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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:aff id="aff1"><addr-line>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands</addr-line></nlm:aff></affiliation></author><author><name sortKey="Wang, Shumei" sort="Wang, Shumei" uniqKey="Wang S" first="Shumei" last="Wang">Shumei Wang</name><affiliation><nlm:aff id="aff2"><addr-line>Cell and Molecular Sciences, The James Hutton Institute, Dundee, United Kingdom</addr-line></nlm:aff></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:aff id="aff1"><addr-line>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands</addr-line></nlm:aff></affiliation></author><author><name sortKey="Bertolin, Nicoletta" sort="Bertolin, Nicoletta" uniqKey="Bertolin N" first="Nicoletta" last="Bertolin">Nicoletta Bertolin</name><affiliation><nlm:aff id="aff1"><addr-line>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands</addr-line></nlm:aff></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:aff id="aff1"><addr-line>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands</addr-line></nlm:aff></affiliation></author><author><name sortKey="Wouters, Doret" sort="Wouters, Doret" uniqKey="Wouters D" first="Doret" last="Wouters">Doret Wouters</name><affiliation><nlm:aff id="aff1"><addr-line>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands</addr-line></nlm:aff></affiliation></author><author><name sortKey="Domazakis, Emmanouil" sort="Domazakis, Emmanouil" uniqKey="Domazakis E" first="Emmanouil" last="Domazakis">Emmanouil Domazakis</name><affiliation><nlm:aff id="aff1"><addr-line>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands</addr-line></nlm:aff></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:aff id="aff1"><addr-line>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands</addr-line></nlm:aff></affiliation></author><author><name sortKey="Win, Joe" sort="Win, Joe" uniqKey="Win J" first="Joe" last="Win">Joe Win</name><affiliation><nlm:aff id="aff3"><addr-line>The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom</addr-line></nlm:aff></affiliation></author><author><name sortKey="Dong, Suomeng" sort="Dong, Suomeng" uniqKey="Dong S" first="Suomeng" last="Dong">Suomeng Dong</name><affiliation><nlm:aff id="aff3"><addr-line>The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom</addr-line></nlm:aff></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:aff id="aff1"><addr-line>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands</addr-line></nlm:aff></affiliation></author><author><name sortKey="Birch, Paul" sort="Birch, Paul" uniqKey="Birch P" first="Paul" last="Birch">Paul Birch</name><affiliation><nlm:aff id="aff2"><addr-line>Cell and Molecular Sciences, The James Hutton Institute, Dundee, United Kingdom</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><addr-line>School of Life Sciences, Division of Plant Sciences, University of Dundee at the James Hutton Institute, Dundee, United Kingdom</addr-line></nlm:aff></affiliation></author><author><name sortKey="Kamoun, Sophien" sort="Kamoun, Sophien" uniqKey="Kamoun S" first="Sophien" last="Kamoun">Sophien Kamoun</name><affiliation><nlm:aff id="aff3"><addr-line>The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom</addr-line></nlm:aff></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:aff id="aff1"><addr-line>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands</addr-line></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">32605983</idno><idno type="pmc">7327169</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7327169</idno><idno type="RBID">PMC:7327169</idno><idno type="doi">10.1128/mBio.00947-20</idno><date when="2020">2020</date><idno type="wicri:Area/Pmc/Corpus">000B60</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000B60</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">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:aff id="aff1"><addr-line>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands</addr-line></nlm:aff></affiliation></author><author><name sortKey="Wang, Shumei" sort="Wang, Shumei" uniqKey="Wang S" first="Shumei" last="Wang">Shumei Wang</name><affiliation><nlm:aff id="aff2"><addr-line>Cell and Molecular Sciences, The James Hutton Institute, Dundee, United Kingdom</addr-line></nlm:aff></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:aff id="aff1"><addr-line>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands</addr-line></nlm:aff></affiliation></author><author><name sortKey="Bertolin, Nicoletta" sort="Bertolin, Nicoletta" uniqKey="Bertolin N" first="Nicoletta" last="Bertolin">Nicoletta Bertolin</name><affiliation><nlm:aff id="aff1"><addr-line>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands</addr-line></nlm:aff></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:aff id="aff1"><addr-line>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands</addr-line></nlm:aff></affiliation></author><author><name sortKey="Wouters, Doret" sort="Wouters, Doret" uniqKey="Wouters D" first="Doret" last="Wouters">Doret Wouters</name><affiliation><nlm:aff id="aff1"><addr-line>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands</addr-line></nlm:aff></affiliation></author><author><name sortKey="Domazakis, Emmanouil" sort="Domazakis, Emmanouil" uniqKey="Domazakis E" first="Emmanouil" last="Domazakis">Emmanouil Domazakis</name><affiliation><nlm:aff id="aff1"><addr-line>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands</addr-line></nlm:aff></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:aff id="aff1"><addr-line>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands</addr-line></nlm:aff></affiliation></author><author><name sortKey="Win, Joe" sort="Win, Joe" uniqKey="Win J" first="Joe" last="Win">Joe Win</name><affiliation><nlm:aff id="aff3"><addr-line>The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom</addr-line></nlm:aff></affiliation></author><author><name sortKey="Dong, Suomeng" sort="Dong, Suomeng" uniqKey="Dong S" first="Suomeng" last="Dong">Suomeng Dong</name><affiliation><nlm:aff id="aff3"><addr-line>The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom</addr-line></nlm:aff></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:aff id="aff1"><addr-line>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands</addr-line></nlm:aff></affiliation></author><author><name sortKey="Birch, Paul" sort="Birch, Paul" uniqKey="Birch P" first="Paul" last="Birch">Paul Birch</name><affiliation><nlm:aff id="aff2"><addr-line>Cell and Molecular Sciences, The James Hutton Institute, Dundee, United Kingdom</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><addr-line>School of Life Sciences, Division of Plant Sciences, University of Dundee at the James Hutton Institute, Dundee, United Kingdom</addr-line></nlm:aff></affiliation></author><author><name sortKey="Kamoun, Sophien" sort="Kamoun, Sophien" uniqKey="Kamoun S" first="Sophien" last="Kamoun">Sophien Kamoun</name><affiliation><nlm:aff id="aff3"><addr-line>The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom</addr-line></nlm:aff></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:aff id="aff1"><addr-line>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands</addr-line></nlm:aff></affiliation></author></analytic><series><title level="j">mBio</title><idno type="eISSN">2150-7511</idno><imprint><date when="2020">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>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 <italic>Phytophthora</italic> 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 <italic>Phytophthora infestans</italic> 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 <italic>Phytophthora</italic> proteins are expected to contribute to disease resistance breeding in potato.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Misas Villamil, Jc" uniqKey="Misas Villamil J">JC Misas-Villamil</name></author><author><name sortKey="Van Der Hoorn, Ra" uniqKey="Van Der Hoorn R">RA van der Hoorn</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="De Wit, P" uniqKey="De Wit P">P de Wit</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Wang, Y" uniqKey="Wang Y">Y Wang</name></author><author><name sortKey="Wang, Y" uniqKey="Wang Y">Y Wang</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Jiang, Rhy" uniqKey="Jiang R">RHY Jiang</name></author><author><name sortKey="Tyler, Bm" uniqKey="Tyler B">BM 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<front><journal-meta><journal-id journal-id-type="nlm-ta">mBio</journal-id><journal-id journal-id-type="iso-abbrev">mBio</journal-id><journal-id journal-id-type="hwp">mbio</journal-id><journal-id journal-id-type="pmc">mbio</journal-id><journal-id journal-id-type="publisher-id">mBio</journal-id><journal-title-group><journal-title>mBio</journal-title></journal-title-group><issn pub-type="epub">2150-7511</issn><publisher><publisher-name>American Society for Microbiology</publisher-name><publisher-loc>1752 N St., N.W., Washington, DC</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">32605983</article-id><article-id pub-id-type="pmc">7327169</article-id><article-id pub-id-type="publisher-id">mBio00947-20</article-id><article-id pub-id-type="doi">10.1128/mBio.00947-20</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="overline"><subject>Host-Microbe Biology</subject></subj-group></article-categories><title-group><article-title>Divergent Evolution of PcF/SCR74 Effectors in Oomycetes Is Associated with Distinct Recognition Patterns in Solanaceous Plants</article-title><alt-title alt-title-type="running-head">Evolution and Recognition of PcF/SCR74 Effectors</alt-title><alt-title alt-title-type="short-authors">Lin et al.