Genomic Investigation of the Strawberry Pathogen Phytophthora fragariae Indicates Pathogenicity Is Associated With Transcriptional Variation in Three Key Races.
Identifieur interne : 000176 ( Main/Exploration ); précédent : 000175; suivant : 000177Genomic Investigation of the Strawberry Pathogen Phytophthora fragariae Indicates Pathogenicity Is Associated With Transcriptional Variation in Three Key Races.
Auteurs : Thomas M. Adams [Royaume-Uni] ; Andrew D. Armitage [Royaume-Uni] ; Maria K. Sobczyk [Royaume-Uni] ; Helen J. Bates [Royaume-Uni] ; Javier F. Tabima [États-Unis] ; Brent A. Kronmiller [États-Unis] ; Brett M. Tyler [États-Unis] ; Niklaus J. Grünwald [États-Unis] ; Jim M. Dunwell [Royaume-Uni] ; Charlotte F. Nellist [Royaume-Uni] ; Richard J. Harrison [Royaume-Uni]Source :
- Frontiers in microbiology [ 1664-302X ] ; 2020.
Abstract
The oomycete Phytophthora fragariae is a highly destructive pathogen of cultivated strawberry (Fragaria × ananassa), causing the root rotting disease, "red core". The host-pathogen interaction has a well described gene-for-gene resistance relationship, but to date neither candidate avirulence nor resistance genes have been identified. We sequenced a set of American, Canadian, and United Kingdom isolates of known race type, along with three representatives of the closely related pathogen of the raspberry (Rubus idaeus), P. rubi, and found a clear population structure, with a high degree of nucleotide divergence seen between some race types and abundant private variation associated with race types 4 and 5. In contrast, between isolates defined as United Kingdom races 1, 2, and 3 (UK1-2-3) there was no evidence of gene loss or gain; or the presence of insertions/deletions (INDELs) or Single Nucleotide Polymorphisms (SNPs) within or in proximity to putative pathogenicity genes could be found associated with race variation. Transcriptomic analysis of representative UK1-2-3 isolates revealed abundant expression variation in key effector family genes associated with pathogen race; however, further long read sequencing did not reveal any long range polymorphisms to be associated with avirulence to race UK2 or UK3 resistance, suggesting either control in trans or other stable forms of epigenetic modification modulating gene expression. This work reveals the combined power of population resequencing to uncover race structure in pathosystems and in planta transcriptomic analysis to identify candidate avirulence genes. This work has implications for the identification of putative avirulence genes in the absence of associated expression data and points toward the need for detailed molecular characterisation of mechanisms of effector regulation and silencing in oomycete plant pathogens.
DOI: 10.3389/fmicb.2020.00490
PubMed: 32351458
PubMed Central: PMC7174552
Affiliations:
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Adams</name><affiliation wicri:level="1"><nlm:affiliation>Department of Genetics, Genomics and Breeding, NIAB EMR, Kent, United Kingdom.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Department of Genetics, Genomics and Breeding, NIAB EMR, Kent</wicri:regionArea><wicri:noRegion>Kent</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>School of Agriculture, Policy and Development, University of Reading, Reading, United Kingdom.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>School of Agriculture, Policy and Development, University of Reading, Reading</wicri:regionArea><wicri:noRegion>Reading</wicri:noRegion></affiliation></author><author><name sortKey="Armitage, Andrew D" sort="Armitage, Andrew D" uniqKey="Armitage A" first="Andrew D" last="Armitage">Andrew D. 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Bates</name><affiliation wicri:level="1"><nlm:affiliation>Department of Genetics, Genomics and Breeding, NIAB EMR, Kent, United Kingdom.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Department of Genetics, Genomics and Breeding, NIAB EMR, Kent</wicri:regionArea><wicri:noRegion>Kent</wicri:noRegion></affiliation></author><author><name sortKey="Tabima, Javier F" sort="Tabima, Javier F" uniqKey="Tabima J" first="Javier F" last="Tabima">Javier F. Tabima</name><affiliation wicri:level="2"><nlm:affiliation>Department of Botany and Plant Pathology, Center for Genome Biology and Biocomputing, Oregon State University, Corvallis, OR, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Botany and Plant Pathology, Center for Genome Biology and Biocomputing, Oregon State University, Corvallis, OR</wicri:regionArea><placeName><region type="state">Oregon</region></placeName></affiliation></author><author><name sortKey="Kronmiller, Brent A" sort="Kronmiller, Brent A" uniqKey="Kronmiller B" first="Brent A" last="Kronmiller">Brent A. Kronmiller</name><affiliation wicri:level="2"><nlm:affiliation>Center for Genome Biology and Biocomputing, Oregon State University, Corvallis, OR, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Center