Thylakoid proteome modulation in pea plants grown at different irradiances: quantitative proteomic profiling in a non-model organism aided by transcriptomic data integration.
Identifieur interne : 000208 ( Main/Exploration ); précédent : 000207; suivant : 000209Thylakoid proteome modulation in pea plants grown at different irradiances: quantitative proteomic profiling in a non-model organism aided by transcriptomic data integration.
Auteurs : Pascal Albanese [Italie] ; Marcello Manfredi [Italie] ; Angela Re [Italie] ; Emilio Marengo [Italie] ; Guido Saracco [Italie] ; Cristina Pagliano [Italie]Source :
- The Plant journal : for cell and molecular biology [ 1365-313X ] ; 2018.
Descripteurs français
- KwdFr :
- Acclimatation (MeSH), Analyse de profil d'expression de gènes (MeSH), Association médicamenteuse (MeSH), Biosynthèse des protéines (MeSH), Caroténoïdes (métabolisme), Chlorophylle (métabolisme), Complexe protéique du photosystème I (métabolisme), Complexe protéique du photosystème II (métabolisme), Extraits de plantes (métabolisme), Pois (MeSH), Protéines végétales (métabolisme), Protéome (métabolisme), Protéomique (MeSH), Régulation de l'expression des gènes végétaux (MeSH), Stress physiologique (génétique), Thylacoïdes (métabolisme), Transcriptome (MeSH), Transport d'électrons (MeSH).
- MESH :
- génétique : Stress physiologique.
- métabolisme : Caroténoïdes, Chlorophylle, Complexe protéique du photosystème I, Complexe protéique du photosystème II, Extraits de plantes, Protéines végétales, Protéome, Thylacoïdes.
- Acclimatation, Analyse de profil d'expression de gènes, Association médicamenteuse, Biosynthèse des protéines, Pois, Protéomique, Régulation de l'expression des gènes végétaux, Transcriptome, Transport d'électrons.
English descriptors
- KwdEn :
- Acclimatization (MeSH), Carotenoids (metabolism), Chlorophyll (metabolism), Drug Combinations (MeSH), Electron Transport (MeSH), Gene Expression Profiling (MeSH), Gene Expression Regulation, Plant (MeSH), Peas (MeSH), Photosystem I Protein Complex (metabolism), Photosystem II Protein Complex (metabolism), Plant Extracts (metabolism), Plant Proteins (metabolism), Protein Biosynthesis (MeSH), Proteome (metabolism), Proteomics (MeSH), Stress, Physiological (genetics), Thylakoids (metabolism), Transcriptome (MeSH).
- MESH :
- chemical , metabolism : Carotenoids, Chlorophyll, Photosystem I Protein Complex, Photosystem II Protein Complex, Plant Extracts, Plant Proteins, Proteome.
- genetics : Stress, Physiological.
- metabolism : Thylakoids.
- Acclimatization, Drug Combinations, Electron Transport, Gene Expression Profiling, Gene Expression Regulation, Plant, Peas, Protein Biosynthesis, Proteomics, Transcriptome.
Abstract
Plant thylakoid membranes contain hundreds of proteins that closely interact to cope with ever-changing environmental conditions. We investigated how Pisum sativum L. (pea) grown at different irradiances optimizes light-use efficiency through the differential accumulation of thylakoid proteins. Thylakoid membranes from plants grown under low (LL), moderate (ML) and high (HL) light intensity were characterized by combining chlorophyll fluorescence measurements with quantitative label-free proteomic analysis. Protein sequences retrieved from available transcriptomic data considerably improved thylakoid proteome profiling, increasing the quantifiable proteins from 63 to 194. The experimental approach used also demonstrates that this integrative omics strategy is powerful for unravelling protein isoforms and functions that are still unknown in non-model organisms. We found that the different growth irradiances affect the electron transport kinetics but not the relative abundance of photosystems (PS) I and II. Two acclimation strategies were evident. The behaviour of plants acclimated to LL was compared at higher irradiances: (i) in ML, plants turn on photoprotective responses mostly modulating the PSII light-harvesting capacity, either accumulating Lhcb4.3 or favouring the xanthophyll cycle; (ii) in HL, plants reduce the pool of light-harvesting complex II and enhance the PSII repair cycle. When growing at ML and HL, plants accumulate ATP synthase, boosting both cyclic and linear electron transport by finely tuning the ΔpH across the membrane and optimizing protein trafficking by adjusting the thylakoid architecture. Our results provide a quantitative snapshot of how plants coordinate light harvesting, electron transport and protein synthesis by adjusting the thylakoid membrane proteome in a light-dependent manner.
