Divergent Evolution of PcF/SCR74 Effectors in Oomycetes Is Associated with Distinct Recognition Patterns in Solanaceous Plants.
Identifieur interne : 000207 ( Main/Corpus ); précédent : 000206; suivant : 000208Divergent Evolution of PcF/SCR74 Effectors in Oomycetes Is Associated with Distinct Recognition Patterns in Solanaceous Plants.
Auteurs : Xiao Lin ; Shumei Wang ; Laura De Rond ; Nicoletta Bertolin ; Roland H M. Wouters ; Doret Wouters ; Emmanouil Domazakis ; Mulusew Kassa Bitew ; Joe Win ; Suomeng Dong ; Richard G F. Visser ; Paul Birch ; Sophien Kamoun ; Vivianne G A A. VleeshouwersSource :
- mBio [ 2150-7511 ] ; 2020.
Abstract
Plants deploy cell surface receptors known as pattern-recognition receptors (PRRs) that recognize non-self molecules from pathogens and microbes to defend against invaders. PRRs typically recognize microbe-associated molecular patterns (MAMPs) that are usually widely conserved, some even across kingdoms. Here, we report an oomycete-specific family of small secreted cysteine-rich (SCR) proteins that displays divergent patterns of sequence variation in the Irish potato famine pathogen Phytophthora infestans A subclass that includes the conserved effector PcF from Phytophthora cactorum activates immunity in a wide range of plant species. In contrast, the more diverse SCR74 subclass is specific to P. infestans and tends to trigger immune responses only in a limited number of wild potato genotypes. The SCR74 response was recently mapped to a G-type lectin receptor kinase (G-LecRK) locus in the wild potato Solanum microdontum subsp. gigantophyllum. The G-LecRK locus displays a high diversity in Solanum host species compared to other solanaceous plants. We propose that the diversification of the SCR74 proteins in P. infestans is driven by a fast coevolutionary arms race with cell surface immune receptors in wild potato, which contrasts the presumed slower dynamics between conserved apoplastic effectors and PRRs. Understanding the molecular determinants of plant immune responses to these divergent molecular patterns in oomycetes is expected to contribute to deploying multiple layers of disease resistance in crop plants.IMPORTANCE Immune receptors at the plant cell surface can recognize invading microbes. The perceived microbial molecules are typically widely conserved and therefore the matching surface receptors can detect a broad spectrum of pathogens. Here we describe a family of Phytophthora small extracellular proteins that consists of conserved subfamilies that are widely recognized by solanaceous plants. Remarkably, one subclass of SCR74 proteins is highly diverse, restricted to the late blight pathogen Phytophthora infestans and is specifically detected in wild potato plants. The diversification of this subfamily exhibits signatures of a coevolutionary arms race with surface receptors in potato. Insights into the molecular interaction between these potato-specific receptors and the recognized Phytophthora proteins are expected to contribute to disease resistance breeding in potato.
DOI: 10.1128/mBio.00947-20
PubMed: 32605983
PubMed Central: PMC7327169
Links to Exploration step
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Divergent Evolution of PcF/SCR74 Effectors in Oomycetes Is Associated with Distinct Recognition Patterns in Solanaceous Plants.</title><author><name sortKey="Lin, Xiao" sort="Lin, Xiao" uniqKey="Lin X" first="Xiao" last="Lin">Xiao Lin</name><affiliation><nlm:affiliation>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Wang, Shumei" sort="Wang, Shumei" uniqKey="Wang S" first="Shumei" last="Wang">Shumei Wang</name><affiliation><nlm:affiliation>Cell and Molecular Sciences, The James Hutton Institute, Dundee, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="De Rond, Laura" sort="De Rond, Laura" uniqKey="De Rond L" first="Laura" last="De Rond">Laura De Rond</name><affiliation><nlm:affiliation>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Bertolin, Nicoletta" sort="Bertolin, Nicoletta" uniqKey="Bertolin N" first="Nicoletta" last="Bertolin">Nicoletta Bertolin</name><affiliation><nlm:affiliation>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Wouters, Roland H M" sort="Wouters, Roland H M" uniqKey="Wouters R" first="Roland H M" last="Wouters">Roland H M. Wouters</name><affiliation><nlm:affiliation>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Wouters, Doret" sort="Wouters, Doret" uniqKey="Wouters D" first="Doret" last="Wouters">Doret Wouters</name><affiliation><nlm:affiliation>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Domazakis, Emmanouil" sort="Domazakis, Emmanouil" uniqKey="Domazakis E" first="Emmanouil" last="Domazakis">Emmanouil Domazakis</name><affiliation><nlm:affiliation>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Bitew, Mulusew