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Thermospermine levels are controlled by an auxin-dependent feedback loop mechanism in Populus xylem.

Identifieur interne : 002448 ( Main/Exploration ); précédent : 002447; suivant : 002449

Thermospermine levels are controlled by an auxin-dependent feedback loop mechanism in Populus xylem.

Auteurs : Ana Milhinhos [Portugal] ; Jakob Prestele ; Benjamin Bollhöner ; Andreia Matos ; Francisco Vera-Sirera ; José L. Rambla ; Karin Ljung ; Juan Carbonell ; Miguel A. Blázquez ; Hannele Tuominen ; Célia M. Miguel

Source :

RBID : pubmed:23647338

Descripteurs français

English descriptors

Abstract

Polyamines are small polycationic amines that are widespread in living organisms. Thermospermine, synthesized by thermospermine synthase ACAULIS5 (ACL5), was recently shown to be an endogenous plant polyamine. Thermospermine is critical for proper vascular development and xylem cell specification, but it is not known how thermospermine homeostasis is controlled in the xylem. We present data in the Populus model system supporting the existence of a negative feedback control of thermospermine levels in stem xylem tissues, the main site of thermospermine biosynthesis. While over-expression of the ACL5 homologue in Populus, POPACAULIS5, resulted in strong up-regulation of ACL5 expression and thermospermine accumulation in leaves, the corresponding levels in the secondary xylem tissues of the stem were similar or lower than those in the wild-type. POPACAULIS5 over-expression had a negative effect on accumulation of indole-3-acetic acid, while exogenous auxin had a positive effect on POPACAULIS5 expression, thus promoting thermospermine accumulation. Further, over-expression of POPACAULIS5 negatively affected expression of the class III homeodomain leucine zipper (HD-Zip III) transcription factor gene PttHB8, a homologue of AtHB8, while up-regulation of PttHB8 positively affected POPACAULIS5 expression. These results indicate that excessive accumulation of thermospermine is prevented by a negative feedback control of POPACAULIS5 transcript levels through suppression of indole-3-acetic acid levels, and that PttHB8 is involved in the control of POPACAULIS5 expression. We propose that this negative feedback loop functions to maintain steady-state levels of thermospermine, which is required for proper xylem development, and that it is dependent on the presence of high concentrations of endogenous indole-3-acetic acid, such as those present in the secondary xylem tissues.