</alt-title></title-group><contrib-group><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0002-3848-0244</contrib-id><name><surname>Lin</surname><given-names>Xiao</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Wang</surname><given-names>Shumei</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref></contrib><contrib contrib-type="author"><name><surname>de Rond</surname><given-names>Laura</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Bertolin</surname><given-names>Nicoletta</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Wouters</surname><given-names>Roland H. M.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Wouters</surname><given-names>Doret</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Domazakis</surname><given-names>Emmanouil</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Bitew</surname><given-names>Mulusew Kassa</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Win</surname><given-names>Joe</given-names></name><xref ref-type="aff" rid="aff3"><sup>c</sup></xref></contrib><contrib contrib-type="author"><name><surname>Dong</surname><given-names>Suomeng</given-names></name><xref ref-type="aff" rid="aff3"><sup>c</sup></xref></contrib><contrib contrib-type="author"><name><surname>Visser</surname><given-names>Richard G. F.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0002-6559-3746</contrib-id><name><surname>Birch</surname><given-names>Paul</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref><xref ref-type="aff" rid="aff4"><sup>d</sup></xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0002-0290-0315</contrib-id><name><surname>Kamoun</surname><given-names>Sophien</given-names></name><xref ref-type="aff" rid="aff3"><sup>c</sup></xref></contrib><contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0002-8160-4556</contrib-id><name><surname>Vleeshouwers</surname><given-names>Vivianne G. A. A.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><aff id="aff1"><label>a</label><addr-line>Wageningen UR Plant Breeding, Wageningen University and Research, Wageningen, The Netherlands</addr-line></aff><aff id="aff2"><label>b</label><addr-line>Cell and Molecular Sciences, The James Hutton Institute, Dundee, United Kingdom</addr-line></aff><aff id="aff3"><label>c</label><addr-line>The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom</addr-line></aff><aff id="aff4"><label>d</label><addr-line>School of Life Sciences, Division of Plant Sciences, University of Dundee at the James Hutton Institute, Dundee, United Kingdom</addr-line></aff></contrib-group><contrib-group><contrib contrib-type="editor"><name><surname>Vidaver</surname><given-names>Anne K.</given-names></name><role>Editor</role><aff>University of Nebraska-Lincoln</aff></contrib></contrib-group><author-notes><corresp id="cor1">Address correspondence to Vivianne G. A. A. Vleeshouwers, <email>vivianne.vleeshouwers@wur.nl</email>.</corresp></author-notes><pub-date pub-type="epub"><day>30</day><month>6</month><year>2020</year></pub-date><pub-date pub-type="collection"><season>May-Jun</season><year>2020</year></pub-date><volume>11</volume><issue>3</issue><elocation-id>e00947-20</elocation-id><history><date date-type="received"><day>20</day><month>4</month><year>2020</year></date><date date-type="accepted"><day>2</day><month>6</month><year>2020</year></date></history><permissions><copyright-statement>Copyright © 2020 Lin et al.</copyright-statement><copyright-year>2020</copyright-year><copyright-holder>Lin et al.</copyright-holder><license license-type="open-access" xlink:href="https://creativecommons.org/licenses/by/4.0/"><license-p>This is an open-access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution 4.0 International license</ext-link>.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="mBio.00947-20.pdf"></self-uri><abstract abstract-type="precis"><p>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 <italic>Phytophthora</italic> 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 <italic>Phytophthora infestans</italic> 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 <italic>Phytophthora</italic> proteins are expected to contribute to disease resistance breeding in potato.</p></abstract><abstract><title>ABSTRACT</title><p>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 <named-content content-type="genus-species">Phytophthora infestans</named-content>. A subclass that includes the conserved effector PcF from <named-content content-type="genus-species">Phytophthora cactorum</named-content> activates immunity in a wide range of plant species. In contrast, the more diverse SCR74 subclass is specific to <italic>P. infestans</italic> 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 (<italic>G-LecRK</italic>) locus in the wild potato <named-content content-type="genus-species">Solanum microdontum</named-content> subsp. <italic>gigantophyllum.</italic> The <italic>G-LecRK</italic> locus displays a high diversity in <italic>Solanum</italic> host species compared to other solanaceous plants. We propose that the diversification of the SCR74 proteins in <italic>P. infestans</italic> 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.</p></abstract><kwd-group><title>KEYWORDS</title><kwd>MAMP</kwd><kwd>apoplastic effector</kwd><kwd>surface immune receptor</kwd><kwd>potato late blight</kwd><kwd><italic>Phytophthora infestans</italic></kwd></kwd-group><funding-group><award-group id="award1"><funding-source><institution-wrap><institution>Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO)</institution><institution-id>https://doi.org/10.13039/501100003246</institution-id></institution-wrap></funding-source><award-id>12378</award-id><principal-award-recipient><name><surname>Vleeshouwers</surname><given-names>Vivianne</given-names></name></principal-award-recipient><principal-award-recipient><name><surname>Visser</surname><given-names>Richard G. F.</given-names></name></principal-award-recipient><principal-award-recipient><name><surname>Lin</surname><given-names>Xiao</given-names></name></principal-award-recipient><principal-award-recipient><name><surname>de Rond</surname><given-names>Laura</given-names></name></principal-award-recipient><principal-award-recipient><name><surname>Bertolin</surname><given-names>Nicoletta</given-names></name></principal-award-recipient><principal-award-recipient><name><surname>Wouters</surname><given-names>Roland H. M.</given-names></name></principal-award-recipient><principal-award-recipient><name><surname>Wouters</surname><given-names>Doret</given-names></name></principal-award-recipient><principal-award-recipient><name><surname>Domazakis</surname><given-names>Emmanouil</given-names></name></principal-award-recipient><principal-award-recipient><name><surname>Bitew</surname><given-names>Mulusew Kassa</given-names></name></principal-award-recipient></award-group></funding-group><counts><count count="10" count-type="supplementary-material"></count><fig-count count="4"></fig-count><table-count count="0"></table-count><equation-count count="0"></equation-count><ref-count count="46"></ref-count><page-count count="12"></page-count><word-count count="8502"></word-count></counts><custom-meta-group><custom-meta><meta-name>cover-date</meta-name><meta-value>May/June 2020</meta-value></custom-meta></custom-meta-group></article-meta></front><body><sec sec-type="intro" id="s1"><title>INTRODUCTION</title><p>The plant apoplast is the battlefront of the plant-pathogen interaction (<xref rid="B1" ref-type="bibr">1</xref>). To colonize plants, pathogens secrete an arsenal of apoplastic effector proteins, including small cysteine-rich (SCR) proteins, proteases, and protease inhibitors for facilitating their infection and manipulating the plant immune system (<xref rid="B2" ref-type="bibr">2</xref>, <xref rid="B3" ref-type="bibr">3</xref>). Many of these apoplastic pathogen molecules are widely conserved, for example necrosis-inducing proteins (NLPs) that occur in bacteria, fungi, and oomycetes. Microbe-associated molecular patterns (MAMPs), such as flagellin of bacteria, chitin of fungi, and elicitins of oomycetes (<xref rid="B4" ref-type="bibr">4</xref>), are typically highly conserved as well, whereas apoplastic effectors that typically represent small SCR proteins exhibit various degrees of conservation, such as AVR2 and AVR4 of <named-content content-type="genus-species">Cladosporium fulvum</named-content> (<xref rid="B5" ref-type="bibr">5</xref>). Plants can monitor the extracellular non-self molecules or epitopes and trigger downstream defense responses by deploying surface immune receptors known as pattern recognition receptors (PRRs) that typically consist of receptor-like proteins (RLPs) or receptor-like kinases (RLKs) (<xref rid="B6" ref-type="bibr">6</xref>). Most RLPs/RLKs cloned to date, such as flagellin sensing 2 (FLS2), EF-Tu receptor (EFR), and elicitin receptor (ELR), contain an extracellular leucine-rich repeat (LRR) domain (<xref rid="B7" ref-type="bibr">7</xref><xref ref-type="bibr" rid="B8">–</xref><xref rid="B9" ref-type="bibr">9</xref>). Recently, various RLKs with other extracellular domains, such as an epidermal growth factor (EGF)-like domain, a LysM domain, or a lectin domain have been found to be involved in plant immunity (<xref rid="B6" ref-type="bibr">6</xref>).