Serveur d'exploration sur les effecteurs de la rouille

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Crystal structure of the Melampsora lini effector AvrP reveals insights into a possible nuclear function and recognition by the flax disease resistance protein P.

Identifieur interne : 000049 ( Main/Exploration ); précédent : 000048; suivant : 000050

Crystal structure of the Melampsora lini effector AvrP reveals insights into a possible nuclear function and recognition by the flax disease resistance protein P.

Auteurs : Xiaoxiao Zhang [Australie] ; Nadya Farah [Australie] ; Laura Rolston [Australie] ; Daniel J. Ericsson [Australie] ; Ann-Maree Catanzariti [Australie] ; Maud Bernoux [Australie] ; Thomas Ve [Australie] ; Katerina Bendak [Australie] ; Chunhong Chen [Australie] ; Joel P. Mackay [Australie] ; Gregory J. Lawrence [Australie] ; Adrienne Hardham [Australie] ; Jeffrey G. Ellis [Australie] ; Simon J. Williams [Australie] ; Peter N. Dodds [Australie] ; David A. Jones [Australie] ; Bostjan Kobe [Australie]

Source :

RBID : pubmed:28817232

Descripteurs français

English descriptors

Abstract

The effector protein AvrP is secreted by the flax rust fungal pathogen (Melampsora lini) and recognized specifically by the flax (Linum usitatissimum) P disease resistance protein, leading to effector-triggered immunity. To investigate the biological function of this effector and the mechanisms of specific recognition by the P resistance protein, we determined the crystal structure of AvrP. The structure reveals an elongated zinc-finger-like structure with a novel interleaved zinc-binding topology. The residues responsible for zinc binding are conserved in AvrP effector variants and mutations of these motifs result in a loss of P-mediated recognition. The first zinc-coordinating region of the structure displays a positively charged surface and shows some limited similarities to nucleic acid-binding and chromatin-associated proteins. We show that the majority of the AvrP protein accumulates in the plant nucleus when transiently expressed in Nicotiana benthamiana cells, suggesting a nuclear pathogenic function. Polymorphic residues in AvrP and its allelic variants map to the protein surface and could be associated with differences in recognition specificity. Several point mutations of residues on the non-conserved surface patch result in a loss of recognition by P, suggesting that these residues are required for recognition.

DOI: 10.1111/mpp.12597
PubMed: 28817232
PubMed Central: PMC6638141


Affiliations:


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Le document en format XML

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<title xml:lang="en">Crystal structure of the Melampsora lini effector AvrP reveals insights into a possible nuclear function and recognition by the flax disease resistance protein P.</title>
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<name sortKey="Zhang, Xiaoxiao" sort="Zhang, Xiaoxiao" uniqKey="Zhang X" first="Xiaoxiao" last="Zhang">Xiaoxiao Zhang</name>
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<name sortKey="Farah, Nadya" sort="Farah, Nadya" uniqKey="Farah N" first="Nadya" last="Farah">Nadya Farah</name>
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<nlm:affiliation>Division of Plant Sciences, Research School of Biology, Australian National University, Acton, Australian Capital Territory 2601, Australia.</nlm:affiliation>
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<name sortKey="Rolston, Laura" sort="Rolston, Laura" uniqKey="Rolston L" first="Laura" last="Rolston">Laura Rolston</name>
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<nlm:affiliation>Division of Plant Sciences, Research School of Biology, Australian National University, Acton, Australian Capital Territory 2601, Australia.</nlm:affiliation>
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<name sortKey="Ericsson, Daniel J" sort="Ericsson, Daniel J" uniqKey="Ericsson D" first="Daniel J" last="Ericsson">Daniel J. Ericsson</name>
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<name sortKey="Bernoux, Maud" sort="Bernoux, Maud" uniqKey="Bernoux M" first="Maud" last="Bernoux">Maud Bernoux</name>
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<name sortKey="Ve, Thomas" sort="Ve, Thomas" uniqKey="Ve T" first="Thomas" last="Ve">Thomas Ve</name>
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<name sortKey="Bendak, Katerina" sort="Bendak, Katerina" uniqKey="Bendak K" first="Katerina" last="Bendak">Katerina Bendak</name>
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<nlm:affiliation>School of Molecular Bioscience, University of Sydney, Sydney, New South Wales 2006, Australia.</nlm:affiliation>
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<name sortKey="Chen, Chunhong" sort="Chen, Chunhong" uniqKey="Chen C" first="Chunhong" last="Chen">Chunhong Chen</name>
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<name sortKey="Mackay, Joel P" sort="Mackay, Joel P" uniqKey="Mackay J" first="Joel P" last="Mackay">Joel P. Mackay</name>
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<nlm:affiliation>School of Molecular Bioscience, University of Sydney, Sydney, New South Wales 2006, Australia.</nlm:affiliation>
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<name sortKey="Lawrence, Gregory J" sort="Lawrence, Gregory J" uniqKey="Lawrence G" first="Gregory J" last="Lawrence">Gregory J. Lawrence</name>
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<nlm:affiliation>Commonwealth Scientific and Industrial Research Organisation Agriculture and Food, Canberra, Australian Capital Territory 2601, Australia.</nlm:affiliation>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>Commonwealth Scientific and Industrial Research Organisation Agriculture and Food, Canberra, Australian Capital Territory 2601</wicri:regionArea>
<wicri:noRegion>Australian Capital Territory 2601</wicri:noRegion>
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<name sortKey="Hardham, Adrienne" sort="Hardham, Adrienne" uniqKey="Hardham A" first="Adrienne" last="Hardham">Adrienne Hardham</name>
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<nlm:affiliation>Division of Plant Sciences, Research School of Biology, Australian National University, Acton, Australian Capital Territory 2601, Australia.</nlm:affiliation>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>Division of Plant Sciences, Research School of Biology, Australian National University, Acton, Australian Capital Territory 2601</wicri:regionArea>
<wicri:noRegion>Australian Capital Territory 2601</wicri:noRegion>
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<name sortKey="Ellis, Jeffrey G" sort="Ellis, Jeffrey G" uniqKey="Ellis J" first="Jeffrey G" last="Ellis">Jeffrey G. Ellis</name>
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<nlm:affiliation>Commonwealth Scientific and Industrial Research Organisation Agriculture and Food, Canberra, Australian Capital Territory 2601, Australia.</nlm:affiliation>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>Commonwealth Scientific and Industrial Research Organisation Agriculture and Food, Canberra, Australian Capital Territory 2601</wicri:regionArea>
<wicri:noRegion>Australian Capital Territory 2601</wicri:noRegion>
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<name sortKey="Williams, Simon J" sort="Williams, Simon J" uniqKey="Williams S" first="Simon J" last="Williams">Simon J. Williams</name>
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<nlm:affiliation>School of Chemistry and Molecular Biosciences, Australian Infectious Diseases Research Centre and Institute for Molecular Bioscience, University of Queensland, Brisbane, Queensland 4072, Australia.</nlm:affiliation>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>School of Chemistry and Molecular Biosciences, Australian Infectious Diseases Research Centre and Institute for Molecular Bioscience, University of Queensland, Brisbane, Queensland 4072</wicri:regionArea>
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<nlm:affiliation>Division of Plant Sciences, Research School of Biology, Australian National University, Acton, Australian Capital Territory 2601, Australia.</nlm:affiliation>