DOI: 10.1111/tpj.12231
PubMed: 23647338


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<term>Amino Acid Sequence (MeSH)</term>
<term>Arabidopsis Proteins (genetics)</term>
<term>Base Sequence (MeSH)</term>
<term>Gene Expression Regulation, Plant (MeSH)</term>
<term>Indoleacetic Acids (analysis)</term>
<term>Indoleacetic Acids (metabolism)</term>
<term>Indoleacetic Acids (pharmacology)</term>
<term>Leucine Zippers (genetics)</term>
<term>Models, Biological (MeSH)</term>
<term>Molecular Sequence Data (MeSH)</term>
<term>Phylogeny (MeSH)</term>
<term>Plant Growth Regulators (analysis)</term>
<term>Plant Growth Regulators (metabolism)</term>
<term>Plant Growth Regulators (pharmacology)</term>
<term>Plant Leaves (cytology)</term>
<term>Plant Leaves (genetics)</term>
<term>Plant Leaves (growth & development)</term>
<term>Plant Leaves (metabolism)</term>
<term>Plant Proteins (genetics)</term>
<term>Plant Proteins (metabolism)</term>
<term>Plant Stems (cytology)</term>
<term>Plant Stems (genetics)</term>
<term>Plant Stems (growth & development)</term>
<term>Plant Stems (metabolism)</term>
<term>Plants, Genetically Modified (MeSH)</term>
<term>Populus (cytology)</term>
<term>Populus (genetics)</term>
<term>Populus (growth & development)</term>
<term>Populus (metabolism)</term>
<term>Sequence Analysis, DNA (MeSH)</term>
<term>Spermine (analogs & derivatives)</term>
<term>Spermine (metabolism)</term>
<term>Trees (MeSH)</term>
<term>Up-Regulation (MeSH)</term>
<term>Wood (cytology)</term>
<term>Wood (genetics)</term>
<term>Wood (growth & development)</term>
<term>Wood (metabolism)</term>
<term>Xylem (cytology)</term>
<term>Xylem (genetics)</term>
<term>Xylem (growth & development)</term>
<term>Xylem (metabolism)</term>
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<term>Acides indolacétiques (métabolisme)</term>
<term>Acides indolacétiques (pharmacologie)</term>
<term>Analyse de séquence d'ADN (MeSH)</term>
<term>Arbres (MeSH)</term>
<term>Bois (croissance et développement)</term>
<term>Bois (cytologie)</term>
<term>Bois (génétique)</term>
<term>Bois (métabolisme)</term>
<term>Données de séquences moléculaires (MeSH)</term>
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<term>Facteur de croissance végétal (métabolisme)</term>
<term>Facteur de croissance végétal (pharmacologie)</term>
<term>Feuilles de plante (croissance et développement)</term>
<term>Feuilles de plante (cytologie)</term>
<term>Feuilles de plante (génétique)</term>
<term>Feuilles de plante (métabolisme)</term>
<term>Glissières à leucine (génétique)</term>
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<term>Phylogenèse (MeSH)</term>
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<term>Populus (cytologie)</term>
<term>Populus (génétique)</term>
<term>Populus (métabolisme)</term>
<term>Protéines d'Arabidopsis (génétique)</term>
<term>Protéines végétales (génétique)</term>
<term>Protéines végétales (métabolisme)</term>
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<term>Régulation positive (MeSH)</term>
<term>Spermine (analogues et dérivés)</term>
<term>Spermine (métabolisme)</term>
<term>Séquence d'acides aminés (MeSH)</term>
<term>Séquence nucléotidique (MeSH)</term>
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<term>Tiges de plante (cytologie)</term>
<term>Tiges de plante (génétique)</term>
<term>Tiges de plante (métabolisme)</term>
<term>Végétaux génétiquement modifiés (MeSH)</term>
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<term>Xylème (cytologie)</term>
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<term>Indoleacetic Acids</term>
<term>Plant Growth Regulators</term>
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<term>Arabidopsis Proteins</term>
<term>Plant Proteins</term>
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<term>Indoleacetic Acids</term>
<term>Plant Growth Regulators</term>
<term>Plant Proteins</term>
<term>Spermine</term>
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<keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en">
<term>Indoleacetic Acids</term>
<term>Plant Growth Regulators</term>
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<keywords scheme="MESH" qualifier="analogues et dérivés" xml:lang="fr">
<term>Spermine</term>
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<keywords scheme="MESH" qualifier="analyse" xml:lang="fr">
<term>Acides indolacétiques</term>
<term>Facteur de croissance végétal</term>
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<keywords scheme="MESH" qualifier="croissance et développement" xml:lang="fr">