for Genome Biology and Biocomputing, Oregon State University, Corvallis, OR</wicri:regionArea><placeName><region type="state">Oregon</region></placeName></affiliation></author><author><name sortKey="Tyler, Brett M" sort="Tyler, Brett M" uniqKey="Tyler B" first="Brett M" last="Tyler">Brett M. Tyler</name><affiliation wicri:level="2"><nlm:affiliation>Department of Botany and Plant Pathology, Center for Genome Biology and Biocomputing, Oregon State University, Corvallis, OR, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Botany and Plant Pathology, Center for Genome Biology and Biocomputing, Oregon State University, Corvallis, OR</wicri:regionArea><placeName><region type="state">Oregon</region></placeName></affiliation><affiliation wicri:level="2"><nlm:affiliation>Center for Genome Biology and Biocomputing, Oregon State University, Corvallis, OR, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Center for Genome Biology and Biocomputing, Oregon State University, Corvallis, OR</wicri:regionArea><placeName><region type="state">Oregon</region></placeName></affiliation></author><author><name sortKey="Grunwald, Niklaus J" sort="Grunwald, Niklaus J" uniqKey="Grunwald N" first="Niklaus J" last="Grünwald">Niklaus J. Grünwald</name><affiliation wicri:level="2"><nlm:affiliation>Horticultural Crops Research Unit, Agricultural Research Service, United States Department of Agriculture, Corvallis, OR, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Horticultural Crops Research Unit, Agricultural Research Service, United States Department of Agriculture, Corvallis, OR</wicri:regionArea><placeName><region type="state">Oregon</region></placeName></affiliation></author><author><name sortKey="Dunwell, Jim M" sort="Dunwell, Jim M" uniqKey="Dunwell J" first="Jim M" last="Dunwell">Jim M. Dunwell</name><affiliation wicri:level="1"><nlm:affiliation>School of Agriculture, Policy and Development, University of Reading, Reading, United Kingdom.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>School of Agriculture, Policy and Development, University of Reading, Reading</wicri:regionArea><wicri:noRegion>Reading</wicri:noRegion></affiliation></author><author><name sortKey="Nellist, Charlotte F" sort="Nellist, Charlotte F" uniqKey="Nellist C" first="Charlotte F" last="Nellist">Charlotte F. Nellist</name><affiliation wicri:level="1"><nlm:affiliation>Department of Genetics, Genomics and Breeding, NIAB EMR, Kent, United Kingdom.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Department of Genetics, Genomics and Breeding, NIAB EMR, Kent</wicri:regionArea><wicri:noRegion>Kent</wicri:noRegion></affiliation></author><author><name sortKey="Harrison, Richard J" sort="Harrison, Richard J" uniqKey="Harrison R" first="Richard J" last="Harrison">Richard J. Harrison</name><affiliation wicri:level="1"><nlm:affiliation>Department of Genetics, Genomics and Breeding, NIAB EMR, Kent, United Kingdom.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Department of Genetics, Genomics and Breeding, NIAB EMR, Kent</wicri:regionArea><wicri:noRegion>Kent</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>NIAB Cambridge Crop Research, NIAB, Cambridge, United Kingdom.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>NIAB Cambridge Crop Research, NIAB, Cambridge</wicri:regionArea><wicri:noRegion>Cambridge</wicri:noRegion></affiliation></author></analytic><series><title level="j">Frontiers in microbiology</title><idno type="ISSN">1664-302X</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">The oomycete <i>Phytophthora fragariae</i> is a highly destructive pathogen of cultivated strawberry (<i>Fragaria</i> × <i>ananassa</i>), causing the root rotting disease, "red core". The host-pathogen interaction has a well described gene-for-gene resistance relationship, but to date neither candidate avirulence nor resistance genes have been identified. We sequenced a set of American, Canadian, and United Kingdom isolates of known race type, along with three representatives of the closely related pathogen of the raspberry (<i>Rubus idaeus</i>), <i>P. rubi</i>, and found a clear population structure, with a high degree of nucleotide divergence seen between some race types and abundant private variation associated with race types 4 and 5. In contrast, between isolates defined as United Kingdom races 1, 2, and 3 (UK1-2-3) there was no evidence of gene loss or gain; or the presence of insertions/deletions (INDELs) or Single Nucleotide Polymorphisms (SNPs) within or in proximity to putative pathogenicity genes could be found associated with race variation. Transcriptomic analysis of representative UK1-2-3 isolates revealed abundant expression variation in key effector family genes associated with pathogen race; however, further long read sequencing did not reveal any long range polymorphisms to be associated with avirulence to race UK2 or UK3 resistance, suggesting either control in <i>trans</i> or other stable forms of epigenetic modification modulating gene expression. This work reveals the combined power of population resequencing to uncover race structure in pathosystems and <i>in planta</i> transcriptomic analysis to identify candidate avirulence genes. This work has implications for the identification of putative avirulence genes in the absence of associated expression data and points toward the need for detailed molecular characterisation of mechanisms of effector regulation and silencing in oomycete plant pathogens.