Effector prediction and characterization in the oomycete pathogen Bremia lactucae reveal host-recognized WY domain proteins that lack the canonical RXLR motif.
Identifieur interne : 000177 ( Main/Exploration ); précédent : 000176; suivant : 000178Effector prediction and characterization in the oomycete pathogen Bremia lactucae reveal host-recognized WY domain proteins that lack the canonical RXLR motif.
Auteurs : Kelsey J. Wood [États-Unis] ; Munir Nur [États-Unis] ; Juliana Gil [États-Unis] ; Kyle Fletcher [États-Unis] ; Kim Lakeman [Pays-Bas] ; Dasan Gann [États-Unis] ; Ayumi Gothberg [États-Unis] ; Tina Khuu [États-Unis] ; Jennifer Kopetzky [États-Unis] ; Sanye Naqvi [États-Unis] ; Archana Pandya [États-Unis] ; Chi Zhang [États-Unis] ; Brigitte Maisonneuve [France] ; Mathieu Pel [Pays-Bas] ; Richard Michelmore [États-Unis]Source :
- PLoS pathogens [ 1553-7374 ] ; 2020.
Abstract
Pathogens that infect plants and animals use a diverse arsenal of effector proteins to suppress the host immune system and promote infection. Identification of effectors in pathogen genomes is foundational to understanding mechanisms of pathogenesis, for monitoring field pathogen populations, and for breeding disease resistance. We identified candidate effectors from the lettuce downy mildew pathogen Bremia lactucae by searching the predicted proteome for the WY domain, a structural fold found in effectors that has been implicated in immune suppression as well as effector recognition by host resistance proteins. We predicted 55 WY domain containing proteins in the genome of B. lactucae and found substantial variation in both sequence and domain architecture. These candidate effectors exhibit several characteristics of pathogen effectors, including an N-terminal signal peptide, lineage specificity, and expression during infection. Unexpectedly, only a minority of B. lactucae WY effectors contain the canonical N-terminal RXLR motif, which is a conserved feature in the majority of cytoplasmic effectors reported in Phytophthora spp. Functional analysis of 21 effectors containing WY domains revealed 11 that elicited cell death on wild accessions and domesticated lettuce lines containing resistance genes, indicative of recognition of these effectors by the host immune system. Only two of the 11 recognized effectors contained the canonical RXLR motif, suggesting that there has been an evolutionary divergence in sequence motifs between genera; this has major consequences for robust effector prediction in oomycete pathogens.
DOI: 10.1371/journal.ppat.1009012
PubMed: 33104763
PubMed Central: PMC7644090
Affiliations:
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Wood</name><affiliation wicri:level="2"><nlm:affiliation>The Genome Center, University of California, Davis, Davis, California, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>The Genome Center, University of California, Davis, Davis, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation><affiliation wicri:level="2"><nlm:affiliation>Integrative Genetics & Genomics Graduate Group, University of California, Davis, Davis, California, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Integrative Genetics & Genomics Graduate Group, University of California, Davis, Davis, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Nur, Munir" sort="Nur, Munir" uniqKey="Nur M" first="Munir" last="Nur">Munir Nur</name><affiliation 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Wood</name><affiliation wicri:level="2"><nlm:affiliation>The Genome Center, University of California, Davis, Davis, California, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>The Genome Center, University of California, Davis, Davis, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation><affiliation wicri:level="2"><nlm:affiliation>Integrative Genetics & Genomics Graduate Group, University of California, Davis, Davis, California, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Integrative Genetics & Genomics Graduate Group, University of California, Davis, Davis, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Nur, Munir" sort="Nur, Munir" uniqKey="Nur M" first="Munir" last="Nur">Munir Nur</name><affiliation wicri:level="2"><nlm:affiliation>The Genome Center, University of California, Davis, Davis, California, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>The Genome Center, University of California, Davis, Davis, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Gil, Juliana" sort="Gil, Juliana" uniqKey="Gil J" first="Juliana" last="Gil">Juliana Gil</name><affiliation wicri:level="2"><nlm:affiliation>The Genome Center, University of California, Davis, Davis, California, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>The Genome Center, University of California, Davis, Davis, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation><affiliation wicri:level="2"><nlm:affiliation>Plant Pathology Graduate Group, University of California, Davis, Davis, California, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Plant Pathology Graduate Group, University of California, Davis, Davis, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Fletcher, Kyle" sort="Fletcher, Kyle" uniqKey="Fletcher K" first="Kyle" last="Fletcher">Kyle Fletcher</name><affiliation wicri:level="2"><nlm:affiliation>The Genome Center, University of California, Davis, Davis, California, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>The Genome Center, University of California, Davis, Davis, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Lakeman, Kim" sort="Lakeman, Kim" uniqKey="Lakeman K" first="Kim" last="Lakeman">Kim Lakeman</name><affiliation wicri:level="1"><nlm:affiliation>Enza Zaden, Enkhuizen, The Netherlands.