Multiparametric real-time sensing of cytosolic physiology links hypoxia responses to mitochondrial electron transport.
Identifieur interne : 000103 ( Main/Exploration ); précédent : 000102; suivant : 000104Multiparametric real-time sensing of cytosolic physiology links hypoxia responses to mitochondrial electron transport.
Auteurs : Stephan Wagner [Allemagne] ; Janina Steinbeck [Allemagne] ; Philippe Fuchs [Allemagne] ; Sophie Lichtenauer [Allemagne] ; Marlene Els Sser [Allemagne] ; Jos H M. Schippers [Allemagne] ; Thomas Nietzel [Allemagne] ; Cristina Ruberti [Allemagne] ; Olivier Van Aken [Suède] ; Andreas J. Meyer [Allemagne] ; Joost T. Van Dongen [Allemagne] ; Romy R. Schmidt [Allemagne] ; Markus Schwarzl Nder [Allemagne]Source :
- The New phytologist [ 1469-8137 ] ; 2019.
Descripteurs français
- KwdFr :
- Adénosine triphosphate (métabolisme), Arabidopsis (cytologie), Arabidopsis (métabolisme), Calcium (métabolisme), Carbone (métabolisme), Cellules végétales (métabolisme), Concentration en ions d'hydrogène (MeSH), Cytosol (métabolisme), Feuilles de plante (cytologie), Feuilles de plante (métabolisme), Glutathion (métabolisme), Mitochondries (métabolisme), NAD (métabolisme), Oxygène (métabolisme), Protéines bactériennes (génétique), Protéines bactériennes (métabolisme), Protéines luminescentes (génétique), Protéines luminescentes (métabolisme), Transport d'électrons (MeSH), Végétaux génétiquement modifiés (MeSH).
- MESH :
- cytologie : Arabidopsis, Feuilles de plante.
- génétique : Protéines bactériennes, Protéines luminescentes.
- métabolisme : Adénosine triphosphate, Arabidopsis, Calcium, Carbone, Cellules végétales, Cytosol, Feuilles de plante, Glutathion, Mitochondries, NAD, Oxygène, Protéines bactériennes, Protéines luminescentes.
- Concentration en ions d'hydrogène, Transport d'électrons, Végétaux génétiquement modifiés.
English descriptors
- KwdEn :
- Adenosine Triphosphate (metabolism), Arabidopsis (cytology), Arabidopsis (metabolism), Bacterial Proteins (genetics), Bacterial Proteins (metabolism), Calcium (metabolism), Carbon (metabolism), Cytosol (metabolism), Electron Transport (MeSH), Glutathione (metabolism), Hydrogen-Ion Concentration (MeSH), Luminescent Proteins (genetics), Luminescent Proteins (metabolism), Mitochondria (metabolism), NAD (metabolism), Oxygen (metabolism), Plant Cells (metabolism), Plant Leaves (cytology), Plant Leaves (metabolism), Plants, Genetically Modified (MeSH).
- MESH :
- chemical , genetics : Bacterial Proteins, Luminescent Proteins.
- chemical , metabolism : Adenosine Triphosphate, Bacterial Proteins, Calcium, Carbon, Glutathione, Luminescent Proteins, NAD, Oxygen.
- cytology : Arabidopsis, Plant Leaves.
- metabolism : Arabidopsis, Cytosol, Mitochondria, Plant Cells, Plant Leaves.
- Electron Transport, Hydrogen-Ion Concentration, Plants, Genetically Modified.
Abstract
Hypoxia regularly occurs during plant development and can be induced by the environment through, for example, flooding. To understand how plant tissue physiology responds to progressing oxygen restriction, we aimed to monitor subcellular physiology in real time and in vivo. We establish a fluorescent protein sensor-based system for multiparametric monitoring of dynamic changes in subcellular physiology of living Arabidopsis thaliana leaves and exemplify its applicability for hypoxia stress. By monitoring cytosolic dynamics of magnesium adenosine 5'-triphosphate, free calcium ion concentration, pH, NAD redox status, and glutathione redox status in parallel, linked to transcriptional and metabolic responses, we generate an integrated picture of the physiological response to progressing hypoxia. We show that the physiological changes are surprisingly robust, even when plant carbon status is modified, as achieved by sucrose feeding or extended night. Inhibition of the mitochondrial respiratory chain causes dynamics of cytosolic physiology that are remarkably similar to those under oxygen depletion, highlighting mitochondrial electron transport as a key determinant of the cellular consequences of hypoxia beyond the organelle. A broadly applicable system for parallel in vivo sensing of plant stress physiology is established to map out the physiological context under which both mitochondrial retrograde signalling and low oxygen signalling occur, indicating shared upstream stimuli.
