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Redox Modification of the Iron-Sulfur Glutaredoxin GRXS17 Activates Holdase Activity and Protects Plants from Heat Stress.

Identifieur interne : 000026 ( Main/Exploration ); précédent : 000025; suivant : 000027

Redox Modification of the Iron-Sulfur Glutaredoxin GRXS17 Activates Holdase Activity and Protects Plants from Heat Stress.

Auteurs : Laura Martins [France] ; Johannes Knuesting [Allemagne] ; Laetitia Bariat [France] ; Avilien Dard [France] ; Sven A. Freibert [Allemagne] ; Christophe H. Marchand [France] ; David Young [Belgique] ; Nguyen Ho Thuy Dung [Belgique] ; Wilhelm Voth [États-Unis] ; Anne Debures [France] ; Julio Saez-Vasquez [France] ; Stéphane D. Lemaire [France] ; Roland Lill [Allemagne] ; Joris Messens [Belgique] ; Renate Scheibe [Allemagne] ; Jean-Philippe Reichheld [France] ; Christophe Riondet [France]

Source :

RBID : pubmed:32826321

Abstract

Heat stress induces misfolding and aggregation of proteins unless they are guarded by chaperone systems. Here, we examined the function of the glutaredoxin GRXS17, a member of thiol reductase families in the model plant Arabidopsis (Arabidopsis thaliana). GRXS17 is a nucleocytosolic monothiol glutaredoxin consisting of an N-terminal thioredoxin domain and three CGFS active-site motif-containing GRX domains that coordinate three iron-sulfur (Fe-S) clusters in a glutathione-dependent manner. As an Fe-S cluster-charged holoenzyme, GRXS17 is likely involved in the maturation of cytosolic and nuclear Fe-S proteins. In addition to its role in cluster biogenesis, GRXS17 presented both foldase and redox-dependent holdase activities. Oxidative stress in combination with heat stress induced loss of its Fe-S clusters followed by subsequent formation of disulfide bonds between conserved active-site cysteines in the corresponding thioredoxin domains. This oxidation led to a shift of GRXS17 to a high-molecular-weight complex and thus activated its holdase activity in vitro. Moreover, GRXS17 was specifically involved in plant tolerance to moderate high temperature and protected root meristematic cells from heat-induced cell death. Finally, GRXS17 interacted with a different set of proteins upon heat stress, possibly protecting them from heat injuries. Therefore, we propose that the Fe-S cluster enzyme GRXS17 is an essential guard that protects proteins against moderate heat stress, likely through a redox-dependent chaperone activity. We reveal the mechanism of an Fe-S cluster-dependent activity shift that converts the holoenzyme GRXS17 into a holdase, thereby preventing damage caused by heat stress.

DOI: 10.1104/pp.20.00906
PubMed: 32826321
PubMed Central: PMC7536686


Affiliations:


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<name sortKey="Knuesting, Johannes" sort="Knuesting, Johannes" uniqKey="Knuesting J" first="Johannes" last="Knuesting">Johannes Knuesting</name>
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<country xml:lang="fr">Allemagne</country>
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<region type="land" nuts="2">Basse-Saxe</region>
<settlement type="city">Osnabrück</settlement>
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<author>
<name sortKey="Dard, Avilien" sort="Dard, Avilien" uniqKey="Dard A" first="Avilien" last="Dard">Avilien Dard</name>
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<author>
<name sortKey="Freibert, Sven A" sort="Freibert, Sven A" uniqKey="Freibert S" first="Sven A" last="Freibert">Sven A. Freibert</name>
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<nlm:affiliation>Institut für Zytobiologie und Zytopathologie, Philipps-Universität, Marburg 35032, Germany.</nlm:affiliation>
<country xml:lang="fr">Allemagne</country>
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<region type="land" nuts="1">Hesse (Land)</region>
<region type="district" nuts="2">District de Giessen</region>
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<name sortKey="Marchand, Christophe H" sort="Marchand, Christophe H" uniqKey="Marchand C" first="Christophe H" last="Marchand">Christophe H. Marchand</name>
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<nlm:affiliation>Institut de Biologie Physico-Chimique, Unité Mixte de Recherche 8226, Centre National de la Recherche Scientifique, Sorbonne Université, F-75005 Paris, France.</nlm:affiliation>
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<region type="region" nuts="2">Île-de-France</region>
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<author>
<name sortKey="Young, David" sort="Young, David" uniqKey="Young D" first="David" last="Young">David Young</name>
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<nlm:affiliation>VIB-VUB Center for Structural Biology, 1050 Brussels, Belgium.</nlm:affiliation>
<country xml:lang="fr">Belgique</country>
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<nlm:affiliation>Brussels Center for Redox Biology, 1050 Brussels, Belgium.</nlm:affiliation>
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<settlement type="city">Bruxelles</settlement>
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<nlm:affiliation>Structural Biology Brussels, Vrije Universiteit Brussel, 1050 Brussels, Belgium.</nlm:affiliation>
<country xml:lang="fr">Belgique</country>
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<settlement type="city">Bruxelles</settlement>
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<author>
<name sortKey="Dung, Nguyen Ho Thuy" sort="Dung, Nguyen Ho Thuy" uniqKey="Dung N" first="Nguyen Ho Thuy" last="Dung">Nguyen Ho Thuy Dung</name>
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<nlm:affiliation>VIB-VUB Center for Structural Biology, 1050 Brussels, Belgium.</nlm:affiliation>
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<nlm:affiliation>Brussels Center for Redox Biology, 1050 Brussels, Belgium.</nlm:affiliation>
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<settlement type="city">Bruxelles</settlement>
<region nuts="2">Région de Bruxelles-Capitale</region>
</placeName>
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<nlm:affiliation>Structural Biology Brussels, Vrije Universiteit Brussel, 1050 Brussels, Belgium.</nlm:affiliation>
<country xml:lang="fr">Belgique</country>
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<settlement type="city">Bruxelles</settlement>
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<name sortKey="Voth, Wilhelm" sort="Voth, Wilhelm" uniqKey="Voth W" first="Wilhelm" last="Voth">Wilhelm Voth</name>
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<nlm:affiliation>Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, Michigan 48109.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Michigan</region>
</placeName>
<wicri:cityArea>Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor</wicri:cityArea>
</affiliation>
</author>
<author>
<name sortKey="Debures, Anne" sort="Debures, Anne" uniqKey="Debures A" first="Anne" last="Debures">Anne Debures</name>
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<nlm:affiliation>Laboratoire Génome et Développement des Plantes, Université Perpignan Via Domitia, F-66860 Perpignan, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
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<author>
<name sortKey="Saez Vasquez, Julio" sort="Saez Vasquez, Julio" uniqKey="Saez Vasquez J" first="Julio" last="Saez-Vasquez">Julio Saez-Vasquez</name>
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<author>
<name sortKey="Lemaire, Stephane D" sort="Lemaire, Stephane D" uniqKey="Lemaire S" first="Stéphane D" last="Lemaire">Stéphane D. Lemaire</name>
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<nlm:affiliation>Institut de Biologie Physico-Chimique, Unité Mixte de Recherche 8226, Centre National de la Recherche Scientifique, Sorbonne Université, F-75005 Paris, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>Institut de Biologie Physico-Chimique, Unité Mixte de Recherche 8226, Centre National de la Recherche Scientifique, Sorbonne Université, F-75005 Paris</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Île-de-France</region>
<settlement type="city">Paris</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="3">
<nlm:affiliation>Institut de Biologie Paris-Seine, Laboratory of Computational and Quantitative Biology, Unité Mixte de Recherche 7238, Centre National de la Recherche Scientifique, Sorbonne Université, F-75005 Paris, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>Institut de Biologie Paris-Seine, Laboratory of Computational and Quantitative Biology, Unité Mixte de Recherche 7238, Centre National de la Recherche Scientifique, Sorbonne Université, F-75005 Paris</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Île-de-France</region>