Kassa" sort="Bitew, Mulusew Kassa" uniqKey="Bitew M" first="Mulusew Kassa" last="Bitew">Mulusew Kassa Bitew</name><affiliation><nlm:affiliation>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Win, Joe" sort="Win, Joe" uniqKey="Win J" first="Joe" last="Win">Joe Win</name><affiliation><nlm:affiliation>The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Dong, Suomeng" sort="Dong, Suomeng" uniqKey="Dong S" first="Suomeng" last="Dong">Suomeng Dong</name><affiliation><nlm:affiliation>The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Visser, Richard G F" sort="Visser, Richard G F" uniqKey="Visser R" first="Richard G F" last="Visser">Richard G F. Visser</name><affiliation><nlm:affiliation>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Birch, Paul" sort="Birch, Paul" uniqKey="Birch P" first="Paul" last="Birch">Paul Birch</name><affiliation><nlm:affiliation>Cell and Molecular Sciences, The James Hutton Institute, Dundee, United Kingdom.</nlm:affiliation></affiliation><affiliation><nlm:affiliation>School of Life Sciences, Division of Plant Sciences, University of Dundee at the James Hutton Institute, Dundee, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Kamoun, Sophien" sort="Kamoun, Sophien" uniqKey="Kamoun S" first="Sophien" last="Kamoun">Sophien Kamoun</name><affiliation><nlm:affiliation>The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Vleeshouwers, Vivianne G A A" sort="Vleeshouwers, Vivianne G A A" uniqKey="Vleeshouwers V" first="Vivianne G A A" last="Vleeshouwers">Vivianne G A A. Vleeshouwers</name><affiliation><nlm:affiliation>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands vivianne.vleeshouwers@wur.nl.</nlm:affiliation></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2020">2020</date><idno type="RBID">pubmed:32605983</idno><idno type="pmid">32605983</idno><idno type="doi">10.1128/mBio.00947-20</idno><idno type="pmc">PMC7327169</idno><idno type="wicri:Area/Main/Corpus">000207</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000207</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Divergent Evolution of PcF/SCR74 Effectors in Oomycetes Is Associated with Distinct Recognition Patterns in Solanaceous Plants.</title><author><name sortKey="Lin, Xiao" sort="Lin, Xiao" uniqKey="Lin X" first="Xiao" last="Lin">Xiao Lin</name><affiliation><nlm:affiliation>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Wang, Shumei" sort="Wang, Shumei" uniqKey="Wang S" first="Shumei" last="Wang">Shumei Wang</name><affiliation><nlm:affiliation>Cell and Molecular Sciences, The James Hutton Institute, Dundee, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="De Rond, Laura" sort="De Rond, Laura" uniqKey="De Rond L" first="Laura" last="De Rond">Laura De Rond</name><affiliation><nlm:affiliation>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Bertolin, Nicoletta" sort="Bertolin, Nicoletta" uniqKey="Bertolin N" first="Nicoletta" last="Bertolin">Nicoletta Bertolin</name><affiliation><nlm:affiliation>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Wouters, Roland H M" sort="Wouters, Roland H M" uniqKey="Wouters R" first="Roland H M" last="Wouters">Roland H M. Wouters</name><affiliation><nlm:affiliation>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Wouters, Doret" sort="Wouters, Doret" uniqKey="Wouters D" first="Doret" last="Wouters">Doret Wouters</name><affiliation><nlm:affiliation>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Domazakis, Emmanouil" sort="Domazakis, Emmanouil" uniqKey="Domazakis E" first="Emmanouil" last="Domazakis">Emmanouil Domazakis</name><affiliation><nlm:affiliation>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Bitew, Mulusew Kassa" sort="Bitew, Mulusew Kassa" uniqKey="Bitew M" first="Mulusew Kassa" last="Bitew">Mulusew Kassa Bitew</name><affiliation><nlm:affiliation>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Win, Joe" sort="Win, Joe" uniqKey="Win J" first="Joe" last="Win">Joe Win</name><affiliation><nlm:affiliation>The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Dong, Suomeng" sort="Dong, Suomeng" uniqKey="Dong S" first="Suomeng" last="Dong">Suomeng Dong</name><affiliation><nlm:affiliation>The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Visser, Richard G F" sort="Visser, Richard G F" uniqKey="Visser R" first="Richard G F" last="Visser">Richard G F. Visser</name><affiliation><nlm:affiliation>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Birch, Paul" sort="Birch, Paul" uniqKey="Birch P" first="Paul" last="Birch">Paul Birch</name><affiliation><nlm:affiliation>Cell and Molecular Sciences, The James Hutton Institute, Dundee, United Kingdom.