V-ATPase-activity in the TGN/EE is required for exocytosis and recycling in Arabidopsis
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Auteurs : Yu Luo [Belgique] ; Stefan Scholl [Allemagne] ; Anett Doering [Allemagne] ; Yi Zhang [Allemagne] ; Niloufer G. Irani [Belgique] ; Simone Di Rubbo [Belgique] ; Lutz Neumetzler [Allemagne] ; Praveen Krishnamoorthy [Allemagne] ; Isabelle Van Houtte [Belgique] ; Evelien Mylle [Belgique] ; Volker Bischoff [France] ; Samantha Vernhettes [France] ; Johan Winne [Belgique] ; Ji Friml [Autriche] ; York-Dieter Stierhof [Allemagne] ; Karin Schumacher [Allemagne] ; Staffan Persson [Allemagne, Australie] ; Eugenia Russinova [Belgique]Source :
- Nature plants [ 2055-0278 ] ; 2015.
Abstract
In plants, vacuolar H+-ATPase (V-ATPase) activity acidifies both the trans-Golgi network/early endosome (TGN/EE) and the vacuole. This dual V-ATPase function has impeded our understanding in how the pH homeostasis within the plant TGN/EE controls exo- and endocytosis. Here, we show that the weak V-ATPase mutant
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DOI: 10.1038/nplants.2015.94
PubMed: 27250258
PubMed Central: 4905525
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<author><name sortKey="Zhang, Yi" sort="Zhang, Yi" uniqKey="Zhang Y" first="Yi" last="Zhang">Yi Zhang</name>
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<author><name sortKey="Irani, Niloufer G" sort="Irani, Niloufer G" uniqKey="Irani N" first="Niloufer G." last="Irani">Niloufer G. Irani</name>
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<author><name sortKey="Rubbo, Simone Di" sort="Rubbo, Simone Di" uniqKey="Rubbo S" first="Simone Di" last="Rubbo">Simone Di Rubbo</name>
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<author><name sortKey="Neumetzler, Lutz" sort="Neumetzler, Lutz" uniqKey="Neumetzler L" first="Lutz" last="Neumetzler">Lutz Neumetzler</name>
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<author><name sortKey="Krishnamoorthy, Praveen" sort="Krishnamoorthy, Praveen" uniqKey="Krishnamoorthy P" first="Praveen" last="Krishnamoorthy">Praveen Krishnamoorthy</name>
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<author><name sortKey="Van Houtte, Isabelle" sort="Van Houtte, Isabelle" uniqKey="Van Houtte I" first="Isabelle" last="Van Houtte">Isabelle Van Houtte</name>
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<author><name sortKey="Mylle, Evelien" sort="Mylle, Evelien" uniqKey="Mylle E" first="Evelien" last="Mylle">Evelien Mylle</name>
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<author><name sortKey="Bischoff, Volker" sort="Bischoff, Volker" uniqKey="Bischoff V" first="Volker" last="Bischoff">Volker Bischoff</name>
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<country xml:lang="fr">France</country>
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<author><name sortKey="Vernhettes, Samantha" sort="Vernhettes, Samantha" uniqKey="Vernhettes S" first="Samantha" last="Vernhettes">Samantha Vernhettes</name>
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<country xml:lang="fr">France</country>
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<author><name sortKey="Winne, Johan" sort="Winne, Johan" uniqKey="Winne J" first="Johan" last="Winne">Johan Winne</name>
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<author><name sortKey="Friml, Ji" sort="Friml, Ji" uniqKey="Friml J" first="Ji" last="Friml">Ji Friml</name>
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<author><name sortKey="Stierhof, York Dieter" sort="Stierhof, York Dieter" uniqKey="Stierhof Y" first="York-Dieter" last="Stierhof">York-Dieter Stierhof</name>
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<author><name sortKey="Schumacher, Karin" sort="Schumacher, Karin" uniqKey="Schumacher K" first="Karin" last="Schumacher">Karin Schumacher</name>
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<author><name sortKey="Persson, Staffan" sort="Persson, Staffan" uniqKey="Persson S" first="Staffan" last="Persson">Staffan Persson</name>
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<country xml:lang="fr">Allemagne</country>