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<name sortKey="Kobe, Bostjan" sort="Kobe, Bostjan" uniqKey="Kobe B" first="Bostjan" last="Kobe">Bostjan Kobe</name>
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<nlm:affiliation>School of Chemistry and Molecular Biosciences, Australian Infectious Diseases Research Centre and Institute for Molecular Bioscience, University of Queensland, Brisbane, Queensland 4072, Australia.</nlm:affiliation>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>School of Chemistry and Molecular Biosciences, Australian Infectious Diseases Research Centre and Institute for Molecular Bioscience, University of Queensland, Brisbane, Queensland 4072</wicri:regionArea>
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<title level="j">Molecular plant pathology</title>
<idno type="eISSN">1364-3703</idno>
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<term>Agrobacterium (metabolism)</term>
<term>Amino Acid Motifs (MeSH)</term>
<term>Amino Acid Sequence (MeSH)</term>
<term>Basidiomycota (metabolism)</term>
<term>Cell Nucleus (metabolism)</term>
<term>Conserved Sequence (MeSH)</term>
<term>Crystallography, X-Ray (MeSH)</term>
<term>Disease Resistance (MeSH)</term>
<term>Flax (microbiology)</term>
<term>Fungal Proteins (chemistry)</term>
<term>Fungal Proteins (metabolism)</term>
<term>Models, Molecular (MeSH)</term>
<term>Plant Cells (metabolism)</term>
<term>Plant Diseases (microbiology)</term>
<term>Plant Proteins (metabolism)</term>
<term>Protein Binding (MeSH)</term>
<term>Protein Domains (MeSH)</term>
<term>Saccharomyces cerevisiae (metabolism)</term>
<term>Structural Homology, Protein (MeSH)</term>
<term>Tobacco (genetics)</term>
<term>Zinc (metabolism)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Agrobacterium (métabolisme)</term>
<term>Basidiomycota (métabolisme)</term>
<term>Cellules végétales (métabolisme)</term>
<term>Cristallographie aux rayons X (MeSH)</term>
<term>Domaines protéiques (MeSH)</term>
<term>Liaison aux protéines (MeSH)</term>
<term>Lin (microbiologie)</term>
<term>Maladies des plantes (microbiologie)</term>
<term>Modèles moléculaires (MeSH)</term>
<term>Motifs d'acides aminés (MeSH)</term>
<term>Noyau de la cellule (métabolisme)</term>
<term>Protéines fongiques (composition chimique)</term>
<term>Protéines fongiques (métabolisme)</term>
<term>Protéines végétales (métabolisme)</term>
<term>Résistance à la maladie (MeSH)</term>
<term>Saccharomyces cerevisiae (métabolisme)</term>
<term>Similitude structurale de protéines (MeSH)</term>
<term>Séquence conservée (MeSH)</term>
<term>Séquence d'acides aminés (MeSH)</term>
<term>Tabac (génétique)</term>
<term>Zinc (métabolisme)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en">
<term>Fungal Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="composition chimique" xml:lang="fr">
<term>Protéines fongiques</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Tobacco</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Tabac</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en">
<term>Agrobacterium</term>
<term>Basidiomycota</term>
<term>Cell Nucleus</term>
<term>Fungal Proteins</term>
<term>Plant Cells</term>
<term>Plant Proteins</term>
<term>Saccharomyces cerevisiae</term>
<term>Zinc</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr">
<term>Lin</term>
<term>Maladies des plantes</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Flax</term>
<term>Plant Diseases</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Agrobacterium</term>
<term>Basidiomycota</term>
<term>Cellules végétales</term>
<term>Noyau de la cellule</term>
<term>Protéines fongiques</term>
<term>Protéines végétales</term>
<term>Saccharomyces cerevisiae</term>
<term>Zinc</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Amino Acid Motifs</term>
<term>Amino Acid Sequence</term>
<term>Conserved Sequence</term>
<term>Crystallography, X-Ray</term>
<term>Disease Resistance</term>
<term>Models, Molecular</term>
<term>Protein Binding</term>
<term>Protein Domains</term>
<term>Structural Homology, Protein</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Cristallographie aux rayons X</term>
<term>Domaines protéiques</term>
<term>Liaison aux protéines</term>
<term>Modèles moléculaires</term>
<term>Motifs d'acides aminés</term>
<term>Résistance à la maladie</term>
<term>Similitude structurale de protéines</term>
<term>Séquence conservée</term>
<term>Séquence d'acides aminés</term>
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<front>
<div type="abstract" xml:lang="en">The effector protein AvrP is secreted by the flax rust fungal pathogen (Melampsora lini) and recognized specifically by the flax (Linum usitatissimum) P disease resistance protein, leading to effector-triggered immunity. To investigate the biological function of this effector and the mechanisms of specific recognition by the P resistance protein, we determined the crystal structure of AvrP. The structure reveals an elongated zinc-finger-like structure with a novel interleaved zinc-binding topology. The residues responsible for zinc binding are conserved in AvrP effector variants and mutations of these motifs result in a loss of P-mediated recognition. The first zinc-coordinating region of the structure displays a positively charged surface and shows some limited similarities to nucleic acid-binding and chromatin-associated proteins. We show that the majority of the AvrP protein accumulates in the plant nucleus when transiently expressed in Nicotiana benthamiana cells, suggesting a nuclear pathogenic function. Polymorphic residues in AvrP and its allelic variants map to the protein surface and could be associated with differences in recognition specificity. Several point mutations of residues on the non-conserved surface patch result in a loss of recognition by P, suggesting that these residues are required for recognition.</div>