DOI: 10.1111/nph.16093
PubMed: 31386759
Affiliations:
- Allemagne, Suède
- District de Cologne, District de Münster, Rhénanie-du-Nord-Westphalie
- Aix-la-Chapelle, Bonn, Cologne, Münster
Links toward previous steps (curation, corpus...)
Le document en format XML
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Schippers</name><affiliation wicri:level="3"><nlm:affiliation>Institute of Biology I, RWTH Aachen University, Worringerweg 1, D-52074, Aachen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Biology I, RWTH Aachen University, Worringerweg 1, D-52074, Aachen</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Aix-la-Chapelle</settlement></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Leibniz-Institut für Pflanzengenetik und Kulturpflanzenforschung (IPK), Gatersleben, Corrensstraße 3, D-06466, Seeland, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Leibniz-Institut für Pflanzengenetik und Kulturpflanzenforschung (IPK), Gatersleben, Corrensstraße 3, D-06466, Seeland</wicri:regionArea><wicri:noRegion>06466, Seeland</wicri:noRegion><wicri:noRegion>06466, Seeland</wicri:noRegion><wicri:noRegion>Seeland</wicri:noRegion></affiliation></author><author><name sortKey="Nietzel, Thomas" sort="Nietzel, Thomas" uniqKey="Nietzel T" first="Thomas" last="Nietzel">Thomas Nietzel</name><affiliation wicri:level="3"><nlm:affiliation>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Münster</region><settlement type="city">Münster</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Friedrich-Ebert-Allee 144, D-53113, Bonn, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Friedrich-Ebert-Allee 144, D-53113, Bonn</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Bonn</settlement></placeName></affiliation></author><author><name sortKey="Ruberti, Cristina" sort="Ruberti, Cristina" uniqKey="Ruberti C" first="Cristina" last="Ruberti">Cristina Ruberti</name><affiliation wicri:level="3"><nlm:affiliation>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Münster</region><settlement type="city">Münster</settlement></placeName></affiliation></author><author><name sortKey="Van Aken, Olivier" sort="Van Aken, Olivier" uniqKey="Van Aken O" first="Olivier" last="Van Aken">Olivier Van Aken</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biology, Lund University, Sölvegatan 35, Lund, 223 62, Sweden.</nlm:affiliation><country xml:lang="fr">Suède</country><wicri:regionArea>Department of Biology, Lund University, Sölvegatan 35, Lund, 223 62</wicri:regionArea><wicri:noRegion>223 62</wicri:noRegion></affiliation></author><author><name sortKey="Meyer, Andreas J" sort="Meyer, Andreas J" uniqKey="Meyer A" first="Andreas J" last="Meyer">Andreas J. Meyer</name><affiliation wicri:level="3"><nlm:affiliation>Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Friedrich-Ebert-Allee 144, D-53113, Bonn, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Friedrich-Ebert-Allee 144, D-53113, Bonn</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Bonn</settlement></placeName></affiliation></author><author><name sortKey="Van Dongen, Joost T" sort="Van Dongen, Joost T" uniqKey="Van Dongen J" first="Joost T" last="Van Dongen">Joost T. Van Dongen</name><affiliation wicri:level="3"><nlm:affiliation>Institute of Biology I, RWTH Aachen University, Worringerweg 1, D-52074, Aachen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Biology I, RWTH Aachen University, Worringerweg 1, D-52074, Aachen</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Aix-la-Chapelle</settlement></placeName></affiliation></author><author><name sortKey="Schmidt, Romy R" sort="Schmidt, Romy R" uniqKey="Schmidt R" first="Romy R" last="Schmidt">Romy R. Schmidt</name><affiliation wicri:level="3"><nlm:affiliation>Institute of Biology I, RWTH Aachen University, Worringerweg 1, D-52074, Aachen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Biology I, RWTH Aachen University, Worringerweg 1, D-52074, Aachen</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Aix-la-Chapelle</settlement></placeName></affiliation></author><author><name sortKey="Schwarzl Nder, Markus" sort="Schwarzl Nder, Markus" uniqKey="Schwarzl Nder M" first="Markus" last="Schwarzl Nder">Markus Schwarzl Nder</name><affiliation wicri:level="3"><nlm:affiliation>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Münster</region><settlement type="city">Münster</settlement></placeName></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2019">2019</date><idno type="RBID">pubmed:31386759</idno><idno type="pmid">31386759</idno><idno type="doi">10.1111/nph.16093</idno><idno type="wicri:Area/Main/Corpus">000090</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000090</idno><idno type="wicri:Area/Main/Curation">000090</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Curation">000090</idno><idno type="wicri:Area/Main/Exploration">000090</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Multiparametric real-time sensing of cytosolic physiology links hypoxia responses to mitochondrial electron transport.