Genome sequencing and transcript analysis of Hemileia vastatrix reveal expression dynamics of candidate effectors dependent on host compatibility.
Identifieur interne : 000032 ( Main/Exploration ); précédent : 000031; suivant : 000033Genome sequencing and transcript analysis of Hemileia vastatrix reveal expression dynamics of candidate effectors dependent on host compatibility.
Auteurs : Brenda Neves Porto [Brésil] ; Eveline Teixeira Caixeta [Brésil] ; Sandra Marisa Mathioni [Brésil] ; Pedro Marcus Pereira Vidigal [Brésil] ; Laércio Zambolim [Brésil] ; Eunize Maciel Zambolim [Brésil] ; Nicole Donofrio [États-Unis] ; Shawn W. Polson [États-Unis] ; Thiago Andrade Maia [Brésil] ; Chuming Chen [États-Unis] ; Modupe Adetunji [États-Unis] ; Brewster Kingham [États-Unis] ; Ronaldo José Durigan Dalio [Brésil] ; Mário Lúcio Vilela De Resende [Brésil]Source :
- PloS one [ 1932-6203 ] ; 2019.
Descripteurs français
- KwdFr :
- MESH :
English descriptors
- KwdEn :
- MESH :
- microbiology : Coffea, Plant Diseases.
- physiology : Basidiomycota.
- Gene Expression Profiling, Gene Expression Regulation, Fungal, Genome, Fungal, Host-Pathogen Interactions, Whole Genome Sequencing.
Abstract
Coffee leaf rust caused by the fungus Hemileia vastatrix is one of the most important leaf diseases of coffee plantations worldwide. Current knowledge of the H. vastatrix genome is limited and only a small fraction of the total fungal secretome has been identified. In order to obtain a more comprehensive understanding of its secretome, we aimed to sequence and assemble the entire H. vastatrix genome using two next-generation sequencing platforms and a hybrid assembly strategy. This resulted in a 547 Mb genome of H. vastatrix race XXXIII (Hv33), with 13,364 predicted genes that encode 13,034 putative proteins with transcriptomic support. Based on this proteome, 615 proteins contain putative secretion peptides, and lack transmembrane domains. From this putative secretome, 111 proteins were identified as candidate effectors (EHv33) unique to H. vastatrix, and a subset consisting of 17 EHv33 genes was selected for a temporal gene expression analysis during infection. Five genes were significantly induced early during an incompatible interaction, indicating their potential role as pre-haustorial effectors possibly recognized by the resistant coffee genotype. Another nine genes were significantly induced after haustorium formation in the compatible interaction. Overall, we suggest that this fungus is able to selectively mount its survival strategy with effectors that depend on the host genotype involved in the infection process.
DOI: 10.1371/journal.pone.0215598
PubMed: 30998802
PubMed Central: PMC6472787
Affiliations:
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Neves" sort="Porto, Brenda Neves" uniqKey="Porto B" first="Brenda Neves" last="Porto">Brenda Neves Porto</name><affiliation wicri:level="2"><nlm:affiliation>Programa de Pós-graduação em Biotecnologia Vegetal, Universidade Federal de Lavras, Lavras, Minas Gerais, Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Programa de Pós-graduação em Biotecnologia Vegetal, Universidade Federal de Lavras, Lavras, Minas Gerais</wicri:regionArea><placeName><region type="state">Minas Gerais</region></placeName></affiliation></author><author><name sortKey="Caixeta, Eveline Teixeira" sort="Caixeta, Eveline Teixeira" uniqKey="Caixeta E" first="Eveline Teixeira" last="Caixeta">Eveline Teixeira Caixeta</name><affiliation wicri:level="1"><nlm:affiliation>Empresa Brasileira de Pesquisa Agropecuária (Embrapa-Café), Brasília, Distrito Federal, Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Empresa Brasileira de Pesquisa Agropecuária (Embrapa-Café), Brasília, Distrito Federal</wicri:regionArea><wicri:noRegion>Distrito Federal</wicri:noRegion></affiliation></author><author><name sortKey="Mathioni, Sandra Marisa" sort="Mathioni, Sandra Marisa" uniqKey="Mathioni S" first="Sandra Marisa" last="Mathioni">Sandra Marisa Mathioni</name><affiliation wicri:level="2"><nlm:affiliation>Departamento de Fitopatologia, Universidade Federal de Lavras, Lavras, Minas Gerais, Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Departamento de Fitopatologia, Universidade Federal de