DOI: 10.1111/tpj.14068
PubMed: 30118564
Affiliations:
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Michel 11, 15121, Alessandria, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>ISALIT-Department of Science and Technological Innovation, University of Eastern Piedmont, Viale T. Michel 11, 15121, Alessandria</wicri:regionArea><wicri:noRegion>Alessandria</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Department of Science and Technological Innovation, University of Eastern Piedmont, Viale T. Michel 11, 15121, Alessandria, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Science and Technological Innovation, University of Eastern Piedmont, Viale T. Michel 11, 15121, Alessandria</wicri:regionArea><wicri:noRegion>Alessandria</wicri:noRegion></affiliation></author><author><name sortKey="Re, Angela" sort="Re, Angela" uniqKey="Re A" first="Angela" last="Re">Angela Re</name><affiliation wicri:level="3"><nlm:affiliation>Center for Sustainable Future Technologies-CSFT@POLITO, Istituto Italiano di Tecnologia, Corso Trento 21, 10129, Torino, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Center for Sustainable Future Technologies-CSFT@POLITO, Istituto Italiano di Tecnologia, Corso Trento 21, 10129, Torino</wicri:regionArea><placeName><settlement type="city">Turin</settlement><region type="région" nuts="2">Piémont</region></placeName></affiliation></author><author><name sortKey="Marengo, Emilio" sort="Marengo, Emilio" uniqKey="Marengo E" first="Emilio" last="Marengo">Emilio Marengo</name><affiliation wicri:level="1"><nlm:affiliation>Department of Science and Technological Innovation, University of Eastern Piedmont, Viale T. Michel 11, 15121, Alessandria, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Science and Technological Innovation, University of Eastern Piedmont, Viale T. 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Technology Department-BioSolar Lab, Politecnico di Torino, Environment Park, Via Livorno 60, 10144, Torino, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Applied Science and Technology Department-BioSolar Lab, Politecnico di Torino, Environment Park, Via Livorno 60, 10144, Torino</wicri:regionArea><placeName><settlement type="city">Turin</settlement><region type="région" nuts="2">Piémont</region></placeName></affiliation></author></analytic><series><title level="j">The Plant journal : for cell and molecular biology</title><idno type="eISSN">1365-313X</idno><imprint><date when="2018" type="published">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Acclimatization (MeSH)</term><term>Carotenoids (metabolism)</term><term>Chlorophyll (metabolism)</term><term>Drug Combinations (MeSH)</term><term>Electron Transport (MeSH)</term><term>Gene Expression Profiling (MeSH)</term><term>Gene Expression Regulation, Plant (MeSH)</term><term>Peas (MeSH)</term><term>Photosystem I Protein Complex (metabolism)</term><term>Photosystem II Protein Complex (metabolism)</term><term>Plant Extracts (metabolism)</term><term>Plant Proteins (metabolism)</term><term>Protein Biosynthesis (MeSH)</term><term>Proteome (metabolism)</term><term>Proteomics (MeSH)</term><term>Stress, Physiological (genetics)</term><term>Thylakoids (metabolism)</term><term>Transcriptome (MeSH)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Acclimatation (MeSH)</term><term>Analyse de profil d'expression de gènes (MeSH)</term><term>Association médicamenteuse (MeSH)</term><term>Biosynthèse des protéines (MeSH)</term><term>Caroténoïdes (métabolisme)</term><term>Chlorophylle (métabolisme)</term><term>Complexe protéique du photosystème I (métabolisme)</term><term>Complexe protéique du photosystème II (métabolisme)</term><term>Extraits de plantes (métabolisme)</term><term>Pois (MeSH)</term><term>Protéines végétales (métabolisme)</term><term>Protéome (métabolisme)</term><term>Protéomique (MeSH)</term><term>Régulation de l'expression des gènes végétaux (MeSH)</term><term>Stress physiologique (génétique)</term><term>Thylacoïdes (métabolisme)</term><term>Transcriptome (MeSH)</term><term>Transport d'électrons (MeSH)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Carotenoids</term><term>Chlorophyll</term><term>Photosystem I Protein Complex</term><term>Photosystem II Protein Complex</term><term>Plant