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Exploring transcriptomic diversity in muscle revealed that cellular signaling pathways mainly differentiate five Western porcine breeds

Identifieur interne : 002E15 ( Main/Exploration ); précédent : 002E14; suivant : 002E16

Exploring transcriptomic diversity in muscle revealed that cellular signaling pathways mainly differentiate five Western porcine breeds

Auteurs : Magali Sancristobal [France] ; Florian Rohart [France, Australie] ; Christine Lascor [France] ; Marcel Bouffaud [France] ; Lidwine Trouilh [France] ; Pascal G. P. Martin [France] ; Yannick Lippi [France] ; Thierry Tribout [France] ; Thomas Faraut [France] ; Marie-José Mercat [France] ; Denis Milan [France] ; Laurence Liaubet [France]

Source :

RBID : PMC:4676870

Descripteurs français

English descriptors

Abstract

Background

Among transcriptomic studies, those comparing species or populations can increase our understanding of the impact of the evolutionary forces on the differentiation of populations. A particular situation is the one of short evolution time with breeds of a domesticated species that underwent strong selective pressures. In this study, the gene expression diversity across five pig breeds has been explored in muscle. Samples came from: 24 Duroc, 33 Landrace, 41 Large White dam line, 10 Large White sire line and 39 Piétrain. From these animals, 147 muscle samples obtained at slaughter were analyzed using the porcine Agilent 44 K v1 microarray.

Results

A total of 12,358 genes were identified as expressed in muscle after normalization and 1,703 genes were declared differential for at least one breed (FDR < 0.001). The functional analysis highlighted that gene expression diversity is mainly linked to cellular signaling pathways such as the PI3K (phosphoinositide 3-kinase) pathway. The PI3K pathway is known to be involved in the control of development of the skeletal muscle mass by affecting extracellular matrix - receptor interactions, regulation of actin cytoskeleton pathways and some metabolic functions. This study also highlighted 228 spots (171 unique genes) that differentiate the breeds from each other. A common subgroup of 15 genes selected by three statistical methods was able to differentiate Duroc, Large White and Piétrain breeds.

Conclusions

This study on transcriptomic differentiation across Western pig breeds highlighted a global picture: mainly signaling pathways were affected. This result is consistent with the selection objective of increasing muscle mass. These transcriptional changes may indicate selection pressure or simply breed differences which may be driven by human selection. Further work aiming at comparing genetic and transcriptomic diversities would further increase our understanding of the consequences of human impact on livestock species.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-015-2259-9) contains supplementary material, which is available to authorized users.


Url:
DOI: 10.1186/s12864-015-2259-9
PubMed: 26651482
PubMed Central: 4676870


Affiliations:


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<nlm:aff id="Aff2">Physiologie et Systèmes d’Elevage, Université de Toulouse INPT ENSAT, UMR1388 Génétique, F-31326 Castanet-Tolosan, France</nlm:aff>
<country xml:lang="fr">France</country>
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<region type="region" nuts="2">Occitanie (région administrative)</region>
<region type="old region" nuts="2">Midi-Pyrénées</region>
<settlement type="city">Castanet-Tolosan</settlement>
</placeName>
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<affiliation wicri:level="3">
<nlm:aff id="Aff3">Physiologie et Systèmes d’Elevage, Université de Toulouse INPT ENVT, UMR1388 Génétique, F-31076 Toulouse, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Physiologie et Systèmes d’Elevage, Université de Toulouse INPT ENVT, UMR1388 Génétique, F-31076 Toulouse</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Occitanie (région administrative)</region>
<region type="old region" nuts="2">Midi-Pyrénées</region>
<settlement type="city">Toulouse</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="Aff4">Australian Institute for Bioengineering and Nanotechnology (AIBN), Corner College and Cooper Rds (Bldg 75), The University of Queensland, Brisbane Qld, 4072 Australia</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>Australian Institute for Bioengineering and Nanotechnology (AIBN), Corner College and Cooper Rds (Bldg 75), The University of Queensland, Brisbane Qld</wicri:regionArea>
<wicri:noRegion>Brisbane Qld</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Lascor, Christine" sort="Lascor, Christine" uniqKey="Lascor C" first="Christine" last="Lascor">Christine Lascor</name>
<affiliation wicri:level="1">
<nlm:aff id="Aff1">INRA, UMR1388 Génétique, Physiologie et Systèmes d’Elevage, F-31326 Castanet-Tolosan, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>INRA, UMR1388 Génétique, Physiologie et Systèmes d’Elevage, F-31326 Castanet-Tolosan</wicri:regionArea>
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<wicri:noRegion>31326 Castanet-Tolosan</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="Aff2">Physiologie et Systèmes d’Elevage, Université de Toulouse INPT ENSAT, UMR1388 Génétique, F-31326 Castanet-Tolosan, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Physiologie et Systèmes d’Elevage, Université de Toulouse INPT ENSAT, UMR1388 Génétique, F-31326 Castanet-Tolosan</wicri:regionArea>
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</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="Aff3">Physiologie et Systèmes d’Elevage, Université de Toulouse INPT ENVT, UMR1388 Génétique, F-31076 Toulouse, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Physiologie et Systèmes d’Elevage, Université de Toulouse INPT ENVT, UMR1388 Génétique, F-31076 Toulouse</wicri:regionArea>
<wicri:noRegion>31076 Toulouse</wicri:noRegion>
<wicri:noRegion>31076 Toulouse</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Bouffaud, Marcel" sort="Bouffaud, Marcel" uniqKey="Bouffaud M" first="Marcel" last="Bouffaud">Marcel Bouffaud</name>
<affiliation wicri:level="1">
<nlm:aff id="Aff5">INRA, UE450 Testage - porcs, F-35653 Le Rheu, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>INRA, UE450 Testage - porcs, F-35653 Le Rheu</wicri:regionArea>
<wicri:noRegion>35653 Le Rheu</wicri:noRegion>
<wicri:noRegion>35653 Le Rheu</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Trouilh, Lidwine" sort="Trouilh, Lidwine" uniqKey="Trouilh L" first="Lidwine" last="Trouilh">Lidwine Trouilh</name>
<affiliation wicri:level="1">
<nlm:aff id="Aff6">Plateforme Transcriptome GeT-Biopuces, Laboratoire d’Ingénierie des Systèmes Biologiques et des Procédés (LISBP), F-31077 Toulouse, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Plateforme Transcriptome GeT-Biopuces, Laboratoire d’Ingénierie des Systèmes Biologiques et des Procédés (LISBP), F-31077 Toulouse</wicri:regionArea>
<wicri:noRegion>31077 Toulouse</wicri:noRegion>
<wicri:noRegion>31077 Toulouse</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Martin, Pascal G P" sort="Martin, Pascal G P" uniqKey="Martin P" first="Pascal G. P." last="Martin">Pascal G. P. Martin</name>
<affiliation wicri:level="1">
<nlm:aff id="Aff7">Plateau Transcriptomic impact of Xenobiotics (TRiX), ToxAlim INRA/INP, F-31027 Toulouse, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Plateau Transcriptomic impact of Xenobiotics (TRiX), ToxAlim INRA/INP, F-31027 Toulouse</wicri:regionArea>
