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Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis.

Identifieur interne : 001A43 ( Main/Corpus ); précédent : 001A42; suivant : 001A44

Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis.

Auteurs : Emilie Tisserant ; Mathilde Malbreil ; Alan Kuo ; Annegret Kohler ; Aikaterini Symeonidi ; Raffaella Balestrini ; Philippe Charron ; Nina Duensing ; Nicolas Frei Dit Frey ; Vivienne Gianinazzi-Pearson ; Luz B. Gilbert ; Yoshihiro Handa ; Joshua R. Herr ; Mohamed Hijri ; Raman Koul ; Masayoshi Kawaguchi ; Franziska Krajinski ; Peter J. Lammers ; Frederic G. Masclaux ; Claude Murat ; Emmanuelle Morin ; Steve Ndikumana ; Marco Pagni ; Denis Petitpierre ; Natalia Requena ; Pawel Rosikiewicz ; Rohan Riley ; Katsuharu Saito ; Hélène San Clemente ; Harris Shapiro ; Diederik Van Tuinen ; Guillaume Bécard ; Paola Bonfante ; Uta Paszkowski ; Yair Y. Shachar-Hill ; Gerald A. Tuskan ; J Peter W. Young ; Peter W. Young ; Ian R. Sanders ; Bernard Henrissat ; Stefan A. Rensing ; Igor V. Grigoriev ; Nicolas Corradi ; Christophe Roux ; Francis Martin

Source :

RBID : pubmed:24277808

English descriptors

Abstract

The mutualistic symbiosis involving Glomeromycota, a distinctive phylum of early diverging Fungi, is widely hypothesized to have promoted the evolution of land plants during the middle Paleozoic. These arbuscular mycorrhizal fungi (AMF) perform vital functions in the phosphorus cycle that are fundamental to sustainable crop plant productivity. The unusual biological features of AMF have long fascinated evolutionary biologists. The coenocytic hyphae host a community of hundreds of nuclei and reproduce clonally through large multinucleated spores. It has been suggested that the AMF maintain a stable assemblage of several different genomes during the life cycle, but this genomic organization has been questioned. Here we introduce the 153-Mb haploid genome of Rhizophagus irregularis and its repertoire of 28,232 genes. The observed low level of genome polymorphism (0.43 SNP per kb) is not consistent with the occurrence of multiple, highly diverged genomes. The expansion of mating-related genes suggests the existence of cryptic sex-related processes. A comparison of gene categories confirms that R. irregularis is close to the Mucoromycotina. The AMF obligate biotrophy is not explained by genome erosion or any related loss of metabolic complexity in central metabolism, but is marked by a lack of genes encoding plant cell wall-degrading enzymes and of genes involved in toxin and thiamine synthesis. A battery of mycorrhiza-induced secreted proteins is expressed in symbiotic tissues. The present comprehensive repertoire of R. irregularis genes provides a basis for future research on symbiosis-related mechanisms in Glomeromycota.

