Obligate biotrophy features unraveled by the genomic analysis of rust fungi.
Identifieur interne : 000107 ( PubMed/Corpus ); précédent : 000106; suivant : 000108Obligate biotrophy features unraveled by the genomic analysis of rust fungi.
Auteurs : Sébastien Duplessis ; Christina A. Cuomo ; Yao-Cheng Lin ; Andrea Aerts ; Emilie Tisserant ; Claire Veneault-Fourrey ; David L. Joly ; Stéphane Hacquard ; Joëlle Amselem ; Brandi L. Cantarel ; Readman Chiu ; Pedro M. Coutinho ; Nicolas Feau ; Matthew Field ; Pascal Frey ; Eric Gelhaye ; Jonathan Goldberg ; Manfred G. Grabherr ; Chinnappa D. Kodira ; Annegret Kohler ; Ursula Kües ; Erika A. Lindquist ; Susan M. Lucas ; Rohit Mago ; Evan Mauceli ; Emmanuelle Morin ; Claude Murat ; Jasmyn L. Pangilinan ; Robert Park ; Matthew Pearson ; Hadi Quesneville ; Nicolas Rouhier ; Sharadha Sakthikumar ; Asaf A. Salamov ; Jeremy Schmutz ; Benjamin Selles ; Harris Shapiro ; Philippe Tanguay ; Gerald A. Tuskan ; Bernard Henrissat ; Yves Van De Peer ; Pierre Rouzé ; Jeffrey G. Ellis ; Peter N. Dodds ; Jacqueline E. Schein ; Shaobin Zhong ; Richard C. Hamelin ; Igor V. Grigoriev ; Les J. Szabo ; Francis MartinSource :
- Proceedings of the National Academy of Sciences of the United States of America [ 1091-6490 ] ; 2011.
English descriptors
- KwdEn :
- Basidiomycota (genetics), Fungi (genetics), Gene Expression Profiling (MeSH), Genes, Fungal (MeSH), Genome (MeSH), Genome, Fungal (MeSH), Models, Genetic (MeSH), Nitrates (chemistry), Oligonucleotide Array Sequence Analysis (MeSH), Phylogeny (MeSH), Plant Diseases (microbiology), Plant Leaves (microbiology), Sequence Analysis, DNA (MeSH), Sulfates (chemistry), Triticum (microbiology).
- MESH :
- chemical , chemistry : Nitrates, Sulfates.
- genetics : Basidiomycota, Fungi.
- microbiology : Plant Diseases, Plant Leaves, Triticum.
- Gene Expression Profiling, Genes, Fungal, Genome, Genome, Fungal, Models, Genetic, Oligonucleotide Array Sequence Analysis, Phylogeny, Sequence Analysis, DNA.
Abstract
Rust fungi are some of the most devastating pathogens of crop plants. They are obligate biotrophs, which extract nutrients only from living plant tissues and cannot grow apart from their hosts. Their lifestyle has slowed the dissection of molecular mechanisms underlying host invasion and avoidance or suppression of plant innate immunity. We sequenced the 101-Mb genome of Melampsora larici-populina, the causal agent of poplar leaf rust, and the 89-Mb genome of Puccinia graminis f. sp. tritici, the causal agent of wheat and barley stem rust. We then compared the 16,399 predicted proteins of M. larici-populina with the 17,773 predicted proteins of P. graminis f. sp tritici. Genomic features related to their obligate biotrophic lifestyle include expanded lineage-specific gene families, a large repertoire of effector-like small secreted proteins, impaired nitrogen and sulfur assimilation pathways, and expanded families of amino acid and oligopeptide membrane transporters. The dramatic up-regulation of transcripts coding for small secreted proteins, secreted hydrolytic enzymes, and transporters in planta suggests that they play a role in host infection and nutrient acquisition. Some of these genomic hallmarks are mirrored in the genomes of other microbial eukaryotes that have independently evolved to infect plants, indicating convergent adaptation to a biotrophic existence inside plant cells.
