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V-ATPase-activity in the TGN/EE is required for exocytosis and recycling in Arabidopsis

Identifieur interne : 002661 ( Main/Merge ); précédent : 002660; suivant : 002662

V-ATPase-activity in the TGN/EE is required for exocytosis and recycling in Arabidopsis

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 :

RBID : PMC:4905525

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 deetiolated3 (det3) 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 det3 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.


Url:
DOI: 10.1038/nplants.2015.94
PubMed: 27250258
PubMed Central: 4905525

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<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>
<placeName>
<region type="land" nuts="2">Brandebourg</region>
<settlement type="city">Potsdam</settlement>
</placeName>
</affiliation>
</author>
<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="4">
<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>
<orgName type="university">Université de Gand</orgName>
<placeName>
<settlement type="city">Gand</settlement>
<region>Région flamande</region>
<region type="district" nuts="2">Province de Flandre-Orientale</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Mylle, Evelien" sort="Mylle, Evelien" uniqKey="Mylle E" first="Evelien" last="Mylle">Evelien Mylle</name>
<affiliation wicri:level="4">
<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>
<orgName type="university">Université de Gand</orgName>
<placeName>
<settlement type="city">Gand</settlement>
<region>Région flamande</region>
<region type="district" nuts="2">Province de Flandre-Orientale</region>
</placeName>
</affiliation>
</author>
<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>
<wicri:noRegion>78000 Versailles</wicri:noRegion>
<wicri:noRegion>78000 Versailles</wicri:noRegion>
</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>
<wicri:noRegion>78000 Versailles</wicri:noRegion>
<wicri:noRegion>78000 Versailles</wicri:noRegion>
</affiliation>
</author>
<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>
<wicri:noRegion>78000 Versailles</wicri:noRegion>
<wicri:noRegion>78000 Versailles</wicri:noRegion>
</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>
<wicri:noRegion>78000 Versailles</wicri:noRegion>
<wicri:noRegion>78000 Versailles</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Winne, Johan" sort="Winne, Johan" uniqKey="Winne J" first="Johan" last="Winne">Johan Winne</name>
<affiliation wicri:level="4">
<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>
<placeName>
<region type="province" nuts="2">Province de Flandre-Orientale</region>
<settlement type="city">Gand</settlement>
<settlement type="city">Gand</settlement>
</placeName>
<orgName type="university">Université de Gand</orgName>
</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>
<wicri:noRegion>3400 Klosterneuburg</wicri:noRegion>
</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>
<wicri:noRegion>72076 Tübingen</wicri:noRegion>
<wicri:noRegion>72076 Tübingen</wicri:noRegion>
<wicri:noRegion>72076 Tübingen</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Schumacher, Karin" sort="Schumacher, Karin" uniqKey="Schumacher K" first="Karin" last="Schumacher">Karin Schumacher</name>
<affiliation wicri:level="3">
<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>
<placeName>
<region type="land" nuts="1">Bade-Wurtemberg</region>
<region type="district" nuts="2">District de Karlsruhe</region>
<settlement type="city">Heidelberg</settlement>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Persson, Staffan" sort="Persson, Staffan" uniqKey="Persson S" first="Staffan" last="Persson">Staffan Persson</name>
<affiliation wicri:level="3">
<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>
<placeName>
<region type="land" nuts="2">Brandebourg</region>
<settlement type="city">Potsdam</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="4">
<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>
<orgName type="university">Université de Melbourne</orgName>
<placeName>
<settlement type="city">Melbourne</settlement>
<region type="état">Victoria (État)</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Russinova, Eugenia" sort="Russinova, Eugenia" uniqKey="Russinova E" first="Eugenia" last="Russinova">Eugenia Russinova</name>
<affiliation wicri:level="4">
<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>
<orgName type="university">Université de Gand</orgName>
<placeName>
<settlement type="city">Gand</settlement>
<region>Région flamande</region>
<region type="district" nuts="2">Province de Flandre-Orientale</region>
</placeName>
</affiliation>
</author>
</analytic>
<series>
<title level="j">Nature plants</title>
<idno type="eISSN">2055-0278</idno>
<imprint>
<date when="2015">2015</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc>
<textClass></textClass>
</profileDesc>
</teiHeader>
<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>
</record>

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