DOI: 10.1073/pnas.1313452110
PubMed: 24277808
PubMed Central: PMC3864322

Links to Exploration step

pubmed:24277808

Le document en format XML

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<title xml:lang="en">Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis.</title>
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<name sortKey="Tisserant, Emilie" sort="Tisserant, Emilie" uniqKey="Tisserant E" first="Emilie" last="Tisserant">Emilie Tisserant</name>
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<nlm:affiliation>Institut National de la Recherche Agronomique, Unité Mixte de Recherche 1136, Interactions Arbres/Microorganismes, Centre de Nancy, Université de Lorraine, 54280 Champenoux, France.</nlm:affiliation>
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<name sortKey="Malbreil, Mathilde" sort="Malbreil, Mathilde" uniqKey="Malbreil M" first="Mathilde" last="Malbreil">Mathilde Malbreil</name>
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<name sortKey="Kuo, Alan" sort="Kuo, Alan" uniqKey="Kuo A" first="Alan" last="Kuo">Alan Kuo</name>
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<name sortKey="Kohler, Annegret" sort="Kohler, Annegret" uniqKey="Kohler A" first="Annegret" last="Kohler">Annegret Kohler</name>
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<name sortKey="Symeonidi, Aikaterini" sort="Symeonidi, Aikaterini" uniqKey="Symeonidi A" first="Aikaterini" last="Symeonidi">Aikaterini Symeonidi</name>
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<name sortKey="Balestrini, Raffaella" sort="Balestrini, Raffaella" uniqKey="Balestrini R" first="Raffaella" last="Balestrini">Raffaella Balestrini</name>
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<name sortKey="Charron, Philippe" sort="Charron, Philippe" uniqKey="Charron P" first="Philippe" last="Charron">Philippe Charron</name>
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<name sortKey="Duensing, Nina" sort="Duensing, Nina" uniqKey="Duensing N" first="Nina" last="Duensing">Nina Duensing</name>
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<name sortKey="Frei Dit Frey, Nicolas" sort="Frei Dit Frey, Nicolas" uniqKey="Frei Dit Frey N" first="Nicolas" last="Frei Dit Frey">Nicolas Frei Dit Frey</name>
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<name sortKey="Gianinazzi Pearson, Vivienne" sort="Gianinazzi Pearson, Vivienne" uniqKey="Gianinazzi Pearson V" first="Vivienne" last="Gianinazzi-Pearson">Vivienne Gianinazzi-Pearson</name>
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<name sortKey="Gilbert, Luz B" sort="Gilbert, Luz B" uniqKey="Gilbert L" first="Luz B" last="Gilbert">Luz B. Gilbert</name>
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<name sortKey="Handa, Yoshihiro" sort="Handa, Yoshihiro" uniqKey="Handa Y" first="Yoshihiro" last="Handa">Yoshihiro Handa</name>
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<name sortKey="Herr, Joshua R" sort="Herr, Joshua R" uniqKey="Herr J" first="Joshua R" last="Herr">Joshua R. Herr</name>
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<name sortKey="Hijri, Mohamed" sort="Hijri, Mohamed" uniqKey="Hijri M" first="Mohamed" last="Hijri">Mohamed Hijri</name>
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<name sortKey="Koul, Raman" sort="Koul, Raman" uniqKey="Koul R" first="Raman" last="Koul">Raman Koul</name>
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<author>
<name sortKey="Kawaguchi, Masayoshi" sort="Kawaguchi, Masayoshi" uniqKey="Kawaguchi M" first="Masayoshi" last="Kawaguchi">Masayoshi Kawaguchi</name>
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<author>
<name sortKey="Krajinski, Franziska" sort="Krajinski, Franziska" uniqKey="Krajinski F" first="Franziska" last="Krajinski">Franziska Krajinski</name>
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<name sortKey="Lammers, Peter J" sort="Lammers, Peter J" uniqKey="Lammers P" first="Peter J" last="Lammers">Peter J. Lammers</name>
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<author>
<name sortKey="Masclaux, Frederic G" sort="Masclaux, Frederic G" uniqKey="Masclaux F" first="Frederic G" last="Masclaux">Frederic G. Masclaux</name>
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<name sortKey="Murat, Claude" sort="Murat, Claude" uniqKey="Murat C" first="Claude" last="Murat">Claude Murat</name>
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<author>
<name sortKey="Morin, Emmanuelle" sort="Morin, Emmanuelle" uniqKey="Morin E" first="Emmanuelle" last="Morin">Emmanuelle Morin</name>
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<name sortKey="Ndikumana, Steve" sort="Ndikumana, Steve" uniqKey="Ndikumana S" first="Steve" last="Ndikumana">Steve Ndikumana</name>
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<name sortKey="Pagni, Marco" sort="Pagni, Marco" uniqKey="Pagni M" first="Marco" last="Pagni">Marco Pagni</name>
</author>
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<name sortKey="Petitpierre, Denis" sort="Petitpierre, Denis" uniqKey="Petitpierre D" first="Denis" last="Petitpierre">Denis Petitpierre</name>
