Structural genomics applied to the rust fungus Melampsora larici-populina reveals two candidate effector proteins adopting cystine knot and NTF2-like protein folds.
Identifieur interne : 000010 ( Main/Exploration ); précédent : 000009; suivant : 000011Structural genomics applied to the rust fungus Melampsora larici-populina reveals two candidate effector proteins adopting cystine knot and NTF2-like protein folds.
Auteurs : Karine De Guillen [France] ; Cécile Lorrain [France] ; Pascale Tsan [France] ; Philippe Barthe [France] ; Benjamin Petre [France] ; Natalya Saveleva [France] ; Nicolas Rouhier [France] ; Sébastien Duplessis [France] ; André Padilla [France] ; Arnaud Hecker [France]Source :
- Scientific reports [ 2045-2322 ] ; 2019.
Abstract
Rust fungi are plant pathogens that secrete an arsenal of effector proteins interfering with plant functions and promoting parasitic infection. Effectors are often species-specific, evolve rapidly, and display low sequence similarities with known proteins. How rust fungal effectors function in host cells remains elusive, and biochemical and structural approaches have been scarcely used to tackle this question. In this study, we produced recombinant proteins of eleven candidate effectors of the leaf rust fungus Melampsora larici-populina in Escherichia coli. We successfully purified and solved the three-dimensional structure of two proteins, MLP124266 and MLP124017, using NMR spectroscopy. Although both MLP124266 and MLP124017 show no sequence similarity with known proteins, they exhibit structural similarities to knottins, which are disulfide-rich small proteins characterized by intricate disulfide bridges, and to nuclear transport factor 2-like proteins, which are molecular containers involved in a wide range of functions, respectively. Interestingly, such structural folds have not been reported so far in pathogen effectors, indicating that MLP124266 and MLP124017 may bear novel functions related to pathogenicity. Our findings show that sequence-unrelated effectors can adopt folds similar to known proteins, and encourage the use of biochemical and structural approaches to functionally characterize effector candidates.
DOI: 10.1038/s41598-019-53816-9
PubMed: 31792250
PubMed Central: PMC6889267
Affiliations:
- France
- Grand Est, Languedoc-Roussillon, Lorraine (région), Occitanie (région administrative)
- Montpellier, Nancy
- Université de Lorraine
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Karine" sort="De Guillen, Karine" uniqKey="De Guillen K" first="Karine" last="De Guillen">Karine De Guillen</name><affiliation wicri:level="3"><nlm:affiliation>Centre de Biochimie Structurale (CBS), INSERM U1054, CNRS UMR 5048, Univ Montpellier, F-34090, Montpellier, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Centre de Biochimie Structurale (CBS), INSERM U1054, CNRS UMR 5048, Univ Montpellier, F-34090, Montpellier</wicri:regionArea><placeName><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Languedoc-Roussillon</region><settlement type="city">Montpellier</settlement></placeName></affiliation></author><author><name sortKey="Lorrain, Cecile" sort="Lorrain, Cecile" uniqKey="Lorrain C" first="Cécile" last="Lorrain">Cécile Lorrain</name><affiliation wicri:level="4"><nlm:affiliation>Université de Lorraine, INRA, IAM, F-54000, Nancy, France.</nlm:affiliation><country 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Lorraine</orgName></affiliation></author><author><name sortKey="Barthe, Philippe" sort="Barthe, Philippe" uniqKey="Barthe P" first="Philippe" last="Barthe">Philippe Barthe</name><affiliation wicri:level="3"><nlm:affiliation>Centre de Biochimie Structurale (CBS), INSERM U1054, CNRS UMR 5048, Univ Montpellier, F-34090, Montpellier, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Centre de Biochimie Structurale (CBS), INSERM U1054, CNRS UMR 5048, Univ Montpellier, F-34090, Montpellier</wicri:regionArea><placeName><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Languedoc-Roussillon</region><settlement type="city">Montpellier</settlement></placeName></affiliation></author><author><name sortKey="Petre, Benjamin" sort="Petre, Benjamin" uniqKey="Petre B" first="Benjamin" last="Petre">Benjamin Petre</name><affiliation wicri:level="4"><nlm:affiliation>Université de Lorraine, INRA, IAM, F-54000, Nancy, 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type="university">Université de Lorraine</orgName></affiliation></author><author><name sortKey="Rouhier, Nicolas" sort="Rouhier, Nicolas" uniqKey="Rouhier