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<term>Feuilles de plante</term>
<term>Populus</term>
<term>Tiges de plante</term>
<term>Xylème</term>
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<keywords scheme="MESH" qualifier="cytologie" xml:lang="fr">
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<term>Feuilles de plante</term>
<term>Populus</term>
<term>Tiges de plante</term>
<term>Xylème</term>
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<keywords scheme="MESH" qualifier="cytology" xml:lang="en">
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<term>Plant Stems</term>
<term>Populus</term>
<term>Wood</term>
<term>Xylem</term>
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<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Leucine Zippers</term>
<term>Plant Leaves</term>
<term>Plant Stems</term>
<term>Populus</term>
<term>Wood</term>
<term>Xylem</term>
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<term>Plant Leaves</term>
<term>Plant Stems</term>
<term>Populus</term>
<term>Wood</term>
<term>Xylem</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Bois</term>
<term>Feuilles de plante</term>
<term>Glissières à leucine</term>
<term>Populus</term>
<term>Protéines d'Arabidopsis</term>
<term>Protéines végétales</term>
<term>Tiges de plante</term>
<term>Xylème</term>
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<term>Plant Leaves</term>
<term>Plant Stems</term>
<term>Populus</term>
<term>Wood</term>
<term>Xylem</term>
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<term>Acides indolacétiques</term>
<term>Bois</term>
<term>Facteur de croissance végétal</term>
<term>Feuilles de plante</term>
<term>Populus</term>
<term>Protéines végétales</term>
<term>Spermine</term>
<term>Tiges de plante</term>
<term>Xylème</term>
</keywords>
<keywords scheme="MESH" qualifier="pharmacologie" xml:lang="fr">
<term>Acides indolacétiques</term>
<term>Facteur de croissance végétal</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Amino Acid Sequence</term>
<term>Base Sequence</term>
<term>Gene Expression Regulation, Plant</term>
<term>Models, Biological</term>
<term>Molecular Sequence Data</term>
<term>Phylogeny</term>
<term>Plants, Genetically Modified</term>
<term>Sequence Analysis, DNA</term>
<term>Trees</term>
<term>Up-Regulation</term>
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<term>Analyse de séquence d'ADN</term>
<term>Arbres</term>
<term>Données de séquences moléculaires</term>
<term>Modèles biologiques</term>
<term>Phylogenèse</term>
<term>Régulation de l'expression des gènes végétaux</term>
<term>Régulation positive</term>
<term>Séquence d'acides aminés</term>
<term>Séquence nucléotidique</term>
<term>Végétaux génétiquement modifiés</term>
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<div type="abstract" xml:lang="en">Polyamines are small polycationic amines that are widespread in living organisms. Thermospermine, synthesized by thermospermine synthase ACAULIS5 (ACL5), was recently shown to be an endogenous plant polyamine. Thermospermine is critical for proper vascular development and xylem cell specification, but it is not known how thermospermine homeostasis is controlled in the xylem. We present data in the Populus model system supporting the existence of a negative feedback control of thermospermine levels in stem xylem tissues, the main site of thermospermine biosynthesis. While over-expression of the ACL5 homologue in Populus, POPACAULIS5, resulted in strong up-regulation of ACL5 expression and thermospermine accumulation in leaves, the corresponding levels in the secondary xylem tissues of the stem were similar or lower than those in the wild-type. POPACAULIS5 over-expression had a negative effect on accumulation of indole-3-acetic acid, while exogenous auxin had a positive effect on POPACAULIS5 expression, thus promoting thermospermine accumulation. Further, over-expression of POPACAULIS5 negatively affected expression of the class III homeodomain leucine zipper (HD-Zip III) transcription factor gene PttHB8, a homologue of AtHB8, while up-regulation of PttHB8 positively affected POPACAULIS5 expression. These results indicate that excessive accumulation of thermospermine is prevented by a negative feedback control of POPACAULIS5 transcript levels through suppression of indole-3-acetic acid levels, and that PttHB8 is involved in the control of POPACAULIS5 expression. We propose that this negative feedback loop functions to maintain steady-state levels of thermospermine, which is required for proper xylem development, and that it is dependent on the presence of high concentrations of endogenous indole-3-acetic acid, such as those present in the secondary xylem tissues. </div>
