rid="a1">1</xref></contrib><contrib contrib-type="author"><name><surname>Chen</surname><given-names>Kun-song</given-names></name><xref ref-type="corresp" rid="c1">a</xref><xref ref-type="aff" rid="a1">1</xref><xref ref-type="aff" rid="a2">2</xref><xref ref-type="aff" rid="a3">3</xref></contrib><aff id="a1"><label>1</label><institution>College of Agriculture & Biotechnology, Zhejiang University, Zijingang Campus</institution>, Hangzhou 310058,<country>P.R. China</country></aff><aff id="a2"><label>2</label><institution>Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Zhejiang University, Zijingang Campus</institution>, Hangzhou 310058,<country>P.R. China</country></aff><aff id="a3"><label>3</label><institution>The State Agriculture Ministry Laboratory of Horticultural Plant Growth, Development and Quality Improvement, Zhejiang University, Zijingang Campus</institution>, Hangzhou 310058,<country>P.R. China</country></aff><aff id="a4"><label>4</label><institution>New Zealand Institute for Plant & Food Research Limited</institution>, Private Bag 92169, Auckland,<country>New Zealand</country></aff><aff id="a5"><label>5</label><institution>School of Biological Sciences, University of Auckland</institution>, Auckland,<country>New Zealand</country></aff></contrib-group><author-notes><corresp id="c1"><label>a</label><email>akun@zju.edu.cn</email></corresp><fn id="n1"><label>*</label><p>These authors contributed equally to this work.</p></fn></author-notes><pub-date pub-type="epub"><day>03</day><month>02</month><year>2016</year></pub-date><pub-date pub-type="collection"><year>2016</year></pub-date><volume>6</volume><elocation-id>20151</elocation-id><history><date date-type="received"><day>11</day><month>08</month><year>2015</year></date><date date-type="accepted"><day>30</day><month>12</month><year>2015</year></date></history><permissions><copyright-statement>Copyright © 2016, Macmillan Publishers Limited</copyright-statement><copyright-year>2016</copyright-year><copyright-holder>Macmillan Publishers Limited</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>Organic acids are essential to fruit flavor. The vacuolar H<sup>+</sup> transporting adenosine triphosphatase (V-ATPase) plays an important role in organic acid transport and accumulation. However, less is known of V-ATPase interacting proteins and their relationship with organic acid accumulation. The relationship between V-ATPase and citric acid was investigated, using the citrus tangerine varieties ‘Ordinary Ponkan (OPK)’ and an early maturing mutant ‘Zaoshu Ponkan (ZPK)’. Five V-ATPase genes (<italic>CitVHA</italic>) were predicted as important to citric acid accumulation. Among the genes, <italic>CitVHA-c4</italic> was observed, using a yeast two-hybrid screen, to interact at the protein level with an ethylene response factor, CitERF13. This was verified using bimolecular fluorescence complementation assays. A similar interaction was also observed between <italic>Arabidopsis</italic> AtERF017 (a CitERF13 homolog) and AtVHA-c4 (a CitVHA-c4 homolog). A synergistic effect on citric acid levels was observed between V-ATPase proteins and interacting ERFs when analyzed using transient over-expression in tobacco and <italic>Arabidopsis</italic> mutants. Furthermore, the transcript abundance of <italic>CitERF13</italic> was concomitant with <italic>CitVHA-c4. CitERF13</italic> or <italic>AtERF017</italic> over-expression leads to significant citric acid accumulation. This accumulation was abolished in an <italic>AtVHA-c4</italic> mutant background. ERF-VHA interactions appear to be involved in citric acid accumulation, which was observed in both citrus and <italic>Arabidopsis</italic>.</p></abstract></article-meta></front><floats-group><fig id="f1"><label>Figure 1</label><caption><title>Changes in the contents of titratable acid (TA,</title><p>(<bold>a</bold>)), total organic acids (<bold>b</bold>), citric acid (<bold>c</bold>), tartaric acid (<bold>d</bold>), malic acid (<bold>e</bold>) and quinic acid (<bold>f</bold>) in flesh of Pokan fruits during fruit development, DAFB means day after full blossom. Error bars on each column indicate ±SE from three biological replicates. LSDs represent least significant differences at 0.05.</p></caption><graphic xlink:href="srep20151-f1"></graphic></fig><fig id="f2"><label>Figure 2</label><caption><title>Expression of the V-ATPase genes in flesh of Ponkan fruits during fruit development, DAFB means day after full blossom.