Lavras, Lavras, Minas Gerais</wicri:regionArea><placeName><region type="state">Minas Gerais</region></placeName></affiliation></author><author><name sortKey="Vidigal, Pedro Marcus Pereira" sort="Vidigal, Pedro Marcus Pereira" uniqKey="Vidigal P" first="Pedro Marcus Pereira" last="Vidigal">Pedro Marcus Pereira Vidigal</name><affiliation wicri:level="2"><nlm:affiliation>Núcleo de Análises de Biomoléculas, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Núcleo de Análises de Biomoléculas, Universidade Federal de Viçosa, Viçosa, Minas Gerais</wicri:regionArea><placeName><region type="state">Minas Gerais</region></placeName></affiliation></author><author><name sortKey="Zambolim, Laercio" sort="Zambolim, Laercio" uniqKey="Zambolim L" first="Laércio" last="Zambolim">Laércio Zambolim</name><affiliation wicri:level="2"><nlm:affiliation>Departamento de Fitopatologia, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Departamento de Fitopatologia, Universidade Federal de Viçosa, Viçosa, Minas Gerais</wicri:regionArea><placeName><region type="state">Minas Gerais</region></placeName></affiliation></author><author><name sortKey="Zambolim, Eunize Maciel" sort="Zambolim, Eunize Maciel" uniqKey="Zambolim E" first="Eunize Maciel" last="Zambolim">Eunize Maciel Zambolim</name><affiliation wicri:level="2"><nlm:affiliation>Departamento de Fitopatologia, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Departamento de Fitopatologia, Universidade Federal de Viçosa, Viçosa, Minas Gerais</wicri:regionArea><placeName><region type="state">Minas Gerais</region></placeName></affiliation></author><author><name sortKey="Donofrio, Nicole" sort="Donofrio, Nicole" uniqKey="Donofrio N" first="Nicole" last="Donofrio">Nicole Donofrio</name><affiliation wicri:level="2"><nlm:affiliation>Department of Plant and Soil Sciences, University of Delaware, Newark, Delaware, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Plant and Soil Sciences, University of Delaware, Newark, Delaware</wicri:regionArea><placeName><region type="state">Delaware</region></placeName></affiliation></author><author><name sortKey="Polson, Shawn W" sort="Polson, Shawn W" uniqKey="Polson S" first="Shawn W" last="Polson">Shawn W. Polson</name><affiliation wicri:level="2"><nlm:affiliation>Center for Bioinformatics and Computational Biology, Delaware Biotechnology Institute, Newark, Delaware, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Center for Bioinformatics and Computational Biology, Delaware Biotechnology Institute, Newark, Delaware</wicri:regionArea><placeName><region type="state">Delaware</region></placeName></affiliation></author><author><name sortKey="Maia, Thiago Andrade" sort="Maia, Thiago Andrade" uniqKey="Maia T" first="Thiago Andrade" last="Maia">Thiago Andrade Maia</name><affiliation wicri:level="2"><nlm:affiliation>Departamento de Fitopatologia, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Departamento de Fitopatologia, Universidade Federal de Viçosa, Viçosa, Minas Gerais</wicri:regionArea><placeName><region type="state">Minas Gerais</region></placeName></affiliation></author><author><name sortKey="Chen, Chuming" sort="Chen, Chuming" uniqKey="Chen C" first="Chuming" last="Chen">Chuming Chen</name><affiliation wicri:level="2"><nlm:affiliation>Center for Bioinformatics and Computational Biology, Delaware Biotechnology Institute, Newark, Delaware, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Center for Bioinformatics and Computational Biology, Delaware Biotechnology Institute, Newark, Delaware</wicri:regionArea><placeName><region type="state">Delaware</region></placeName></affiliation></author><author><name sortKey="Adetunji, Modupe" sort="Adetunji, Modupe" uniqKey="Adetunji M" first="Modupe" last="Adetunji">Modupe Adetunji</name><affiliation wicri:level="2"><nlm:affiliation>Center for Bioinformatics and Computational Biology, Delaware Biotechnology Institute, Newark, Delaware, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Center for Bioinformatics and Computational Biology, Delaware Biotechnology Institute, Newark, Delaware</wicri:regionArea><placeName><region type="state">Delaware</region></placeName></affiliation></author><author><name sortKey="Kingham, Brewster" sort="Kingham, Brewster" uniqKey="Kingham