N" first="Nicolas" last="Rouhier">Nicolas Rouhier</name><affiliation wicri:level="4"><nlm:affiliation>Université de Lorraine, INRA, IAM, F-54000, Nancy, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Université de Lorraine, INRA, IAM, F-54000, Nancy</wicri:regionArea><placeName><region type="region" nuts="2">Grand Est</region><region type="old region" nuts="2">Lorraine (région)</region><settlement type="city">Nancy</settlement></placeName><orgName type="university">Université de Lorraine</orgName></affiliation></author><author><name sortKey="Duplessis, Sebastien" sort="Duplessis, Sebastien" uniqKey="Duplessis S" first="Sébastien" last="Duplessis">Sébastien Duplessis</name><affiliation wicri:level="4"><nlm:affiliation>Université de Lorraine, INRA, IAM, F-54000, Nancy, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Université de Lorraine, INRA, IAM, F-54000, Nancy</wicri:regionArea><placeName><region type="region" nuts="2">Grand Est</region><region type="old region" nuts="2">Lorraine (région)</region><settlement type="city">Nancy</settlement></placeName><orgName type="university">Université de Lorraine</orgName></affiliation></author><author><name sortKey="Padilla, Andre" sort="Padilla, Andre" uniqKey="Padilla A" first="André" last="Padilla">André Padilla</name><affiliation wicri:level="3"><nlm:affiliation>Centre de Biochimie Structurale (CBS), INSERM U1054, CNRS UMR 5048, Univ Montpellier, F-34090, Montpellier, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Centre de Biochimie Structurale (CBS), INSERM U1054, CNRS UMR 5048, Univ Montpellier, F-34090, Montpellier</wicri:regionArea><placeName><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Languedoc-Roussillon</region><settlement type="city">Montpellier</settlement></placeName></affiliation></author><author><name sortKey="Hecker, Arnaud" sort="Hecker, Arnaud" uniqKey="Hecker A" first="Arnaud" last="Hecker">Arnaud Hecker</name><affiliation wicri:level="4"><nlm:affiliation>Université de Lorraine, INRA, IAM, F-54000, Nancy, France. arnaud.hecker@univ-lorraine.fr.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Université de Lorraine, INRA, IAM, F-54000, Nancy</wicri:regionArea><placeName><region type="region" nuts="2">Grand Est</region><region type="old region" nuts="2">Lorraine (région)</region><settlement type="city">Nancy</settlement></placeName><orgName type="university">Université de Lorraine</orgName></affiliation></author></analytic><series><title level="j">Scientific reports</title><idno type="eISSN">2045-2322</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Rust fungi are plant pathogens that secrete an arsenal of effector proteins interfering with plant functions and promoting parasitic infection. Effectors are often species-specific, evolve rapidly, and display low sequence similarities with known proteins. How rust fungal effectors function in host cells remains elusive, and biochemical and structural approaches have been scarcely used to tackle this question. In this study, we produced recombinant proteins of eleven candidate effectors of the leaf rust fungus Melampsora larici-populina in Escherichia coli. We successfully purified and solved the three-dimensional structure of two proteins, MLP124266 and MLP124017, using NMR spectroscopy. Although both MLP124266 and MLP124017 show no sequence similarity with known proteins, they exhibit structural similarities to knottins, which are disulfide-rich small proteins characterized by intricate disulfide bridges, and to nuclear transport factor 2-like proteins, which are molecular containers involved in a wide range of functions, respectively. Interestingly, such structural folds have not been reported so far in pathogen effectors, indicating that MLP124266 and MLP124017 may bear novel functions related to pathogenicity. Our findings show that sequence-unrelated effectors can adopt folds similar to known proteins, and encourage the use of biochemical and structural approaches to functionally characterize effector candidates.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">31792250</PMID><DateRevised><Year>2020</Year><Month>05</Month><Day>20</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">2045-2322</ISSN><JournalIssue CitedMedium="Internet"><Volume>9</Volume><Issue>1</Issue><PubDate><Year>2019</Year><Month>12</Month><Day>02</Day></PubDate></JournalIssue><Title>Scientific reports</Title><ISOAbbreviation>Sci Rep</ISOAbbreviation></Journal><ArticleTitle>Structural genomics applied to the rust fungus Melampsora larici-populina reveals two candidate effector proteins adopting cystine knot and NTF2-like protein folds.