DOI: 10.1073/pnas.1019315108
PubMed: 21536894
PubMed Central: PMC3107277
Links to Exploration step
pubmed:21536894Le document en format XML
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<author><name sortKey="Duplessis, Sebastien" sort="Duplessis, Sebastien" uniqKey="Duplessis S" first="Sébastien" last="Duplessis">Sébastien Duplessis</name>
<affiliation><nlm:affiliation>Unité Mixte de Recherche 1136, Institut National de la Recherche Agronomique/Nancy Université, Interactions Arbres/Micro-organismes, Centre de Nancy, 54280 Champenoux, France. duplessi@nancy.inra.fr</nlm:affiliation>
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<author><name sortKey="Cuomo, Christina A" sort="Cuomo, Christina A" uniqKey="Cuomo C" first="Christina A" last="Cuomo">Christina A. Cuomo</name>
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<author><name sortKey="Lin, Yao Cheng" sort="Lin, Yao Cheng" uniqKey="Lin Y" first="Yao-Cheng" last="Lin">Yao-Cheng Lin</name>
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<sourceDesc><biblStruct><analytic><title xml:lang="en">Obligate biotrophy features unraveled by the genomic analysis of rust fungi.</title>
<author><name sortKey="Duplessis, Sebastien" sort="Duplessis, Sebastien" uniqKey="Duplessis S" first="Sébastien" last="Duplessis">Sébastien Duplessis</name>
<affiliation><nlm:affiliation>Unité Mixte de Recherche 1136, Institut National de la Recherche Agronomique/Nancy Université, Interactions Arbres/Micro-organismes, Centre de Nancy, 54280 Champenoux, France. duplessi@nancy.inra.fr</nlm:affiliation>
</affiliation>
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<author><name sortKey="Cuomo, Christina A" sort="Cuomo, Christina A" uniqKey="Cuomo C" first="Christina A" last="Cuomo">Christina A. Cuomo</name>
</author>
<author><name sortKey="Lin, Yao Cheng" sort="Lin, Yao Cheng" uniqKey="Lin Y" first="Yao-Cheng" last="Lin">Yao-Cheng Lin</name>
</author>
<author><name sortKey="Aerts, Andrea" sort="Aerts, Andrea" uniqKey="Aerts A" first="Andrea" last="Aerts">Andrea Aerts</name>
</author>
<author><name sortKey="Tisserant, Emilie" sort="Tisserant, Emilie" uniqKey="Tisserant E" first="Emilie" last="Tisserant">Emilie Tisserant</name>
</author>
<author><name sortKey="Veneault Fourrey, Claire" sort="Veneault Fourrey, Claire" uniqKey="Veneault Fourrey C" first="Claire" last="Veneault-Fourrey">Claire Veneault-Fourrey</name>
</author>
<author><name sortKey="Joly, David L" sort="Joly, David L" uniqKey="Joly D" first="David L" last="Joly">David L. Joly</name>
</author>
<author><name sortKey="Hacquard, Stephane" sort="Hacquard, Stephane" uniqKey="Hacquard S" first="Stéphane" last="Hacquard">Stéphane Hacquard</name>
</author>
<author><name sortKey="Amselem, Joelle" sort="Amselem, Joelle" uniqKey="Amselem J" first="Joëlle" last="Amselem">Joëlle Amselem</name>
</author>
<author><name sortKey="Cantarel, Brandi L" sort="Cantarel, Brandi L" uniqKey="Cantarel B" first="Brandi L" last="Cantarel">Brandi L. Cantarel</name>
</author>
<author><name sortKey="Chiu, Readman" sort="Chiu, Readman" uniqKey="Chiu R" first="Readman" last="Chiu">Readman Chiu</name>
</author>
<author><name sortKey="Coutinho, Pedro M" sort="Coutinho, Pedro M" uniqKey="Coutinho P" first="Pedro M" last="Coutinho">Pedro M. Coutinho</name>
</author>
<author><name sortKey="Feau, Nicolas" sort="Feau, Nicolas" uniqKey="Feau N" first="Nicolas" last="Feau">Nicolas Feau</name>
</author>
<author><name sortKey="Field, Matthew" sort="Field, Matthew" uniqKey="Field M" first="Matthew" last="Field">Matthew Field</name>
</author>
<author><name sortKey="Frey, Pascal" sort="Frey, Pascal" uniqKey="Frey P" first="Pascal" last="Frey">Pascal Frey</name>
</author>
<author><name sortKey="Gelhaye, Eric" sort="Gelhaye, Eric" uniqKey="Gelhaye E" first="Eric" last="Gelhaye">Eric Gelhaye</name>
</author>
<author><name sortKey="Goldberg, Jonathan" sort="Goldberg, Jonathan" uniqKey="Goldberg J" first="Jonathan" last="Goldberg">Jonathan Goldberg</name>
</author>
<author><name sortKey="Grabherr, Manfred G" sort="Grabherr, Manfred G" uniqKey="Grabherr M" first="Manfred G" last="Grabherr">Manfred G. Grabherr</name>
</author>
<author><name sortKey="Kodira, Chinnappa D" sort="Kodira, Chinnappa D" uniqKey="Kodira C" first="Chinnappa D" last="Kodira">Chinnappa D. Kodira</name>