</div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">32351458</PMID><DateRevised><Year>2020</Year><Month>09</Month><Day>28</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">1664-302X</ISSN><JournalIssue CitedMedium="Print"><Volume>11</Volume><PubDate><Year>2020</Year></PubDate></JournalIssue><Title>Frontiers in microbiology</Title><ISOAbbreviation>Front Microbiol</ISOAbbreviation></Journal><ArticleTitle>Genomic Investigation of the Strawberry Pathogen <i>Phytophthora fragariae</i> Indicates Pathogenicity Is Associated With Transcriptional Variation in Three Key Races.</ArticleTitle><Pagination><MedlinePgn>490</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.3389/fmicb.2020.00490</ELocationID><Abstract><AbstractText>The oomycete <i>Phytophthora fragariae</i> is a highly destructive pathogen of cultivated strawberry (<i>Fragaria</i> × <i>ananassa</i>), causing the root rotting disease, "red core". The host-pathogen interaction has a well described gene-for-gene resistance relationship, but to date neither candidate avirulence nor resistance genes have been identified. We sequenced a set of American, Canadian, and United Kingdom isolates of known race type, along with three representatives of the closely related pathogen of the raspberry (<i>Rubus idaeus</i>), <i>P. rubi</i>, and found a clear population structure, with a high degree of nucleotide divergence seen between some race types and abundant private variation associated with race types 4 and 5. In contrast, between isolates defined as United Kingdom races 1, 2, and 3 (UK1-2-3) there was no evidence of gene loss or gain; or the presence of insertions/deletions (INDELs) or Single Nucleotide Polymorphisms (SNPs) within or in proximity to putative pathogenicity genes could be found associated with race variation. Transcriptomic analysis of representative UK1-2-3 isolates revealed abundant expression variation in key effector family genes associated with pathogen race; however, further long read sequencing did not reveal any long range polymorphisms to be associated with avirulence to race UK2 or UK3 resistance, suggesting either control in <i>trans</i> or other stable forms of epigenetic modification modulating gene expression. This work reveals the combined power of population resequencing to uncover race structure in pathosystems and <i>in planta</i> transcriptomic analysis to identify candidate avirulence genes. This work has implications for the identification of putative avirulence genes in the absence of associated expression data and points toward the need for detailed molecular characterisation of mechanisms of effector regulation and silencing in oomycete plant pathogens.</AbstractText><CopyrightInformation>Copyright © 2020 Adams, Armitage, Sobczyk, Bates, Tabima, Kronmiller, Tyler, Grünwald, Dunwell, Nellist and Harrison.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Adams</LastName><ForeName>Thomas M</ForeName><Initials>TM</Initials><AffiliationInfo><Affiliation>Department of Genetics, Genomics and Breeding, NIAB EMR, Kent, United Kingdom.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>School of Agriculture, Policy and Development, University of Reading, Reading, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Armitage</LastName><ForeName>Andrew D</ForeName><Initials>AD</Initials><AffiliationInfo><Affiliation>Department of Genetics, Genomics and Breeding, NIAB EMR, Kent, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sobczyk</LastName><ForeName>Maria K</ForeName><Initials>MK</Initials><AffiliationInfo><Affiliation>Department of Genetics, Genomics and Breeding, NIAB EMR, Kent, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bates</LastName><ForeName>Helen J</ForeName><Initials>HJ</Initials><AffiliationInfo><Affiliation>Department of Genetics, Genomics and Breeding, NIAB EMR, Kent, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tabima</LastName><ForeName>Javier F</ForeName><Initials>JF</Initials><AffiliationInfo><Affiliation>Department of Botany and Plant Pathology, Center for Genome Biology and Biocomputing, Oregon State University, Corvallis, OR, United States.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kronmiller</LastName><ForeName>Brent A</ForeName><Initials>BA</Initials><AffiliationInfo><Affiliation>Center for Genome Biology and Biocomputing, Oregon State University, Corvallis, OR, United States.