</title><author><name sortKey="Wagner, Stephan" sort="Wagner, Stephan" uniqKey="Wagner S" first="Stephan" last="Wagner">Stephan Wagner</name><affiliation wicri:level="3"><nlm:affiliation>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Münster</region><settlement type="city">Münster</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Friedrich-Ebert-Allee 144, D-53113, Bonn, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Friedrich-Ebert-Allee 144, D-53113, Bonn</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Bonn</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>Max-Planck-Institute for Plant Breeding Research, Carl-von-Linné Weg 10, D-50829, Cologne, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Max-Planck-Institute for Plant Breeding Research, Carl-von-Linné Weg 10, D-50829, Cologne</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Cologne</settlement></placeName></affiliation></author><author><name sortKey="Steinbeck, Janina" sort="Steinbeck, Janina" uniqKey="Steinbeck J" first="Janina" last="Steinbeck">Janina Steinbeck</name><affiliation wicri:level="3"><nlm:affiliation>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Münster</region><settlement type="city">Münster</settlement></placeName></affiliation></author><author><name sortKey="Fuchs, Philippe" sort="Fuchs, Philippe" uniqKey="Fuchs P" first="Philippe" last="Fuchs">Philippe Fuchs</name><affiliation wicri:level="3"><nlm:affiliation>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Münster</region><settlement type="city">Münster</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Friedrich-Ebert-Allee 144, D-53113, Bonn, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Friedrich-Ebert-Allee 144, D-53113, Bonn</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Bonn</settlement></placeName></affiliation></author><author><name sortKey="Lichtenauer, Sophie" sort="Lichtenauer, Sophie" uniqKey="Lichtenauer S" first="Sophie" last="Lichtenauer">Sophie Lichtenauer</name><affiliation wicri:level="3"><nlm:affiliation>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Münster</region><settlement type="city">Münster</settlement></placeName></affiliation></author><author><name sortKey="Els Sser, Marlene" sort="Els Sser, Marlene" uniqKey="Els Sser M" first="Marlene" last="Els Sser">Marlene Els Sser</name><affiliation wicri:level="3"><nlm:affiliation>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Münster</region><settlement type="city">Münster</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Friedrich-Ebert-Allee 144, D-53113, Bonn, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Friedrich-Ebert-Allee 144, D-53113, Bonn</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Bonn</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>Institute for Cellular and Molecular Botany (IZMB), University of Bonn, Kirschallee 1, D-53115, Bonn, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute for Cellular and Molecular Botany (IZMB), University of Bonn, Kirschallee 1, D-53115, Bonn</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Bonn</settlement></placeName></affiliation></author><author><name sortKey="Schippers, Jos H M" sort="Schippers, Jos H M" uniqKey="Schippers J" first="Jos H M" last="Schippers">Jos H M. Schippers</name><affiliation wicri:level="3"><nlm:affiliation>Institute of Biology I, RWTH Aachen University, Worringerweg 1, D-52074, Aachen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Biology I, RWTH Aachen University, Worringerweg 1, D-52074, Aachen</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Aix-la-Chapelle</settlement></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Leibniz-Institut für Pflanzengenetik und Kulturpflanzenforschung (IPK), Gatersleben, Corrensstraße 3, D-06466, Seeland, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Leibniz-Institut für Pflanzengenetik