</author>
<author><name sortKey="Kohler, Annegret" sort="Kohler, Annegret" uniqKey="Kohler A" first="Annegret" last="Kohler">Annegret Kohler</name>
</author>
<author><name sortKey="Kues, Ursula" sort="Kues, Ursula" uniqKey="Kues U" first="Ursula" last="Kües">Ursula Kües</name>
</author>
<author><name sortKey="Lindquist, Erika A" sort="Lindquist, Erika A" uniqKey="Lindquist E" first="Erika A" last="Lindquist">Erika A. Lindquist</name>
</author>
<author><name sortKey="Lucas, Susan M" sort="Lucas, Susan M" uniqKey="Lucas S" first="Susan M" last="Lucas">Susan M. Lucas</name>
</author>
<author><name sortKey="Mago, Rohit" sort="Mago, Rohit" uniqKey="Mago R" first="Rohit" last="Mago">Rohit Mago</name>
</author>
<author><name sortKey="Mauceli, Evan" sort="Mauceli, Evan" uniqKey="Mauceli E" first="Evan" last="Mauceli">Evan Mauceli</name>
</author>
<author><name sortKey="Morin, Emmanuelle" sort="Morin, Emmanuelle" uniqKey="Morin E" first="Emmanuelle" last="Morin">Emmanuelle Morin</name>
</author>
<author><name sortKey="Murat, Claude" sort="Murat, Claude" uniqKey="Murat C" first="Claude" last="Murat">Claude Murat</name>
</author>
<author><name sortKey="Pangilinan, Jasmyn L" sort="Pangilinan, Jasmyn L" uniqKey="Pangilinan J" first="Jasmyn L" last="Pangilinan">Jasmyn L. Pangilinan</name>
</author>
<author><name sortKey="Park, Robert" sort="Park, Robert" uniqKey="Park R" first="Robert" last="Park">Robert Park</name>
</author>
<author><name sortKey="Pearson, Matthew" sort="Pearson, Matthew" uniqKey="Pearson M" first="Matthew" last="Pearson">Matthew Pearson</name>
</author>
<author><name sortKey="Quesneville, Hadi" sort="Quesneville, Hadi" uniqKey="Quesneville H" first="Hadi" last="Quesneville">Hadi Quesneville</name>
</author>
<author><name sortKey="Rouhier, Nicolas" sort="Rouhier, Nicolas" uniqKey="Rouhier N" first="Nicolas" last="Rouhier">Nicolas Rouhier</name>
</author>
<author><name sortKey="Sakthikumar, Sharadha" sort="Sakthikumar, Sharadha" uniqKey="Sakthikumar S" first="Sharadha" last="Sakthikumar">Sharadha Sakthikumar</name>
</author>
<author><name sortKey="Salamov, Asaf A" sort="Salamov, Asaf A" uniqKey="Salamov A" first="Asaf A" last="Salamov">Asaf A. Salamov</name>
</author>
<author><name sortKey="Schmutz, Jeremy" sort="Schmutz, Jeremy" uniqKey="Schmutz J" first="Jeremy" last="Schmutz">Jeremy Schmutz</name>
</author>
<author><name sortKey="Selles, Benjamin" sort="Selles, Benjamin" uniqKey="Selles B" first="Benjamin" last="Selles">Benjamin Selles</name>
</author>
<author><name sortKey="Shapiro, Harris" sort="Shapiro, Harris" uniqKey="Shapiro H" first="Harris" last="Shapiro">Harris Shapiro</name>
</author>
<author><name sortKey="Tanguay, Philippe" sort="Tanguay, Philippe" uniqKey="Tanguay P" first="Philippe" last="Tanguay">Philippe Tanguay</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="Henrissat, Bernard" sort="Henrissat, Bernard" uniqKey="Henrissat B" first="Bernard" last="Henrissat">Bernard Henrissat</name>
</author>
<author><name sortKey="Van De Peer, Yves" sort="Van De Peer, Yves" uniqKey="Van De Peer Y" first="Yves" last="Van De Peer">Yves Van De Peer</name>
</author>
<author><name sortKey="Rouze, Pierre" sort="Rouze, Pierre" uniqKey="Rouze P" first="Pierre" last="Rouzé">Pierre Rouzé</name>
</author>
<author><name sortKey="Ellis, Jeffrey G" sort="Ellis, Jeffrey G" uniqKey="Ellis J" first="Jeffrey G" last="Ellis">Jeffrey G. Ellis</name>
</author>
<author><name sortKey="Dodds, Peter N" sort="Dodds, Peter N" uniqKey="Dodds P" first="Peter N" last="Dodds">Peter N. Dodds</name>
</author>
<author><name sortKey="Schein, Jacqueline E" sort="Schein, Jacqueline E" uniqKey="Schein J" first="Jacqueline E" last="Schein">Jacqueline E. Schein</name>
</author>
<author><name sortKey="Zhong, Shaobin" sort="Zhong, Shaobin" uniqKey="Zhong S" first="Shaobin" last="Zhong">Shaobin Zhong</name>
</author>
<author><name sortKey="Hamelin, Richard C" sort="Hamelin, Richard C" uniqKey="Hamelin R" first="Richard C" last="Hamelin">Richard C. Hamelin</name>
</author>
<author><name sortKey="Grigoriev, Igor V" sort="Grigoriev, Igor V" uniqKey="Grigoriev I" first="Igor V" last="Grigoriev">Igor V. Grigoriev</name>
</author>
