Pathogen enrichment sequencing (PenSeq) enables population genomic studies in oomycetes.
Identifieur interne : 000429 ( Main/Exploration ); précédent : 000428; suivant : 000430Pathogen enrichment sequencing (PenSeq) enables population genomic studies in oomycetes.
Auteurs : Gaetan J A. Thilliez [Royaume-Uni] ; Miles R. Armstrong [Royaume-Uni] ; Tze-Yin Lim [Royaume-Uni] ; Katie Baker [Royaume-Uni] ; Agathe Jouet [Royaume-Uni] ; Ben Ward [Royaume-Uni] ; Cock Van Oosterhout [Royaume-Uni] ; Jonathan D G. Jones [Royaume-Uni] ; Edgar Huitema [Royaume-Uni] ; Paul R J. Birch [Royaume-Uni] ; Ingo Hein [Royaume-Uni]Source :
- The New phytologist [ 1469-8137 ] ; 2019.
Descripteurs français
- KwdFr :
- Allèles (MeSH), Analyse de séquence d'ADN (méthodes), Génome (MeSH), Génomique (MeSH), Génétique des populations (MeSH), Hétérozygote (MeSH), Normes de référence (MeSH), Nucléotides (génétique), Oomycetes (génétique), Phytophthora infestans (génétique), Polymorphisme génétique (MeSH), Séquence nucléotidique (MeSH).
- MESH :
English descriptors
- KwdEn :
- MESH :
- chemical , genetics : Nucleotides.
- genetics : Oomycetes, Phytophthora infestans.
- methods : Sequence Analysis, DNA.
- Alleles, Base Sequence, Genetics, Population, Genome, Genomics, Heterozygote, Polymorphism, Genetic, Reference Standards.
Abstract
The oomycete pathogens Phytophthora infestans and P. capsici cause significant crop losses world-wide, threatening food security. In each case, pathogenicity factors, called RXLR effectors, contribute to virulence. Some RXLRs are perceived by resistance proteins to trigger host immunity, but our understanding of the demographic processes and adaptive evolution of pathogen virulence remains poor. Here, we describe PenSeq, a highly efficient enrichment sequencing approach for genes encoding pathogenicity determinants which, as shown for the infamous potato blight pathogen Phytophthora infestans, make up < 1% of the entire genome. PenSeq facilitates the characterization of allelic diversity in pathogen effectors, enabling evolutionary and population genomic analyses of Phytophthora species. Furthermore, PenSeq enables the massively parallel identification of presence/absence variations and sequence polymorphisms in key pathogen genes, which is a prerequisite for the efficient deployment of host resistance genes. PenSeq represents a cost-effective alternative to whole-genome sequencing and addresses crucial limitations of current plant pathogen population studies, which are often based on selectively neutral markers and consequently have limited utility in the analysis of adaptive evolution. The approach can be adapted to diverse microbes and pathogens.