</p><p>In oomycetes, a wide diversity of apoplastic proteins that play a role in modulating host defense responses has been characterized. Most identified apoplastic effectors represent SCR proteins, such as elicitins (<xref rid="B10" ref-type="bibr">10</xref>), PcF (<italic>Phytophthora cactorum</italic>-<italic>Fragaria</italic>), SCR74, and SCR91 (<xref rid="B11" ref-type="bibr">11</xref><xref ref-type="bibr" rid="B12">–</xref><xref rid="B13" ref-type="bibr">13</xref>). PcF is a 7.67-kDa SCR protein of 73 amino acids, which forms three disulfide bridges by six conserved cysteines, and triggers defense-related responses on strawberry and tomato (<xref rid="B11" ref-type="bibr">11</xref>, <xref rid="B14" ref-type="bibr">14</xref>). Additional SCR proteins with a similar domain (the PcF domain; Pfam PF09461) have been further identified, i.e., SCR74 and SCR96, consisting of 74 and 96 amino acids, respectively. <italic>Scr74</italic> belongs to a highly polymorphic gene family that is under positive selection in <italic>P. infestans</italic>. Expression of <italic>Scr74</italic> is significantly upregulated during the early infection stages into host plants (<xref rid="B12" ref-type="bibr">12</xref>). Recently, the putative SCR74 receptor gene was fine mapped to a <italic>G-LecRK</italic> locus in wild potato (<xref rid="B15" ref-type="bibr">15</xref>). SCR96 is another related protein from <italic>P. cactorum</italic>; however, it lacks the PcF domain. SCR96 triggers cell death responses in some Solanaceae, including <named-content content-type="genus-species">Nicotiana benthamiana</named-content> and tomato (<xref rid="B16" ref-type="bibr">16</xref>). So far, very little is known about the function and evolution of these PcF-like effectors, and their targets or receptors in plants are unknown.</p><p>In the course of the arms race, effector genes are expected to be the direct target of the evolutionary forces that drive the antagonistic interplay between pathogen and host (<xref rid="B17" ref-type="bibr">17</xref>). The evolutionary dynamics of intracellular nucleotide-binding domain and leucine-rich repeat containing (NLR) receptors that mount a hypersensitive response (HR) to host-translocated effectors and delimit pathogen growth are well understood (<xref rid="B18" ref-type="bibr">18</xref>, <xref rid="B19" ref-type="bibr">19</xref>). Many plant <italic>NLR</italic> genes are located in highly polymorphic loci and are under strong selection pressure (<xref rid="B20" ref-type="bibr">20</xref>). The coevolution of a number of pathogen avirulence (<italic>Avr</italic>) and plant <italic>NLR</italic> genes have been reported to follow the arms race model, such as the <italic>ATR1</italic> from <named-content content-type="genus-species">Hyaloperonospora parasitica</named-content> and <italic>RPP1</italic> from <italic>Arabidopsis</italic> (<xref rid="B21" ref-type="bibr">21</xref>), and <italic>AvrL567</italic> in the flax rust fungus <named-content content-type="genus-species">Melampsora lini</named-content> and <italic>L5</italic>, <italic>L6</italic>, and <italic>L7</italic> from flax (<xref rid="B22" ref-type="bibr">22</xref>). In contrast, most PRRs are extremely conserved, for example, FLS2 occurs across a wide range of monocotyledonous and dicotyledonous plant species and detects a conserved epitope of bacterial flagellin (<xref rid="B7" ref-type="bibr">7</xref>). EFR that recognizes conserved peptides of bacterial EF-Tu is highly conserved within the extensive family of the <italic>Brassicaceae</italic> (<xref rid="B8" ref-type="bibr">8</xref>).</p><p><italic>Phytophthora infestans</italic> is a devastating hemi-biotrophic oomycete that causes late blight of potato (<xref rid="B23" ref-type="bibr">23</xref>). During early infection phases, hyphae ramify through the intercellular space and form haustoria inside host cells. So far, cytoplasmic effectors of <italic>P. infestans</italic> and the molecular determinants that perceive them have been characterized extensively, but studies on the first line of defense based on apoplastic effectors and their receptors are relatively scarce. Here, we study the PcF/SCR effectors from oomycete plant pathogens by sequence and genome analysis, functional studies <italic>in planta</italic> and we compare the <italic>G-LecRK</italic> loci in different solanaceous genomes. Our findings show that the conserved PcF effector of the PcF/SCR family is widely recognized in solanaceous plant species, whereas SCR74 in <italic>P. infestans</italic> is differentially recognized in wild potato accessions and experiences accelerated evolution rates, potentially in an arms race with a family of <italic>G-LecRK</italic> kinases.</p></sec><sec sec-type="results" id="s2"><title>RESULTS</title><sec id="s2.1"><title>PcF/SCR effectors are specific to oomycetes.</title><p>To study the PcF/SCR family, 57 PcF domain-containing proteins (PF09461) were obtained from InterPro. The PcF/SCR proteins were only present in oomycetes, including <named-content content-type="genus-species">Hyaloperonospora arabidopsidis</named-content> (<xref rid="B2" ref-type="bibr">2</xref>), <named-content content-type="genus-species">Phytophthora cactorum</named-content> (<xref rid="B2" ref-type="bibr">2</xref>), <named-content content-type="genus-species">Phytophthora capsici</named-content> (<xref rid="B1" ref-type="bibr">1</xref>), <named-content content-type="genus-species">Phytophthora parasitica</named-content> (<xref rid="B16" ref-type="bibr">16</xref>), <named-content content-type="genus-species">Phytophthora ramorum</named-content> (<xref rid="B1" ref-type="bibr">1</xref>), <named-content content-type="genus-species">Phytophthora sojae</named-content> (<xref rid="B4" ref-type="bibr">4</xref>), and <named-content content-type="genus-species">Phytophthora infestans</named-content> (<xref rid="B24" ref-type="bibr">24</xref>). Eleven redundant PcF-like proteins were removed, and the remaining 45 PcF/SCR proteins were renamed by the species abbreviation and the number of amino acids of the full-length protein (<xref ref-type="supplementary-material" rid="tabS1">Table S1</xref> in the supplemental material). Furthermore, by using SCR74 and PcF as the query, we performed tBlastn against 23 public available <italic>Phytophthora</italic> genomes, including <named-content content-type="genus-species">P. mirabilis</named-content>, <named-content content-type="genus-species">P. ipomoeae</named-content>, <named-content content-type="genus-species">P. andina</named-content>, and <named-content content-type="genus-species">P. phaseoli</named-content>, which are close relatives of <italic>P. infestans</italic> (<xref rid="B25" ref-type="bibr">25</xref>), and 20 extra PcF/SCR proteins were identified (<xref ref-type="supplementary-material" rid="tabS1">Table S1</xref>). Our data suggest that the PcF/SCR family is restricted to <italic>Peronosporales</italic> and has expanded dramatically in <italic>P. infestans</italic>.</p><supplementary-material content-type="local-data" id="tabS1"><object-id pub-id-type="doi">10.1128/mBio.00947-20.8</object-id><label>TABLE S1</label><p>List of PcF/SCR proteins and <italic>P. cactorum</italic> isolates used in this study. Download <inline-supplementary-material id="tS1" mimetype="application" mime-subtype="vnd.openxmlformats-officedocument.spreadsheetml.sheet" xlink:href="mBio.00947-20-st001.xlsx" content-type="local-data">Table S1, XLSX file, 0.02 MB</inline-supplementary-material>.</p><permissions><copyright-statement>Copyright © 2020 Lin et al.</copyright-statement><copyright-year>2020</copyright-year><copyright-holder>Lin et al.</copyright-holder><license license-type="open-access" xlink:href="https://creativecommons.org/licenses/by/4.0/"><license-p>This content is distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution 4.0 International license</ext-link>.</license-p></license></permissions></supplementary-material></sec><sec id="s2.2"><title>SCR74 is expanded in <italic>P. infestans</italic>.</title><p>To analyze the sequence diversity and phylogeny of the PcF/SCR family, the PcF domains of the 65 PcF/SCR proteins were subjected to sequence alignment by MAFFT and a NJ tree was generated (<xref ref-type="supplementary-material" rid="figS1">Fig. S1</xref>). Due to reticulate sequence exchange events that might have happened in this family (<xref rid="B12" ref-type="bibr">12</xref>), a network analysis was also made to reflect the phylogeny (<xref ref-type="fig" rid="fig1">Fig. 1</xref>). PcSCR96 from <italic>P. cactorum</italic> was included as an outgroup. Based on the alignment and network analysis, the PcF/SCR proteins were classified into three clades, i.e., a PcF clade, an SCR74 clade, and a PcF/SCR clade, respectively (<xref ref-type="fig" rid="fig1">Fig. 1</xref>, <xref ref-type="supplementary-material" rid="figS1">Fig. S1</xref>). All full-length PcF/SCR proteins from <italic>Phytophthora</italic> contain 6 to 8 highly conserved cysteines that are involved in S-bridge formation, and a conserved motif, Y/HSxS/ANXXI/VSQ/K of 18 to 27 amino acids (aa). A highly variable region from amino acid position 31 to 51 is present in these PcF/SCR proteins; members of the SCR74 clade share an AINA/PD/EPV/IA motif, that is different in the other clades (<xref ref-type="supplementary-material" rid="figS1">Fig. S1</xref>). Of note, this SCR74 clade consists only of variants from <italic>P. infestans</italic>, and 1 SCR74 protein from <italic>P. andina</italic>, which is a hybrid of <italic>P. infestans</italic> (<xref rid="B26" ref-type="bibr">26</xref>). In contrast, the PcF clade and the PcF/SCR clade contains proteins from various species. Overall, the PcF/SCR family occurs as three clades, from which the SCR74 clade seems to have evolved specifically in <italic>P. infestans</italic> (<xref ref-type="fig" rid="fig1">Fig. 1</xref>).