A substrate of the ABC transporter PEN3 stimulates bacterial flagellin (flg22)-induced callose deposition in Arabidopsis thaliana.
Identifieur interne : 000591 ( Main/Exploration ); précédent : 000590; suivant : 000592A substrate of the ABC transporter PEN3 stimulates bacterial flagellin (flg22)-induced callose deposition in Arabidopsis thaliana.
Auteurs : Andreas Matern ; Christoph Böttcher ; Lennart Eschen-Lippold ; Bernhard Westermann ; Ulrike Smolka ; Stefanie Döll ; Fabian Trempel ; Bibek Aryal [Suisse] ; Dierk Scheel ; Markus Geisler [Suisse] ; Sabine Rosahl [Allemagne]Source :
- The Journal of biological chemistry [ 1083-351X ] ; 2019.
Descripteurs français
- KwdFr :
- Arabidopsis (microbiologie), Arabidopsis (métabolisme), Calcium (métabolisme), Cytosol (métabolisme), Feuilles de plante (métabolisme), Flagelline (métabolisme), Glucanes (métabolisme), Indoles (métabolisme), Phytophthora infestans (isolement et purification), Spécificité du substrat (MeSH), Transporteurs ABC (métabolisme).
- MESH :
- isolement et purification : Phytophthora infestans.
- microbiologie : Arabidopsis.
- métabolisme : Arabidopsis, Calcium, Cytosol, Feuilles de plante, Flagelline, Glucanes, Indoles, Transporteurs ABC.
- Spécificité du substrat.
English descriptors
- KwdEn :
- ATP-Binding Cassette Transporters (metabolism), Arabidopsis (metabolism), Arabidopsis (microbiology), Calcium (metabolism), Cytosol (metabolism), Flagellin (metabolism), Glucans (metabolism), Indoles (metabolism), Phytophthora infestans (isolation & purification), Plant Leaves (metabolism), Substrate Specificity (MeSH).
- MESH :
- chemical , metabolism : ATP-Binding Cassette Transporters, Calcium, Flagellin, Glucans, Indoles.
- isolation & purification : Phytophthora infestans.
- metabolism : Arabidopsis, Cytosol, Plant Leaves.
- microbiology : Arabidopsis.
- Substrate Specificity.
Abstract
Nonhost resistance of Arabidopsis thaliana against Phytophthora infestans, a filamentous eukaryotic microbe and the causal agent of potato late blight, is based on a multilayered defense system. Arabidopsis thaliana controls pathogen entry through the penetration-resistance genes PEN2 and PEN3, encoding an atypical myrosinase and an ABC transporter, respectively, required for synthesis and export of unknown indole compounds. To identify pathogen-elicited leaf surface metabolites and further unravel nonhost resistance in Arabidopsis, we performed untargeted metabolite profiling by incubating a P. infestans zoospore suspension on leaves of WT or pen3 mutant Arabidopsis plants. Among the plant-secreted metabolites, 4-methoxyindol-3-yl-methanol and S-(4-methoxy-indol-3-yl-methyl) cysteine were detected in spore suspensions recollected from WT plants, but at reduced levels from the pen3 mutant plants. In both whole-cell and microsome-based assays, 4-methoxyindol-3-yl-methanol was transported in a PEN3-dependent manner, suggesting that this compound is a PEN3 substrate. The syntheses of both compounds were dependent on functional PEN2 and phytochelatin synthase 1. None of these compounds inhibited mycelial growth of P. infestans in vitro Of note, exogenous application of 4-methoxyindol-3-yl methanol slightly elevated cytosolic Ca2+ levels and enhanced callose deposition in hydathodes of seedlings treated with a bacterial pathogen-associated molecular pattern (PAMP), flagellin (flg22). Loss of flg22-induced callose deposition in leaves of pen3 seedlings was partially reverted by the addition of 4-methoxyindol-3-yl methanol. In conclusion, we have identified a specific indole compound that is a substrate for PEN3 and contributes to the plant defense response against microbial pathogens.