und Kulturpflanzenforschung (IPK), Gatersleben, Corrensstraße 3, D-06466, Seeland</wicri:regionArea><wicri:noRegion>06466, Seeland</wicri:noRegion><wicri:noRegion>06466, Seeland</wicri:noRegion><wicri:noRegion>Seeland</wicri:noRegion></affiliation></author><author><name sortKey="Nietzel, Thomas" sort="Nietzel, Thomas" uniqKey="Nietzel T" first="Thomas" last="Nietzel">Thomas Nietzel</name><affiliation wicri:level="3"><nlm:affiliation>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Münster</region><settlement type="city">Münster</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Friedrich-Ebert-Allee 144, D-53113, Bonn, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Friedrich-Ebert-Allee 144, D-53113, Bonn</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Bonn</settlement></placeName></affiliation></author><author><name sortKey="Ruberti, Cristina" sort="Ruberti, Cristina" uniqKey="Ruberti C" first="Cristina" last="Ruberti">Cristina Ruberti</name><affiliation wicri:level="3"><nlm:affiliation>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Münster</region><settlement type="city">Münster</settlement></placeName></affiliation></author><author><name sortKey="Van Aken, Olivier" sort="Van Aken, Olivier" uniqKey="Van Aken O" first="Olivier" last="Van Aken">Olivier Van Aken</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biology, Lund University, Sölvegatan 35, Lund, 223 62, Sweden.</nlm:affiliation><country xml:lang="fr">Suède</country><wicri:regionArea>Department of Biology, Lund University, Sölvegatan 35, Lund, 223 62</wicri:regionArea><wicri:noRegion>223 62</wicri:noRegion></affiliation></author><author><name sortKey="Meyer, Andreas J" sort="Meyer, Andreas J" uniqKey="Meyer A" first="Andreas J" last="Meyer">Andreas J. Meyer</name><affiliation wicri:level="3"><nlm:affiliation>Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Friedrich-Ebert-Allee 144, D-53113, Bonn, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Friedrich-Ebert-Allee 144, D-53113, Bonn</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Bonn</settlement></placeName></affiliation></author><author><name sortKey="Van Dongen, Joost T" sort="Van Dongen, Joost T" uniqKey="Van Dongen J" first="Joost T" last="Van Dongen">Joost T. Van Dongen</name><affiliation wicri:level="3"><nlm:affiliation>Institute of Biology I, RWTH Aachen University, Worringerweg 1, D-52074, Aachen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Biology I, RWTH Aachen University, Worringerweg 1, D-52074, Aachen</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Aix-la-Chapelle</settlement></placeName></affiliation></author><author><name sortKey="Schmidt, Romy R" sort="Schmidt, Romy R" uniqKey="Schmidt R" first="Romy R" last="Schmidt">Romy R. Schmidt</name><affiliation wicri:level="3"><nlm:affiliation>Institute of Biology I, RWTH Aachen University, Worringerweg 1, D-52074, Aachen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Biology I, RWTH Aachen University, Worringerweg 1, D-52074, Aachen</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Aix-la-Chapelle</settlement></placeName></affiliation></author><author><name sortKey="Schwarzl Nder, Markus" sort="Schwarzl Nder, Markus" uniqKey="Schwarzl Nder M" first="Markus" last="Schwarzl Nder">Markus Schwarzl Nder</name><affiliation wicri:level="3"><nlm:affiliation>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Münster</region><settlement type="city">Münster</settlement></placeName></affiliation></author></analytic><series><title level="j">The New phytologist</title><idno type="eISSN">1469-8137</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Adenosine Triphosphate (metabolism)</term><term>Arabidopsis (cytology)</term><term>Arabidopsis (metabolism)</term><term>Bacterial Proteins (genetics)</term><term>Bacterial Proteins (metabolism)</term><term>Calcium (metabolism)</term><term>Carbon (metabolism)</term><term>Cytosol (metabolism)</term><term>Electron Transport (MeSH)</term><term>Glutathione (metabolism)</term><term>Hydrogen-Ion Concentration (MeSH)</term><term>Luminescent Proteins (genetics)</term><term>Luminescent Proteins (metabolism)</term><term>Mitochondria (metabolism)</term><term>NAD (metabolism)</term><term>Oxygen (metabolism)</term><term>Plant Cells (metabolism)</term><term>Plant Leaves (cytology)</term><term>Plant Leaves (metabolism)</term><term>Plants, Genetically Modified (MeSH)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Adénosine