B" first="Brewster" last="Kingham">Brewster Kingham</name><affiliation wicri:level="2"><nlm:affiliation>Sequencing and Genotyping Center, Delaware Biotechnology Institute, University of Delaware, Newark, Delaware, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Sequencing and Genotyping Center, Delaware Biotechnology Institute, University of Delaware, Newark, Delaware</wicri:regionArea><placeName><region type="state">Delaware</region></placeName></affiliation></author><author><name sortKey="Dalio, Ronaldo Jose Durigan" sort="Dalio, Ronaldo Jose Durigan" uniqKey="Dalio R" first="Ronaldo José Durigan" last="Dalio">Ronaldo José Durigan Dalio</name><affiliation wicri:level="3"><nlm:affiliation>Instituto Agronômico de Campinas, Centro de Citricultura "Sylvio Moreira", Cordeirópolis, São Paulo, Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Instituto Agronômico de Campinas, Centro de Citricultura "Sylvio Moreira", Cordeirópolis, São Paulo</wicri:regionArea><placeName><settlement type="city">São Paulo</settlement><region type="state">État de São Paulo</region></placeName></affiliation></author><author><name sortKey="Resende, Mario Lucio Vilela De" sort="Resende, Mario Lucio Vilela De" uniqKey="Resende M" first="Mário Lúcio Vilela De" last="Resende">Mário Lúcio Vilela De Resende</name><affiliation wicri:level="2"><nlm:affiliation>Departamento de Fitopatologia, Universidade Federal de Lavras, Lavras, Minas Gerais, Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Departamento de Fitopatologia, Universidade Federal de Lavras, Lavras, Minas Gerais</wicri:regionArea><placeName><region type="state">Minas Gerais</region></placeName></affiliation></author></analytic><series><title level="j">PloS one</title><idno type="eISSN">1932-6203</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Basidiomycota (physiology)</term><term>Coffea (microbiology)</term><term>Gene Expression Profiling (MeSH)</term><term>Gene Expression Regulation, Fungal (MeSH)</term><term>Genome, Fungal (MeSH)</term><term>Host-Pathogen Interactions (MeSH)</term><term>Plant Diseases (microbiology)</term><term>Whole Genome Sequencing (MeSH)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Analyse de profil d'expression de gènes (MeSH)</term><term>Basidiomycota (physiologie)</term><term>Coffea (microbiologie)</term><term>Génome fongique (MeSH)</term><term>Interactions hôte-pathogène (MeSH)</term><term>Maladies des plantes (microbiologie)</term><term>Régulation de l'expression des gènes fongiques (MeSH)</term><term>Séquençage du génome entier (MeSH)</term></keywords><keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr"><term>Coffea</term><term>Maladies des plantes</term></keywords><keywords scheme="MESH" qualifier="microbiology" xml:lang="en"><term>Coffea</term><term>Plant Diseases</term></keywords><keywords scheme="MESH" qualifier="physiologie" xml:lang="fr"><term>Basidiomycota</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Basidiomycota</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Gene Expression Profiling</term><term>Gene Expression Regulation, Fungal</term><term>Genome, Fungal</term><term>Host-Pathogen Interactions</term><term>Whole Genome Sequencing</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Analyse de profil d'expression de gènes</term><term>Génome fongique</term><term>Interactions hôte-pathogène</term><term>Régulation de l'expression des gènes fongiques</term><term>Séquençage du génome entier</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Coffee leaf rust caused by the fungus Hemileia vastatrix is one of the most important leaf diseases of coffee plantations worldwide. Current knowledge of the H. vastatrix genome is limited and only a small fraction of the total fungal secretome has been identified. In order to obtain a more comprehensive understanding of its secretome, we aimed to sequence and assemble the entire H. vastatrix genome using two next-generation sequencing platforms and a hybrid assembly strategy. This resulted in a 547 Mb genome of H. vastatrix race XXXIII (Hv33), with 13,364 predicted genes that encode 13,034 putative proteins with transcriptomic support. Based on this proteome, 615 proteins contain putative secretion peptides, and lack