DOI: 10.1074/jbc.RA119.007676
PubMed: 30833326
PubMed Central: PMC6497936
Affiliations:
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sortKey="Eschen Lippold, Lennart" sort="Eschen Lippold, Lennart" uniqKey="Eschen Lippold L" first="Lennart" last="Eschen-Lippold">Lennart Eschen-Lippold</name><affiliation><nlm:affiliation>From the Department of Stress and Developmental Biology and.</nlm:affiliation><wicri:noCountry code="no comma">From the Department of Stress and Developmental Biology and.</wicri:noCountry></affiliation></author><author><name sortKey="Westermann, Bernhard" sort="Westermann, Bernhard" uniqKey="Westermann B" first="Bernhard" last="Westermann">Bernhard Westermann</name><affiliation><nlm:affiliation>Department of Bioorganic Chemistry, Leibniz Institute of Plant Biochemistry, Weinberg 3, D-06120 Halle (Saale), Germany and.</nlm:affiliation><wicri:noCountry code="subField">Germany and</wicri:noCountry></affiliation></author><author><name sortKey="Smolka, Ulrike" sort="Smolka, Ulrike" uniqKey="Smolka U" first="Ulrike" last="Smolka">Ulrike Smolka</name><affiliation><nlm:affiliation>From the Department of 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Matern</name><affiliation><nlm:affiliation>From the Department of Stress and Developmental Biology and.</nlm:affiliation><wicri:noCountry code="no comma">From the Department of Stress and Developmental Biology and.</wicri:noCountry></affiliation></author><author><name sortKey="Bottcher, Christoph" sort="Bottcher, Christoph" uniqKey="Bottcher C" first="Christoph" last="Böttcher">Christoph Böttcher</name><affiliation><nlm:affiliation>From the Department of Stress and Developmental Biology and.</nlm:affiliation><wicri:noCountry code="no comma">From the Department of Stress and Developmental Biology and.</wicri:noCountry></affiliation></author><author><name sortKey="Eschen Lippold, Lennart" sort="Eschen Lippold, Lennart" uniqKey="Eschen Lippold L" first="Lennart" last="Eschen-Lippold">Lennart Eschen-Lippold</name><affiliation><nlm:affiliation>From the Department of Stress and Developmental Biology and.</nlm:affiliation><wicri:noCountry code="no comma">From the Department of Stress and Developmental Biology and.</wicri:noCountry></affiliation></author><author><name sortKey="Westermann, Bernhard" sort="Westermann, Bernhard" uniqKey="Westermann B" first="Bernhard" last="Westermann">Bernhard Westermann</name><affiliation><nlm:affiliation>Department of Bioorganic Chemistry, Leibniz Institute of Plant Biochemistry, Weinberg 3, D-06120 Halle (Saale), Germany and.</nlm:affiliation><wicri:noCountry code="subField">Germany and</wicri:noCountry></affiliation></author><author><name sortKey="Smolka, Ulrike" sort="Smolka, Ulrike" uniqKey="Smolka U" first="Ulrike" last="Smolka">Ulrike Smolka</name><affiliation><nlm:affiliation>From the Department of Stress and Developmental Biology and.</nlm:affiliation><wicri:noCountry code="no comma">From the Department of Stress and Developmental Biology and.</wicri:noCountry></affiliation></author><author><name sortKey="Doll, Stefanie" sort="Doll, Stefanie" uniqKey="Doll S" first="Stefanie" last="Döll">Stefanie Döll</name><affiliation><nlm:affiliation>From the Department of Stress and Developmental Biology and.</nlm:affiliation><wicri:noCountry code="no comma">From the Department of Stress and Developmental Biology and.</wicri:noCountry></affiliation></author><author><name sortKey="Trempel, Fabian" sort="Trempel, Fabian" uniqKey="Trempel F" first="Fabian" last="Trempel">Fabian Trempel</name><affiliation><nlm:affiliation>From the Department of Stress and Developmental Biology and.</nlm:affiliation><wicri:noCountry code="no comma">From the Department of Stress and Developmental Biology and.</wicri:noCountry></affiliation></author><author><name sortKey="Aryal, Bibek" sort="Aryal, Bibek" uniqKey="Aryal B" first="Bibek" last="Aryal">Bibek Aryal</name><affiliation wicri:level="4"><nlm:affiliation>the Department of Biology, University of Fribourg, Chemin du Musée 10, CH-1700 Fribourg, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>the Department of Biology, University of Fribourg, Chemin du Musée 10, CH-1700 Fribourg</wicri:regionArea><orgName type="university">Université de Fribourg</orgName><placeName><settlement type="city">Fribourg</settlement><region nuts="3" type="region">Canton de Fribourg</region></placeName></affiliation></author><author><name sortKey="Scheel, Dierk" sort="Scheel, Dierk" uniqKey="Scheel D" first="Dierk" last="Scheel">Dierk Scheel</name><affiliation><nlm:affiliation>From the Department of Stress and Developmental Biology and.