</nlm:affiliation></affiliation><affiliation><nlm:affiliation>School of Life Sciences, Division of Plant Sciences, University of Dundee at the James Hutton Institute, Dundee, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Kamoun, Sophien" sort="Kamoun, Sophien" uniqKey="Kamoun S" first="Sophien" last="Kamoun">Sophien Kamoun</name><affiliation><nlm:affiliation>The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Vleeshouwers, Vivianne G A A" sort="Vleeshouwers, Vivianne G A A" uniqKey="Vleeshouwers V" first="Vivianne G A A" last="Vleeshouwers">Vivianne G A A. Vleeshouwers</name><affiliation><nlm:affiliation>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands vivianne.vleeshouwers@wur.nl.</nlm:affiliation></affiliation></author></analytic><series><title level="j">mBio</title><idno type="eISSN">2150-7511</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">Plants deploy cell surface receptors known as pattern-recognition receptors (PRRs) that recognize non-self molecules from pathogens and microbes to defend against invaders. PRRs typically recognize microbe-associated molecular patterns (MAMPs) that are usually widely conserved, some even across kingdoms. Here, we report an oomycete-specific family of small secreted cysteine-rich (SCR) proteins that displays divergent patterns of sequence variation in the Irish potato famine pathogen <i>Phytophthora infestans</i> A subclass that includes the conserved effector PcF from <i>Phytophthora cactorum</i> activates immunity in a wide range of plant species. In contrast, the more diverse SCR74 subclass is specific to <i>P. infestans</i> and tends to trigger immune responses only in a limited number of wild potato genotypes. The SCR74 response was recently mapped to a G-type lectin receptor kinase (<i>G-LecRK</i>) locus in the wild potato <i>Solanum microdontum</i> subsp. <i>gigantophyllum.</i> The <i>G-LecRK</i> locus displays a high diversity in <i>Solanum</i> host species compared to other solanaceous plants. We propose that the diversification of the SCR74 proteins in <i>P. infestans</i> is driven by a fast coevolutionary arms race with cell surface immune receptors in wild potato, which contrasts the presumed slower dynamics between conserved apoplastic effectors and PRRs. Understanding the molecular determinants of plant immune responses to these divergent molecular patterns in oomycetes is expected to contribute to deploying multiple layers of disease resistance in crop plants.<b>IMPORTANCE</b> Immune receptors at the plant cell surface can recognize invading microbes. The perceived microbial molecules are typically widely conserved and therefore the matching surface receptors can detect a broad spectrum of pathogens. Here we describe a family of <i>Phytophthora</i> small extracellular proteins that consists of conserved subfamilies that are widely recognized by solanaceous plants. Remarkably, one subclass of SCR74 proteins is highly diverse, restricted to the late blight pathogen <i>Phytophthora infestans</i> and is specifically detected in wild potato plants. The diversification of this subfamily exhibits signatures of a coevolutionary arms race with surface receptors in potato. Insights into the molecular interaction between these potato-specific receptors and the recognized <i>Phytophthora</i> proteins are expected to contribute to disease resistance breeding in potato.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">32605983</PMID><DateRevised><Year>2020</Year><Month>07</Month><Day>23</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">2150-7511</ISSN><JournalIssue CitedMedium="Internet"><Volume>11</Volume><Issue>3</Issue><PubDate><Year>2020</Year><Month>06</Month><Day>30</Day></PubDate></JournalIssue><Title>mBio</Title><ISOAbbreviation>mBio</ISOAbbreviation></Journal><ArticleTitle>Divergent Evolution of PcF/SCR74 Effectors in Oomycetes Is Associated with Distinct Recognition Patterns in Solanaceous Plants.</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">e00947-20</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1128/mBio.00947-20</ELocationID><Abstract><AbstractText>Plants deploy cell surface receptors known as pattern-recognition receptors (PRRs) that recognize non-self molecules from pathogens and microbes to defend against invaders. PRRs typically recognize microbe-associated molecular patterns (MAMPs) that are usually widely conserved, some even across kingdoms. Here, we report an oomycete-specific family of small secreted cysteine-rich (SCR) proteins that displays divergent patterns of sequence variation in the Irish potato famine pathogen <i>Phytophthora infestans</i> A subclass that includes the conserved effector PcF from <i>Phytophthora cactorum</i> activates immunity in a wide range of plant species. In contrast, the more diverse SCR74 subclass is specific to <i>P. infestans</i> and tends to trigger immune responses only in a limited number of wild potato genotypes. The SCR74 response was recently mapped to a G-type lectin receptor kinase (<i>G-LecRK</i>) locus in the wild potato <i>Solanum microdontum</i> subsp. <i>gigantophyllum.