</nlm:affiliation><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Enza Zaden, Enkhuizen</wicri:regionArea><wicri:noRegion>Enkhuizen</wicri:noRegion></affiliation></author><author><name sortKey="Gann, Dasan" sort="Gann, Dasan" uniqKey="Gann D" first="Dasan" last="Gann">Dasan Gann</name><affiliation wicri:level="2"><nlm:affiliation>The Genome Center, University of California, Davis, Davis, California, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>The Genome Center, University of California, Davis, Davis, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Gothberg, Ayumi" sort="Gothberg, Ayumi" uniqKey="Gothberg A" first="Ayumi" last="Gothberg">Ayumi Gothberg</name><affiliation wicri:level="2"><nlm:affiliation>The Genome Center, University of California, Davis, Davis, California, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>The Genome Center, University of California, Davis, Davis, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Khuu, Tina" sort="Khuu, Tina" uniqKey="Khuu T" first="Tina" last="Khuu">Tina Khuu</name><affiliation wicri:level="2"><nlm:affiliation>The Genome Center, University of California, Davis, Davis, California, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>The Genome Center, University of California, Davis, Davis, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Kopetzky, Jennifer" sort="Kopetzky, Jennifer" uniqKey="Kopetzky J" first="Jennifer" last="Kopetzky">Jennifer Kopetzky</name><affiliation wicri:level="2"><nlm:affiliation>The Genome Center, University of California, Davis, Davis, California, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>The Genome Center, University of California, Davis, Davis, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Naqvi, Sanye" sort="Naqvi, Sanye" uniqKey="Naqvi S" first="Sanye" last="Naqvi">Sanye Naqvi</name><affiliation wicri:level="2"><nlm:affiliation>The Genome Center, University of California, Davis, Davis, California, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>The Genome Center, University of California, Davis, Davis, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Pandya, Archana" sort="Pandya, Archana" uniqKey="Pandya A" first="Archana" last="Pandya">Archana Pandya</name><affiliation wicri:level="2"><nlm:affiliation>The Genome Center, University of California, Davis, Davis, California, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>The Genome Center, University of California, Davis, Davis, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Zhang, Chi" sort="Zhang, Chi" uniqKey="Zhang C" first="Chi" last="Zhang">Chi Zhang</name><affiliation wicri:level="2"><nlm:affiliation>The Genome Center, University of California, Davis, Davis, California, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>The Genome Center, University of California, Davis, Davis, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Maisonneuve, Brigitte" sort="Maisonneuve, Brigitte" uniqKey="Maisonneuve B" first="Brigitte" last="Maisonneuve">Brigitte Maisonneuve</name><affiliation wicri:level="1"><nlm:affiliation>INRAE, UR1052, GAFL, Montfavet, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INRAE, UR1052, GAFL, Montfavet</wicri:regionArea><wicri:noRegion>Montfavet</wicri:noRegion><wicri:noRegion>Montfavet</wicri:noRegion></affiliation></author><author><name sortKey="Pel, Mathieu" sort="Pel, Mathieu" uniqKey="Pel M" first="Mathieu" last="Pel">Mathieu Pel</name><affiliation wicri:level="1"><nlm:affiliation>Enza Zaden, Enkhuizen, The Netherlands.</nlm:affiliation><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Enza Zaden, Enkhuizen</wicri:regionArea><wicri:noRegion>Enkhuizen</wicri:noRegion></affiliation></author><author><name sortKey="Michelmore, Richard" sort="Michelmore, Richard" uniqKey="Michelmore R" first="Richard" last="Michelmore">Richard Michelmore</name><affiliation wicri:level="2"><nlm:affiliation>The Genome Center, University of California, Davis, Davis, California, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>The Genome Center, University of California, Davis, Davis, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation><affiliation wicri:level="2"><nlm:affiliation>Departments of Plant Sciences, Molecular & Cellular Biology, Medical Microbiology & Immunology, University of California, Davis, Davis, California, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Departments of Plant Sciences, Molecular & Cellular Biology, Medical Microbiology & Immunology, University of California, Davis, Davis, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author></analytic><series><title level="j">PLoS pathogens</title><idno type="eISSN">1553-7374</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">Pathogens that infect plants and animals use a diverse arsenal of effector proteins to suppress the host immune system and promote infection. Identification of effectors in pathogen genomes is foundational to understanding mechanisms of pathogenesis, for monitoring field pathogen populations, and for breeding disease resistance. We identified candidate effectors from the lettuce downy mildew pathogen Bremia lactucae by searching the predicted proteome for the WY domain, a structural fold found in effectors that has been implicated in immune suppression as well as effector recognition by host resistance proteins. We predicted 55 WY domain containing proteins in the genome of B. lactucae and found substantial variation in both sequence and domain architecture. These candidate effectors exhibit several characteristics of pathogen effectors, including an N-terminal signal peptide, lineage specificity, and expression during infection. Unexpectedly, only a minority of B. lactucae WY effectors contain the canonical N-terminal RXLR motif, which is a conserved feature in the majority of cytoplasmic effectors reported in Phytophthora spp. Functional analysis of 21 effectors containing WY domains revealed 11 that elicited cell death on wild accessions and domesticated lettuce lines containing resistance genes, indicative of recognition of these effectors by the host immune system. Only two of the 11 recognized effectors contained the canonical RXLR motif, suggesting that there has been an evolutionary divergence in sequence motifs between genera; this has major consequences for robust effector prediction in oomycete pathogens.