triphosphate (métabolisme)</term><term>Arabidopsis (cytologie)</term><term>Arabidopsis (métabolisme)</term><term>Calcium (métabolisme)</term><term>Carbone (métabolisme)</term><term>Cellules végétales (métabolisme)</term><term>Concentration en ions d'hydrogène (MeSH)</term><term>Cytosol (métabolisme)</term><term>Feuilles de plante (cytologie)</term><term>Feuilles de plante (métabolisme)</term><term>Glutathion (métabolisme)</term><term>Mitochondries (métabolisme)</term><term>NAD (métabolisme)</term><term>Oxygène (métabolisme)</term><term>Protéines bactériennes (génétique)</term><term>Protéines bactériennes (métabolisme)</term><term>Protéines luminescentes (génétique)</term><term>Protéines luminescentes (métabolisme)</term><term>Transport d'électrons (MeSH)</term><term>Végétaux génétiquement modifiés (MeSH)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Bacterial Proteins</term><term>Luminescent Proteins</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Adenosine Triphosphate</term><term>Bacterial Proteins</term><term>Calcium</term><term>Carbon</term><term>Glutathione</term><term>Luminescent Proteins</term><term>NAD</term><term>Oxygen</term></keywords><keywords scheme="MESH" qualifier="cytologie" xml:lang="fr"><term>Arabidopsis</term><term>Feuilles de plante</term></keywords><keywords scheme="MESH" qualifier="cytology" xml:lang="en"><term>Arabidopsis</term><term>Plant Leaves</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Protéines bactériennes</term><term>Protéines luminescentes</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Arabidopsis</term><term>Cytosol</term><term>Mitochondria</term><term>Plant Cells</term><term>Plant Leaves</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Adénosine triphosphate</term><term>Arabidopsis</term><term>Calcium</term><term>Carbone</term><term>Cellules végétales</term><term>Cytosol</term><term>Feuilles de plante</term><term>Glutathion</term><term>Mitochondries</term><term>NAD</term><term>Oxygène</term><term>Protéines bactériennes</term><term>Protéines luminescentes</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Electron Transport</term><term>Hydrogen-Ion Concentration</term><term>Plants, Genetically Modified</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Concentration en ions d'hydrogène</term><term>Transport d'électrons</term><term>Végétaux génétiquement modifiés</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Hypoxia regularly occurs during plant development and can be induced by the environment through, for example, flooding. To understand how plant tissue physiology responds to progressing oxygen restriction, we aimed to monitor subcellular physiology in real time and in vivo. We establish a fluorescent protein sensor-based system for multiparametric monitoring of dynamic changes in subcellular physiology of living Arabidopsis thaliana leaves and exemplify its applicability for hypoxia stress. By monitoring cytosolic dynamics of magnesium adenosine 5'-triphosphate, free calcium ion concentration, pH, NAD redox status, and glutathione redox status in parallel, linked to transcriptional and metabolic responses, we generate an integrated picture of the physiological response to progressing hypoxia. We show that the physiological changes are surprisingly robust, even when plant carbon status is modified, as achieved by sucrose feeding or extended night. Inhibition of the mitochondrial respiratory chain causes dynamics of cytosolic physiology that are remarkably similar to those under oxygen depletion, highlighting mitochondrial electron transport as a key determinant of the cellular consequences of hypoxia beyond the organelle. A broadly applicable system for parallel in vivo sensing of plant stress physiology is established to map out the physiological context under which both mitochondrial retrograde signalling and low oxygen signalling occur, indicating shared upstream stimuli.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">31386759</PMID><DateCompleted><Year>2020</Year><Month>08</Month><Day>05</Day></DateCompleted><DateRevised><Year>2020</Year><Month>09</Month><Day>30</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1469-8137</ISSN><JournalIssue CitedMedium="Internet"><Volume>224</Volume><Issue>4</Issue><PubDate><Year>2019</Year><Month>12</Month></PubDate></JournalIssue><Title>The New phytologist</Title><ISOAbbreviation>New Phytol</ISOAbbreviation></Journal><ArticleTitle>Multiparametric real-time sensing of cytosolic physiology links hypoxia responses to mitochondrial electron transport.