<wicri:noRegion>31027 Toulouse</wicri:noRegion>
<wicri:noRegion>31027 Toulouse</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Lippi, Yannick" sort="Lippi, Yannick" uniqKey="Lippi Y" first="Yannick" last="Lippi">Yannick Lippi</name>
<affiliation wicri:level="1">
<nlm:aff id="Aff7">Plateau Transcriptomic impact of Xenobiotics (TRiX), ToxAlim INRA/INP, F-31027 Toulouse, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Plateau Transcriptomic impact of Xenobiotics (TRiX), ToxAlim INRA/INP, F-31027 Toulouse</wicri:regionArea>
<wicri:noRegion>31027 Toulouse</wicri:noRegion>
<wicri:noRegion>31027 Toulouse</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Tribout, Thierry" sort="Tribout, Thierry" uniqKey="Tribout T" first="Thierry" last="Tribout">Thierry Tribout</name>
<affiliation wicri:level="1">
<nlm:aff id="Aff8">INRA GABI, F-78351 Jouy-en-Josas cedex, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>INRA GABI, F-78351 Jouy-en-Josas cedex</wicri:regionArea>
<wicri:noRegion>78351 Jouy-en-Josas cedex</wicri:noRegion>
<wicri:noRegion>78351 Jouy-en-Josas cedex</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Faraut, Thomas" sort="Faraut, Thomas" uniqKey="Faraut T" first="Thomas" last="Faraut">Thomas Faraut</name>
<affiliation wicri:level="1">
<nlm:aff id="Aff1">INRA, UMR1388 Génétique, Physiologie et Systèmes d’Elevage, F-31326 Castanet-Tolosan, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>INRA, UMR1388 Génétique, Physiologie et Systèmes d’Elevage, F-31326 Castanet-Tolosan</wicri:regionArea>
<wicri:noRegion>31326 Castanet-Tolosan</wicri:noRegion>
<wicri:noRegion>31326 Castanet-Tolosan</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="Aff2">Physiologie et Systèmes d’Elevage, Université de Toulouse INPT ENSAT, UMR1388 Génétique, F-31326 Castanet-Tolosan, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Physiologie et Systèmes d’Elevage, Université de Toulouse INPT ENSAT, UMR1388 Génétique, F-31326 Castanet-Tolosan</wicri:regionArea>
<wicri:noRegion>31326 Castanet-Tolosan</wicri:noRegion>
<wicri:noRegion>31326 Castanet-Tolosan</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="Aff3">Physiologie et Systèmes d’Elevage, Université de Toulouse INPT ENVT, UMR1388 Génétique, F-31076 Toulouse, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Physiologie et Systèmes d’Elevage, Université de Toulouse INPT ENVT, UMR1388 Génétique, F-31076 Toulouse</wicri:regionArea>
<wicri:noRegion>31076 Toulouse</wicri:noRegion>
<wicri:noRegion>31076 Toulouse</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Mercat, Marie Jose" sort="Mercat, Marie Jose" uniqKey="Mercat M" first="Marie-José" last="Mercat">Marie-José Mercat</name>
<affiliation wicri:level="1">
<nlm:aff id="Aff9">IFIP/BIOPORC, F-35651 Le Rheu Cedex, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>IFIP/BIOPORC, F-35651 Le Rheu Cedex</wicri:regionArea>
<wicri:noRegion>35651 Le Rheu Cedex</wicri:noRegion>
<wicri:noRegion>35651 Le Rheu Cedex</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Milan, Denis" sort="Milan, Denis" uniqKey="Milan D" first="Denis" last="Milan">Denis Milan</name>
<affiliation wicri:level="1">
<nlm:aff id="Aff1">INRA, UMR1388 Génétique, Physiologie et Systèmes d’Elevage, F-31326 Castanet-Tolosan, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>INRA, UMR1388 Génétique, Physiologie et Systèmes d’Elevage, F-31326 Castanet-Tolosan</wicri:regionArea>
<wicri:noRegion>31326 Castanet-Tolosan</wicri:noRegion>
<wicri:noRegion>31326 Castanet-Tolosan</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="Aff2">Physiologie et Systèmes d’Elevage, Université de Toulouse INPT ENSAT, UMR1388 Génétique, F-31326 Castanet-Tolosan, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Physiologie et Systèmes d’Elevage, Université de Toulouse INPT ENSAT, UMR1388 Génétique, F-31326 Castanet-Tolosan</wicri:regionArea>
<wicri:noRegion>31326 Castanet-Tolosan</wicri:noRegion>
<wicri:noRegion>31326 Castanet-Tolosan</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="Aff3">Physiologie et Systèmes d’Elevage, Université de Toulouse INPT ENVT, UMR1388 Génétique, F-31076 Toulouse, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Physiologie et Systèmes d’Elevage, Université de Toulouse INPT ENVT, UMR1388 Génétique, F-31076 Toulouse</wicri:regionArea>
<wicri:noRegion>31076 Toulouse</wicri:noRegion>