Extracts</term><term>Plant Proteins</term><term>Proteome</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Stress, Physiological</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Stress physiologique</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Thylakoids</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Caroténoïdes</term><term>Chlorophylle</term><term>Complexe protéique du photosystème I</term><term>Complexe protéique du photosystème II</term><term>Extraits de plantes</term><term>Protéines végétales</term><term>Protéome</term><term>Thylacoïdes</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Acclimatization</term><term>Drug Combinations</term><term>Electron Transport</term><term>Gene Expression Profiling</term><term>Gene Expression Regulation, Plant</term><term>Peas</term><term>Protein Biosynthesis</term><term>Proteomics</term><term>Transcriptome</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Acclimatation</term><term>Analyse de profil d'expression de gènes</term><term>Association médicamenteuse</term><term>Biosynthèse des protéines</term><term>Pois</term><term>Protéomique</term><term>Régulation de l'expression des gènes végétaux</term><term>Transcriptome</term><term>Transport d'électrons</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Plant thylakoid membranes contain hundreds of proteins that closely interact to cope with ever-changing environmental conditions. We investigated how Pisum sativum L. (pea) grown at different irradiances optimizes light-use efficiency through the differential accumulation of thylakoid proteins. Thylakoid membranes from plants grown under low (LL), moderate (ML) and high (HL) light intensity were characterized by combining chlorophyll fluorescence measurements with quantitative label-free proteomic analysis. Protein sequences retrieved from available transcriptomic data considerably improved thylakoid proteome profiling, increasing the quantifiable proteins from 63 to 194. The experimental approach used also demonstrates that this integrative omics strategy is powerful for unravelling protein isoforms and functions that are still unknown in non-model organisms. We found that the different growth irradiances affect the electron transport kinetics but not the relative abundance of photosystems (PS) I and II. Two acclimation strategies were evident. The behaviour of plants acclimated to LL was compared at higher irradiances: (i) in ML, plants turn on photoprotective responses mostly modulating the PSII light-harvesting capacity, either accumulating Lhcb4.3 or favouring the xanthophyll cycle; (ii) in HL, plants reduce the pool of light-harvesting complex II and enhance the PSII repair cycle. When growing at ML and HL, plants accumulate ATP synthase, boosting both cyclic and linear electron transport by finely tuning the ΔpH across the membrane and optimizing protein trafficking by adjusting the thylakoid architecture. Our results provide a quantitative snapshot of how plants coordinate light harvesting, electron transport and protein synthesis by adjusting the thylakoid membrane proteome in a light-dependent manner.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">30118564</PMID><DateCompleted><Year>2019</Year><Month>08</Month><Day>06</Day></DateCompleted><DateRevised><Year>2019</Year><Month>08</Month><Day>06</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1365-313X</ISSN><JournalIssue CitedMedium="Internet"><Volume>96</Volume><Issue>4</Issue><PubDate><Year>2018</Year><Month>11</Month></PubDate></JournalIssue><Title>The Plant journal : for cell and molecular biology</Title><ISOAbbreviation>Plant J</ISOAbbreviation></Journal><ArticleTitle>Thylakoid proteome modulation in pea plants grown at different irradiances: quantitative proteomic profiling in a non-model organism aided by transcriptomic data integration.