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<author>
<name sortKey="Requena, Natalia" sort="Requena, Natalia" uniqKey="Requena N" first="Natalia" last="Requena">Natalia Requena</name>
</author>
<author>
<name sortKey="Rosikiewicz, Pawel" sort="Rosikiewicz, Pawel" uniqKey="Rosikiewicz P" first="Pawel" last="Rosikiewicz">Pawel Rosikiewicz</name>
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<author>
<name sortKey="Riley, Rohan" sort="Riley, Rohan" uniqKey="Riley R" first="Rohan" last="Riley">Rohan Riley</name>
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<author>
<name sortKey="Saito, Katsuharu" sort="Saito, Katsuharu" uniqKey="Saito K" first="Katsuharu" last="Saito">Katsuharu Saito</name>
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<author>
<name sortKey="San Clemente, Helene" sort="San Clemente, Helene" uniqKey="San Clemente H" first="Hélène" last="San Clemente">Hélène San Clemente</name>
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<author>
<name sortKey="Shapiro, Harris" sort="Shapiro, Harris" uniqKey="Shapiro H" first="Harris" last="Shapiro">Harris Shapiro</name>
</author>
<author>
<name sortKey="Van Tuinen, Diederik" sort="Van Tuinen, Diederik" uniqKey="Van Tuinen D" first="Diederik" last="Van Tuinen">Diederik Van Tuinen</name>
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<name sortKey="Becard, Guillaume" sort="Becard, Guillaume" uniqKey="Becard G" first="Guillaume" last="Bécard">Guillaume Bécard</name>
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<name sortKey="Bonfante, Paola" sort="Bonfante, Paola" uniqKey="Bonfante P" first="Paola" last="Bonfante">Paola Bonfante</name>
</author>
<author>
<name sortKey="Paszkowski, Uta" sort="Paszkowski, Uta" uniqKey="Paszkowski U" first="Uta" last="Paszkowski">Uta Paszkowski</name>
</author>
<author>
<name sortKey="Shachar Hill, Yair Y" sort="Shachar Hill, Yair Y" uniqKey="Shachar Hill Y" first="Yair Y" last="Shachar-Hill">Yair Y. Shachar-Hill</name>
</author>
<author>
<name sortKey="Tuskan, Gerald A" sort="Tuskan, Gerald A" uniqKey="Tuskan G" first="Gerald A" last="Tuskan">Gerald A. Tuskan</name>
</author>
<author>
<name sortKey="Young, J Peter W" sort="Young, J Peter W" uniqKey="Young J" first="J Peter W" last="Young">J Peter W. Young</name>
</author>
<author>
<name sortKey="Young, Peter W" sort="Young, Peter W" uniqKey="Young P" first="Peter W" last="Young">Peter W. Young</name>
</author>
<author>
<name sortKey="Sanders, Ian R" sort="Sanders, Ian R" uniqKey="Sanders I" first="Ian R" last="Sanders">Ian R. Sanders</name>
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<author>
<name sortKey="Henrissat, Bernard" sort="Henrissat, Bernard" uniqKey="Henrissat B" first="Bernard" last="Henrissat">Bernard Henrissat</name>
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<author>
<name sortKey="Rensing, Stefan A" sort="Rensing, Stefan A" uniqKey="Rensing S" first="Stefan A" last="Rensing">Stefan A. Rensing</name>
</author>
<author>
<name sortKey="Grigoriev, Igor V" sort="Grigoriev, Igor V" uniqKey="Grigoriev I" first="Igor V" last="Grigoriev">Igor V. Grigoriev</name>
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<author>
<name sortKey="Corradi, Nicolas" sort="Corradi, Nicolas" uniqKey="Corradi N" first="Nicolas" last="Corradi">Nicolas Corradi</name>
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<name sortKey="Roux, Christophe" sort="Roux, Christophe" uniqKey="Roux C" first="Christophe" last="Roux">Christophe Roux</name>
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<author>
<name sortKey="Martin, Francis" sort="Martin, Francis" uniqKey="Martin F" first="Francis" last="Martin">Francis Martin</name>
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</analytic>
<series>
<title level="j">Proceedings of the National Academy of Sciences of the United States of America</title>
<idno type="eISSN">1091-6490</idno>
<imprint>
<date when="2013" type="published">2013</date>
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<keywords scheme="KwdEn" xml:lang="en">
<term>Base Sequence (MeSH)</term>
<term>Evolution, Molecular (MeSH)</term>
<term>Genome, Fungal (genetics)</term>
<term>Glomeromycota (genetics)</term>
<term>Molecular Sequence Data (MeSH)</term>
<term>Mycorrhizae (genetics)</term>
<term>Plants (microbiology)</term>
<term>Sequence Analysis, DNA (MeSH)</term>
<term>Symbiosis (genetics)</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Genome, Fungal</term>
<term>Glomeromycota</term>
<term>Mycorrhizae</term>
<term>Symbiosis</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Plants</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Base Sequence</term>
<term>Evolution, Molecular</term>
<term>Molecular Sequence Data</term>
<term>Sequence Analysis, DNA</term>
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<front>