</p><fig id="fig1" orientation="portrait" position="float"><label>FIG 1</label><caption><p>Network of PcF/SCR74 effectors. The network of the 65 PcF/SCR proteins are shown for 19 <italic>Phytophthora</italic> species (including <italic>P. infestans</italic>, <italic>P. andina</italic>, <italic>P. sojae</italic>, <italic>P. parasitica</italic>, <italic>P. cactorum</italic>, <italic>P. capsici</italic>, and <italic>P. ramorum</italic>) (the others are shown in <xref ref-type="supplementary-material" rid="figS1">Fig. S1</xref> and <xref ref-type="supplementary-material" rid="tabS1">Table S1</xref>) and <italic>Hyaloperonospora arabidopsidis</italic> (spp. marked by colored dots). The PcF and PcF/SCR74 clades are shaded gray, and the <italic>P. infestans</italic>-specific SCR74 clade is shaded red. PcF orthologs are marked with a black triangle (see <xref ref-type="fig" rid="fig2">Fig. 2A</xref>).</p></caption><graphic xlink:href="mBio.00947-20-f0001"></graphic></fig><supplementary-material content-type="local-data" id="figS1"><object-id pub-id-type="doi">10.1128/mBio.00947-20.1</object-id><label>FIG S1</label><p>Alignment of the PcF domain (PF09461) of 65 PcF/SCR proteins. The 65 PcF/SCR proteins are classified into 3 clades, i.e., a PcF clade, a PcF/SCR clade, and an SCR74 clade. PcSCR96 was used as outgroup for phylogeny analysis. Download <inline-supplementary-material id="fS1" mimetype="image" mime-subtype="tif" xlink:href="mBio.00947-20-sf001.tif" content-type="local-data">FIG S1, TIF file, 2.4 MB</inline-supplementary-material>.</p><permissions><copyright-statement>Copyright © 2020 Lin et al.</copyright-statement><copyright-year>2020</copyright-year><copyright-holder>Lin et al.</copyright-holder><license license-type="open-access" xlink:href="https://creativecommons.org/licenses/by/4.0/"><license-p>This content is distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution 4.0 International license</ext-link>.</license-p></license></permissions></supplementary-material></sec><sec id="s2.3"><title>PcF is a conserved apoplastic effector of <italic>Phytophthora</italic>.</title><p>So far, two PcF variants from <italic>P. cactorum</italic> were reported (<xref rid="B11" ref-type="bibr">11</xref>, <xref rid="B16" ref-type="bibr">16</xref>). To study the sequence polymorphism that occurs for <italic>PcF</italic> genes, <italic>PcF</italic> orthologs from nine <italic>P. cactorum</italic> strains, isolated from the United States or Europe, were amplified and sequenced. The sequence alignments indicate that <italic>PcF</italic> genes are highly conserved in all tested <italic>P. cactorum</italic> isolates (<xref ref-type="fig" rid="fig2">Fig. 2A</xref>). Only one nonsynonymous mutation was found in the predicted signal peptide of PcF (PcF-<ext-link ext-link-type="uri" xlink:href="https://www.ncbi.nlm.nih.gov/nuccore/AF354650" assigning-authority="genbank">AF354650</ext-link>), and another synonymous mutation was found in the effector domain of NL2003-3 (<xref ref-type="fig" rid="fig2">Fig. 2A</xref>, <xref ref-type="supplementary-material" rid="figS2">Fig. S2</xref>). The amino acid sequence of the effector domain was fully conserved for all identified <italic>PcF</italic> homologs. Our results indicate that <italic>PcF</italic> genes are highly conserved and appear to undergo purifying selection in <italic>P. cactorum</italic> strains from different geographic locations.</p><fig id="fig2" orientation="portrait" position="float"><label>FIG 2</label><caption><p>PcF and Scr74 possess MAMP and effector characteristics, respectively. (A) Graphical representation of a sequence alignment of <italic>PcF</italic> genes from nine <italic>P. cactorum</italic> isolates from the USA and Europe (<xref ref-type="supplementary-material" rid="tabS1">Table S1</xref>). The polymorphic amino acids are highlighted by different colors in the alignment, the synonymous and nonsynonymous SNP are shown by black and red dots, respectively. The cysteine residues are shaded by blue, the cysteines and the predicted disulfide bridge are marked by black lines. (B) <italic>PcF</italic> flanking sequences from <italic>P. infestans</italic> (500 kb), <italic>P. sojae</italic>, <italic>P. ramorum</italic>, <italic>P. capsici</italic> (200 kb), and <italic>P. cactorum</italic> (a short contig) containing the <italic>PcF</italic> orthologs <italic>PiScr70</italic>, <italic>PsScr77</italic>, <italic>PrScr74</italic>, <italic>PcapScr82</italic>, and <italic>PcF</italic> (red arrows), respectively, were aligned by Mauve. Regions of significant synteny are displayed as colored locally colinear blocks (LCBs) based on Mauve’s progressive algorithm. (C) Graphical representation of a DNA sequence alignment of 13 <italic>Scr74</italic> variants from <italic>P. infestans</italic>. The predicted polymorphic amino acids are highlighted by different colors in the alignment, the synonymous and nonsynonymous SNP are shown by black and red dots above the illustration, respectively. The predicted cysteines are shaded blue, and the disulfide bridges are marked by black lines. (D) The <italic>Scr74</italic> homologs (red arrows) <italic>PITG_14645</italic>, <italic>PITG_18592</italic>, and a pseudogene originate from supercontigs 1.36, 1.73, and 1.4, respectively. Regions (15 kb) from supercontig 1.73 and supercontig 1.4 were extracted for alignment. The pairwise identity is illustrated by the bars above the sequence alignment (100%, green; 30 to 100%, yellow; <30%, red). The <italic>Scr74</italic> genes and the flanking 3 kb show synteny in these two supercontigs. The gypsy retrotransposons are annotated by green arrows. (E) The distance between flanking genes of the reference <italic>P. infestans</italic> isolate T30-4 were plotted in a heatmap, where the <italic>x</italic> and <italic>y</italic> axes present the 3′ and 5′ intergenic distances, respectively. The gene density is shown by different colors. The intergenic gene distances of <italic>Epi1</italic> (<italic>PITG_22681</italic>), <italic>PiScr70</italic> (<italic>PITG_22677</italic>), <italic>Avr3a</italic> (<italic>PITG_14371</italic>), and <italic>Avrblb2</italic> (<italic>PITG_20300</italic>), as well as two <italic>Scr74</italic> homologs (<italic>PITG_14645</italic> and <italic>PITG_18592</italic>), are plotted on the heatmap. (F) The relative expression pattern of <italic>Avr3a</italic> (<italic>PITG_14371</italic>), <italic>Inf1</italic> (<italic>PITG_12551</italic>), <italic>Epi1</italic> (<italic>PITG_22681</italic>), <italic>Avrblb2</italic> (<italic>PITG_20300</italic>), and <italic>PiSCR70</italic> (<italic>PITG_22677</italic>) in different structures and infection stages, including sporangia, zoospores, and 2, 3, and 4 days after inoculation on potato. (G) Confocal projections reveal that SCR74-B3b-mRFP fusion proteins of <italic>P. infestans</italic> transformants are secreted at haustoria (H) during infection of <named-content content-type="genus-species">Nicotiana benthamiana</named-content>. GFP was imaged with 488 nm excitation and emissions collected between 500 and 530 nm, respectively. mRFP fluorescent proteins were excited with 561 nm light and fluorophore emission was detected between 600 and 630 nm. Projections were collected from leaf tissue infected by <italic>P. infestans</italic> transformants.</p></caption><graphic xlink:href="mBio.00947-20-f0002"></graphic></fig><supplementary-material content-type="local-data" id="figS2"><object-id pub-id-type="doi">10.1128/mBio.00947-20.2</object-id><label>FIG S2</label><p><italic>PcF</italic> loci are conserved in different oomycetes and <italic>PcF</italic> genes are conserved in different <named-content content-type="genus-species">P. cactorum</named-content> isolates. (A) Amino acid alignment of PcF proteins from nine <italic>P. cactorum</italic> isolates from the USA and Europe. (B) Flanking sequences of 500 kb of PcF from <named-content content-type="genus-species">P. infestans</named-content> and 200 kb of PcF from <named-content content-type="genus-species">P. sojae</named-content>, <named-content content-type="genus-species">P. ramorum</named-content>, and <named-content content-type="genus-species">P. capsici</named-content>, along with a short contig from <italic>P. cactorum</italic>, were aligned by Mauve. Regions of significant synteny are displayed as colored locally collinear blocks (LCBs) based on Mauve’s progressive algorithm. The LCBs are connected by colored lines between the species. The <italic>PcF</italic> orthologs (<italic>PiSCR70</italic>, <italic>PsSCR77</italic>, <italic>PrSCR74</italic>, <italic>PcapSCR82</italic>, and <italic>PcF</italic>) from the 5 <italic>Phytophthora</italic> species are shown with black arrows. Download <inline-supplementary-material id="fS2" mimetype="image" mime-subtype="tif" xlink:href="mBio.00947-20-sf002.tif" content-type="local-data">FIG S2, TIF file, 1.7 MB</inline-supplementary-material>.</p><permissions><copyright-statement>Copyright © 2020 Lin et al.</copyright-statement><copyright-year>2020</copyright-year><copyright-holder>Lin et al.</copyright-holder><license license-type="open-access" xlink:href="https://creativecommons.org/licenses/by/4.0/"><license-p>This content is distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution 4.0 International license</ext-link>.</license-p></license></permissions></supplementary-material><p>To further study whether <italic>PcF</italic> loci are conserved in diverse <italic>Phytophthora</italic> species, we extracted the <italic>PcF</italic> loci and the flanking 250-kb region from the genome of <italic>P. infestans</italic>, the 100-kb flanking sequence from <named-content content-type="genus-species">P. sojae</named-content>, <named-content content-type="genus-species">P. ramorum</named-content>, and <named-content content-type="genus-species">P. capsici</named-content>, and a short contig containing <italic>PcF</italic> from <italic>P. cactorum.