transmembrane domains. From this putative secretome, 111 proteins were identified as candidate effectors (EHv33) unique to H. vastatrix, and a subset consisting of 17 EHv33 genes was selected for a temporal gene expression analysis during infection. Five genes were significantly induced early during an incompatible interaction, indicating their potential role as pre-haustorial effectors possibly recognized by the resistant coffee genotype. Another nine genes were significantly induced after haustorium formation in the compatible interaction. Overall, we suggest that this fungus is able to selectively mount its survival strategy with effectors that depend on the host genotype involved in the infection process.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">30998802</PMID><DateCompleted><Year>2020</Year><Month>01</Month><Day>07</Day></DateCompleted><DateRevised><Year>2020</Year><Month>03</Month><Day>09</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Electronic">1932-6203</ISSN><JournalIssue CitedMedium="Internet"><Volume>14</Volume><Issue>4</Issue><PubDate><Year>2019</Year></PubDate></JournalIssue><Title>PloS one</Title><ISOAbbreviation>PLoS One</ISOAbbreviation></Journal><ArticleTitle>Genome sequencing and transcript analysis of Hemileia vastatrix reveal expression dynamics of candidate effectors dependent on host compatibility.</ArticleTitle><Pagination><MedlinePgn>e0215598</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1371/journal.pone.0215598</ELocationID><Abstract><AbstractText>Coffee leaf rust caused by the fungus Hemileia vastatrix is one of the most important leaf diseases of coffee plantations worldwide. Current knowledge of the H. vastatrix genome is limited and only a small fraction of the total fungal secretome has been identified. In order to obtain a more comprehensive understanding of its secretome, we aimed to sequence and assemble the entire H. vastatrix genome using two next-generation sequencing platforms and a hybrid assembly strategy. This resulted in a 547 Mb genome of H. vastatrix race XXXIII (Hv33), with 13,364 predicted genes that encode 13,034 putative proteins with transcriptomic support. Based on this proteome, 615 proteins contain putative secretion peptides, and lack transmembrane domains. From this putative secretome, 111 proteins were identified as candidate effectors (EHv33) unique to H. vastatrix, and a subset consisting of 17 EHv33 genes was selected for a temporal gene expression analysis during infection. Five genes were significantly induced early during an incompatible interaction, indicating their potential role as pre-haustorial effectors possibly recognized by the resistant coffee genotype. Another nine genes were significantly induced after haustorium formation in the compatible interaction. Overall, we suggest that this fungus is able to selectively mount its survival strategy with effectors that depend on the host genotype involved in the infection process.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Porto</LastName><ForeName>Brenda Neves</ForeName><Initials>BN</Initials><AffiliationInfo><Affiliation>Programa de Pós-graduação em Biotecnologia Vegetal, Universidade Federal de Lavras, Lavras, Minas Gerais, Brazil.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Caixeta</LastName><ForeName>Eveline Teixeira</ForeName><Initials>ET</Initials><Identifier Source="ORCID">0000-0001-8850-6273</Identifier><AffiliationInfo><Affiliation>Empresa Brasileira de Pesquisa Agropecuária (Embrapa-Café), Brasília, Distrito Federal, Brazil.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mathioni</LastName><ForeName>Sandra Marisa</ForeName><Initials>SM</Initials><AffiliationInfo><Affiliation>Departamento de Fitopatologia, Universidade Federal de Lavras, Lavras, Minas Gerais, Brazil.