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<affiliation wicri:level="1"><nlm:aff id="A9">Australian Research Council, Centre of Excellence in Plant Cell Walls, School of Botany, University of Melbourne, Parkville, Victoria 3010, Australia</nlm:aff>
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<author><name sortKey="Scholl, Stefan" sort="Scholl, Stefan" uniqKey="Scholl S" first="Stefan" last="Scholl">Stefan Scholl</name>
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<author><name sortKey="Doering, Anett" sort="Doering, Anett" uniqKey="Doering A" first="Anett" last="Doering">Anett Doering</name>
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<author><name sortKey="Zhang, Yi" sort="Zhang, Yi" uniqKey="Zhang Y" first="Yi" last="Zhang">Yi Zhang</name>
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<country xml:lang="fr">Allemagne</country>
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<author><name sortKey="Irani, Niloufer G" sort="Irani, Niloufer G" uniqKey="Irani N" first="Niloufer G." last="Irani">Niloufer G. Irani</name>
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<country xml:lang="fr">Belgique</country>
<wicri:regionArea>Department of Plant Systems Biology, VIB, 9052 Gent, Belgium; Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Gent</wicri:regionArea>
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<author><name sortKey="Rubbo, Simone Di" sort="Rubbo, Simone Di" uniqKey="Rubbo S" first="Simone Di" last="Rubbo">Simone Di Rubbo</name>
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<wicri:regionArea>Department of Plant Systems Biology, VIB, 9052 Gent, Belgium; Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Gent</wicri:regionArea>
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<author><name sortKey="Neumetzler, Lutz" sort="Neumetzler, Lutz" uniqKey="Neumetzler L" first="Lutz" last="Neumetzler">Lutz Neumetzler</name>
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<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Max-Planck Institute for Molecular Plant Physiology, 14476 Potsdam</wicri:regionArea>
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<author><name sortKey="Krishnamoorthy, Praveen" sort="Krishnamoorthy, Praveen" uniqKey="Krishnamoorthy P" first="Praveen" last="Krishnamoorthy">Praveen Krishnamoorthy</name>
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<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Max-Planck Institute for Molecular Plant Physiology, 14476 Potsdam</wicri:regionArea>
</affiliation>
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<author><name sortKey="Van Houtte, Isabelle" sort="Van Houtte, Isabelle" uniqKey="Van Houtte I" first="Isabelle" last="Van Houtte">Isabelle Van Houtte</name>
<affiliation wicri:level="1"><nlm:aff id="A1">Department of Plant Systems Biology, VIB, 9052 Gent, Belgium; Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Gent, Belgium</nlm:aff>
<country xml:lang="fr">Belgique</country>
<wicri:regionArea>Department of Plant Systems Biology, VIB, 9052 Gent, Belgium; Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Gent</wicri:regionArea>
</affiliation>
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<author><name sortKey="Mylle, Evelien" sort="Mylle, Evelien" uniqKey="Mylle E" first="Evelien" last="Mylle">Evelien Mylle</name>
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<country xml:lang="fr">Belgique</country>
<wicri:regionArea>Department of Plant Systems Biology, VIB, 9052 Gent, Belgium; Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Gent</wicri:regionArea>
</affiliation>
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<author><name sortKey="Bischoff, Volker" sort="Bischoff, Volker" uniqKey="Bischoff V" first="Volker" last="Bischoff">Volker Bischoff</name>
<affiliation wicri:level="1"><nlm:aff id="A4">Institut National de la Recherche Agronomique, Unité Mixte de Recherche 1318, Institut Jean-Pierre Bourgin, Saclay Plant Sciences, 78000 Versailles, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Institut National de la Recherche Agronomique, Unité Mixte de Recherche 1318, Institut Jean-Pierre Bourgin, Saclay Plant Sciences, 78000 Versailles</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="A5">AgroParisTech,Institut Jean-Pierre Bourgin, 78000 Versailles, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>AgroParisTech,Institut Jean-Pierre Bourgin, 78000 Versailles</wicri:regionArea>