<author><name sortKey="Szabo, Les J" sort="Szabo, Les J" uniqKey="Szabo L" first="Les J" last="Szabo">Les J. Szabo</name>
</author>
<author><name sortKey="Martin, Francis" sort="Martin, Francis" uniqKey="Martin F" first="Francis" last="Martin">Francis Martin</name>
</author>
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<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="2011" type="published">2011</date>
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<profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Basidiomycota (genetics)</term>
<term>Fungi (genetics)</term>
<term>Gene Expression Profiling (MeSH)</term>
<term>Genes, Fungal (MeSH)</term>
<term>Genome (MeSH)</term>
<term>Genome, Fungal (MeSH)</term>
<term>Models, Genetic (MeSH)</term>
<term>Nitrates (chemistry)</term>
<term>Oligonucleotide Array Sequence Analysis (MeSH)</term>
<term>Phylogeny (MeSH)</term>
<term>Plant Diseases (microbiology)</term>
<term>Plant Leaves (microbiology)</term>
<term>Sequence Analysis, DNA (MeSH)</term>
<term>Sulfates (chemistry)</term>
<term>Triticum (microbiology)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en"><term>Nitrates</term>
<term>Sulfates</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Basidiomycota</term>
<term>Fungi</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en"><term>Plant Diseases</term>
<term>Plant Leaves</term>
<term>Triticum</term>
</keywords>
<keywords scheme="MESH" xml:lang="en"><term>Gene Expression Profiling</term>
<term>Genes, Fungal</term>
<term>Genome</term>
<term>Genome, Fungal</term>
<term>Models, Genetic</term>
<term>Oligonucleotide Array Sequence Analysis</term>
<term>Phylogeny</term>
<term>Sequence Analysis, DNA</term>
</keywords>
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<front><div type="abstract" xml:lang="en">Rust fungi are some of the most devastating pathogens of crop plants. They are obligate biotrophs, which extract nutrients only from living plant tissues and cannot grow apart from their hosts. Their lifestyle has slowed the dissection of molecular mechanisms underlying host invasion and avoidance or suppression of plant innate immunity. We sequenced the 101-Mb genome of Melampsora larici-populina, the causal agent of poplar leaf rust, and the 89-Mb genome of Puccinia graminis f. sp. tritici, the causal agent of wheat and barley stem rust. We then compared the 16,399 predicted proteins of M. larici-populina with the 17,773 predicted proteins of P. graminis f. sp tritici. Genomic features related to their obligate biotrophic lifestyle include expanded lineage-specific gene families, a large repertoire of effector-like small secreted proteins, impaired nitrogen and sulfur assimilation pathways, and expanded families of amino acid and oligopeptide membrane transporters. The dramatic up-regulation of transcripts coding for small secreted proteins, secreted hydrolytic enzymes, and transporters in planta suggests that they play a role in host infection and nutrient acquisition. Some of these genomic hallmarks are mirrored in the genomes of other microbial eukaryotes that have independently evolved to infect plants, indicating convergent adaptation to a biotrophic existence inside plant cells.</div>
</front>
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<Month>08</Month>
<Day>23</Day>
</DateCompleted>
<DateRevised><Year>2018</Year>
<Month>11</Month>
<Day>13</Day>
</DateRevised>
<Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1091-6490</ISSN>
<JournalIssue CitedMedium="Internet"><Volume>108</Volume>
<Issue>22</Issue>
<PubDate><Year>2011</Year>
<Month>May</Month>
<Day>31</Day>
</PubDate>
</JournalIssue>
<Title>Proceedings of the National Academy of Sciences of the United States of America</Title>
<ISOAbbreviation>Proc Natl Acad Sci U S A</ISOAbbreviation>
</Journal>
<ArticleTitle>Obligate biotrophy features unraveled by the genomic analysis of rust fungi.</ArticleTitle>
<Pagination><MedlinePgn>9166-71</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1073/pnas.1019315108</ELocationID>