</front>
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<PMID Version="1">28817232</PMID>
<DateCompleted>
<Year>2019</Year>
<Month>02</Month>
<Day>27</Day>
</DateCompleted>
<DateRevised>
<Year>2020</Year>
<Month>02</Month>
<Day>25</Day>
</DateRevised>
<Article PubModel="Print-Electronic">
<Journal>
<ISSN IssnType="Electronic">1364-3703</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>19</Volume>
<Issue>5</Issue>
<PubDate>
<Year>2018</Year>
<Month>05</Month>
</PubDate>
</JournalIssue>
<Title>Molecular plant pathology</Title>
<ISOAbbreviation>Mol Plant Pathol</ISOAbbreviation>
</Journal>
<ArticleTitle>Crystal structure of the Melampsora lini effector AvrP reveals insights into a possible nuclear function and recognition by the flax disease resistance protein P.</ArticleTitle>
<Pagination>
<MedlinePgn>1196-1209</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1111/mpp.12597</ELocationID>
<Abstract>
<AbstractText>The effector protein AvrP is secreted by the flax rust fungal pathogen (Melampsora lini) and recognized specifically by the flax (Linum usitatissimum) P disease resistance protein, leading to effector-triggered immunity. To investigate the biological function of this effector and the mechanisms of specific recognition by the P resistance protein, we determined the crystal structure of AvrP. The structure reveals an elongated zinc-finger-like structure with a novel interleaved zinc-binding topology. The residues responsible for zinc binding are conserved in AvrP effector variants and mutations of these motifs result in a loss of P-mediated recognition. The first zinc-coordinating region of the structure displays a positively charged surface and shows some limited similarities to nucleic acid-binding and chromatin-associated proteins. We show that the majority of the AvrP protein accumulates in the plant nucleus when transiently expressed in Nicotiana benthamiana cells, suggesting a nuclear pathogenic function. Polymorphic residues in AvrP and its allelic variants map to the protein surface and could be associated with differences in recognition specificity. Several point mutations of residues on the non-conserved surface patch result in a loss of recognition by P, suggesting that these residues are required for recognition.</AbstractText>
<CopyrightInformation>© 2017 BSPP AND JOHN WILEY & SONS LTD.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Zhang</LastName>
<ForeName>Xiaoxiao</ForeName>
<Initials>X</Initials>
<AffiliationInfo>
<Affiliation>School of Chemistry and Molecular Biosciences, Australian Infectious Diseases Research Centre and Institute for Molecular Bioscience, University of Queensland, Brisbane, Queensland 4072, Australia.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Commonwealth Scientific and Industrial Research Organisation Agriculture and Food, Canberra, Australian Capital Territory 2601, Australia.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Farah</LastName>
<ForeName>Nadya</ForeName>
<Initials>N</Initials>
<AffiliationInfo>
<Affiliation>Division of Plant Sciences, Research School of Biology, Australian National University, Acton, Australian Capital Territory 2601, Australia.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Rolston</LastName>
<ForeName>Laura</ForeName>
<Initials>L</Initials>
<AffiliationInfo>
<Affiliation>Division of Plant Sciences, Research School of Biology, Australian National University, Acton, Australian Capital Territory 2601, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Ericsson</LastName>
<ForeName>Daniel J</ForeName>
<Initials>DJ</Initials>
<AffiliationInfo>
<Affiliation>School of Chemistry and Molecular Biosciences, Australian Infectious Diseases Research Centre and Institute for Molecular Bioscience, University of Queensland, Brisbane, Queensland 4072, Australia.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Australian Synchrotron, Macromolecular crystallography, Clayton, Victoria 3168, Australia.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Catanzariti</LastName>
<ForeName>Ann-Maree</ForeName>
<Initials>AM</Initials>
<AffiliationInfo>
<Affiliation>Division of Plant Sciences, Research School of Biology, Australian National University, Acton, Australian Capital Territory 2601, Australia.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Bernoux</LastName>
<ForeName>Maud</ForeName>
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</AffiliationInfo>
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<AffiliationInfo>
<Affiliation>School of Chemistry and Molecular Biosciences, Australian Infectious Diseases Research Centre and Institute for Molecular Bioscience, University of Queensland, Brisbane, Queensland 4072, Australia.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Institute for Glycomics, Griffith University, Southport, Queensland 4222, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Bendak</LastName>
<ForeName>Katerina</ForeName>
<Initials>K</Initials>
<AffiliationInfo>
<Affiliation>School of Molecular Bioscience, University of Sydney, Sydney, New South Wales 2006, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Chen</LastName>
<ForeName>Chunhong</ForeName>
<Initials>C</Initials>
<AffiliationInfo>
<Affiliation>Commonwealth Scientific and Industrial Research Organisation Agriculture and Food, Canberra, Australian Capital Territory 2601, Australia.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Mackay</LastName>
<ForeName>Joel P</ForeName>
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<AffiliationInfo>
<Affiliation>School of Molecular Bioscience, University of Sydney, Sydney, New South Wales 2006, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Lawrence</LastName>