</ArticleTitle><Pagination><MedlinePgn>1668-1684</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1111/nph.16093</ELocationID><Abstract><AbstractText>Hypoxia regularly occurs during plant development and can be induced by the environment through, for example, flooding. To understand how plant tissue physiology responds to progressing oxygen restriction, we aimed to monitor subcellular physiology in real time and in vivo. We establish a fluorescent protein sensor-based system for multiparametric monitoring of dynamic changes in subcellular physiology of living Arabidopsis thaliana leaves and exemplify its applicability for hypoxia stress. By monitoring cytosolic dynamics of magnesium adenosine 5'-triphosphate, free calcium ion concentration, pH, NAD redox status, and glutathione redox status in parallel, linked to transcriptional and metabolic responses, we generate an integrated picture of the physiological response to progressing hypoxia. We show that the physiological changes are surprisingly robust, even when plant carbon status is modified, as achieved by sucrose feeding or extended night. Inhibition of the mitochondrial respiratory chain causes dynamics of cytosolic physiology that are remarkably similar to those under oxygen depletion, highlighting mitochondrial electron transport as a key determinant of the cellular consequences of hypoxia beyond the organelle. A broadly applicable system for parallel in vivo sensing of plant stress physiology is established to map out the physiological context under which both mitochondrial retrograde signalling and low oxygen signalling occur, indicating shared upstream stimuli.</AbstractText><CopyrightInformation>© 2019 The Authors. New Phytologist © 2019 New Phytologist Trust.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Wagner</LastName><ForeName>Stephan</ForeName><Initials>S</Initials><Identifier Source="ORCID">0000-0001-5369-7911</Identifier><AffiliationInfo><Affiliation>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster, Germany.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Friedrich-Ebert-Allee 144, D-53113, Bonn, Germany.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Max-Planck-Institute for Plant Breeding Research, Carl-von-Linné Weg 10, D-50829, Cologne, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Steinbeck</LastName><ForeName>Janina</ForeName><Initials>J</Initials><Identifier Source="ORCID">0000-0002-7793-5053</Identifier><AffiliationInfo><Affiliation>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Fuchs</LastName><ForeName>Philippe</ForeName><Initials>P</Initials><Identifier Source="ORCID">0000-0001-6379-853X</Identifier><AffiliationInfo><Affiliation>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster, Germany.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Friedrich-Ebert-Allee 144, D-53113, Bonn, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lichtenauer</LastName><ForeName>Sophie</ForeName><Initials>S</Initials><Identifier Source="ORCID">0000-0003-4525-6555</Identifier><AffiliationInfo><Affiliation>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Elsässer</LastName><ForeName>Marlene</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster, Germany.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Friedrich-Ebert-Allee 144, D-53113, Bonn, Germany.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Institute for Cellular and Molecular Botany (IZMB), University of Bonn, Kirschallee 1, D-53115, Bonn, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Schippers</LastName><ForeName>Jos H M</ForeName><Initials>JHM</Initials><Identifier Source="ORCID">0000-0001-7934-126X</Identifier><AffiliationInfo><Affiliation>Institute of Biology I, RWTH Aachen University, Worringerweg 1, D-52074, Aachen, Germany.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Leibniz-Institut für Pflanzengenetik und Kulturpflanzenforschung (IPK), Gatersleben, Corrensstraße 3, D-06466, Seeland, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Nietzel</LastName><ForeName>Thomas</ForeName><Initials>T</Initials><Identifier Source="ORCID">0000-0002-1934-1732</Identifier><AffiliationInfo><Affiliation>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster, Germany.