</italic> Sequence alignment of the <italic>PcF</italic> loci (<xref ref-type="fig" rid="fig2">Fig. 2B</xref>, <xref ref-type="supplementary-material" rid="figS2">Fig. S2</xref>) shows a colinear structure of <italic>PcF</italic> loci in <italic>Phytophthora</italic>. Considering that these <italic>Phytophthora</italic> species cover the breadth of diversity of the genus, we postulate that <italic>PcF</italic> is an ancient and fairly conserved gene in <italic>Phytophthora</italic>.</p></sec><sec id="s2.4"><title><italic>Scr74</italic> is a fast-evolving apoplastic effector.</title><p>SCR74 proteins were reported to be highly diverse and under strong positive selection pressure, based on 21 <italic>scr74</italic> variants from 8 <italic>P. infestans</italic> strains (<xref rid="B12" ref-type="bibr">12</xref>) (<xref ref-type="fig" rid="fig2">Fig. 2C</xref>). With the increased amount of NGS data, we reevaluated the sequence diversity of SCR74 for 52 <italic>P. infestans</italic> isolates present in the public databases and two <italic>P. infestans</italic> isolates sequenced in this study (<xref ref-type="supplementary-material" rid="figS3">Fig. S3</xref>). Our observation supports the previous findings, that: (i) <italic>Scr74</italic> genes are present in all sequenced <italic>P. infestans</italic> isolates; (ii) the sequences of <italic>Scr74</italic> genes are highly diverse and display a marked signature of positive selection as previously reported by Liu et al. (<xref rid="B12" ref-type="bibr">12</xref>); and (iii) the cysteine residues are conserved in all tested SCR74 proteins.</p><supplementary-material content-type="local-data" id="figS3"><object-id pub-id-type="doi">10.1128/mBio.00947-20.3</object-id><label>FIG S3</label><p>Polymorphisms of SCR74 genes from 52 sequenced <italic>P. infestans</italic> isolates. The sequencing reads from 52 <italic>P. infestans</italic> isolates were mapped to the SCR74-B3b sequence, and the SNPs are shown as black dots. The protein consists of a 21-amino-acid signal peptide (SP, blue bar), and a 53-amino-acid mature protein (black bar). The cysteine residues are highlighted in yellow and they are conserved in most of the variants. Other conserved amino acids with no change or only synonymous mutation are highlighted in blue. The highly diverse amino acids with nonsynonymous mutations are highlighted in red. Download <inline-supplementary-material id="fS3" mimetype="image" mime-subtype="tif" xlink:href="mBio.00947-20-sf003.tif" content-type="local-data">FIG S3, TIF file, 2.6 MB</inline-supplementary-material>.</p><permissions><copyright-statement>Copyright © 2020 Lin et al.</copyright-statement><copyright-year>2020</copyright-year><copyright-holder>Lin et al.</copyright-holder><license license-type="open-access" xlink:href="https://creativecommons.org/licenses/by/4.0/"><license-p>This content is distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution 4.0 International license</ext-link>.</license-p></license></permissions></supplementary-material><p>To study the genomic architecture of <italic>Scr74</italic> genes in the <italic>P. infestans</italic> reference genome, we extracted three <italic>Scr74</italic>-containing supercontigs (1.36, 1.73 and 1.4) (<xref ref-type="fig" rid="fig2">Fig. 2D</xref>) from the <italic>P. infestans</italic> reference genome. There are three <italic>Scr74</italic> homologs, including a pseudogene in supercontig 1.4. By comparing the flanking region of these <italic>Scr74</italic> loci, we found the <italic>Scr74</italic> genes and the flanking regions (∼2 kb) from supercontigs 1.73 and 1.4 showed a high level of identity (<xref ref-type="fig" rid="fig2">Fig. 2D</xref>). This observation points to a translocation event at the <italic>Scr74</italic> loci, which might have been driven by gypsy transposons surrounding these <italic>Scr74</italic> genes.</p><p>Most oomycete genomes have gene-dense housekeeping regions (GDRs) and gene-sparse repeat-rich regions (GSRs), and rapidly evolving effectors tend to be located in the GSR (<xref rid="B27" ref-type="bibr">27</xref>). To visualize whether <italic>Scr74</italic> and <italic>PcF</italic> localize in GSR or gene-dense regions (GDRs), we plotted two <italic>Scr74</italic> genes and <italic>PiScr70</italic>, the <italic>PcF</italic> ortholog of <italic>P. infestans</italic>, as well as known apoplastic effectors <italic>Inf1</italic> and <italic>Epi1</italic>, and the well-characterized cytoplasmic <italic>Avrblb2</italic> and <italic>Avr3a</italic> on the flanking intergenic regions (FIRs) map of <italic>P. infestans</italic> reference genome (T30-4). The <italic>Scr74</italic> genes localize to the extreme GSR region, similar to the <italic>Avr</italic> genes <italic>Avrblb2</italic> and <italic>Avr3a</italic>. In contrast, the <italic>P. infestans PcF</italic> ortholog <italic>PiScr70</italic> lands closer to the GDR, similar to <italic>Inf1</italic>, which shares features with MAMPs (<xref rid="B28" ref-type="bibr">28</xref>) (<xref ref-type="fig" rid="fig2">Fig. 2E</xref>). Additionally, to study the expression profile of selected apoplastic and cytoplasmic effectors, cDNA microarray data of <italic>P. infestans</italic> reference isolate T30-4-infected samples were plotted for various stages (<xref rid="B29" ref-type="bibr">29</xref>). We found the expression of <italic>Scr74</italic> genes peaked at 2 to 3 days after infection (dpi), which is similar to typical <italic>Avr</italic> genes, whereas the expression pattern of <italic>PiScr70</italic> rather resembles Epi1 (<xref ref-type="fig" rid="fig2">Fig. 2F</xref>).</p><p>To investigate the localization of SCR74-B3b <italic>in planta</italic>, <italic>P. infestans</italic> transformants were generated that constitutively express free green fluorescent protein (GFP) in the cytoplasm, and stably expressed either SCR74-B3b or a cysteine mutant SCR74-27A, both with monomeric red fluorescent protein (mRFP) under the control of the constitutive Ham34 promoter (<xref ref-type="supplementary-material" rid="figS4">Fig. S4</xref>). The transformed <italic>P. infestans</italic> strains were spot-inoculated on <named-content content-type="genus-species">N. benthamiana</named-content> leaves. Confocal microscopy revealed that SCR74-B3b-mRFP proteins clearly accumulate at haustoria (<xref ref-type="fig" rid="fig2">Fig. 2G</xref>, <xref ref-type="supplementary-material" rid="figS4">Fig. S4</xref>), indicating that haustoria are the main secretion sites for SCR74, as also reported for <italic>Avr</italic> genes (<xref rid="B30" ref-type="bibr">30</xref>, <xref rid="B31" ref-type="bibr">31</xref>).</p><supplementary-material content-type="local-data" id="figS4"><object-id pub-id-type="doi">10.1128/mBio.00947-20.4</object-id><label>FIG S4</label><p><italic>Phytophthora infestans</italic> apoplastic effector SCR74-B3b is secreted at haustoria. (A) The expression of SCR74-B3b-mRFP and a cysteine mutant SCR74-B3b-27A-mRFP were confirmed in mycelium (M) and culture filtrate (CF) using immunoblotting with αmRFP antibody, and αGFP primary antibody was used to detect intercellular protein GFP to show there was no leakage in the CF with cellular proteins. Ponceau stain (PS) was used for protein loading control. Protein size markers are indicated in kDa. (B) Confocal projections reveal that both fusion proteins of SCR74-B3b-mRFP and SCR74-B3b-27A-mRFP are secreted at haustoria (H) in infected tissues by <italic>P. infestans</italic> transformants expressing SCR74-B3b-mRFP and SCR74-B3b-27A-mRFP, respectively. Download <inline-supplementary-material id="fS4" mimetype="image" mime-subtype="tif" xlink:href="mBio.00947-20-sf004.tif" content-type="local-data">FIG S4, TIF file, 2.3 MB</inline-supplementary-material>.</p><permissions><copyright-statement>Copyright © 2020 Lin et al.</copyright-statement><copyright-year>2020</copyright-year><copyright-holder>Lin et al.</copyright-holder><license license-type="open-access" xlink:href="https://creativecommons.org/licenses/by/4.0/"><license-p>This content is distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution 4.0 International license</ext-link>.</license-p></license></permissions></supplementary-material></sec><sec id="s2.5"><title>PcF and SCR74 exhibit different recognition patterns.</title><p>To bridge the sequence analysis with the function of these PcF/SCR proteins, we performed an effectoromics screening in a wide range of solanaceous plants. We tested 245 genotypes, which included 206 wild tuber-bearing potato (<italic>Solanum</italic> section <italic>Petota</italic>), 23 tomato, 7 eggplant, 10 pepper, and 8 <italic>Nicotiana</italic> genotypes. <italic>PcF</italic> and SCR96 from <italic>P. cactorum</italic>, SCR68 from <italic>P. sojae</italic>, and 13 SCR74 variants from <italic>P. infestans</italic> were cloned into potato virus X (PVX) vectors pGWC-PVX or pGR106, and transformed into <named-content content-type="genus-species">Agrobacterium tumefaciens</named-content> strain GV3101 for transient expression. The <italic>Agrobacterium</italic> clones carrying single PcF/SCR genes were toothpick-inoculated onto at least 6 leaves from 3 plants. The general necrosis-inducing CRN2 and the empty vector were used as positive and negative controls, respectively. The symptoms were scored 12 to 14 days after infection, on a range of 0 to 10, reflecting no visible response up to clear cell death in all replicates, respectively. After removing genotypes that showed unspecific cell death to pGR106 treatment, or failed to show cell death to pGR106-CRN2, there were a total of 4 <italic>Nicotiana</italic>, 2 pepper, 3 eggplant, 17 tomato, and 136 potato genotypes that were scored for their response to the effectors (<xref ref-type="fig" rid="fig3">Fig. 3</xref>, <xref ref-type="supplementary-material" rid="tabS2">Table S2</xref>).