<Abstract><AbstractText>Rust fungi are some of the most devastating pathogens of crop plants. They are obligate biotrophs, which extract nutrients only from living plant tissues and cannot grow apart from their hosts. Their lifestyle has slowed the dissection of molecular mechanisms underlying host invasion and avoidance or suppression of plant innate immunity. We sequenced the 101-Mb genome of Melampsora larici-populina, the causal agent of poplar leaf rust, and the 89-Mb genome of Puccinia graminis f. sp. tritici, the causal agent of wheat and barley stem rust. We then compared the 16,399 predicted proteins of M. larici-populina with the 17,773 predicted proteins of P. graminis f. sp tritici. Genomic features related to their obligate biotrophic lifestyle include expanded lineage-specific gene families, a large repertoire of effector-like small secreted proteins, impaired nitrogen and sulfur assimilation pathways, and expanded families of amino acid and oligopeptide membrane transporters. The dramatic up-regulation of transcripts coding for small secreted proteins, secreted hydrolytic enzymes, and transporters in planta suggests that they play a role in host infection and nutrient acquisition. Some of these genomic hallmarks are mirrored in the genomes of other microbial eukaryotes that have independently evolved to infect plants, indicating convergent adaptation to a biotrophic existence inside plant cells.</AbstractText>
</Abstract>
<AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Duplessis</LastName>
<ForeName>Sébastien</ForeName>
<Initials>S</Initials>
<AffiliationInfo><Affiliation>Unité Mixte de Recherche 1136, Institut National de la Recherche Agronomique/Nancy Université, Interactions Arbres/Micro-organismes, Centre de Nancy, 54280 Champenoux, France. duplessi@nancy.inra.fr</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Cuomo</LastName>
<ForeName>Christina A</ForeName>
<Initials>CA</Initials>
</Author>
<Author ValidYN="Y"><LastName>Lin</LastName>
<ForeName>Yao-Cheng</ForeName>
<Initials>YC</Initials>
</Author>
<Author ValidYN="Y"><LastName>Aerts</LastName>
<ForeName>Andrea</ForeName>
<Initials>A</Initials>
</Author>
<Author ValidYN="Y"><LastName>Tisserant</LastName>
<ForeName>Emilie</ForeName>
<Initials>E</Initials>
</Author>
<Author ValidYN="Y"><LastName>Veneault-Fourrey</LastName>
<ForeName>Claire</ForeName>
<Initials>C</Initials>
</Author>
<Author ValidYN="Y"><LastName>Joly</LastName>
<ForeName>David L</ForeName>
<Initials>DL</Initials>
</Author>
<Author ValidYN="Y"><LastName>Hacquard</LastName>
<ForeName>Stéphane</ForeName>
<Initials>S</Initials>
</Author>
<Author ValidYN="Y"><LastName>Amselem</LastName>
<ForeName>Joëlle</ForeName>
<Initials>J</Initials>
</Author>
<Author ValidYN="Y"><LastName>Cantarel</LastName>
<ForeName>Brandi L</ForeName>
<Initials>BL</Initials>
</Author>
<Author ValidYN="Y"><LastName>Chiu</LastName>
<ForeName>Readman</ForeName>
<Initials>R</Initials>
</Author>
<Author ValidYN="Y"><LastName>Coutinho</LastName>
<ForeName>Pedro M</ForeName>
<Initials>PM</Initials>
</Author>
<Author ValidYN="Y"><LastName>Feau</LastName>
<ForeName>Nicolas</ForeName>
<Initials>N</Initials>
</Author>
<Author ValidYN="Y"><LastName>Field</LastName>
<ForeName>Matthew</ForeName>
<Initials>M</Initials>
</Author>
<Author ValidYN="Y"><LastName>Frey</LastName>
<ForeName>Pascal</ForeName>
<Initials>P</Initials>
</Author>
<Author ValidYN="Y"><LastName>Gelhaye</LastName>
<ForeName>Eric</ForeName>
<Initials>E</Initials>
</Author>
<Author ValidYN="Y"><LastName>Goldberg</LastName>
<ForeName>Jonathan</ForeName>
<Initials>J</Initials>
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<Initials>MG</Initials>
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<ForeName>Chinnappa D</ForeName>
<Initials>CD</Initials>
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<Author ValidYN="Y"><LastName>Kohler</LastName>
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<Initials>A</Initials>
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<Initials>U</Initials>
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<Initials>M</Initials>
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<Initials>H</Initials>
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<Initials>N</Initials>
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<Author ValidYN="Y"><LastName>Sakthikumar</LastName>
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<Initials>S</Initials>