</ArticleTitle><Pagination><MedlinePgn>786-800</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1111/tpj.14068</ELocationID><Abstract><AbstractText>Plant thylakoid membranes contain hundreds of proteins that closely interact to cope with ever-changing environmental conditions. We investigated how Pisum sativum L. (pea) grown at different irradiances optimizes light-use efficiency through the differential accumulation of thylakoid proteins. Thylakoid membranes from plants grown under low (LL), moderate (ML) and high (HL) light intensity were characterized by combining chlorophyll fluorescence measurements with quantitative label-free proteomic analysis. Protein sequences retrieved from available transcriptomic data considerably improved thylakoid proteome profiling, increasing the quantifiable proteins from 63 to 194. The experimental approach used also demonstrates that this integrative omics strategy is powerful for unravelling protein isoforms and functions that are still unknown in non-model organisms. We found that the different growth irradiances affect the electron transport kinetics but not the relative abundance of photosystems (PS) I and II. Two acclimation strategies were evident. The behaviour of plants acclimated to LL was compared at higher irradiances: (i) in ML, plants turn on photoprotective responses mostly modulating the PSII light-harvesting capacity, either accumulating Lhcb4.3 or favouring the xanthophyll cycle; (ii) in HL, plants reduce the pool of light-harvesting complex II and enhance the PSII repair cycle. When growing at ML and HL, plants accumulate ATP synthase, boosting both cyclic and linear electron transport by finely tuning the ΔpH across the membrane and optimizing protein trafficking by adjusting the thylakoid architecture. Our results provide a quantitative snapshot of how plants coordinate light harvesting, electron transport and protein synthesis by adjusting the thylakoid membrane proteome in a light-dependent manner.</AbstractText><CopyrightInformation>© 2018 The Authors The Plant Journal © 2018 John Wiley & Sons Ltd.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Albanese</LastName><ForeName>Pascal</ForeName><Initials>P</Initials><Identifier Source="ORCID">0000-0002-0940-8534</Identifier><AffiliationInfo><Affiliation>Applied Science and Technology Department-BioSolar Lab, Politecnico di Torino, Environment Park, Via Livorno 60, 10144, Torino, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Manfredi</LastName><ForeName>Marcello</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>ISALIT-Department of Science and Technological Innovation, University of Eastern Piedmont, Viale T. Michel 11, 15121, Alessandria, Italy.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Science and Technological Innovation, University of Eastern Piedmont, Viale T. Michel 11, 15121, Alessandria, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Re</LastName><ForeName>Angela</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Center for Sustainable Future Technologies-CSFT@POLITO, Istituto Italiano di Tecnologia, Corso Trento 21, 10129, Torino, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Marengo</LastName><ForeName>Emilio</ForeName><Initials>E</Initials><AffiliationInfo><Affiliation>Department of Science and Technological Innovation, University of Eastern Piedmont, Viale T. Michel 11, 15121, Alessandria, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Saracco</LastName><ForeName>Guido</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Applied Science and Technology Department-BioSolar Lab, Politecnico di Torino, Environment Park, Via Livorno 60, 10144, Torino, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Pagliano</LastName><ForeName>Cristina</ForeName><Initials>C</Initials><Identifier Source="ORCID">0000-0002-5532-8658</Identifier><AffiliationInfo><Affiliation>Applied Science and Technology Department-BioSolar Lab, Politecnico di Torino, Environment Park, Via Livorno 60, 10144, Torino, Italy.</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>2018</Year><Month>09</Month><Day>19</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Plant J</MedlineTA><NlmUniqueID>9207397</NlmUniqueID><ISSNLinking>0960-7412</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D004338">Drug Combinations</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D045331">Photosystem I Protein Complex</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D045332">Photosystem II Protein Complex</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D010936">Plant Extracts</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D020543">Proteome</NameOfSubstance></Chemical><Chemical><RegistryNumber>12750-97-9</RegistryNumber><NameOfSubstance