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tyler</LastName><ForeName>Brett M</ForeName><Initials>BM</Initials><AffiliationInfo><Affiliation>Department of Botany and Plant Pathology, Center for Genome Biology and Biocomputing, Oregon State University, Corvallis, OR, United States.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Center for Genome Biology and Biocomputing, Oregon State University, Corvallis, OR, United States.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Grünwald</LastName><ForeName>Niklaus J</ForeName><Initials>NJ</Initials><AffiliationInfo><Affiliation>Horticultural Crops Research Unit, Agricultural Research Service, United States Department of Agriculture, Corvallis, OR, United States.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Dunwell</LastName><ForeName>Jim M</ForeName><Initials>JM</Initials><AffiliationInfo><Affiliation>School of Agriculture, Policy and Development, University of Reading, Reading, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Nellist</LastName><ForeName>Charlotte F</ForeName><Initials>CF</Initials><AffiliationInfo><Affiliation>Department of Genetics, Genomics and Breeding, NIAB EMR, Kent, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Harrison</LastName><ForeName>Richard J</ForeName><Initials>RJ</Initials><AffiliationInfo><Affiliation>Department of Genetics, Genomics and Breeding, NIAB EMR, Kent, United Kingdom.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>NIAB Cambridge Crop Research, NIAB, Cambridge, United Kingdom.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>04</Month><Day>15</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Front Microbiol</MedlineTA><NlmUniqueID>101548977</NlmUniqueID><ISSNLinking>1664-302X</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">RNA-Seq</Keyword><Keyword MajorTopicYN="N">host–microbe interactions</Keyword><Keyword MajorTopicYN="N">nanopore sequencing</Keyword><Keyword MajorTopicYN="N">oomycete</Keyword><Keyword MajorTopicYN="N">population resequencing</Keyword><Keyword MajorTopicYN="N">race structure</Keyword><Keyword MajorTopicYN="N">red core</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>11</Month><Day>30</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>03</Month><Day>06</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>5</Month><Day>1</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>5</Month><Day>1</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>5</Month><Day>1</Day><Hour>6</Hour><Minute>1</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32351458</ArticleId><ArticleId IdType="doi">10.3389/fmicb.2020.00490</ArticleId><ArticleId IdType="pmc">PMC7174552</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>Royaume-Uni</li><li>États-Unis</li></country><region><li>Oregon</li></region></list><tree><country name="Royaume-Uni"><noRegion><name sortKey="Adams, Thomas M" sort="Adams, Thomas M" uniqKey="Adams T" first="Thomas M" last="Adams">Thomas M. Adams</name></noRegion><name sortKey="Adams, Thomas M" sort="Adams, Thomas M" uniqKey="Adams T" first="Thomas M" last="Adams">Thomas M. Adams</name><name sortKey="Armitage, Andrew D" sort="Armitage, Andrew D" uniqKey="Armitage A" first="Andrew D" last="Armitage">Andrew D. Armitage</name><name sortKey="Bates, Helen J" sort="Bates, Helen J" uniqKey="Bates H" first="Helen J" last="Bates">Helen J. Bates</name><name sortKey="Dunwell, Jim M" sort="Dunwell, Jim M" uniqKey="Dunwell J" first="Jim M" last="Dunwell">Jim M. Dunwell</name><name sortKey="Harrison, Richard J" sort="Harrison, Richard J" uniqKey="Harrison R" first="Richard J" last="Harrison">Richard J. Harrison</name><name sortKey="Harrison, Richard J" sort="Harrison, Richard J" uniqKey="Harrison R" first="Richard J" last="Harrison">Richard J. Harrison</name><name sortKey="Nellist, Charlotte F" sort="Nellist, Charlotte F" uniqKey="Nellist C" first="Charlotte F" last="Nellist">Charlotte F. Nellist</name><name sortKey="Sobczyk, Maria K" sort="Sobczyk, Maria K" uniqKey="Sobczyk M" first="Maria K" last="Sobczyk">Maria K. Sobczyk</name></country><country name="États-Unis"><region name="Oregon"><name sortKey="Tabima, Javier F" sort="Tabima, Javier F" uniqKey="Tabima J" first="Javier F" last="Tabima">Javier F. Tabima</name></region><name sortKey="Grunwald, Niklaus J" sort="Grunwald, Niklaus J" uniqKey="Grunwald N" first="Niklaus J" last="Grünwald">Niklaus J. Grünwald</name><name sortKey="Kronmiller, Brent A" sort="Kronmiller, Brent A" uniqKey="Kronmiller B" first="Brent A" last="Kronmiller">Brent A. Kronmiller</name><name sortKey="Tyler, Brett M" sort="Tyler, Brett M" uniqKey="Tyler B" first="Brett M" last="Tyler">Brett M. Tyler</name><name sortKey="Tyler, Brett M" sort="Tyler, Brett M" uniqKey="Tyler B" first="Brett M" last="Tyler">Brett M. Tyler</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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