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<Initials>AA</Initials>
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<Initials>B</Initials>
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<Initials>H</Initials>
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<Initials>GA</Initials>
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<Initials>Y</Initials>
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<Author ValidYN="Y"><LastName>Rouzé</LastName>
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<Initials>P</Initials>
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<Author ValidYN="Y"><LastName>Ellis</LastName>
<ForeName>Jeffrey G</ForeName>
<Initials>JG</Initials>
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<Author ValidYN="Y"><LastName>Dodds</LastName>
<ForeName>Peter N</ForeName>
<Initials>PN</Initials>
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<Author ValidYN="Y"><LastName>Schein</LastName>
<ForeName>Jacqueline E</ForeName>
<Initials>JE</Initials>
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<Author ValidYN="Y"><LastName>Zhong</LastName>
<ForeName>Shaobin</ForeName>
<Initials>S</Initials>
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<Initials>RC</Initials>
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<Initials>IV</Initials>
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<Author ValidYN="Y"><LastName>Martin</LastName>
<ForeName>Francis</ForeName>
<Initials>F</Initials>
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</AuthorList>
<Language>eng</Language>
<DataBankList CompleteYN="Y"><DataBank><DataBankName>GEO</DataBankName>
<AccessionNumberList><AccessionNumber>GSE23097</AccessionNumber>
<AccessionNumber>GSE25020</AccessionNumber>
</AccessionNumberList>
</DataBank>
</DataBankList>
<PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType>
<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>
</PublicationTypeList>
<ArticleDate DateType="Electronic"><Year>2011</Year>
<Month>05</Month>
<Day>02</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo><Country>United States</Country>
<MedlineTA>Proc Natl Acad Sci U S A</MedlineTA>
<NlmUniqueID>7505876</NlmUniqueID>
<ISSNLinking>0027-8424</ISSNLinking>
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<ChemicalList><Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D009566">Nitrates</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D013431">Sulfates</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<CommentsCorrectionsList><CommentsCorrections RefType="CommentIn"><RefSource>Proc Natl Acad Sci U S A. 2011 May 31;108(22):8921-2</RefSource>
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<MeshHeadingList><MeshHeading><DescriptorName UI="D001487" MajorTopicYN="N">Basidiomycota</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D005658" MajorTopicYN="N">Fungi</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D020869" MajorTopicYN="N">Gene Expression Profiling</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D005800" MajorTopicYN="N">Genes, Fungal</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D016678" MajorTopicYN="N">Genome</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D016681" MajorTopicYN="N">Genome, Fungal</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D008957" MajorTopicYN="N">Models, Genetic</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D009566" MajorTopicYN="N">Nitrates</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D020411" MajorTopicYN="N">Oligonucleotide Array Sequence Analysis</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D010802" MajorTopicYN="N">Phylogeny</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D010935" MajorTopicYN="N">Plant Diseases</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D018515" MajorTopicYN="N">Plant Leaves</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D017422" MajorTopicYN="N">Sequence Analysis, DNA</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D013431" MajorTopicYN="N">Sulfates</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D014908" MajorTopicYN="N">Triticum</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
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