</affiliation>
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<author><name sortKey="Vernhettes, Samantha" sort="Vernhettes, Samantha" uniqKey="Vernhettes S" first="Samantha" last="Vernhettes">Samantha Vernhettes</name>
<affiliation wicri:level="1"><nlm:aff id="A4">Institut National de la Recherche Agronomique, Unité Mixte de Recherche 1318, Institut Jean-Pierre Bourgin, Saclay Plant Sciences, 78000 Versailles, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Institut National de la Recherche Agronomique, Unité Mixte de Recherche 1318, Institut Jean-Pierre Bourgin, Saclay Plant Sciences, 78000 Versailles</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="A5">AgroParisTech,Institut Jean-Pierre Bourgin, 78000 Versailles, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>AgroParisTech,Institut Jean-Pierre Bourgin, 78000 Versailles</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Winne, Johan" sort="Winne, Johan" uniqKey="Winne J" first="Johan" last="Winne">Johan Winne</name>
<affiliation wicri:level="1"><nlm:aff id="A6">Department of Organic Chemistry, Polymer Chemistry Research Group and Laboratory for Organic Synthesis, Ghent University, 9000 Gent, Belgium</nlm:aff>
<country xml:lang="fr">Belgique</country>
<wicri:regionArea>Department of Organic Chemistry, Polymer Chemistry Research Group and Laboratory for Organic Synthesis, Ghent University, 9000 Gent</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Friml, Ji" sort="Friml, Ji" uniqKey="Friml J" first="Ji" last="Friml">Ji Friml</name>
<affiliation wicri:level="1"><nlm:aff id="A7">Institute of Science and Technology Austria (IST Austria), 3400 Klosterneuburg, Austria</nlm:aff>
<country xml:lang="fr">Autriche</country>
<wicri:regionArea>Institute of Science and Technology Austria (IST Austria), 3400 Klosterneuburg</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Stierhof, York Dieter" sort="Stierhof, York Dieter" uniqKey="Stierhof Y" first="York-Dieter" last="Stierhof">York-Dieter Stierhof</name>
<affiliation wicri:level="1"><nlm:aff id="A8">Center for Plant Molecular Biology (ZMBP), University of Tübingen, 72076 Tübingen, Germany</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Center for Plant Molecular Biology (ZMBP), University of Tübingen, 72076 Tübingen</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Schumacher, Karin" sort="Schumacher, Karin" uniqKey="Schumacher K" first="Karin" last="Schumacher">Karin Schumacher</name>
<affiliation wicri:level="1"><nlm:aff id="A2">Developmental Biology of Plants, Centre for Organismal Studies (COS), Heidelberg University, 69120 Heidelberg, Germany</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Developmental Biology of Plants, Centre for Organismal Studies (COS), Heidelberg University, 69120 Heidelberg</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Persson, Staffan" sort="Persson, Staffan" uniqKey="Persson S" first="Staffan" last="Persson">Staffan Persson</name>
<affiliation wicri:level="1"><nlm:aff id="A3">Max-Planck Institute for Molecular Plant Physiology, 14476 Potsdam, Germany</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Max-Planck Institute for Molecular Plant Physiology, 14476 Potsdam</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="A9">Australian Research Council, Centre of Excellence in Plant Cell Walls, School of Botany, University of Melbourne, Parkville, Victoria 3010, Australia</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>Australian Research Council, Centre of Excellence in Plant Cell Walls, School of Botany, University of Melbourne, Parkville, Victoria 3010</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Russinova, Eugenia" sort="Russinova, Eugenia" uniqKey="Russinova E" first="Eugenia" last="Russinova">Eugenia Russinova</name>
<affiliation wicri:level="1"><nlm:aff id="A1">Department of Plant Systems Biology, VIB, 9052 Gent, Belgium; Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Gent, Belgium</nlm:aff>
<country xml:lang="fr">Belgique</country>