DOI: 10.1111/nph.15441
PubMed: 30288743
PubMed Central: PMC6492278
Affiliations:
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Thilliez</name><affiliation wicri:level="1"><nlm:affiliation>Cell and Molecular Sciences, The James Hutton Institute, Errol Road, Invergowrie, Dundee, DD2 5DA, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Cell and Molecular Sciences, The James Hutton Institute, Errol Road, Invergowrie, Dundee, DD2 5DA</wicri:regionArea><wicri:noRegion>DD2 5DA</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Division of Plant Sciences at the James Hutton Institute, School of Life Sciences, University of Dundee, Dundee, DD2 5DA, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Division of Plant Sciences at the James Hutton Institute, School of Life Sciences, University of Dundee, Dundee, DD2 5DA</wicri:regionArea><wicri:noRegion>DD2 5DA</wicri:noRegion></affiliation></author><author><name sortKey="Armstrong, Miles R" sort="Armstrong, Miles R" uniqKey="Armstrong M" first="Miles R" last="Armstrong">Miles R. Armstrong</name><affiliation wicri:level="1"><nlm:affiliation>Cell and Molecular Sciences, The James Hutton Institute, Errol Road, Invergowrie, Dundee, DD2 5DA, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Cell and Molecular Sciences, The James Hutton Institute, Errol Road, Invergowrie, Dundee, DD2 5DA</wicri:regionArea><wicri:noRegion>DD2 5DA</wicri:noRegion></affiliation></author><author><name sortKey="Lim, Tze Yin" sort="Lim, Tze Yin" uniqKey="Lim T" first="Tze-Yin" last="Lim">Tze-Yin Lim</name><affiliation wicri:level="1"><nlm:affiliation>Information and Computational Sciences, The James Hutton Institute, Dundee, DD2 5DA, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Information and Computational Sciences, The James Hutton Institute, Dundee, DD2 5DA</wicri:regionArea><wicri:noRegion>DD2 5DA</wicri:noRegion></affiliation></author><author><name sortKey="Baker, Katie" sort="Baker, Katie" uniqKey="Baker K" first="Katie" last="Baker">Katie Baker</name><affiliation wicri:level="1"><nlm:affiliation>Information and Computational Sciences, The James Hutton Institute, Dundee, DD2 5DA, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Information and Computational Sciences, The James Hutton Institute, Dundee, DD2 5DA</wicri:regionArea><wicri:noRegion>DD2 5DA</wicri:noRegion></affiliation></author><author><name sortKey="Jouet, Agathe" sort="Jouet, Agathe" uniqKey="Jouet A" first="Agathe" last="Jouet">Agathe Jouet</name><affiliation wicri:level="1"><nlm:affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7GJ, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>The Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7GJ</wicri:regionArea><wicri:noRegion>NR4 7GJ</wicri:noRegion></affiliation></author><author><name sortKey="Ward, Ben" sort="Ward, Ben" uniqKey="Ward B" first="Ben" last="Ward">Ben Ward</name><affiliation wicri:level="1"><nlm:affiliation>The Earlham Institute, Norwich Research Park, Norwich, NR4 7UH, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>The Earlham Institute, Norwich Research Park, Norwich, NR4 7UH</wicri:regionArea><wicri:noRegion>NR4 7UH</wicri:noRegion></affiliation></author><author><name sortKey="Van Oosterhout, Cock" sort="Van Oosterhout, Cock" uniqKey="Van Oosterhout C" first="Cock" last="Van Oosterhout">Cock Van Oosterhout</name><affiliation wicri:level="1"><nlm:affiliation>University of East Anglia, Norwich Research Park, Norwich, NR4 7TJ, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>University of East Anglia, Norwich Research Park, Norwich, NR4 7TJ</wicri:regionArea><wicri:noRegion>NR4 7TJ</wicri:noRegion></affiliation></author><author><name sortKey="Jones, Jonathan D G" sort="Jones, Jonathan D G" uniqKey="Jones J" first="Jonathan D G" last="Jones">Jonathan D G. Jones</name><affiliation wicri:level="1"><nlm:affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7GJ, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>The Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7GJ</wicri:regionArea><wicri:noRegion>NR4 7GJ</wicri:noRegion></affiliation></author><author><name sortKey="Huitema, Edgar" sort="Huitema, Edgar" uniqKey="Huitema E" first="Edgar" last="Huitema">Edgar Huitema</name><affiliation wicri:level="1"><nlm:affiliation>Division of Plant Sciences at the James Hutton Institute, School of Life Sciences, University of Dundee, Dundee, DD2 5DA, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Division of Plant Sciences at the James Hutton Institute, School of Life Sciences, University of Dundee, Dundee, DD2 5DA</wicri:regionArea><wicri:noRegion>DD2 5DA</wicri:noRegion></affiliation></author><author><name