<div type="abstract" xml:lang="en">The mutualistic symbiosis involving Glomeromycota, a distinctive phylum of early diverging Fungi, is widely hypothesized to have promoted the evolution of land plants during the middle Paleozoic. These arbuscular mycorrhizal fungi (AMF) perform vital functions in the phosphorus cycle that are fundamental to sustainable crop plant productivity. The unusual biological features of AMF have long fascinated evolutionary biologists. The coenocytic hyphae host a community of hundreds of nuclei and reproduce clonally through large multinucleated spores. It has been suggested that the AMF maintain a stable assemblage of several different genomes during the life cycle, but this genomic organization has been questioned. Here we introduce the 153-Mb haploid genome of Rhizophagus irregularis and its repertoire of 28,232 genes. The observed low level of genome polymorphism (0.43 SNP per kb) is not consistent with the occurrence of multiple, highly diverged genomes. The expansion of mating-related genes suggests the existence of cryptic sex-related processes. A comparison of gene categories confirms that R. irregularis is close to the Mucoromycotina. The AMF obligate biotrophy is not explained by genome erosion or any related loss of metabolic complexity in central metabolism, but is marked by a lack of genes encoding plant cell wall-degrading enzymes and of genes involved in toxin and thiamine synthesis. A battery of mycorrhiza-induced secreted proteins is expressed in symbiotic tissues. The present comprehensive repertoire of R. irregularis genes provides a basis for future research on symbiosis-related mechanisms in Glomeromycota. </div>
</front>
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<DateCompleted>
<Year>2014</Year>
<Month>02</Month>
<Day>21</Day>
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<DateRevised>
<Year>2018</Year>
<Month>11</Month>
<Day>13</Day>
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<ISSN IssnType="Electronic">1091-6490</ISSN>
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<Volume>110</Volume>
<Issue>50</Issue>
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<Year>2013</Year>
<Month>Dec</Month>
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<Title>Proceedings of the National Academy of Sciences of the United States of America</Title>
<ISOAbbreviation>Proc Natl Acad Sci U S A</ISOAbbreviation>
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<ArticleTitle>Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis.</ArticleTitle>
<Pagination>
<MedlinePgn>20117-22</MedlinePgn>
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<Abstract>
<AbstractText>The mutualistic symbiosis involving Glomeromycota, a distinctive phylum of early diverging Fungi, is widely hypothesized to have promoted the evolution of land plants during the middle Paleozoic. These arbuscular mycorrhizal fungi (AMF) perform vital functions in the phosphorus cycle that are fundamental to sustainable crop plant productivity. The unusual biological features of AMF have long fascinated evolutionary biologists. The coenocytic hyphae host a community of hundreds of nuclei and reproduce clonally through large multinucleated spores. It has been suggested that the AMF maintain a stable assemblage of several different genomes during the life cycle, but this genomic organization has been questioned. Here we introduce the 153-Mb haploid genome of Rhizophagus irregularis and its repertoire of 28,232 genes. The observed low level of genome polymorphism (0.43 SNP per kb) is not consistent with the occurrence of multiple, highly diverged genomes. The expansion of mating-related genes suggests the existence of cryptic sex-related processes. A comparison of gene categories confirms that R. irregularis is close to the Mucoromycotina. The AMF obligate biotrophy is not explained by genome erosion or any related loss of metabolic complexity in central metabolism, but is marked by a lack of genes encoding plant cell wall-degrading enzymes and of genes involved in toxin and thiamine synthesis. A battery of mycorrhiza-induced secreted proteins is expressed in symbiotic tissues. The present comprehensive repertoire of R. irregularis genes provides a basis for future research on symbiosis-related mechanisms in Glomeromycota. </AbstractText>
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<ForeName>Emilie</ForeName>
<Initials>E</Initials>
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<Affiliation>Institut National de la Recherche Agronomique, Unité Mixte de Recherche 1136, Interactions Arbres/Microorganismes, Centre de Nancy, Université de Lorraine, 54280 Champenoux, France.</Affiliation>
</AffiliationInfo>
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<LastName>Malbreil</LastName>
<ForeName>Mathilde</ForeName>
<Initials>M</Initials>
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<LastName>Kuo</LastName>
<ForeName>Alan</ForeName>
<Initials>A</Initials>
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<LastName>Kohler</LastName>
<ForeName>Annegret</ForeName>
<Initials>A</Initials>
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<LastName>Symeonidi</LastName>
<ForeName>Aikaterini</ForeName>
<Initials>A</Initials>