</title><p>Error bars on each column indicate ±SE from three biological replicates. LSDs represent least significant differences at 0.05.</p></caption><graphic xlink:href="srep20151-f2"></graphic></fig><fig id="f3"><label>Figure 3</label><caption><title>Yeast two-hybrid assays show that AtERF017 interacts with AtVHA-c4 and CitERF13 interacts with CitVHA-c4.</title><p>AtERF017 and AtVHA-c4 are homologs of CitERF13 and CitVHA-c4 in <italic>Arabidopsis</italic>. Liquid cultures of double transformants are plated at OD<sub>600</sub> = 0.1 dilutions of the cultures on synthetic dropout selective medium: (1) SD medium lacks Trp and Leu (DDO); (2) SD medium lacks Trp, Leu, His and Ade (QDO); (3) SD medium lacks Trp, Leu, His, Ade, and was supplemented with 10 mM 3-amino-1,2,4-triazole (QDO+3AT). Protein-protein interactions were determined on QDO and QDO + 3AT. pOst1-NubI, positive control; pPR3-N, negative control.</p></caption><graphic xlink:href="srep20151-f3"></graphic></fig><fig id="f4"><label>Figure 4</label><caption><title><italic>In vivo</italic> interaction between CitERF13 and CitVHA-c4, using BiFC.</title><p>BiFC analysis for interaction between CitERF13 and CitVHA-c4. N- and C-terminal fragments of YFP (YFP<sup>N</sup> and YFP<sup>C</sup>) were fused to the C terminus of CitERF13 and CitVHA-c4, respectively. Combination of YFP<sup>C</sup> or YFP<sup>N</sup> with corresponding CitERF13 or CitVHA-c4 constructs were used as negative controls. Fluorescence of YFP represents protein-protein interaction. The bars indicated the length of 50 μm.</p></caption><graphic xlink:href="srep20151-f4"></graphic></fig><fig id="f5"><label>Figure 5</label><caption><title>Expression of the <italic>CitERF13</italic> and <italic>CitVHA-c4</italic> genes in flesh of Pokan fruits during fruit development, DAFB means day after full blossom.</title><p>Error bars on each column indicate ±SE from three biological replicates. LSDs represent least significant differences at 0.05.</p></caption><graphic xlink:href="srep20151-f5"></graphic></fig><fig id="f6"><label>Figure 6</label><caption><title>Transient overexpression of <italic>CitERF13</italic> and <italic>CitVHA-c4</italic> in <italic>N. tabacum</italic> leaves.</title><p>Both <italic>CitERF13</italic> and <italic>CitVHA-c4</italic> genes were driven by the CaMV 35S promoter. SK represents empty vector. Citric acid was analyzed at 5 d after infiltration, with three biological replicates. Different letters indicate a significant difference (<italic>p</italic> < 0.05), which were calculated using Student’s <italic>t</italic>-test. +, present of the construct; −, absence of the construct.</p></caption><graphic xlink:href="srep20151-f6"></graphic></fig><fig id="f7"><label>Figure 7</label><caption><title>Transient overexpression of <italic>AtERF017</italic> and <italic>CitERF13</italic> in <italic>Arabidopsis</italic> leaves.</title><p>CS848548 is a mutant for <italic>AtVHA-c4</italic> and was obtained from TAIR. (<bold>a</bold>,<bold>b</bold>) Citric acid was analyzed at 3 d after infiltration, with three biological replicates. The statistical significance of differences was calculated using Student’s <italic>t</italic>-test. Asterisks *indicate significant differences (<italic>p</italic> < 0.05), double asterisks **indicate significant differences (<italic>p</italic> < 0.01). (<bold>c</bold>) AtVHA-c4 mRNA abundance in wild type and CS848548. <italic>AtERF017</italic> and <italic>CitERF13</italic> gene was driven by the CaMV 35S promoter. SK represents empty vector.</p></caption><graphic xlink:href="srep20151-f7"></graphic></fig></floats-group></pmc><affiliations><list><country><li>Nouvelle-Zélande</li></country></list><tree><noCountry><name sortKey="Chen, Kun Song" sort="Chen, Kun Song" uniqKey="Chen K" first="Kun-Song" last="Chen">Kun-Song Chen</name><name sortKey="Ge, Hang" sort="Ge, Hang" uniqKey="Ge H" first="Hang" last="Ge">Hang Ge</name><name sortKey="Li, Shao Jia" sort="Li, Shao Jia" uniqKey="Li S" first="Shao-Jia" last="Li">Shao-Jia Li</name><name sortKey="Shen, Shu Ling" sort="Shen, Shu Ling" uniqKey="Shen S" first="Shu-Ling" last="Shen">Shu-Ling Shen</name><name sortKey="Xie, Xiu Lan" sort="Xie, Xiu Lan" uniqKey="Xie X" first="Xiu-Lan" last="Xie">Xiu-Lan Xie</name><name sortKey="Yin, Xue Ren" sort="Yin, Xue Ren" uniqKey="Yin X" first="Xue-Ren" last="Yin">Xue-Ren Yin</name></noCountry><country name="Nouvelle-Zélande"><noRegion><name sortKey="Allan, Andrew C" sort="Allan, Andrew C" uniqKey="Allan A" first="Andrew C." last="Allan">Andrew C. 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