<settlement type="city">Paris</settlement>
</placeName>
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<author>
<name sortKey="Lill, Roland" sort="Lill, Roland" uniqKey="Lill R" first="Roland" last="Lill">Roland Lill</name>
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<nlm:affiliation>Institut für Zytobiologie und Zytopathologie, Philipps-Universität, Marburg 35032, Germany.</nlm:affiliation>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Institut für Zytobiologie und Zytopathologie, Philipps-Universität, Marburg 35032</wicri:regionArea>
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<region type="land" nuts="1">Hesse (Land)</region>
<region type="district" nuts="2">District de Giessen</region>
<settlement type="city">Marbourg</settlement>
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<author>
<name sortKey="Messens, Joris" sort="Messens, Joris" uniqKey="Messens J" first="Joris" last="Messens">Joris Messens</name>
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<nlm:affiliation>VIB-VUB Center for Structural Biology, 1050 Brussels, Belgium.</nlm:affiliation>
<country xml:lang="fr">Belgique</country>
<wicri:regionArea>VIB-VUB Center for Structural Biology, 1050 Brussels</wicri:regionArea>
<placeName>
<settlement type="city">Bruxelles</settlement>
<region nuts="2">Région de Bruxelles-Capitale</region>
</placeName>
</affiliation>
<affiliation wicri:level="1">
<nlm:affiliation>Brussels Center for Redox Biology, 1050 Brussels, Belgium.</nlm:affiliation>
<country xml:lang="fr">Belgique</country>
<wicri:regionArea>Brussels Center for Redox Biology, 1050 Brussels</wicri:regionArea>
<placeName>
<settlement type="city">Bruxelles</settlement>
<region nuts="2">Région de Bruxelles-Capitale</region>
</placeName>
</affiliation>
<affiliation wicri:level="1">
<nlm:affiliation>Structural Biology Brussels, Vrije Universiteit Brussel, 1050 Brussels, Belgium.</nlm:affiliation>
<country xml:lang="fr">Belgique</country>
<wicri:regionArea>Structural Biology Brussels, Vrije Universiteit Brussel, 1050 Brussels</wicri:regionArea>
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<settlement type="city">Bruxelles</settlement>
<region nuts="2">Région de Bruxelles-Capitale</region>
</placeName>
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<author>
<name sortKey="Scheibe, Renate" sort="Scheibe, Renate" uniqKey="Scheibe R" first="Renate" last="Scheibe">Renate Scheibe</name>
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<nlm:affiliation>Institut für Zytobiologie und Zytopathologie, Philipps-Universität, Marburg 35032, Germany.</nlm:affiliation>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Institut für Zytobiologie und Zytopathologie, Philipps-Universität, Marburg 35032</wicri:regionArea>
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<region type="land" nuts="1">Hesse (Land)</region>
<region type="district" nuts="2">District de Giessen</region>
<settlement type="city">Marbourg</settlement>
</placeName>
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</author>
<author>
<name sortKey="Reichheld, Jean Philippe" sort="Reichheld, Jean Philippe" uniqKey="Reichheld J" first="Jean-Philippe" last="Reichheld">Jean-Philippe Reichheld</name>
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<nlm:affiliation>Laboratoire Génome et Développement des Plantes, Université Perpignan Via Domitia, F-66860 Perpignan, France jpr@univ-perp.fr.</nlm:affiliation>
<country wicri:rule="url">France</country>
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<region type="region" nuts="2">Occitanie (région administrative)</region>
<region type="old region" nuts="2">Languedoc-Roussillon</region>
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</placeName>
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<author>
<name sortKey="Riondet, Christophe" sort="Riondet, Christophe" uniqKey="Riondet C" first="Christophe" last="Riondet">Christophe Riondet</name>
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<nlm:affiliation>Laboratoire Génome et Développement des Plantes, Université Perpignan Via Domitia, F-66860 Perpignan, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>Laboratoire Génome et Développement des Plantes, Université Perpignan Via Domitia, F-66860 Perpignan</wicri:regionArea>
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<region type="region" nuts="2">Occitanie (région administrative)</region>
<region type="old region" nuts="2">Languedoc-Roussillon</region>
<settlement type="city">Perpignan</settlement>
</placeName>
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<nlm:affiliation>Laboratoire Génome et Développement des Plantes, Centre National de la Recherche Scientifique, F-66860 Perpignan, France.</nlm:affiliation>
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<series>
<title level="j">Plant physiology</title>
<idno type="eISSN">1532-2548</idno>
<imprint>
<date when="2020" type="published">2020</date>
</imprint>
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<front>
<div type="abstract" xml:lang="en">Heat stress induces misfolding and aggregation of proteins unless they are guarded by chaperone systems. Here, we examined the function of the glutaredoxin GRXS17, a member of thiol reductase families in the model plant Arabidopsis (
<i>Arabidopsis thaliana</i>