sortKey="Birch, Paul R J" sort="Birch, Paul R J" uniqKey="Birch P" first="Paul R J" last="Birch">Paul R J. Birch</name><affiliation wicri:level="1"><nlm:affiliation>Cell and Molecular Sciences, The James Hutton Institute, Errol Road, Invergowrie, Dundee, DD2 5DA, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Cell and Molecular Sciences, The James Hutton Institute, Errol Road, Invergowrie, Dundee, DD2 5DA</wicri:regionArea><wicri:noRegion>DD2 5DA</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Division of Plant Sciences at the James Hutton Institute, School of Life Sciences, University of Dundee, Dundee, DD2 5DA, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Division of Plant Sciences at the James Hutton Institute, School of Life Sciences, University of Dundee, Dundee, DD2 5DA</wicri:regionArea><wicri:noRegion>DD2 5DA</wicri:noRegion></affiliation></author><author><name sortKey="Hein, Ingo" sort="Hein, Ingo" uniqKey="Hein I" first="Ingo" last="Hein">Ingo Hein</name><affiliation wicri:level="1"><nlm:affiliation>Cell and Molecular Sciences, The James Hutton Institute, Errol Road, Invergowrie, Dundee, DD2 5DA, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Cell and Molecular Sciences, The James Hutton Institute, Errol Road, Invergowrie, Dundee, DD2 5DA</wicri:regionArea><wicri:noRegion>DD2 5DA</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Division of Plant Sciences at the James Hutton Institute, School of Life Sciences, University of Dundee, Dundee, DD2 5DA, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Division of Plant Sciences at the James Hutton Institute, School of Life Sciences, University of Dundee, Dundee, DD2 5DA</wicri:regionArea><wicri:noRegion>DD2 5DA</wicri:noRegion></affiliation></author></analytic><series><title level="j">The New phytologist</title><idno type="eISSN">1469-8137</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Alleles (MeSH)</term><term>Base Sequence (MeSH)</term><term>Genetics, Population (MeSH)</term><term>Genome (MeSH)</term><term>Genomics (MeSH)</term><term>Heterozygote (MeSH)</term><term>Nucleotides (genetics)</term><term>Oomycetes (genetics)</term><term>Phytophthora infestans (genetics)</term><term>Polymorphism, Genetic (MeSH)</term><term>Reference Standards (MeSH)</term><term>Sequence Analysis, DNA (methods)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Allèles (MeSH)</term><term>Analyse de séquence d'ADN (méthodes)</term><term>Génome (MeSH)</term><term>Génomique (MeSH)</term><term>Génétique des populations (MeSH)</term><term>Hétérozygote (MeSH)</term><term>Normes de référence (MeSH)</term><term>Nucléotides (génétique)</term><term>Oomycetes (génétique)</term><term>Phytophthora infestans (génétique)</term><term>Polymorphisme génétique (MeSH)</term><term>Séquence nucléotidique (MeSH)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Nucleotides</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Oomycetes</term><term>Phytophthora infestans</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Nucléotides</term><term>Oomycetes</term><term>Phytophthora infestans</term></keywords><keywords scheme="MESH" qualifier="methods" xml:lang="en"><term>Sequence Analysis, DNA</term></keywords><keywords scheme="MESH" qualifier="méthodes" xml:lang="fr"><term>Analyse de séquence d'ADN</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Alleles</term><term>Base Sequence</term><term>Genetics, Population</term><term>Genome</term><term>Genomics</term><term>Heterozygote</term><term>Polymorphism, Genetic</term><term>Reference Standards</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Allèles</term><term>Génome</term><term>Génomique</term><term>Génétique des populations</term><term>Hétérozygote</term><term>Normes de référence</term><term>Polymorphisme génétique</term><term>Séquence nucléotidique</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">The oomycete pathogens Phytophthora infestans and P. capsici cause significant crop losses world-wide, threatening food security. In each case, pathogenicity factors, called RXLR effectors, contribute to virulence. Some RXLRs are perceived by resistance proteins to trigger host immunity, but our understanding of the demographic processes and adaptive evolution of pathogen virulence remains poor. Here, we describe PenSeq, a highly efficient enrichment sequencing approach for genes encoding pathogenicity determinants which, as shown for the infamous potato blight pathogen Phytophthora infestans, make up < 1% of the entire genome. PenSeq facilitates the characterization of allelic diversity in pathogen effectors, enabling evolutionary and population genomic analyses of Phytophthora species. Furthermore, PenSeq enables the massively parallel identification of presence/absence variations and sequence polymorphisms in key pathogen genes, which is a prerequisite for the efficient deployment of host resistance genes. PenSeq represents a cost-effective alternative to whole-genome sequencing and addresses crucial limitations of current plant pathogen population studies, which are often based on selectively neutral markers and consequently have limited utility in the analysis of adaptive evolution. The approach can be adapted to diverse microbes and pathogens.