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<AbstractText>Polyamines are small polycationic amines that are widespread in living organisms. Thermospermine, synthesized by thermospermine synthase ACAULIS5 (ACL5), was recently shown to be an endogenous plant polyamine. Thermospermine is critical for proper vascular development and xylem cell specification, but it is not known how thermospermine homeostasis is controlled in the xylem. We present data in the Populus model system supporting the existence of a negative feedback control of thermospermine levels in stem xylem tissues, the main site of thermospermine biosynthesis. While over-expression of the ACL5 homologue in Populus, POPACAULIS5, resulted in strong up-regulation of ACL5 expression and thermospermine accumulation in leaves, the corresponding levels in the secondary xylem tissues of the stem were similar or lower than those in the wild-type. POPACAULIS5 over-expression had a negative effect on accumulation of indole-3-acetic acid, while exogenous auxin had a positive effect on POPACAULIS5 expression, thus promoting thermospermine accumulation. Further, over-expression of POPACAULIS5 negatively affected expression of the class III homeodomain leucine zipper (HD-Zip III) transcription factor gene PttHB8, a homologue of AtHB8, while up-regulation of PttHB8 positively affected POPACAULIS5 expression. These results indicate that excessive accumulation of thermospermine is prevented by a negative feedback control of POPACAULIS5 transcript levels through suppression of indole-3-acetic acid levels, and that PttHB8 is involved in the control of POPACAULIS5 expression. We propose that this negative feedback loop functions to maintain steady-state levels of thermospermine, which is required for proper xylem development, and that it is dependent on the presence of high concentrations of endogenous indole-3-acetic acid, such as those present in the secondary xylem tissues. </AbstractText>
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</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>2FZ7Y3VOQX</RegistryNumber>
<NameOfSubstance UI="D013096">Spermine</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>6U1S09C61L</RegistryNumber>
<NameOfSubstance UI="C030737">indoleacetic acid</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>70862-11-2</RegistryNumber>
<NameOfSubstance UI="C021097">thermospermine</NameOfSubstance>
</Chemical>
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<MeshHeading>
<DescriptorName UI="D000595" MajorTopicYN="N">Amino Acid Sequence</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D029681" MajorTopicYN="N">Arabidopsis Proteins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
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<MeshHeading>
<DescriptorName UI="D001483" MajorTopicYN="N">Base Sequence</DescriptorName>
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<MeshHeading>
<DescriptorName UI="D018506" MajorTopicYN="Y">Gene Expression Regulation, Plant</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D007210" MajorTopicYN="N">Indoleacetic Acids</DescriptorName>
<QualifierName UI="Q000032" MajorTopicYN="N">analysis</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
<QualifierName UI="Q000494" MajorTopicYN="N">pharmacology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D016350" MajorTopicYN="N">Leucine Zippers</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D008954" MajorTopicYN="N">Models, Biological</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D008969" MajorTopicYN="N">Molecular Sequence Data</DescriptorName>
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<MeshHeading>
<DescriptorName UI="D010802" MajorTopicYN="N">Phylogeny</DescriptorName>
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<MeshHeading>
<DescriptorName UI="D010937" MajorTopicYN="N">Plant Growth Regulators</DescriptorName>
<QualifierName UI="Q000032" MajorTopicYN="N">analysis</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
<QualifierName UI="Q000494" MajorTopicYN="N">pharmacology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018515" MajorTopicYN="N">Plant Leaves</DescriptorName>
<QualifierName UI="Q000166" MajorTopicYN="N">cytology</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000254" MajorTopicYN="N">growth & development</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018547" MajorTopicYN="N">Plant Stems</DescriptorName>