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<LastName>Balestrini</LastName>
<ForeName>Raffaella</ForeName>
<Initials>R</Initials>
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<LastName>Charron</LastName>
<ForeName>Philippe</ForeName>
<Initials>P</Initials>
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<LastName>Duensing</LastName>
<ForeName>Nina</ForeName>
<Initials>N</Initials>
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<LastName>Frei dit Frey</LastName>
<ForeName>Nicolas</ForeName>
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<LastName>Gianinazzi-Pearson</LastName>
<ForeName>Vivienne</ForeName>
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<ForeName>Luz B</ForeName>
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<ForeName>Yoshihiro</ForeName>
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<LastName>San Clemente</LastName>
<ForeName>Hélène</ForeName>
<Initials>H</Initials>
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<LastName>Shapiro</LastName>
<ForeName>Harris</ForeName>
<Initials>H</Initials>
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<ForeName>Diederik</ForeName>
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<ForeName>Guillaume</ForeName>
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<LastName>Bonfante</LastName>
<ForeName>Paola</ForeName>
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<LastName>Paszkowski</LastName>
<ForeName>Uta</ForeName>
<Initials>U</Initials>
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<ForeName>Yair Y</ForeName>
<Initials>YY</Initials>
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<LastName>Tuskan</LastName>
<ForeName>Gerald A</ForeName>
<Initials>GA</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Young</LastName>
<ForeName>J Peter W</ForeName>
<Initials>JP</Initials>
</Author>
<Author ValidYN="N">
<LastName>Young</LastName>
<ForeName>Peter W</ForeName>
<Initials>PW</Initials>
</Author>
<Author ValidYN="Y">
<LastName>Sanders</LastName>
<ForeName>Ian R</ForeName>
<Initials>IR</Initials>
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<LastName>Henrissat</LastName>
<ForeName>Bernard</ForeName>
<Initials>B</Initials>
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<LastName>Rensing</LastName>
<ForeName>Stefan A</ForeName>
<Initials>SA</Initials>
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<LastName>Grigoriev</LastName>
<ForeName>Igor V</ForeName>
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<LastName>Martin</LastName>
<ForeName>Francis</ForeName>
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<Language>eng</Language>
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<DataBankName>GENBANK</DataBankName>
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<AccessionNumber>AUPC00000000</AccessionNumber>
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<DataBankName>SRA</DataBankName>
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<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
<PublicationType UI="D013486">Research Support, U.S. Gov't, Non-P.H.S.</PublicationType>
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<Year>2013</Year>
<Month>11</Month>
<Day>25</Day>
</ArticleDate>
</Article>
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<Country>United States</Country>
<MedlineTA>Proc Natl Acad Sci U S A</MedlineTA>
<NlmUniqueID>7505876</NlmUniqueID>
<ISSNLinking>0027-8424</ISSNLinking>
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<RefSource>Proc Natl Acad Sci U S A. 2014 Jan 7;111(1):563</RefSource>
<Note>Young, Peter W [corrected to Young, J Peter W]</Note>
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<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D001483" MajorTopicYN="N">Base Sequence</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D019143" MajorTopicYN="Y">Evolution, Molecular</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D016681" MajorTopicYN="N">Genome, Fungal</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
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<MeshHeading>
<DescriptorName UI="D055137" MajorTopicYN="N">Glomeromycota</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D008969" MajorTopicYN="N">Molecular Sequence Data</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D038821" MajorTopicYN="N">Mycorrhizae</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010944" MajorTopicYN="N">Plants</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D017422" MajorTopicYN="N">Sequence Analysis, DNA</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D013559" MajorTopicYN="N">Symbiosis</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
</MeshHeading>
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<Keyword MajorTopicYN="N">carbohydrate-active enzymes</Keyword>
<Keyword MajorTopicYN="N">effector</Keyword>
<Keyword MajorTopicYN="N">fungal evolution</Keyword>
<Keyword MajorTopicYN="N">glomales</Keyword>
<Keyword MajorTopicYN="N">mutualism</Keyword>
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