<wicri:regionArea>Department of Plant Systems Biology, VIB, 9052 Gent, Belgium; Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Gent</wicri:regionArea>
</affiliation>
</author>
</analytic>
<series><title level="j">Nature plants</title>
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<front><div type="abstract" xml:lang="en"><p id="P2">In plants, vacuolar H<sup>+</sup>
-ATPase (V-ATPase) activity acidifies both the trans-Golgi network/early endosome (TGN/EE) and the vacuole. This dual V-ATPase function has impeded our understanding in how the pH homeostasis within the plant TGN/EE controls exo- and endocytosis. Here, we show that the weak V-ATPase mutant <italic>deetiolated3</italic>
(<italic>det3</italic>
) displayed a pH increase in the TGN/EE, but not in the vacuole, strongly impairing secretion and recycling of the brassinosteroid receptor and the cellulose synthase complexes to the plasma membrane, in contrast to mutants lacking tonoplast-localized V-ATPase activity only. The brassinosteroid insensitivity and the cellulose deficiency defects in <italic>det3</italic>
were tightly correlated with reduced Golgi and TGN/EE motility. Thus, our results provide strong evidence that acidification of the TGN/EE, but not of the vacuole, is indispensable for functional secretion and recycling in plants.</p>
</div>
</front>
</TEI>
<pmc article-type="research-article"><pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<pmc-dir>properties manuscript</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-journal-id">101651677</journal-id>
<journal-id journal-id-type="pubmed-jr-id">43556</journal-id>
<journal-id journal-id-type="nlm-ta">Nat Plants</journal-id>
<journal-id journal-id-type="iso-abbrev">Nat Plants</journal-id>
<journal-title-group><journal-title>Nature plants</journal-title>
</journal-title-group>
<issn pub-type="epub">2055-0278</issn>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">27250258</article-id>
<article-id pub-id-type="pmc">4905525</article-id>
<article-id pub-id-type="doi">10.1038/nplants.2015.94</article-id>
<article-id pub-id-type="manuscript">EMS68478</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>V-ATPase-activity in the TGN/EE is required for exocytosis and recycling in <italic>Arabidopsis</italic>
</article-title>
</title-group>
<contrib-group><contrib contrib-type="author" equal-contrib="yes"><name><surname>Luo</surname>
<given-names>Yu</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
</contrib>
<contrib contrib-type="author" equal-contrib="yes"><name><surname>Scholl</surname>
<given-names>Stefan</given-names>
</name>
<xref ref-type="aff" rid="A2">2</xref>
</contrib>
<contrib contrib-type="author" equal-contrib="yes"><name><surname>Doering</surname>
<given-names>Anett</given-names>
</name>
<xref ref-type="aff" rid="A3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Zhang</surname>
<given-names>Yi</given-names>
</name>
<xref ref-type="aff" rid="A3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Irani</surname>
<given-names>Niloufer G.</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
<xref ref-type="author-notes" rid="FN1">‡</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Rubbo</surname>
<given-names>Simone Di</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Neumetzler</surname>
<given-names>Lutz</given-names>
</name>
<xref ref-type="aff" rid="A3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Krishnamoorthy</surname>
<given-names>Praveen</given-names>
</name>
<xref ref-type="aff" rid="A3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Van Houtte</surname>
<given-names>Isabelle</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Mylle</surname>
<given-names>Evelien</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Bischoff</surname>
<given-names>Volker</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>Vernhettes</surname>
<given-names>Samantha</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>Winne</surname>
<given-names>Johan</given-names>
</name>
<xref ref-type="aff" rid="A6">6</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Friml</surname>
<given-names>Jiří</given-names>
</name>