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Vidigal</LastName><ForeName>Pedro Marcus Pereira</ForeName><Initials>PMP</Initials><Identifier Source="ORCID">0000-0002-5116-9856</Identifier><AffiliationInfo><Affiliation>Núcleo de Análises de Biomoléculas, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zambolim</LastName><ForeName>Laércio</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Departamento de Fitopatologia, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zambolim</LastName><ForeName>Eunize Maciel</ForeName><Initials>EM</Initials><AffiliationInfo><Affiliation>Departamento de Fitopatologia, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Donofrio</LastName><ForeName>Nicole</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>Department of Plant and Soil Sciences, University of Delaware, Newark, Delaware, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Polson</LastName><ForeName>Shawn W</ForeName><Initials>SW</Initials><AffiliationInfo><Affiliation>Center for Bioinformatics and Computational Biology, Delaware Biotechnology Institute, Newark, Delaware, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Maia</LastName><ForeName>Thiago Andrade</ForeName><Initials>TA</Initials><AffiliationInfo><Affiliation>Departamento de Fitopatologia, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Chen</LastName><ForeName>Chuming</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Center for Bioinformatics and Computational Biology, Delaware Biotechnology Institute, Newark, Delaware, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Adetunji</LastName><ForeName>Modupe</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Center for Bioinformatics and Computational Biology, Delaware Biotechnology Institute, Newark, Delaware, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kingham</LastName><ForeName>Brewster</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>Sequencing and Genotyping Center, Delaware Biotechnology Institute, University of Delaware, Newark, Delaware, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Dalio</LastName><ForeName>Ronaldo José Durigan</ForeName><Initials>RJD</Initials><AffiliationInfo><Affiliation>Instituto Agronômico de Campinas, Centro de Citricultura "Sylvio Moreira", Cordeirópolis, São Paulo, Brazil.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Resende</LastName><ForeName>Mário Lúcio Vilela de</ForeName><Initials>MLV</Initials><AffiliationInfo><Affiliation>Departamento de Fitopatologia, Universidade Federal de Lavras, Lavras, Minas Gerais, Brazil.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><DataBankList CompleteYN="Y"><DataBank><DataBankName>figshare</DataBankName><AccessionNumberList><AccessionNumber>10.6084/m9.figshare.7940411</AccessionNumber></AccessionNumberList></DataBank></DataBankList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>04</Month><Day>18</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>PLoS One</MedlineTA><NlmUniqueID>101285081</NlmUniqueID><ISSNLinking>1932-6203</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D001487" MajorTopicYN="N">Basidiomycota</DescriptorName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D040503" MajorTopicYN="N">Coffea</DescriptorName><QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D020869" MajorTopicYN="Y">Gene Expression Profiling</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D015966" MajorTopicYN="Y">Gene Expression Regulation, Fungal</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D016681" MajorTopicYN="Y">Genome, Fungal</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D054884" MajorTopicYN="Y">Host-Pathogen Interactions</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D010935" MajorTopicYN="N">Plant Diseases</DescriptorName><QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D000073336" MajorTopicYN="Y">Whole Genome Sequencing</DescriptorName></MeshHeading></MeshHeadingList><CoiStatement>The authors have declared that no competing interests exist.</CoiStatement></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2018</Year><Month>11</Month><Day>23</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2019</Year><Month>04</Month><Day>04</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2019</Year><Month>4</Month><Day>19</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2019</Year><Month>4</Month><Day>19</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate 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|texte= Genome sequencing and transcript analysis of Hemileia vastatrix reveal expression dynamics of candidate effectors dependent on host compatibility.
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