</p><fig id="fig3" orientation="portrait" position="float"><label>FIG 3</label><caption><p>Effectoromics screening of PcF/SCR effectors on plants of the <italic>Solanaceae</italic>. The intensity of cell-death response after PVX agro-infection of apoplastic effectors in leaves is represented by a heat map that ranges from dark red (strong response, average score >8), dark orange (score 7 to 8), light orange (score 5 to 6), to beige (score 0 to 4). CRN2 and the empty pGR106 vector were used as positive and negative controls, respectively. The asterisks highlight a pepper and an eggplant accession that failed to respond to CRN2-pGR106, however, PcF response were reproducible in three independent agro-infiltration experiments with coinfiltration of R3b and Avr3b as positive controls. A Bayesian tree of <italic>Solanum</italic> section <italic>Petota</italic> was generated based on previously produced AFLP data, and <named-content content-type="genus-species">S. etuberosum</named-content> genotypes were used as outgroup (<xref rid="B45" ref-type="bibr">45</xref>). The phylogeny of other <italic>Solanaceae</italic> species is the illustration based on classical taxonomy (<xref rid="B46" ref-type="bibr">46</xref>). For the PcF/SCR effectors, a NJ tree was made based on the PcF domain, and PcSCR96 was used as outgroup. The gray blocks represent spacers between plant clades. (A) Widespread recognition of PcF and SCR96 in various <italic>Solanaceae</italic>. (B) Similar recognition pattern of SCR74-C10, SCR74-B10-1, and SCR74-D4 in various wild potato species. (C) Specific response to SCR74-B3b and SCR74-B7 in <italic>Solanum microdontum</italic> subsp. <italic>gigantophyllum</italic> GIG362-6. (D) Highly restricted response to SCR74-C10 in <italic>Solanum stoloniferum</italic> STO389-4 (<xref ref-type="supplementary-material" rid="tabS2">Table S2</xref>). (E) Broad response to all SCR74 variants in <italic>Solanum chacoense</italic> CHC338-1.</p></caption><graphic xlink:href="mBio.00947-20-f0003"></graphic></fig><supplementary-material content-type="local-data" id="tabS2"><object-id pub-id-type="doi">10.1128/mBio.00947-20.9</object-id><label>TABLE S2</label><p>Effectoromics screening on <italic>Solanaceae</italic> genotypes. The intensity of cell-death response after PVX agro-infection of apoplastic effectors in leaves is represented by a heat map that ranges from dark red (strong response, average score >8), dark orange (score 7 to 8), light orange (score 5 to 6), to beige (score 0 to 4). CRN2 and empty pGR106 vector were used as positive and negative controls, respectively. Download <inline-supplementary-material id="tS2" mimetype="application" mime-subtype="vnd.openxmlformats-officedocument.spreadsheetml.sheet" xlink:href="mBio.00947-20-st002.xlsx" content-type="local-data">Table S2, XLSX file, 0.03 MB</inline-supplementary-material>.</p><permissions><copyright-statement>Copyright © 2020 Lin et al.</copyright-statement><copyright-year>2020</copyright-year><copyright-holder>Lin et al.</copyright-holder><license license-type="open-access" xlink:href="https://creativecommons.org/licenses/by/4.0/"><license-p>This content is distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution 4.0 International license</ext-link>.</license-p></license></permissions></supplementary-material><p>Our effectoromics screens showed that PcF and SCR96 from <italic>P. cactorum</italic> caused cell death responses in a wide range of diverse <italic>Solanaceae</italic>. Recognition was detected in various wild potato species, as well as tomato, pepper, eggplant, and some tobacco accessions (<xref ref-type="fig" rid="fig3">Fig. 3A</xref>, <xref ref-type="supplementary-material" rid="figS5">Fig. S5</xref>). In contrast, recognition of the <italic>P. infestans-</italic>specific effector SCR74 was restricted to <italic>Solanum</italic> section <italic>Petota</italic> and no response was noted in any other Solanaceous plants (<xref ref-type="fig" rid="fig3">Fig. 3B</xref>). The pattern of responses to SCR74 variants was highly specific, but did not seem to show any correlation to clade, species, or geographic origin. For example, most genotypes from <italic>Solanum microdontum</italic> and <italic>Solanum microdontum</italic> subsp. <italic>gigantophyllum</italic> did not recognize any of the tested SCR74 variants, but GIG362-6 showed very clear responses to SCR74-B3b and SCR74-B7 (<xref ref-type="fig" rid="fig3">Fig. 3C</xref>, <xref ref-type="supplementary-material" rid="figS5">Fig. S5</xref>). In contrast, some genotypes, such as <named-content content-type="genus-species">Solanum chacoense</named-content> CHC338-1 (<xref ref-type="fig" rid="fig3">Fig. 3E</xref>), showed response to all tested SCR74 variants, as well as PcF and SCR96, but not to SCR68. SCR68 failed to cause cell death in most tested plants, and we only detected a specific response in <named-content content-type="genus-species">S. stoloniferum</named-content> STO389-4 (<xref ref-type="supplementary-material" rid="tabS2">Table S2</xref>). Collectively, our functional screening indicates that the recognition of the conserved PcF effector is widespread in the <italic>Solanaceae</italic>, whereas recognition of the highly diverse, <italic>P. infestans</italic>-specific SCR74 is restricted to tuber-bearing potato accessions.</p><supplementary-material content-type="local-data" id="figS5"><object-id pub-id-type="doi">10.1128/mBio.00947-20.5</object-id><label>FIG S5</label><p>PcF and SCR74 responsiveness in the <italic>Solanaceae</italic>. (A) PVX agro-infection of PcF in <named-content content-type="genus-species">Capsicum annuum</named-content> (<ext-link ext-link-type="uri" xlink:href="https://www.ncbi.nlm.nih.gov/protein/CGN16796" assigning-authority="ncbi:protein">CGN16796</ext-link>), <named-content content-type="genus-species">Solanum incanum</named-content> (<ext-link ext-link-type="uri" xlink:href="https://www.ncbi.nlm.nih.gov/protein/CGN18575" assigning-authority="ncbi:protein">CGN18575</ext-link>), <named-content content-type="genus-species">Solanum hjertingii</named-content> (HJT350-1), and <named-content content-type="genus-species">Solanum polytrichon</named-content> (PLT789-6), and agro-infiltration in <named-content content-type="genus-species">Solanum lycopersicum</named-content> (<ext-link ext-link-type="uri" xlink:href="https://www.ncbi.nlm.nih.gov/protein/CGN14330" assigning-authority="ncbi:protein">CGN14330</ext-link>). (B and C) PVX agro-infection of SCR74 variants on <italic>S. polytrichon</italic> (PLT378-1) (B) and <named-content content-type="genus-species">Solanum microdontum</named-content> subsp. <italic>gigantophyllum</italic> (GIG362-6) (C). CRN2 is included as a positive control for PVX agro-infection, and coinfiltration of R3b and Avr3b for agro-infiltration. The empty PVX vector is used as negative control. Download <inline-supplementary-material id="fS5" mimetype="image" mime-subtype="tif" xlink:href="mBio.00947-20-sf005.tif" content-type="local-data">FIG S5, TIF file, 2.4 MB</inline-supplementary-material>.</p><permissions><copyright-statement>Copyright © 2020 Lin et al.</copyright-statement><copyright-year>2020</copyright-year><copyright-holder>Lin et al.</copyright-holder><license license-type="open-access" xlink:href="https://creativecommons.org/licenses/by/4.0/"><license-p>This content is distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution 4.0 International license</ext-link>.</license-p></license></permissions></supplementary-material><p>To further explore the specificity of SCR74 recognition in wild potato, we compared the responses of the potato genotypes with the phylogenic relationships of the SCR74 members. For all individual SCR74 variants, at least one responding wild potato was identified and patterns of recognition were discerned. We noted that SCR74 variants that were classified in a same cluster, such as SCR74-C10, -B10-1, and -D4 (<xref ref-type="fig" rid="fig3">Fig. 3D</xref>, <xref ref-type="supplementary-material" rid="figS1">Fig. S1</xref>) were in many cases causing cell death in the same set of genotypes, apart from exceptions such as PLT378-2 (<xref ref-type="supplementary-material" rid="figS6">Fig. S6</xref>). Similarly, examples such as SCR74-B3b and SCR74-B7, which only differ in two polymorphic amino acids (<xref ref-type="supplementary-material" rid="figS1">Fig. S1</xref>), share specific cell death profiles of some sets of <italic>Solanum</italic> genotypes (<xref ref-type="fig" rid="fig3">Fig. 3C</xref>, <xref ref-type="supplementary-material" rid="tabS2">Table S2</xref>). These results indicate that multiple SCR74 receptors are present and that they recognize different but closely related SCR74 variants.</p><supplementary-material content-type="local-data" id="figS6"><object-id pub-id-type="doi">10.1128/mBio.00947-20.6</object-id><label>FIG S6</label><p>Single amino acid change of SCR74 leads to altered recognition specificity. (A) Protein alignment of SCR74-D4, -B4, and -C10 The predicted S-S bridges (yellow bars) and the α-helix (green bars) are indicated. (B) Predicted structure of the mature SCR74 protein, where the polymorphic amino acid between SCR74-D4, - B4, and -C10 at position 28 is shown. (C) PTA767-1 recognizes SCR74-D4, -B4, and -C10, whereas PLT378-2 can only recognize SCR74-C10. (D) Two SCR74 cysteine mutations SCR74-synB3b-27A and SCR74-synB3b-47A were synthesized and PVX agro-infected on GIG362-6 leaves together with SCR74-B3b and a codon-optimized SCR74-B3b. CRN2 and empty vector were used as positive and negative controls, respectively. The photo was taken 14 dpi. Download <inline-supplementary-material id="fS6" mimetype="image" mime-subtype="tif" xlink:href="mBio.00947-20-sf006.tif" content-type="local-data">FIG S6, TIF file, 2.2 MB</inline-supplementary-material>.