). GRXS17 is a nucleocytosolic monothiol glutaredoxin consisting of an N-terminal thioredoxin domain and three CGFS active-site motif-containing GRX domains that coordinate three iron-sulfur (Fe-S) clusters in a glutathione-dependent manner. As an Fe-S cluster-charged holoenzyme, GRXS17 is likely involved in the maturation of cytosolic and nuclear Fe-S proteins. In addition to its role in cluster biogenesis, GRXS17 presented both foldase and redox-dependent holdase activities. Oxidative stress in combination with heat stress induced loss of its Fe-S clusters followed by subsequent formation of disulfide bonds between conserved active-site cysteines in the corresponding thioredoxin domains. This oxidation led to a shift of GRXS17 to a high-molecular-weight complex and thus activated its holdase activity in vitro. Moreover, GRXS17 was specifically involved in plant tolerance to moderate high temperature and protected root meristematic cells from heat-induced cell death. Finally, GRXS17 interacted with a different set of proteins upon heat stress, possibly protecting them from heat injuries. Therefore, we propose that the Fe-S cluster enzyme GRXS17 is an essential guard that protects proteins against moderate heat stress, likely through a redox-dependent chaperone activity. We reveal the mechanism of an Fe-S cluster-dependent activity shift that converts the holoenzyme GRXS17 into a holdase, thereby preventing damage caused by heat stress.</div>
</front>
</TEI>
<pubmed>
<MedlineCitation Status="In-Process" Owner="NLM">
<PMID Version="1">32826321</PMID>
<DateRevised>
<Year>2020</Year>
<Month>10</Month>
<Day>16</Day>
</DateRevised>
<Article PubModel="Print-Electronic">
<Journal>
<ISSN IssnType="Electronic">1532-2548</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>184</Volume>
<Issue>2</Issue>
<PubDate>
<Year>2020</Year>
<Month>10</Month>
</PubDate>
</JournalIssue>
<Title>Plant physiology</Title>
<ISOAbbreviation>Plant Physiol</ISOAbbreviation>
</Journal>
<ArticleTitle>Redox Modification of the Iron-Sulfur Glutaredoxin GRXS17 Activates Holdase Activity and Protects Plants from Heat Stress.</ArticleTitle>
<Pagination>
<MedlinePgn>676-692</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1104/pp.20.00906</ELocationID>
<Abstract>
<AbstractText>Heat stress induces misfolding and aggregation of proteins unless they are guarded by chaperone systems. Here, we examined the function of the glutaredoxin GRXS17, a member of thiol reductase families in the model plant Arabidopsis (
<i>Arabidopsis thaliana</i>
). GRXS17 is a nucleocytosolic monothiol glutaredoxin consisting of an N-terminal thioredoxin domain and three CGFS active-site motif-containing GRX domains that coordinate three iron-sulfur (Fe-S) clusters in a glutathione-dependent manner. As an Fe-S cluster-charged holoenzyme, GRXS17 is likely involved in the maturation of cytosolic and nuclear Fe-S proteins. In addition to its role in cluster biogenesis, GRXS17 presented both foldase and redox-dependent holdase activities. Oxidative stress in combination with heat stress induced loss of its Fe-S clusters followed by subsequent formation of disulfide bonds between conserved active-site cysteines in the corresponding thioredoxin domains. This oxidation led to a shift of GRXS17 to a high-molecular-weight complex and thus activated its holdase activity in vitro. Moreover, GRXS17 was specifically involved in plant tolerance to moderate high temperature and protected root meristematic cells from heat-induced cell death. Finally, GRXS17 interacted with a different set of proteins upon heat stress, possibly protecting them from heat injuries. Therefore, we propose that the Fe-S cluster enzyme GRXS17 is an essential guard that protects proteins against moderate heat stress, likely through a redox-dependent chaperone activity. We reveal the mechanism of an Fe-S cluster-dependent activity shift that converts the holoenzyme GRXS17 into a holdase, thereby preventing damage caused by heat stress.</AbstractText>
<CopyrightInformation>© 2020 American Society of Plant Biologists. All Rights Reserved.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Martins</LastName>
<ForeName>Laura</ForeName>
<Initials>L</Initials>
<AffiliationInfo>
<Affiliation>Laboratoire Génome et Développement des Plantes, Université Perpignan Via Domitia, F-66860 Perpignan, France.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Laboratoire Génome et Développement des Plantes, Centre National de la Recherche Scientifique, F-66860 Perpignan, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Knuesting</LastName>
<ForeName>Johannes</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Physiology, FB5, University of Osnabrück, D-49069 Osnabrueck, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Bariat</LastName>
<ForeName>Laetitia</ForeName>
<Initials>L</Initials>
<AffiliationInfo>
<Affiliation>Laboratoire Génome et Développement des Plantes, Université Perpignan Via Domitia, F-66860 Perpignan, France.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Laboratoire Génome et Développement des Plantes, Centre National de la Recherche Scientifique, F-66860 Perpignan, France.</Affiliation>
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<name sortKey="Scheibe, Renate" sort="Scheibe, Renate" uniqKey="Scheibe R" first="Renate" last="Scheibe">Renate Scheibe</name>
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<name sortKey="Young, David" sort="Young, David" uniqKey="Young D" first="David" last="Young">David Young</name>
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<name sortKey="Dung, Nguyen Ho Thuy" sort="Dung, Nguyen Ho Thuy" uniqKey="Dung N" first="Nguyen Ho Thuy" last="Dung">Nguyen Ho Thuy Dung</name>
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<name sortKey="Messens, Joris" sort="Messens, Joris" uniqKey="Messens J" first="Joris" last="Messens">Joris Messens</name>
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<name sortKey="Young, David" sort="Young, David" uniqKey="Young D" first="David" last="Young">David Young</name>
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<name sortKey="Voth, Wilhelm" sort="Voth, Wilhelm" uniqKey="Voth W" first="Wilhelm" last="Voth">Wilhelm Voth</name>
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</record>

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