<wicri:noRegion>31076 Toulouse</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Liaubet, Laurence" sort="Liaubet, Laurence" uniqKey="Liaubet L" first="Laurence" last="Liaubet">Laurence Liaubet</name>
<affiliation wicri:level="1">
<nlm:aff id="Aff1">INRA, UMR1388 Génétique, Physiologie et Systèmes d’Elevage, F-31326 Castanet-Tolosan, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>INRA, UMR1388 Génétique, Physiologie et Systèmes d’Elevage, F-31326 Castanet-Tolosan</wicri:regionArea>
<wicri:noRegion>31326 Castanet-Tolosan</wicri:noRegion>
<wicri:noRegion>31326 Castanet-Tolosan</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="Aff2">Physiologie et Systèmes d’Elevage, Université de Toulouse INPT ENSAT, UMR1388 Génétique, F-31326 Castanet-Tolosan, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Physiologie et Systèmes d’Elevage, Université de Toulouse INPT ENSAT, UMR1388 Génétique, F-31326 Castanet-Tolosan</wicri:regionArea>
<wicri:noRegion>31326 Castanet-Tolosan</wicri:noRegion>
<wicri:noRegion>31326 Castanet-Tolosan</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="Aff3">Physiologie et Systèmes d’Elevage, Université de Toulouse INPT ENVT, UMR1388 Génétique, F-31076 Toulouse, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Physiologie et Systèmes d’Elevage, Université de Toulouse INPT ENVT, UMR1388 Génétique, F-31076 Toulouse</wicri:regionArea>
<wicri:noRegion>31076 Toulouse</wicri:noRegion>
<wicri:noRegion>31076 Toulouse</wicri:noRegion>
</affiliation>
</author>
</analytic>
<series>
<title level="j">BMC Genomics</title>
<idno type="eISSN">1471-2164</idno>
<imprint>
<date when="2015">2015</date>
</imprint>
</series>
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<keywords scheme="KwdEn" xml:lang="en">
<term>Animals</term>
<term>Breeding</term>
<term>Female</term>
<term>Gene Expression Profiling (methods)</term>
<term>Gene Expression Profiling (veterinary)</term>
<term>Gene Expression Regulation</term>
<term>Male</term>
<term>Muscle, Skeletal (metabolism)</term>
<term>Oligonucleotide Array Sequence Analysis (methods)</term>
<term>Oligonucleotide Array Sequence Analysis (veterinary)</term>
<term>Signal Transduction</term>
<term>Sus scrofa (classification)</term>
<term>Sus scrofa (genetics)</term>
<term>Sus scrofa (metabolism)</term>
<term>Swine</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Analyse de profil d'expression de gènes ()</term>
<term>Analyse de profil d'expression de gènes (médecine vétérinaire)</term>
<term>Animaux</term>
<term>Femelle</term>
<term>Muscles squelettiques (métabolisme)</term>
<term>Mâle</term>
<term>Régulation de l'expression des gènes</term>
<term>Suidae</term>
<term>Sus scrofa ()</term>
<term>Sus scrofa (génétique)</term>
<term>Sus scrofa (métabolisme)</term>
<term>Sélection</term>
<term>Séquençage par oligonucléotides en batterie ()</term>
<term>Séquençage par oligonucléotides en batterie (médecine vétérinaire)</term>
<term>Transduction du signal</term>
</keywords>
<keywords scheme="MESH" qualifier="classification" xml:lang="en">
<term>Sus scrofa</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Sus scrofa</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Sus scrofa</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en">
<term>Muscle, Skeletal</term>
<term>Sus scrofa</term>
</keywords>
<keywords scheme="MESH" qualifier="methods" xml:lang="en">
<term>Gene Expression Profiling</term>
<term>Oligonucleotide Array Sequence Analysis</term>
</keywords>
<keywords scheme="MESH" qualifier="médecine vétérinaire" xml:lang="fr">
<term>Analyse de profil d'expression de gènes</term>
<term>Séquençage par oligonucléotides en batterie</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Muscles squelettiques</term>
<term>Sus scrofa</term>
</keywords>
<keywords scheme="MESH" qualifier="veterinary" xml:lang="en">
<term>Gene Expression Profiling</term>
<term>Oligonucleotide Array Sequence Analysis</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Animals</term>
<term>Breeding</term>
<term>Female</term>
<term>Gene Expression Regulation</term>
<term>Male</term>
<term>Signal Transduction</term>
<term>Swine</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Analyse de profil d'expression de gènes</term>
<term>Animaux</term>
<term>Femelle</term>
<term>Mâle</term>
<term>Régulation de l'expression des gènes</term>
<term>Suidae</term>
<term>Sus scrofa</term>
<term>Sélection</term>
<term>Séquençage par oligonucléotides en batterie</term>
<term>Transduction du signal</term>