</nlm:affiliation><wicri:noCountry code="no comma">From the Department of Stress and Developmental Biology and.</wicri:noCountry></affiliation></author><author><name sortKey="Geisler, Markus" sort="Geisler, Markus" uniqKey="Geisler M" first="Markus" last="Geisler">Markus Geisler</name><affiliation wicri:level="4"><nlm:affiliation>the Department of Biology, University of Fribourg, Chemin du Musée 10, CH-1700 Fribourg, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>the Department of Biology, University of Fribourg, Chemin du Musée 10, CH-1700 Fribourg</wicri:regionArea><orgName type="university">Université de Fribourg</orgName><placeName><settlement type="city">Fribourg</settlement><region nuts="3" type="region">Canton de Fribourg</region></placeName></affiliation></author><author><name sortKey="Rosahl, Sabine" sort="Rosahl, Sabine" uniqKey="Rosahl S" first="Sabine" last="Rosahl">Sabine Rosahl</name><affiliation wicri:level="1"><nlm:affiliation>From the Department of Stress and Developmental Biology and srosahl@ipb-halle.de.</nlm:affiliation><country wicri:rule="url">Allemagne</country></affiliation></author></analytic><series><title level="j">The Journal of biological chemistry</title><idno type="eISSN">1083-351X</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>ATP-Binding Cassette Transporters (metabolism)</term><term>Arabidopsis (metabolism)</term><term>Arabidopsis (microbiology)</term><term>Calcium (metabolism)</term><term>Cytosol (metabolism)</term><term>Flagellin (metabolism)</term><term>Glucans (metabolism)</term><term>Indoles (metabolism)</term><term>Phytophthora infestans (isolation & purification)</term><term>Plant Leaves (metabolism)</term><term>Substrate Specificity (MeSH)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Arabidopsis (microbiologie)</term><term>Arabidopsis (métabolisme)</term><term>Calcium (métabolisme)</term><term>Cytosol (métabolisme)</term><term>Feuilles de plante (métabolisme)</term><term>Flagelline (métabolisme)</term><term>Glucanes (métabolisme)</term><term>Indoles (métabolisme)</term><term>Phytophthora infestans (isolement et purification)</term><term>Spécificité du substrat (MeSH)</term><term>Transporteurs ABC (métabolisme)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>ATP-Binding Cassette Transporters</term><term>Calcium</term><term>Flagellin</term><term>Glucans</term><term>Indoles</term></keywords><keywords scheme="MESH" qualifier="isolation & purification" xml:lang="en"><term>Phytophthora infestans</term></keywords><keywords scheme="MESH" qualifier="isolement et purification" xml:lang="fr"><term>Phytophthora infestans</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Arabidopsis</term><term>Cytosol</term><term>Plant Leaves</term></keywords><keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr"><term>Arabidopsis</term></keywords><keywords scheme="MESH" qualifier="microbiology" xml:lang="en"><term>Arabidopsis</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Arabidopsis</term><term>Calcium</term><term>Cytosol</term><term>Feuilles de plante</term><term>Flagelline</term><term>Glucanes</term><term>Indoles</term><term>Transporteurs ABC</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Substrate Specificity</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Spécificité du substrat</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Nonhost resistance of <i>Arabidopsis thaliana</i> against <i>Phytophthora infestans</i>, a filamentous eukaryotic microbe and the causal agent of potato late blight, is based on a multilayered defense system. <i>Arabidopsis thaliana</i> controls pathogen entry through the penetration-resistance genes <i>PEN2</i> and <i>PEN3</i>, encoding an atypical myrosinase and an ABC transporter, respectively, required for synthesis and export of unknown indole compounds. To identify pathogen-elicited leaf surface metabolites and further unravel nonhost resistance in <i>Arabidopsis</i>, we performed untargeted metabolite profiling by incubating a <i>P. infestans</i> zoospore suspension on leaves of WT or <i>pen3</i> mutant <i>Arabidopsis</i> plants. Among the plant-secreted metabolites, 4-methoxyindol-3-yl-methanol and <i>S</i>-(4-methoxy-indol-3-yl-methyl) cysteine were detected in spore suspensions recollected from WT plants, but at reduced levels from the <i>pen3</i> mutant plants. In both whole-cell and microsome-based assays, 4-methoxyindol-3-yl-methanol was transported in a PEN3-dependent manner, suggesting that this compound is a PEN3 substrate. The syntheses of both compounds were dependent on functional PEN2 and phytochelatin synthase 1. None of these compounds inhibited mycelial growth of <i>P. infestans in vitro</i> Of note, exogenous application of 4-methoxyindol-3-yl methanol slightly elevated cytosolic Ca<sup>2+</sup> levels and enhanced callose deposition in hydathodes of seedlings treated with a bacterial pathogen-associated molecular pattern (PAMP), flagellin (flg22). Loss of flg22-induced callose deposition in leaves of <i>pen3</i> seedlings was partially reverted by the addition of 4-methoxyindol-3-yl methanol. In conclusion, we have identified a specific indole compound that is a substrate for PEN3 and contributes to the plant defense response against microbial pathogens.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">30833326</PMID><DateCompleted><Year>2020</Year><Month>01</Month><Day>07</Day></DateCompleted><DateRevised><Year>2020</Year><Month>04</Month><Day>26</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1083-351X</ISSN><JournalIssue CitedMedium="Internet"><Volume>294</Volume><Issue>17</Issue><PubDate><Year>2019</Year><Month>04</Month><Day>26</Day></PubDate></JournalIssue><Title>The Journal of biological chemistry</Title><ISOAbbreviation>J Biol Chem</ISOAbbreviation></Journal><ArticleTitle>A substrate of the ABC transporter PEN3 stimulates bacterial flagellin (flg22)-induced callose deposition in <i>Arabidopsis thaliana</i>.</ArticleTitle><Pagination><MedlinePgn>6857-6870</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1074/jbc.RA119.007676</ELocationID><Abstract><AbstractText>Nonhost resistance of <i>Arabidopsis thaliana</i> against <i>Phytophthora infestans</i>, a filamentous eukaryotic microbe and the causal agent of potato late blight, is based on a multilayered defense system. <i>Arabidopsis thaliana</i> controls pathogen entry through the penetration-resistance genes <i>PEN2</i> and <i>PEN3</i>, encoding an atypical myrosinase and an ABC transporter, respectively, required for synthesis and export of unknown indole compounds. To identify pathogen-elicited leaf surface metabolites and further unravel nonhost resistance in <i>Arabidopsis</i>, we performed untargeted metabolite profiling by incubating a <i>P. infestans</i> zoospore suspension on leaves of WT or <i>pen3</i> mutant <i>Arabidopsis</i> plants. Among the plant-secreted metabolites, 4-methoxyindol-3-yl-methanol and <i>S</i>-(4-methoxy-indol-3-yl-methyl) cysteine were detected in spore suspensions recollected from WT plants, but at reduced levels from the <i>pen3</i> mutant plants. In both whole-cell and microsome-based assays, 4-methoxyindol-3-yl-methanol was transported in a PEN3-dependent manner, suggesting that this compound is a PEN3 substrate. The syntheses of both compounds were dependent on functional PEN2 and phytochelatin synthase 1. None of these compounds inhibited mycelial growth of <i>P. infestans in vitro</i> Of note, exogenous application of 4-methoxyindol-3-yl methanol slightly elevated cytosolic Ca<sup>2+</sup> levels and enhanced callose deposition in hydathodes of seedlings treated with a bacterial pathogen-associated molecular pattern (PAMP), flagellin (flg22). Loss of flg22-induced callose deposition in leaves of <i>pen3</i> seedlings was partially reverted by the addition of 4-methoxyindol-3-yl methanol. In conclusion, we have identified a specific indole compound that is a substrate for PEN3 and contributes to the plant defense response against microbial pathogens.</AbstractText><CopyrightInformation>© 2019 Matern et al.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Matern</LastName><ForeName>Andreas</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>From the Department of Stress and Developmental Biology and.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Böttcher</LastName><ForeName>Christoph</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>From the Department of Stress and Developmental Biology and.