</p><permissions><copyright-statement>Copyright © 2020 Lin et al.</copyright-statement><copyright-year>2020</copyright-year><copyright-holder>Lin et al.</copyright-holder><license license-type="open-access" xlink:href="https://creativecommons.org/licenses/by/4.0/"><license-p>This content is distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution 4.0 International license</ext-link>.</license-p></license></permissions></supplementary-material><p>To test if the cysteines are important for the SCR74 activity, we synthesized two SCR74-B3b cysteine mutants and functionally tested them in SCR74-responding <italic>Solanum microdontum</italic> subsp. <italic>gigantophyllum</italic> genotype GIG362-6 plants. The mutants failed to cause cell death, showing that S-bridges are critical for SCR74 function (<xref ref-type="supplementary-material" rid="figS6">Fig. S6D</xref>).</p></sec><sec id="s2.6"><title><italic>G-LecRK</italic> locus in wild potato mediates the response to SCR74-B3b.</title><p>Recently, with a newly developed RLP/RLK gene enrichment sequencing (RLP/KSeq), we mapped the response to SCR74 to a locus at the top of chromosome 9 in GIG362-6 (<xref rid="B15" ref-type="bibr">15</xref>). Based on the reference genome <italic>S. tuberosum</italic> Group <italic>Phureja</italic> clone DM1-3, the mapping interval contains eight genes, i.e., three receptor-like kinases with a G-type lectin domain (<italic>G-LecRK</italic>) genes, a putative reticulate-related 1 like gene, a serine/threonine-protein kinase ATG1c-like (autophagy-related protein) gene, a prenylated rab acceptor family gene, and a uracil phosphoribosyltransferase-encoding gene (<xref ref-type="fig" rid="fig4">Fig. 4C</xref>, <xref ref-type="supplementary-material" rid="figS7">Fig. S7</xref>). Previously, we had isolated the BAC clone on the responsiveness haplotype of GIG362-6 (<xref rid="B15" ref-type="bibr">15</xref>), here we isolated the BAC clone from another haplotype of GIG362-6, and, strikingly, two and five <italic>G-LecRK</italic> genes were found in the responsive and nonresponsive haplotypes, respectively (<xref ref-type="fig" rid="fig4">Fig. 4B</xref>).</p><fig id="fig4" orientation="portrait" position="float"><label>FIG 4</label><caption><p>The candidate SCR74 receptor is located on a highly diverse <italic>G-LecRK</italic> locus. (A) The candidate SCR74-B3b receptor is located in a 73-kb (0.1cM) region between marker S111 and S105 on chromosome 9, based on the reference clone DM1-3 genome, and 43-kb on GIG-BAC013A. The numbers of recombination events are shown in red (<xref rid="B15" ref-type="bibr">15</xref>). (B) Two BAC clones GIG-BAC013A and GIG-BAC012B from GIG362-6 were isolated and sequenced. GIG-BAC013A (red) represents the haplotype with the candidate SCR74 receptor. GIG-BAC012B (blue) represents another haplotype from GIG362-6. The genomic region of pepper (<named-content content-type="genus-species">C. annuum</named-content>), eggplant (<named-content content-type="genus-species">S. melongena</named-content>), tomato (<named-content content-type="genus-species">S. lycopersicum</named-content>), <named-content content-type="genus-species">S. verrucosum</named-content>, <named-content content-type="genus-species">S. chacoense</named-content> M6, and of 2 haploytypes from <italic>S. microdontum</italic> subsp. <italic>gigantophyllum</italic> (genotype GIG362-6) are shown. Predicted genes are represented as arrows, i.e., <italic>G-LecRK</italic> (red), putative reticulata related 1-like genes (yellow), ATG1c-like genes (blue), prenylated rab acceptor family (green), and uracil phosphoribosyltransfease genes (pink).</p></caption><graphic xlink:href="mBio.00947-20-f0004"></graphic></fig><supplementary-material content-type="local-data" id="figS7"><object-id pub-id-type="doi">10.1128/mBio.00947-20.7</object-id><label>FIG S7</label><p>Differential expression of candidate genes on haplotype 1 of GIG362-6. (A) The mapping interval on GIG362-6 with the RNA-seq reads from GIG362-6, mapped to haplotype 1 (BAC03-H3 and BAC01-3A). The blue peaks present the coverage of RNA-seq reads. The samples of water treatment and UK3928A inoculation are shown. The two <italic>G-LecRKs</italic> are upregulated after UK3928A infection. (B) Differential expression of candidate genes in the mapping interval. The raw read counts and transcript per million (TPM) for each sample, as well as the differential expression ratio and the <italic>P</italic> value, are shown for the four treatments of GIG_water versus GIG_UK3928A and MCD_UK3928A versus GIG_UK3928A. The upregulated genes are highlighted in red, the downregulated genes are highlighted in blue. The significant (<italic>P</italic> < 0.05) differential expression <italic>P</italic> values are shown in red font, otherwise in blue font. Download <inline-supplementary-material id="fS7" mimetype="image" mime-subtype="tif" xlink:href="mBio.00947-20-sf007.tif" content-type="local-data">FIG S7, TIF file, 2.3 MB</inline-supplementary-material>.</p><permissions><copyright-statement>Copyright © 2020 Lin et al.</copyright-statement><copyright-year>2020</copyright-year><copyright-holder>Lin et al.</copyright-holder><license license-type="open-access" xlink:href="https://creativecommons.org/licenses/by/4.0/"><license-p>This content is distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution 4.0 International license</ext-link>.</license-p></license></permissions></supplementary-material><p>To investigate whether the <italic>G-LecRK</italic> loci are conserved among different <italic>Solanaceae</italic>, we analyzed the <italic>G-LecRK</italic> loci from various other available solanaceous genomes. We found that <italic>Solanum chacoense</italic>, which is closely related to <italic>S. microdontum</italic> and clone DM1-3, contains four partial and three full-length <italic>G-LecRK</italic> genes in the locus. In another wild potato, <named-content content-type="genus-species">Solanum verrucosum</named-content>, we detected four <italic>G-LecRK</italic> genes (<xref rid="B24" ref-type="bibr">24</xref>). The more distantly related pepper and tomato isolates contained only one <italic>G-LecRK</italic>, and eggplant contained two (<xref ref-type="fig" rid="fig4">Fig. 4B</xref>). The copy number variation (CNV) data indicate that the <italic>G-LecRK</italic> loci are highly diverse and they seem expanded in wild potato species.</p><p>To evaluate the gene expression level of the candidate genes during <italic>P. infestans</italic> infection, we performed a transcriptome sequencing (RNA-seq) experiment on the mapping parents GIG362-6 and MCD360-1, 48 h postinoculation (hpi) with <italic>P. infestans</italic> isolate UK3928A or mock-inoculated with water. The RNA-seq reads were mapped to the BAC sequences of GIG362-6 and show that the <italic>G-LecRK</italic> genes are upregulated after infection (<xref ref-type="supplementary-material" rid="figS7">Fig. S7</xref>), which suggests they may play role in the interaction with <italic>P. infestans</italic>.</p></sec></sec><sec sec-type="discussion" id="s3"><title>DISCUSSION</title><p>Plants and pathogens undergo an endless coevolutionary tug of war. Until now, the far majority of molecular studies have focused on cytoplasmic effectors representing <italic>Avr</italic> genes that coevolve with plant NLR receptors (<xref rid="B32" ref-type="bibr">32</xref>). However, the degree of coevolution between surface immune receptors and apoplastic effectors has been understudied. Traditionally, many apoplastic effectors were thought to be conserved, MAMP-like molecules. However, the boundary between the MAMPs and effectors, and consequently between MAMP-triggered immunity (MTI) and effector-triggered immunity (ETI), is less strict in many cases. The invasion model describes recognition between those ligand/receptor molecules as a process that continuously takes place during host infection (<xref rid="B33" ref-type="bibr">33</xref>, <xref rid="B34" ref-type="bibr">34</xref>). In this study, we build further on the invasion model and show that subclades of an apoplastic effector family in oomycetes have undergone divergent evolutionary paths.</p><p>A family of PcF/SCR74 effectors that share a PcF domain occurs in <italic>Peronosporales</italic>, and four subclades can be distinguished (<xref rid="B11" ref-type="bibr">11</xref>). We found that the subclade of <italic>PcF</italic> is conserved in <italic>Phytophthora</italic> species, as <italic>PcF</italic> orthologs share a high sequence identity and a colinear structure among various <italic>Phytophthora</italic> genomes. Similar to typical MAMPs, such as flagellin, PcF is widely recognized by diverse plant species, like pepper, eggplant, tomato, and potato, and recognition even occurs beyond the <italic>Solanaceae</italic>, e.g., strawberry (<xref rid="B11" ref-type="bibr">11</xref>). In contrast, SCR74 variants are exclusively present in <italic>P. infestans</italic>, with their sequences highly diverse and under strong positive selection pressure (<xref rid="B12" ref-type="bibr">12</xref>). We found the recognition of SCR74 variants is restricted to wild potato host plants. Therefore, we conclude that although PcF and SCR74 belong to the same effector family, they are shaped under a divergent evolutionary path during coevolution with their host. PcF/SCR74 clades 1 and 2 represent intermediates, leading to blurred boundaries between typical MAMPs and effectors (<xref rid="B34" ref-type="bibr">34</xref>). Our findings suggest that the apoplastic (SCR74) effectors likely evolved from the conserved PcF molecules and underwent a coevolutionary arms race in the host species of <italic>P. infestans</italic>.