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Friedrich-Ebert-Allee 144, D-53113, Bonn, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ruberti</LastName><ForeName>Cristina</ForeName><Initials>C</Initials><Identifier Source="ORCID">0000-0002-9013-1412</Identifier><AffiliationInfo><Affiliation>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Van Aken</LastName><ForeName>Olivier</ForeName><Initials>O</Initials><Identifier Source="ORCID">0000-0003-4024-968X</Identifier><AffiliationInfo><Affiliation>Department of Biology, Lund University, Sölvegatan 35, Lund, 223 62, Sweden.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Meyer</LastName><ForeName>Andreas J</ForeName><Initials>AJ</Initials><Identifier Source="ORCID">0000-0001-8144-4364</Identifier><AffiliationInfo><Affiliation>Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Friedrich-Ebert-Allee 144, D-53113, Bonn, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Van Dongen</LastName><ForeName>Joost T</ForeName><Initials>JT</Initials><Identifier Source="ORCID">0000-0001-7944-9289</Identifier><AffiliationInfo><Affiliation>Institute of Biology I, RWTH Aachen University, Worringerweg 1, D-52074, Aachen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Schmidt</LastName><ForeName>Romy R</ForeName><Initials>RR</Initials><Identifier Source="ORCID">0000-0002-3395-0673</Identifier><AffiliationInfo><Affiliation>Institute of Biology I, RWTH Aachen University, Worringerweg 1, D-52074, Aachen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Schwarzländer</LastName><ForeName>Markus</ForeName><Initials>M</Initials><Identifier Source="ORCID">0000-0003-0796-8308</Identifier><AffiliationInfo><Affiliation>Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143, Münster, Germany.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>09</Month><Day>18</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>New Phytol</MedlineTA><NlmUniqueID>9882884</NlmUniqueID><ISSNLinking>0028-646X</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D001426">Bacterial Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D008164">Luminescent Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="C054562">yellow fluorescent protein, Bacteria</NameOfSubstance></Chemical><Chemical><RegistryNumber>0U46U6E8UK</RegistryNumber><NameOfSubstance UI="D009243">NAD</NameOfSubstance></Chemical><Chemical><RegistryNumber>7440-44-0</RegistryNumber><NameOfSubstance UI="D002244">Carbon</NameOfSubstance></Chemical><Chemical><RegistryNumber>8L70Q75FXE</RegistryNumber><NameOfSubstance UI="D000255">Adenosine Triphosphate</NameOfSubstance></Chemical><Chemical><RegistryNumber>GAN16C9B8O</RegistryNumber><NameOfSubstance UI="D005978">Glutathione</NameOfSubstance></Chemical><Chemical><RegistryNumber>S88TT14065</RegistryNumber><NameOfSubstance UI="D010100">Oxygen</NameOfSubstance></Chemical><Chemical><RegistryNumber>SY7Q814VUP</RegistryNumber><NameOfSubstance UI="D002118">Calcium</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000255" MajorTopicYN="N">Adenosine Triphosphate</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D017360" MajorTopicYN="N">Arabidopsis</DescriptorName><QualifierName UI="Q000166" MajorTopicYN="N">cytology</QualifierName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D001426" MajorTopicYN="N">Bacterial Proteins</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D002118" MajorTopicYN="N">Calcium</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D002244" MajorTopicYN="N">Carbon</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D003600" MajorTopicYN="N">Cytosol</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D004579" MajorTopicYN="N">Electron Transport</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D005978" MajorTopicYN="N">Glutathione</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D006863" MajorTopicYN="N">Hydrogen-Ion Concentration</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D008164" MajorTopicYN="N">Luminescent Proteins</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D008928" MajorTopicYN="N">Mitochondria</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D009243" MajorTopicYN="N">NAD</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D010100" MajorTopicYN="N">Oxygen</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D059828" MajorTopicYN="N">Plant Cells</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D018515" MajorTopicYN="N">Plant Leaves</DescriptorName><QualifierName UI="Q000166" MajorTopicYN="N">cytology</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D030821" MajorTopicYN="N">Plants, Genetically