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Eschen-Lippold</LastName><ForeName>Lennart</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>From the Department of Stress and Developmental Biology and.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Westermann</LastName><ForeName>Bernhard</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>Department of Bioorganic Chemistry, Leibniz Institute of Plant Biochemistry, Weinberg 3, D-06120 Halle (Saale), Germany and.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Smolka</LastName><ForeName>Ulrike</ForeName><Initials>U</Initials><AffiliationInfo><Affiliation>From the Department of Stress and Developmental Biology and.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Döll</LastName><ForeName>Stefanie</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>From the Department of Stress and Developmental Biology and.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Trempel</LastName><ForeName>Fabian</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>From the Department of Stress and Developmental Biology and.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Aryal</LastName><ForeName>Bibek</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>the Department of Biology, University of Fribourg, Chemin du Musée 10, CH-1700 Fribourg, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Scheel</LastName><ForeName>Dierk</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>From the Department of Stress and Developmental Biology and.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Geisler</LastName><ForeName>Markus</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>the Department of Biology, University of Fribourg, Chemin du Musée 10, CH-1700 Fribourg, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Rosahl</LastName><ForeName>Sabine</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>From the Department of Stress and Developmental Biology and srosahl@ipb-halle.de.</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>03</Month><Day>04</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>J Biol Chem</MedlineTA><NlmUniqueID>2985121R</NlmUniqueID><ISSNLinking>0021-9258</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D018528">ATP-Binding Cassette Transporters</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D005936">Glucans</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D007211">Indoles</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="C510424">PDR8 protein, Arabidopsis</NameOfSubstance></Chemical><Chemical><RegistryNumber>12777-81-0</RegistryNumber><NameOfSubstance UI="D005408">Flagellin</NameOfSubstance></Chemical><Chemical><RegistryNumber>9064-51-1</RegistryNumber><NameOfSubstance UI="C048306">callose</NameOfSubstance></Chemical><Chemical><RegistryNumber>SY7Q814VUP</RegistryNumber><NameOfSubstance UI="D002118">Calcium</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D018528" MajorTopicYN="N">ATP-Binding Cassette Transporters</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D017360" MajorTopicYN="N">Arabidopsis</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName><QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D002118" MajorTopicYN="N">Calcium</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D003600" MajorTopicYN="N">Cytosol</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D005408" MajorTopicYN="N">Flagellin</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D005936" MajorTopicYN="N">Glucans</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D007211" MajorTopicYN="N">Indoles</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D055750" MajorTopicYN="N">Phytophthora infestans</DescriptorName><QualifierName UI="Q000302" MajorTopicYN="N">isolation & 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uniqKey="Aryal B" first="Bibek" last="Aryal">Bibek Aryal</name></region><name sortKey="Geisler, Markus" sort="Geisler, Markus" uniqKey="Geisler M" first="Markus" last="Geisler">Markus Geisler</name></country><country name="Allemagne"><noRegion><name sortKey="Rosahl, Sabine" sort="Rosahl, Sabine" uniqKey="Rosahl S" first="Sabine" last="Rosahl">Sabine Rosahl</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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