<ForeName>Gregory J</ForeName>
<Initials>GJ</Initials>
<AffiliationInfo>
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</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Hardham</LastName>
<ForeName>Adrienne</ForeName>
<Initials>A</Initials>
<AffiliationInfo>
<Affiliation>Division of Plant Sciences, Research School of Biology, Australian National University, Acton, Australian Capital Territory 2601, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Ellis</LastName>
<ForeName>Jeffrey G</ForeName>
<Initials>JG</Initials>
<AffiliationInfo>
<Affiliation>Commonwealth Scientific and Industrial Research Organisation Agriculture and Food, Canberra, Australian Capital Territory 2601, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Williams</LastName>
<ForeName>Simon J</ForeName>
<Initials>SJ</Initials>
<AffiliationInfo>
<Affiliation>School of Chemistry and Molecular Biosciences, Australian Infectious Diseases Research Centre and Institute for Molecular Bioscience, University of Queensland, Brisbane, Queensland 4072, Australia.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Division of Plant Sciences, Research School of Biology, Australian National University, Acton, Australian Capital Territory 2601, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Dodds</LastName>
<ForeName>Peter N</ForeName>
<Initials>PN</Initials>
<AffiliationInfo>
<Affiliation>Commonwealth Scientific and Industrial Research Organisation Agriculture and Food, Canberra, Australian Capital Territory 2601, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Jones</LastName>
<ForeName>David A</ForeName>
<Initials>DA</Initials>
<AffiliationInfo>
<Affiliation>Division of Plant Sciences, Research School of Biology, Australian National University, Acton, Australian Capital Territory 2601, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Kobe</LastName>
<ForeName>Bostjan</ForeName>
<Initials>B</Initials>
<AffiliationInfo>
<Affiliation>School of Chemistry and Molecular Biosciences, Australian Infectious Diseases Research Centre and Institute for Molecular Bioscience, University of Queensland, Brisbane, Queensland 4072, Australia.</Affiliation>
</AffiliationInfo>
</Author>
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<Language>eng</Language>
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<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
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<ArticleDate DateType="Electronic">
<Year>2017</Year>
<Month>11</Month>
<Day>16</Day>
</ArticleDate>
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<Country>England</Country>
<MedlineTA>Mol Plant Pathol</MedlineTA>
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<ISSNLinking>1364-3703</ISSNLinking>
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<MeshHeading>
<DescriptorName UI="D060054" MajorTopicYN="N">Agrobacterium</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D020816" MajorTopicYN="N">Amino Acid Motifs</DescriptorName>
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<MeshHeading>
<DescriptorName UI="D000595" MajorTopicYN="N">Amino Acid Sequence</DescriptorName>
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<MeshHeading>
<DescriptorName UI="D001487" MajorTopicYN="N">Basidiomycota</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
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<MeshHeading>
<DescriptorName UI="D002467" MajorTopicYN="N">Cell Nucleus</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
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<MeshHeading>
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<MeshHeading>
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</MeshHeading>
<MeshHeading>
<DescriptorName UI="D060467" MajorTopicYN="Y">Disease Resistance</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D019597" MajorTopicYN="N">Flax</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
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<MeshHeading>
<DescriptorName UI="D005656" MajorTopicYN="N">Fungal Proteins</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="Y">chemistry</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
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<MeshHeading>
<DescriptorName UI="D010935" MajorTopicYN="N">Plant Diseases</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
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<MeshHeading>
<DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
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<MeshHeading>
<DescriptorName UI="D011485" MajorTopicYN="N">Protein Binding</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D000072417" MajorTopicYN="N">Protein Domains</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D012441" MajorTopicYN="N">Saccharomyces cerevisiae</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D040681" MajorTopicYN="N">Structural Homology, Protein</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D014026" MajorTopicYN="N">Tobacco</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D015032" MajorTopicYN="N">Zinc</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
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<Keyword MajorTopicYN="Y">NLR [nucleotide-binding and oligomerization domain (NOD)-like receptor</Keyword>
<Keyword MajorTopicYN="Y">crystal structure</Keyword>
<Keyword MajorTopicYN="Y">effector-triggered immunity</Keyword>
<Keyword MajorTopicYN="Y">flax rust (Melampsora lini) effector</Keyword>
<Keyword MajorTopicYN="Y">nuclear localization</Keyword>
<Keyword MajorTopicYN="Y">nucleotide-binding/leucine-rich repeat receptor]</Keyword>
<Keyword MajorTopicYN="Y">plant disease resistance</Keyword>
<Keyword MajorTopicYN="Y">zinc finger</Keyword>
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