UI="C002969">chlorophyllypt</NameOfSubstance></Chemical><Chemical><RegistryNumber>1406-65-1</RegistryNumber><NameOfSubstance UI="D002734">Chlorophyll</NameOfSubstance></Chemical><Chemical><RegistryNumber>36-88-4</RegistryNumber><NameOfSubstance UI="D002338">Carotenoids</NameOfSubstance></Chemical></ChemicalList><MeshHeadingList><MeshHeading><DescriptorName UI="D000064" MajorTopicYN="N">Acclimatization</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D002338" MajorTopicYN="N">Carotenoids</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D002734" MajorTopicYN="N">Chlorophyll</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D004338" MajorTopicYN="N">Drug Combinations</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D004579" MajorTopicYN="N">Electron Transport</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D020869" MajorTopicYN="Y">Gene Expression Profiling</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D018506" MajorTopicYN="N">Gene Expression Regulation, Plant</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D018532" MajorTopicYN="N">Peas</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D045331" MajorTopicYN="N">Photosystem I Protein Complex</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D045332" MajorTopicYN="N">Photosystem II Protein Complex</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D010936" MajorTopicYN="N">Plant Extracts</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D014176" MajorTopicYN="N">Protein Biosynthesis</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D020543" MajorTopicYN="N">Proteome</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D040901" MajorTopicYN="Y">Proteomics</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D013312" MajorTopicYN="N">Stress, Physiological</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D020524" MajorTopicYN="N">Thylakoids</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D059467" MajorTopicYN="Y">Transcriptome</DescriptorName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">Pisum sativum
</Keyword><Keyword MajorTopicYN="Y">SWATH analysis</Keyword><Keyword MajorTopicYN="Y">light acclimation</Keyword><Keyword MajorTopicYN="Y">omics data integration</Keyword><Keyword MajorTopicYN="Y">quantitative proteomics</Keyword><Keyword MajorTopicYN="Y">thylakoid membrane</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2018</Year><Month>07</Month><Day>16</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2018</Year><Month>08</Month><Day>03</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2018</Year><Month>08</Month><Day>13</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2018</Year><Month>8</Month><Day>18</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2019</Year><Month>8</Month><Day>7</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2018</Year><Month>8</Month><Day>18</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">30118564</ArticleId><ArticleId IdType="doi">10.1111/tpj.14068</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>Italie</li></country><region><li>Piémont</li></region><settlement><li>Turin</li></settlement></list><tree><country name="Italie"><region name="Piémont"><name sortKey="Albanese, Pascal" sort="Albanese, Pascal" uniqKey="Albanese P" first="Pascal" last="Albanese">Pascal Albanese</name></region><name sortKey="Manfredi, Marcello" sort="Manfredi, Marcello" uniqKey="Manfredi M" first="Marcello" last="Manfredi">Marcello Manfredi</name><name sortKey="Manfredi, Marcello" sort="Manfredi, Marcello" uniqKey="Manfredi M" first="Marcello" last="Manfredi">Marcello Manfredi</name><name sortKey="Marengo, Emilio" sort="Marengo, Emilio" uniqKey="Marengo E" first="Emilio" last="Marengo">Emilio Marengo</name><name sortKey="Pagliano, Cristina" sort="Pagliano, Cristina" uniqKey="Pagliano C" first="Cristina" last="Pagliano">Cristina Pagliano</name><name sortKey="Re, Angela" sort="Re, Angela" uniqKey="Re A" first="Angela" last="Re">Angela Re</name><name sortKey="Saracco, Guido" sort="Saracco, Guido" uniqKey="Saracco G" first="Guido" last="Saracco">Guido Saracco</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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