</keywords>
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<front>
<div type="abstract" xml:lang="en">
<sec>
<title>Background</title>
<p>Among transcriptomic studies, those comparing species or populations can increase our understanding of the impact of the evolutionary forces on the differentiation of populations. A particular situation is the one of short evolution time with breeds of a domesticated species that underwent strong selective pressures. In this study, the gene expression diversity across five pig breeds has been explored in muscle. Samples came from: 24 Duroc, 33 Landrace, 41 Large White dam line, 10 Large White sire line and 39 Piétrain. From these animals, 147 muscle samples obtained at slaughter were analyzed using the porcine Agilent 44 K v1 microarray.</p>
</sec>
<sec>
<title>Results</title>
<p>A total of 12,358 genes were identified as expressed in muscle after normalization and 1,703 genes were declared differential for at least one breed (FDR < 0.001). The functional analysis highlighted that gene expression diversity is mainly linked to cellular signaling pathways such as the PI3K (phosphoinositide 3-kinase) pathway. The PI3K pathway is known to be involved in the control of development of the skeletal muscle mass by affecting extracellular matrix - receptor interactions, regulation of actin cytoskeleton pathways and some metabolic functions. This study also highlighted 228 spots (171 unique genes) that differentiate the breeds from each other. A common subgroup of 15 genes selected by three statistical methods was able to differentiate Duroc, Large White and Piétrain breeds.</p>
</sec>
<sec>
<title>Conclusions</title>
<p>This study on transcriptomic differentiation across Western pig breeds highlighted a global picture: mainly signaling pathways were affected. This result is consistent with the selection objective of increasing muscle mass. These transcriptional changes may indicate selection pressure or simply breed differences which may be driven by human selection. Further work aiming at comparing genetic and transcriptomic diversities would further increase our understanding of the consequences of human impact on livestock species.</p>
</sec>
<sec>
<title>Electronic supplementary material</title>
<p>The online version of this article (doi:10.1186/s12864-015-2259-9) contains supplementary material, which is available to authorized users.</p>
</sec>
</div>
</front>
<back>
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<author>
<name sortKey="Lin, H" uniqKey="Lin H">H Lin</name>
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<author>
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<name sortKey="Williams, Br" uniqKey="Williams B">BR Williams</name>
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<author>
<name sortKey="Yang, Yc" uniqKey="Yang Y">YC Yang</name>
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<name sortKey="Nguyen, M" uniqKey="Nguyen M">M Nguyen</name>
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<author>
<name sortKey="Braunschweig, M" uniqKey="Braunschweig M">M Braunschweig</name>
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<name sortKey="Nezer, C" uniqKey="Nezer C">C Nezer</name>
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<author>
<name sortKey="Janssens, S" uniqKey="Janssens S">S Janssens</name>
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<author>
<name sortKey="Bruggeman, V" uniqKey="Bruggeman V">V Bruggeman</name>
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<name sortKey="Onagbesan, Om" uniqKey="Onagbesan O">OM Onagbesan</name>
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<author>
<name sortKey="Muller, N" uniqKey="Muller N">N Mûller</name>
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<author>
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<list>
<country>
<li>Australie</li>
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</country>
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<li>Midi-Pyrénées</li>
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<li>Castanet-Tolosan</li>
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<name sortKey="Milan, Denis" sort="Milan, Denis" uniqKey="Milan D" first="Denis" last="Milan">Denis Milan</name>
<name sortKey="Rohart, Florian" sort="Rohart, Florian" uniqKey="Rohart F" first="Florian" last="Rohart">Florian Rohart</name>
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