</i> The <i>G-LecRK</i> locus displays a high diversity in <i>Solanum</i> host species compared to other solanaceous plants. We propose that the diversification of the SCR74 proteins in <i>P. infestans</i> is driven by a fast coevolutionary arms race with cell surface immune receptors in wild potato, which contrasts the presumed slower dynamics between conserved apoplastic effectors and PRRs. Understanding the molecular determinants of plant immune responses to these divergent molecular patterns in oomycetes is expected to contribute to deploying multiple layers of disease resistance in crop plants.<b>IMPORTANCE</b> Immune receptors at the plant cell surface can recognize invading microbes. The perceived microbial molecules are typically widely conserved and therefore the matching surface receptors can detect a broad spectrum of pathogens. Here we describe a family of <i>Phytophthora</i> small extracellular proteins that consists of conserved subfamilies that are widely recognized by solanaceous plants. Remarkably, one subclass of SCR74 proteins is highly diverse, restricted to the late blight pathogen <i>Phytophthora infestans</i> and is specifically detected in wild potato plants. The diversification of this subfamily exhibits signatures of a coevolutionary arms race with surface receptors in potato. Insights into the molecular interaction between these potato-specific receptors and the recognized <i>Phytophthora</i> proteins are expected to contribute to disease resistance breeding in potato.</AbstractText><CopyrightInformation>Copyright © 2020 Lin et al.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Lin</LastName><ForeName>Xiao</ForeName><Initials>X</Initials><Identifier Source="ORCID">0000-0002-3848-0244</Identifier><AffiliationInfo><Affiliation>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Shumei</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Cell and Molecular Sciences, The James Hutton Institute, Dundee, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>de Rond</LastName><ForeName>Laura</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bertolin</LastName><ForeName>Nicoletta</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wouters</LastName><ForeName>Roland H M</ForeName><Initials>RHM</Initials><AffiliationInfo><Affiliation>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wouters</LastName><ForeName>Doret</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Domazakis</LastName><ForeName>Emmanouil</ForeName><Initials>E</Initials><AffiliationInfo><Affiliation>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bitew</LastName><ForeName>Mulusew Kassa</ForeName><Initials>MK</Initials><AffiliationInfo><Affiliation>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Win</LastName><ForeName>Joe</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Dong</LastName><ForeName>Suomeng</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Visser</LastName><ForeName>Richard G F</ForeName><Initials>RGF</Initials><AffiliationInfo><Affiliation>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Birch</LastName><ForeName>Paul</ForeName><Initials>P</Initials><Identifier Source="ORCID">0000-0002-6559-3746</Identifier><AffiliationInfo><Affiliation>Cell and Molecular Sciences, The James Hutton Institute, Dundee, United Kingdom.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>School of Life Sciences, Division of Plant Sciences, University of Dundee at the James Hutton Institute, Dundee, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kamoun</LastName><ForeName>Sophien</ForeName><Initials>S</Initials><Identifier Source="ORCID">0000-0002-0290-0315</Identifier><AffiliationInfo><Affiliation>The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Vleeshouwers</LastName><ForeName>Vivianne G A A</ForeName><Initials>VGAA</Initials><Identifier Source="ORCID">0000-0002-8160-4556</Identifier><AffiliationInfo><Affiliation>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands vivianne.vleeshouwers@wur.nl.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><Acronym>BB_</Acronym><Agency>Biotechnology and Biological Sciences Research Council</Agency><Country>United Kingdom</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>06</Month><Day>30</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>mBio</MedlineTA><NlmUniqueID>101519231</NlmUniqueID></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">MAMP</Keyword><Keyword MajorTopicYN="Y">Phytophthora infestans
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