<QualifierName UI="Q000166" MajorTopicYN="N">cytology</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000254" MajorTopicYN="N">growth & development</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D030821" MajorTopicYN="N">Plants, Genetically Modified</DescriptorName>
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<MeshHeading>
<DescriptorName UI="D032107" MajorTopicYN="N">Populus</DescriptorName>
<QualifierName UI="Q000166" MajorTopicYN="N">cytology</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000254" MajorTopicYN="N">growth & development</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D017422" MajorTopicYN="N">Sequence Analysis, DNA</DescriptorName>
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<MeshHeading>
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<MeshHeading>
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<MeshHeading>
<DescriptorName UI="D014934" MajorTopicYN="N">Wood</DescriptorName>
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<QualifierName UI="Q000254" MajorTopicYN="N">growth & development</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D052584" MajorTopicYN="N">Xylem</DescriptorName>
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<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000254" MajorTopicYN="N">growth & development</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="N">ACAULIS5 (ACL5)</Keyword>
<Keyword MajorTopicYN="N">POPACAULIS5</Keyword>
<Keyword MajorTopicYN="N">Populus tremula × Populus tremuloides</Keyword>
<Keyword MajorTopicYN="N">Populus trichocarpa</Keyword>
<Keyword MajorTopicYN="N">class III homeodomain leucine zipper transcription factors (HD-Zip III)</Keyword>
<Keyword MajorTopicYN="N">polyamine</Keyword>
<Keyword MajorTopicYN="N">wood development</Keyword>
</KeywordList>
</MedlineCitation>
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<PubMedPubDate PubStatus="received">
<Year>2013</Year>
<Month>03</Month>
<Day>28</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="revised">
<Year>2013</Year>
<Month>04</Month>
<Day>29</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted">
<Year>2013</Year>
<Month>05</Month>
<Day>01</Day>
</PubMedPubDate>
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<Year>2013</Year>
<Month>5</Month>
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<Hour>6</Hour>
<Minute>0</Minute>
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<PubMedPubDate PubStatus="medline">
<Year>2014</Year>
<Month>4</Month>
<Day>29</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
</History>
<PublicationStatus>ppublish</PublicationStatus>
<ArticleIdList>
<ArticleId IdType="pubmed">23647338</ArticleId>
<ArticleId IdType="doi">10.1111/tpj.12231</ArticleId>
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</pubmed>
<affiliations>
<list>
<country>
<li>Portugal</li>
</country>
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<tree>
<noCountry>
<name sortKey="Blazquez, Miguel A" sort="Blazquez, Miguel A" uniqKey="Blazquez M" first="Miguel A" last="Blázquez">Miguel A. Blázquez</name>
<name sortKey="Bollhoner, Benjamin" sort="Bollhoner, Benjamin" uniqKey="Bollhoner B" first="Benjamin" last="Bollhöner">Benjamin Bollhöner</name>
<name sortKey="Carbonell, Juan" sort="Carbonell, Juan" uniqKey="Carbonell J" first="Juan" last="Carbonell">Juan Carbonell</name>
<name sortKey="Ljung, Karin" sort="Ljung, Karin" uniqKey="Ljung K" first="Karin" last="Ljung">Karin Ljung</name>
<name sortKey="Matos, Andreia" sort="Matos, Andreia" uniqKey="Matos A" first="Andreia" last="Matos">Andreia Matos</name>
<name sortKey="Miguel, Celia M" sort="Miguel, Celia M" uniqKey="Miguel C" first="Célia M" last="Miguel">Célia M. Miguel</name>
<name sortKey="Prestele, Jakob" sort="Prestele, Jakob" uniqKey="Prestele J" first="Jakob" last="Prestele">Jakob Prestele</name>
<name sortKey="Rambla, Jose L" sort="Rambla, Jose L" uniqKey="Rambla J" first="José L" last="Rambla">José L. Rambla</name>
<name sortKey="Tuominen, Hannele" sort="Tuominen, Hannele" uniqKey="Tuominen H" first="Hannele" last="Tuominen">Hannele Tuominen</name>
<name sortKey="Vera Sirera, Francisco" sort="Vera Sirera, Francisco" uniqKey="Vera Sirera F" first="Francisco" last="Vera-Sirera">Francisco Vera-Sirera</name>
</noCountry>
<country name="Portugal">
<noRegion>
<name sortKey="Milhinhos, Ana" sort="Milhinhos, Ana" uniqKey="Milhinhos A" first="Ana" last="Milhinhos">Ana Milhinhos</name>
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</country>
</tree>
</affiliations>
</record>

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