Modified</DescriptorName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">cytosol</Keyword><Keyword MajorTopicYN="Y">genetically encoded fluorescent protein sensors</Keyword><Keyword MajorTopicYN="Y">hypoxia stress</Keyword><Keyword MajorTopicYN="Y">in vivo sensing</Keyword><Keyword MajorTopicYN="Y">mitochondrial electron transport chain</Keyword><Keyword MajorTopicYN="Y">retrograde signalling</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>05</Month><Day>21</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2019</Year><Month>08</Month><Day>01</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2019</Year><Month>8</Month><Day>7</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>8</Month><Day>6</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2019</Year><Month>8</Month><Day>7</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">31386759</ArticleId><ArticleId IdType="doi">10.1111/nph.16093</ArticleId></ArticleIdList><ReferenceList><Title>References</Title><Reference><Citation>Albrecht SC, Barata AG, Grosshans J, Teleman 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Nature Protocols 13: 2362-2386.</Citation></Reference></ReferenceList></PubmedData></pubmed><affiliations><list><country><li>Allemagne</li><li>Suède</li></country><region><li>District de Cologne</li><li>District de Münster</li><li>Rhénanie-du-Nord-Westphalie</li></region><settlement><li>Aix-la-Chapelle</li><li>Bonn</li><li>Cologne</li><li>Münster</li></settlement></list><tree><country name="Allemagne"><region name="Rhénanie-du-Nord-Westphalie"><name sortKey="Wagner, Stephan" sort="Wagner, Stephan" uniqKey="Wagner S" first="Stephan" last="Wagner">Stephan Wagner</name></region><name sortKey="Els Sser, Marlene" sort="Els Sser, Marlene" uniqKey="Els Sser M" first="Marlene" last="Els Sser">Marlene Els Sser</name><name sortKey="Els Sser, Marlene" sort="Els Sser, Marlene" uniqKey="Els Sser M" first="Marlene" last="Els Sser">Marlene Els Sser</name><name sortKey="Els Sser, Marlene" sort="Els Sser, Marlene" uniqKey="Els Sser M" first="Marlene" last="Els Sser">Marlene Els Sser</name><name sortKey="Fuchs, Philippe" sort="Fuchs, Philippe" uniqKey="Fuchs P" first="Philippe" last="Fuchs">Philippe Fuchs</name><name sortKey="Fuchs, Philippe" sort="Fuchs, Philippe" uniqKey="Fuchs P" first="Philippe" last="Fuchs">Philippe Fuchs</name><name sortKey="Lichtenauer, Sophie" sort="Lichtenauer, Sophie" uniqKey="Lichtenauer S" first="Sophie" last="Lichtenauer">Sophie Lichtenauer</name><name sortKey="Meyer, Andreas J" sort="Meyer, Andreas J" uniqKey="Meyer A" first="Andreas J" last="Meyer">Andreas J. Meyer</name><name sortKey="Nietzel, Thomas" sort="Nietzel, Thomas" uniqKey="Nietzel T" first="Thomas" last="Nietzel">Thomas Nietzel</name><name sortKey="Nietzel, Thomas" sort="Nietzel, Thomas" uniqKey="Nietzel T" first="Thomas" last="Nietzel">Thomas Nietzel</name><name sortKey="Ruberti, Cristina" sort="Ruberti, Cristina" uniqKey="Ruberti C" first="Cristina" last="Ruberti">Cristina Ruberti</name><name sortKey="Schippers, Jos H M" sort="Schippers, Jos H M" uniqKey="Schippers J" first="Jos H M" last="Schippers">Jos H M. Schippers</name><name sortKey="Schippers, Jos H M" sort="Schippers, Jos H M" uniqKey="Schippers J" first="Jos H M" last="Schippers">Jos H M. Schippers</name><name sortKey="Schmidt, Romy R" sort="Schmidt, Romy R" uniqKey="Schmidt R" first="Romy R" last="Schmidt">Romy R. Schmidt</name><name sortKey="Schwarzl Nder, Markus" sort="Schwarzl Nder, Markus" uniqKey="Schwarzl Nder M" first="Markus" last="Schwarzl Nder">Markus Schwarzl Nder</name><name sortKey="Steinbeck, Janina" sort="Steinbeck, Janina" uniqKey="Steinbeck J" first="Janina" last="Steinbeck">Janina Steinbeck</name><name sortKey="Van Dongen, Joost T" sort="Van Dongen, Joost T" uniqKey="Van Dongen J" first="Joost T" last="Van Dongen">Joost T. Van Dongen</name><name sortKey="Wagner, Stephan" sort="Wagner, Stephan" uniqKey="Wagner S" first="Stephan" last="Wagner">Stephan Wagner</name><name sortKey="Wagner, Stephan" sort="Wagner, Stephan" uniqKey="Wagner S" first="Stephan" last="Wagner">Stephan Wagner</name></country><country name="Suède"><noRegion><name sortKey="Van Aken, Olivier" sort="Van Aken, Olivier" uniqKey="Van Aken O" first="Olivier" last="Van Aken">Olivier Van Aken</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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