</ArticleTitle><Pagination><MedlinePgn>18084</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1038/s41598-019-53816-9</ELocationID><Abstract><AbstractText>Rust fungi are plant pathogens that secrete an arsenal of effector proteins interfering with plant functions and promoting parasitic infection. Effectors are often species-specific, evolve rapidly, and display low sequence similarities with known proteins. How rust fungal effectors function in host cells remains elusive, and biochemical and structural approaches have been scarcely used to tackle this question. In this study, we produced recombinant proteins of eleven candidate effectors of the leaf rust fungus Melampsora larici-populina in Escherichia coli. We successfully purified and solved the three-dimensional structure of two proteins, MLP124266 and MLP124017, using NMR spectroscopy. Although both MLP124266 and MLP124017 show no sequence similarity with known proteins, they exhibit structural similarities to knottins, which are disulfide-rich small proteins characterized by intricate disulfide bridges, and to nuclear transport factor 2-like proteins, which are molecular containers involved in a wide range of functions, respectively. Interestingly, such structural folds have not been reported so far in pathogen effectors, indicating that MLP124266 and MLP124017 may bear novel functions related to pathogenicity. Our findings show that sequence-unrelated effectors can adopt folds similar to known proteins, and encourage the use of biochemical and structural approaches to functionally characterize effector candidates.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>de Guillen</LastName><ForeName>Karine</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>Centre de Biochimie Structurale (CBS), INSERM U1054, CNRS UMR 5048, Univ Montpellier, F-34090, Montpellier, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lorrain</LastName><ForeName>Cécile</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Université de Lorraine, INRA, IAM, F-54000, Nancy, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tsan</LastName><ForeName>Pascale</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>Université de Lorraine, CNRS, CRM2, F-54000, Nancy, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Barthe</LastName><ForeName>Philippe</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>Centre de Biochimie Structurale (CBS), INSERM U1054, CNRS UMR 5048, Univ Montpellier, F-34090, Montpellier, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Petre</LastName><ForeName>Benjamin</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>Université de Lorraine, INRA, IAM, F-54000, Nancy, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Saveleva</LastName><ForeName>Natalya</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>Université de Lorraine, INRA, IAM, F-54000, Nancy, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Rouhier</LastName><ForeName>Nicolas</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>Université de Lorraine, INRA, IAM, F-54000, Nancy, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Duplessis</LastName><ForeName>Sébastien</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Université de Lorraine, INRA, IAM, F-54000, Nancy, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Padilla</LastName><ForeName>André</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Centre de Biochimie Structurale (CBS), INSERM U1054, CNRS UMR 5048, Univ Montpellier, F-34090, Montpellier, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hecker</LastName><ForeName>Arnaud</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Université de Lorraine, INRA, IAM, F-54000, Nancy, France. arnaud.hecker@univ-lorraine.fr.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>12</Month><Day>02</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Sci Rep</MedlineTA><NlmUniqueID>101563288</NlmUniqueID><ISSNLinking>2045-2322</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>09</Month><Day>04</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2019</Year><Month>10</Month><Day>31</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2019</Year><Month>12</Month><Day>4</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2019</Year><Month>12</Month><Day>4</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate 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