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">30288743</PMID><DateCompleted><Year>2020</Year><Month>01</Month><Day>14</Day></DateCompleted><DateRevised><Year>2020</Year><Month>09</Month><Day>30</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1469-8137</ISSN><JournalIssue CitedMedium="Internet"><Volume>221</Volume><Issue>3</Issue><PubDate><Year>2019</Year><Month>02</Month></PubDate></JournalIssue><Title>The New phytologist</Title><ISOAbbreviation>New Phytol</ISOAbbreviation></Journal><ArticleTitle>Pathogen enrichment sequencing (PenSeq) enables population genomic studies in oomycetes.</ArticleTitle><Pagination><MedlinePgn>1634-1648</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1111/nph.15441</ELocationID><Abstract><AbstractText>The oomycete pathogens Phytophthora infestans and P. capsici cause significant crop losses world-wide, threatening food security. In each case, pathogenicity factors, called RXLR effectors, contribute to virulence. Some RXLRs are perceived by resistance proteins to trigger host immunity, but our understanding of the demographic processes and adaptive evolution of pathogen virulence remains poor. Here, we describe PenSeq, a highly efficient enrichment sequencing approach for genes encoding pathogenicity determinants which, as shown for the infamous potato blight pathogen Phytophthora infestans, make up < 1% of the entire genome. PenSeq facilitates the characterization of allelic diversity in pathogen effectors, enabling evolutionary and population genomic analyses of Phytophthora species. Furthermore, PenSeq enables the massively parallel identification of presence/absence variations and sequence polymorphisms in key pathogen genes, which is a prerequisite for the efficient deployment of host resistance genes. PenSeq represents a cost-effective alternative to whole-genome sequencing and addresses crucial limitations of current plant pathogen population studies, which are often based on selectively neutral markers and consequently have limited utility in the analysis of adaptive evolution. The approach can be adapted to diverse microbes and pathogens.</AbstractText><CopyrightInformation>© 2018 The Authors. New Phytologist © 2018 New Phytologist Trust.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Thilliez</LastName><ForeName>Gaetan J A</ForeName><Initials>GJA</Initials><Identifier Source="ORCID">0000-0001-8650-4477</Identifier><AffiliationInfo><Affiliation>Cell and Molecular Sciences, The James Hutton Institute, Errol Road, Invergowrie, Dundee, DD2 5DA, UK.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Division of Plant Sciences at the James Hutton Institute, School of Life Sciences, University of Dundee, Dundee, DD2 5DA, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Armstrong</LastName><ForeName>Miles R</ForeName><Initials>MR</Initials><Identifier Source="ORCID">0000-0002-9441-476X</Identifier><AffiliationInfo><Affiliation>Cell and Molecular Sciences, The James Hutton Institute, Errol Road, Invergowrie, Dundee, DD2 5DA, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lim</LastName><ForeName>Tze-Yin</ForeName><Initials>TY</Initials><AffiliationInfo><Affiliation>Information and Computational Sciences, The James Hutton Institute, Dundee, DD2 5DA, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Baker</LastName><ForeName>Katie</ForeName><Initials>K</Initials><Identifier Source="ORCID">0000-0002-6265-9252</Identifier><AffiliationInfo><Affiliation>Information and Computational Sciences, The James Hutton Institute, Dundee, DD2 5DA, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jouet</LastName><ForeName>Agathe</ForeName><Initials>A</Initials><Identifier Source="ORCID">0000-0003-4998-9596</Identifier><AffiliationInfo><Affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7GJ, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ward</LastName><ForeName>Ben</ForeName><Initials>B</Initials><Identifier Source="ORCID">0000-0001-6337-5238</Identifier><AffiliationInfo><Affiliation>The Earlham Institute, Norwich Research Park, Norwich, NR4 