<xref ref-type="aff" rid="A7">7</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Stierhof</surname>
<given-names>York-Dieter</given-names>
</name>
<xref ref-type="aff" rid="A8">8</xref>
</contrib>
<contrib contrib-type="author" equal-contrib="yes"><name><surname>Schumacher</surname>
<given-names>Karin</given-names>
</name>
<xref ref-type="aff" rid="A2">2</xref>
<xref ref-type="corresp" rid="CR1">⋆</xref>
</contrib>
<contrib contrib-type="author" equal-contrib="yes"><name><surname>Persson</surname>
<given-names>Staffan</given-names>
</name>
<xref ref-type="aff" rid="A3">3</xref>
<xref ref-type="aff" rid="A9">9</xref>
<xref ref-type="corresp" rid="CR1">⋆</xref>
</contrib>
<contrib contrib-type="author" equal-contrib="yes"><name><surname>Russinova</surname>
<given-names>Eugenia</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
<xref ref-type="corresp" rid="CR1">⋆</xref>
</contrib>
</contrib-group>
<aff id="A1"><label>1</label>
Department of Plant Systems Biology, VIB, 9052 Gent, Belgium; Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Gent, Belgium</aff>
<aff id="A2"><label>2</label>
Developmental Biology of Plants, Centre for Organismal Studies (COS), Heidelberg University, 69120 Heidelberg, Germany</aff>
<aff id="A3"><label>3</label>
Max-Planck Institute for Molecular Plant Physiology, 14476 Potsdam, Germany</aff>
<aff id="A4"><label>4</label>
Institut National de la Recherche Agronomique, Unité Mixte de Recherche 1318, Institut Jean-Pierre Bourgin, Saclay Plant Sciences, 78000 Versailles, France</aff>
<aff id="A5"><label>5</label>
AgroParisTech,Institut Jean-Pierre Bourgin, 78000 Versailles, France</aff>
<aff id="A6"><label>6</label>
Department of Organic Chemistry, Polymer Chemistry Research Group and Laboratory for Organic Synthesis, Ghent University, 9000 Gent, Belgium</aff>
<aff id="A7"><label>7</label>
Institute of Science and Technology Austria (IST Austria), 3400 Klosterneuburg, Austria</aff>
<aff id="A8"><label>8</label>
Center for Plant Molecular Biology (ZMBP), University of Tübingen, 72076 Tübingen, Germany</aff>
<aff id="A9"><label>9</label>
Australian Research Council, Centre of Excellence in Plant Cell Walls, School of Botany, University of Melbourne, Parkville, Victoria 3010, Australia</aff>
<author-notes><corresp id="CR1"><label>⋆</label>
<email>Staffan.Persson@unimelb.au.edu</email>
, <email>karin.schumacher@cos.uni-heidelberg.de</email>
, and <email>eugenia.russinova@psb.vib-ugent.be</email>
</corresp>
<fn fn-type="present-address" id="FN1"><label>‡</label>
<p id="P1">Present address: Department of Plant Sciences, University of Oxford, Oxford OX1 3RB, UK.</p>
</fn>
</author-notes>
<pub-date pub-type="nihms-submitted"><day>8</day>
<month>6</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="epub"><day>06</day>
<month>7</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="collection"><year>2015</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>13</day>
<month>6</month>
<year>2016</year>
</pub-date>
<volume>1</volume>
<fpage>15094</fpage>
<lpage>15094</lpage>
<pmc-comment>elocation-id from pubmed: 10.1038/nplants.2015.94</pmc-comment>
<abstract><p id="P2">In plants, vacuolar H<sup>+</sup>
-ATPase (V-ATPase) activity acidifies both the trans-Golgi network/early endosome (TGN/EE) and the vacuole. This dual V-ATPase function has impeded our understanding in how the pH homeostasis within the plant TGN/EE controls exo- and endocytosis. Here, we show that the weak V-ATPase mutant <italic>deetiolated3</italic>
(<italic>det3</italic>
) displayed a pH increase in the TGN/EE, but not in the vacuole, strongly impairing secretion and recycling of the brassinosteroid receptor and the cellulose synthase complexes to the plasma membrane, in contrast to mutants lacking tonoplast-localized V-ATPase activity only. The brassinosteroid insensitivity and the cellulose deficiency defects in <italic>det3</italic>
were tightly correlated with reduced Golgi and TGN/EE motility. Thus, our results provide strong evidence that acidification of the TGN/EE, but not of the vacuole, is indispensable for functional secretion and recycling in plants.</p>
</abstract>
</article-meta>
</front>
</pmc>
</record>
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