</p><p>The gene conferring response to SCR74 has been fine mapped to a locus of <italic>G-lecRK</italic> that shows upregulation upon <italic>P. infestans</italic> infection (<xref rid="B15" ref-type="bibr">15</xref>), which suggests that these <italic>G-LecRK</italic> genes are the most likely candidates for encoding the SCR74 receptor. A few other <italic>G-LecRK</italic> genes have recently been reported to be involved in plant immunity, e.g: <italic>I-3</italic> from tomato conferring resistance to <named-content content-type="genus-species">Fusarium oxysporum</named-content>. Also for <italic>I-3</italic>, functional complementation of the candidate <italic>G-LecRK</italic> gene has not been achieved yet, perhaps because some surfaces receptors often act in networks and require multiple components (<xref rid="B35" ref-type="bibr">35</xref>). Other <italic>G-LecRK</italic> examples are <italic>Pi-d2</italic> and <italic>OsLecRK1-3</italic>, conferring resistance to <named-content content-type="genus-species">Magnaporthe oryzae</named-content> and brown planthopper, respectively, and <italic>LORE</italic> from <italic>Arabidopsis</italic> that can mediate bacterial lipopolysaccharide-copurified medium-chain 3-hydroxy fatty acid (mc-3-OH-FA) sensing (<xref rid="B24" ref-type="bibr">24</xref>, <xref rid="B32" ref-type="bibr">32</xref><xref ref-type="bibr" rid="B33">–</xref><xref rid="B35" ref-type="bibr">35</xref>). Additionally, <italic>SRK</italic>, a well-characterized <italic>G-LecRK</italic> from <italic>Brassica</italic> is the female determinant of self-incompatibility (SI) (<xref rid="B36" ref-type="bibr">36</xref>) that recognizes the S-haplotype-specific SCR/SP11 from self-pollen (<xref rid="B36" ref-type="bibr">36</xref>, <xref rid="B37" ref-type="bibr">37</xref>). This points to remarkable parallels between plant immunity and SI as a “social disease,” where both systems include the invading of a host cell by a tubular cell; both interactions are driven by highly diverse G-LecRK receptors and SCR ligands; and both outcomes of the incompatible responses lead to cell death (<xref rid="B38" ref-type="bibr">38</xref>).</p><p>The <italic>G-LecRK</italic> genes show CNV in the two haplotypes of GIG362-6, with two or five copies, respectively. The copy number of these <italic>G-LecRKs</italic> in different potato genomes varies dramatically, namely, three, four and seven full-length or partial <italic>G-LecRK</italic> genes were found in the DM1-3 potato, <italic>Solanum verrucosum</italic>, and <italic>Solanum chacoense</italic> genomes, respectively, which suggests this locus has been under evolutionary pressure in wild potato species. Other, more distant <italic>Solanaceae</italic>, such as tomato, pepper, and eggplant, only contained one or a maximum of two <italic>G-LecRK</italic> genes in their genome. Our genetic data provide further evidence about the coevolution hypothesis that the highly diverse apoplastic SCR74 effectors coevolve with the receptors in their wild potato host species.</p><p>This study contributes to deeper insight into the molecular dialogue between oomycetes and their hosts, in particular for <italic>P. infestans</italic> and potato. We showed that the PcF/SCR effector family acts as “invasion patterns” (<xref rid="B33" ref-type="bibr">33</xref>, <xref rid="B34" ref-type="bibr">34</xref>) that have experienced distinct evolutionary trajectories during coevolution with their host. This work also has implications for breeding sustainable resistance to <italic>P. infestans</italic>. To date, breeding for resistance against late blight has had an emphasis on the <italic>NLR</italic> genes, which are typically defeated rapidly by the fast-evolving and highly adaptable <italic>P. infestans</italic>. The <italic>G-LecRK</italic> locus we identified as mediating response to SCR74-B3b is a new source of immune receptors from wild potatoes that complements other recently discovered PRRs that operate against <italic>P. infestans</italic> (<xref rid="B9" ref-type="bibr">9</xref>, <xref rid="B39" ref-type="bibr">39</xref>). Stacking these surface immune receptors and combining them with NLRs might provide a tool to target a wide spectrum of the <italic>P. infestans</italic> population and contribute a new source of disease resistance into potato breeding.</p></sec><sec sec-type="materials|methods" id="s4"><title>MATERIALS AND METHODS</title><sec id="s4.1"><title>Phylogenetic analysis of PcF/SCR proteins.</title><p>PcF domain-containing proteins (IPR018570) were obtained from InterPro. The protein sequences were aligned by MAFFT v7.309 (<xref rid="B40" ref-type="bibr">40</xref>) and Geneious R10. Redundant sequences were removed manually based on the alignment outputs. A neighbor-joining tree was performed by Geneious R10, using the Jukes-Cantor model. The phylogeny network was made by SplitTree4 (<xref rid="B41" ref-type="bibr">41</xref>). More details are in the Materials and Methods section of the supplemental materials.</p></sec><sec id="s4.2"><title>Genome data and sequence analysis.</title><p>The oomycete genomes were obtained from EnsemblProtists (<ext-link ext-link-type="uri" xlink:href="http://protists.ensembl.org/">http://protists.ensembl.org/</ext-link>) or JGI genome portal (<ext-link ext-link-type="uri" xlink:href="https://genome.jgi.doe.gov">https://genome.jgi.doe.gov</ext-link>), including <italic>P. infestans</italic> (ASM14294v1) (<xref rid="B29" ref-type="bibr">29</xref>), <italic>P. sojae</italic> (<italic>P. sojae</italic> V3.0), <italic>P. ramorum</italic> (ASM14973v1) (<xref rid="B42" ref-type="bibr">42</xref>), and <italic>P. capsici</italic> (LT1534 v11.0) (<xref rid="B43" ref-type="bibr">43</xref>). The draft genome of <italic>P. cactorum</italic> strain LV007 can be obtained from GenBank (<ext-link ext-link-type="uri" xlink:href="https://www.ncbi.nlm.nih.gov/nuccore/NBIJ01000000" assigning-authority="genbank">NBIJ01000000</ext-link>) (<xref rid="B44" ref-type="bibr">44</xref>). More details are in the Materials and Methods section of the supplemental materials.</p><p><bold><italic>Phytophthora</italic> isolates.</bold><italic>Phytophthora cactorum</italic> isolates that were used in this study are listed in <xref ref-type="supplementary-material" rid="tabS1">Table S1</xref>.</p></sec><sec id="s4.3"><title>Plant material.</title><p>The seeds of tomato, pepper, and eggplant were obtained from the Centre for Genetic Resources, Wageningen, The Netherlands (CGN). The potato genotypes were clonally maintained at the <italic>in vitro Solanum</italic> collection of Plant Breeding at Wageningen University and Research.</p></sec><sec id="s4.4"><title>PVX agro-infection and agro-infiltration in plants.</title><p>The effectors were cloned into pGR106 vector and then transformed into <named-content content-type="genus-species">Agrobacterium tumefaciens</named-content> strain GV3101 for PVX agro-infection or into pK7WG2 for agro-infiltration. More details are in the Materials and Methods section of the supplemental materials.</p><supplementary-material content-type="local-data" id="textS1"><object-id pub-id-type="doi">10.1128/mBio.00947-20.10</object-id><label>TEXT S1</label><p>Detailed Materials and Methods used in this study. Download <inline-supplementary-material id="txS1" mimetype="application" mime-subtype="vnd.openxmlformats-officedocument.wordprocessingml.document" xlink:href="mBio.00947-20-s0001.docx" content-type="local-data">Text S1, DOCX file, 0.04 MB</inline-supplementary-material>.</p><permissions><copyright-statement>Copyright © 2020 Lin et al.</copyright-statement><copyright-year>2020</copyright-year><copyright-holder>Lin et al.</copyright-holder><license license-type="open-access" xlink:href="https://creativecommons.org/licenses/by/4.0/"><license-p>This content is distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution 4.0 International license</ext-link>.</license-p></license></permissions></supplementary-material></sec></sec></body><back><fn-group><fn fn-type="other"><p><bold>Citation</bold> Lin X, Wang S, de Rond L, Bertolin N, Wouters RHM, Wouters D, Domazakis E, Bitew MK, Win J, Dong S, Visser RGF, Birch P, Kamoun S, Vleeshouwers VGAA. 2020. Divergent evolution of PcF/SCR74 effectors in oomycetes is associated with distinct recognition patterns in solanaceous plants. mBio 11:e00947-20. <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.1128/mBio.00947-20">https://doi.org/10.1128/mBio.00947-20</ext-link>.</p></fn></fn-group><ack><title>ACKNOWLEDGMENTS</title><p>We thank Natalia A. Peres and Marcus Marin from the University of Florida (USA) for kindly providing us the <italic>P. cactorum</italic> isolates from the USA, Thijs van Dijk for providing the <italic>P. cactorum</italic> isolates from Europe, Juan Antonio Garcia for the pGWC-PVX vector, Isolde Bertram-Pereira for culturing <italic>Solanum</italic> plants, Henk Smid and Harm Wiegersma for help in the greenhouse, and Evert Jacobsen for reviewing the manuscript. We thank Klaas Bouwmeester for the inspiring discussions. We thank Glenn Bryan (James Hutton Institute) for sharing the genome of <italic>S. verrucosum</italic> and Stefanie Ranf (Technical University of Munich) for discussion. We thank Helene Berges and Caroline Callot from the French Plant Genomic Resource Center (INRA-CNRGV) for their help in sequencing the BAC clones.</p><p>This work was supported by NWO-VIDI grant 12378, China Scholarship Council (CSC). 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