7UH, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>van Oosterhout</LastName><ForeName>Cock</ForeName><Initials>C</Initials><Identifier Source="ORCID">0000-0002-5653-738X</Identifier><AffiliationInfo><Affiliation>University of East Anglia, Norwich Research Park, Norwich, NR4 7TJ, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jones</LastName><ForeName>Jonathan D G</ForeName><Initials>JDG</Initials><AffiliationInfo><Affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7GJ, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Huitema</LastName><ForeName>Edgar</ForeName><Initials>E</Initials><Identifier Source="ORCID">0000-0002-5766-0830</Identifier><AffiliationInfo><Affiliation>Division of Plant Sciences at the James Hutton Institute, School of Life Sciences, University of Dundee, Dundee, DD2 5DA, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Birch</LastName><ForeName>Paul R J</ForeName><Initials>PRJ</Initials><Identifier Source="ORCID">0000-0002-6559-3746</Identifier><AffiliationInfo><Affiliation>Cell and Molecular Sciences, The James Hutton Institute, Errol Road, Invergowrie, Dundee, DD2 5DA, UK.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Division of Plant Sciences at the James Hutton Institute, School of Life Sciences, University of Dundee, Dundee, DD2 5DA, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hein</LastName><ForeName>Ingo</ForeName><Initials>I</Initials><Identifier Source="ORCID">0000-0002-0128-2084</Identifier><AffiliationInfo><Affiliation>Cell and Molecular Sciences, The James Hutton Institute, Errol Road, Invergowrie, Dundee, DD2 5DA, UK.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Division of Plant Sciences at the James Hutton Institute, School of Life Sciences, University of Dundee, Dundee, DD2 5DA, UK.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><Agency>Rural & Environment Science & Analytical Services Division of the Scottish Government</Agency><Country>International</Country></Grant><Grant><GrantID>BB/L008025/1</GrantID><Agency>Biotechnology and Biological Sciences Research Council (BBSRC)</Agency><Country>International</Country></Grant><Grant><GrantID>BB/K018299/1</GrantID><Agency>Biotechnology and Biological Sciences Research Council (BBSRC)</Agency><Country>International</Country></Grant><Grant><GrantID>BB/C007522/1</GrantID><Agency>Biotechnology and Biological Sciences Research Council</Agency><Country>United Kingdom</Country></Grant><Grant><GrantID>2011-68004-30154</GrantID><Agency>US Department of Agriculture National Institute of Food and Agriculture (USDA NIFA)</Agency><Country>International</Country></Grant><Grant><GrantID>BB/N02317X/1</GrantID><Agency>Biotechnology and Biological Sciences Research Council (BBSRC)</Agency><Country>International</Country></Grant></GrantList><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>2018</Year><Month>10</Month><Day>05</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>New Phytol</MedlineTA><NlmUniqueID>9882884</NlmUniqueID><ISSNLinking>0028-646X</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D009711">Nucleotides</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><CommentsCorrectionsList><CommentsCorrections RefType="CommentIn"><RefSource>New Phytol. 2019 Feb;221(3):1177-1179</RefSource><PMID Version="1">30644579</PMID></CommentsCorrections></CommentsCorrectionsList><MeshHeadingList><MeshHeading><DescriptorName UI="D000483" MajorTopicYN="N">Alleles</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D001483" MajorTopicYN="N">Base Sequence</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D005828" MajorTopicYN="N">Genetics, Population</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D016678" MajorTopicYN="N">Genome</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D023281" MajorTopicYN="Y">Genomics</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D006579" MajorTopicYN="N">Heterozygote</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D009711" MajorTopicYN="N">Nucleotides</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D009868" MajorTopicYN="N">Oomycetes</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D055750" MajorTopicYN="N">Phytophthora infestans</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D011110" MajorTopicYN="N">Polymorphism, Genetic</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D012015" MajorTopicYN="N">Reference Standards</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D017422" MajorTopicYN="N">Sequence Analysis, DNA</DescriptorName><QualifierName UI="Q000379" MajorTopicYN="Y">methods</QualifierName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">Phytophthora capsici
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