</div></front></TEI><pubmed><MedlineCitation Status="In-Data-Review" Owner="NLM"><PMID Version="1">33104763</PMID><DateRevised><Year>2020</Year><Month>11</Month><Day>17</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Electronic">1553-7374</ISSN><JournalIssue CitedMedium="Internet"><Volume>16</Volume><Issue>10</Issue><PubDate><Year>2020</Year><Month>Oct</Month></PubDate></JournalIssue><Title>PLoS pathogens</Title><ISOAbbreviation>PLoS Pathog</ISOAbbreviation></Journal><ArticleTitle>Effector prediction and characterization in the oomycete pathogen Bremia lactucae reveal host-recognized WY domain proteins that lack the canonical RXLR motif.</ArticleTitle><Pagination><MedlinePgn>e1009012</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1371/journal.ppat.1009012</ELocationID><Abstract><AbstractText>Pathogens that infect plants and animals use a diverse arsenal of effector proteins to suppress the host immune system and promote infection. Identification of effectors in pathogen genomes is foundational to understanding mechanisms of pathogenesis, for monitoring field pathogen populations, and for breeding disease resistance. We identified candidate effectors from the lettuce downy mildew pathogen Bremia lactucae by searching the predicted proteome for the WY domain, a structural fold found in effectors that has been implicated in immune suppression as well as effector recognition by host resistance proteins. We predicted 55 WY domain containing proteins in the genome of B. lactucae and found substantial variation in both sequence and domain architecture. These candidate effectors exhibit several characteristics of pathogen effectors, including an N-terminal signal peptide, lineage specificity, and expression during infection. Unexpectedly, only a minority of B. lactucae WY effectors contain the canonical N-terminal RXLR motif, which is a conserved feature in the majority of cytoplasmic effectors reported in Phytophthora spp. Functional analysis of 21 effectors containing WY domains revealed 11 that elicited cell death on wild accessions and domesticated lettuce lines containing resistance genes, indicative of recognition of these effectors by the host immune system. Only two of the 11 recognized effectors contained the canonical RXLR motif, suggesting that there has been an evolutionary divergence in sequence motifs between genera; this has major consequences for robust effector prediction in oomycete pathogens.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Wood</LastName><ForeName>Kelsey J</ForeName><Initials>KJ</Initials><Identifier Source="ORCID">https://orcid.org/0000-0001-5725-9222</Identifier><AffiliationInfo><Affiliation>The Genome Center, University of California, Davis, Davis, California, United States of America.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Integrative Genetics & Genomics Graduate Group, University of California, Davis, Davis, California, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Nur</LastName><ForeName>Munir</ForeName><Initials>M</Initials><Identifier Source="ORCID">https://orcid.org/0000-0001-6766-0597</Identifier><AffiliationInfo><Affiliation>The Genome Center, University of California, Davis, Davis, California, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gil</LastName><ForeName>Juliana</ForeName><Initials>J</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-9042-7459</Identifier><AffiliationInfo><Affiliation>The Genome Center, University of California, Davis, Davis, California, United States of America.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Plant Pathology Graduate Group, University of California, Davis, Davis, California, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Fletcher</LastName><ForeName>Kyle</ForeName><Initials>K</Initials><Identifier Source="ORCID">https://orcid.org/0000-0003-1191-9939</Identifier><AffiliationInfo><Affiliation>The Genome Center, University of California, Davis, Davis, California, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lakeman</LastName><ForeName>Kim</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>Enza Zaden, Enkhuizen, The Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gann</LastName><ForeName>Dasan</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>The Genome Center, University of California, Davis, Davis, California, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gothberg</LastName><ForeName>Ayumi</ForeName><Initials>A</Initials><Identifier Source="ORCID">https://orcid.org/0000-0001-9530-8793</Identifier><AffiliationInfo><Affiliation>The Genome Center, University of California, Davis, Davis, California, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Khuu</LastName><ForeName>Tina</ForeName><Initials>T</Initials><AffiliationInfo><Affiliation>The Genome Center, University of California, Davis, Davis, California, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kopetzky</LastName><ForeName>Jennifer</ForeName><Initials>J</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-5040-9977</Identifier><AffiliationInfo><Affiliation>The Genome Center, University of California, Davis, Davis, California, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Naqvi</LastName><ForeName>Sanye</ForeName><Initials>S</Initials><Identifier Source="ORCID">https://orcid.org/0000-0003-2369-8109</Identifier><AffiliationInfo><Affiliation>The Genome Center, University of California, Davis, Davis, California, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Pandya</LastName><ForeName>Archana</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>The Genome Center, University of California, Davis, Davis, California, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Chi</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>The Genome Center, University of California, Davis, Davis, California, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Maisonneuve</LastName><ForeName>Brigitte</ForeName><Initials>B</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-8665-6304</Identifier><AffiliationInfo><Affiliation>INRAE, UR1052, GAFL, Montfavet, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Pel</LastName><ForeName>Mathieu</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Enza Zaden, Enkhuizen, The 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