PhytophthoraV1, Main, Exploration, bibRecord, 000447

Natural allelic variations provide insights into host adaptation of Phytophthora avirulence effector PsAvr3c.

Identifieur interne : 000447 ( Main/Exploration ); précédent : 000446; suivant : 000448

Natural allelic variations provide insights into host adaptation of Phytophthora avirulence effector PsAvr3c.

Source :

The New phytologist [ 1469-8137 ] ; 2019.

RBID : pubmed:30169906

Descripteurs français

KwdFr :
- Acclimatation (MeSH), Facteurs de virulence (métabolisme), Génotype (MeSH), Immunité des plantes (MeSH), Maladies des plantes (génétique), Maladies des plantes (immunologie), Maladies des plantes (microbiologie), Phytophthora (génétique), Phytophthora (physiologie), Polymorphisme génétique (génétique), Soja (génétique), Soja (physiologie), Virulence (MeSH).
MESH :
- génétique : Maladies des plantes, Phytophthora, Polymorphisme génétique, Soja.
- immunologie : Maladies des plantes.
- microbiologie : Maladies des plantes.
- métabolisme : Facteurs de virulence.
- physiologie : Phytophthora, Soja.
- Acclimatation, Génotype, Immunité des plantes, Virulence.

English descriptors

KwdEn :
- Acclimatization (MeSH), Genotype (MeSH), Phytophthora (genetics), Phytophthora (physiology), Plant Diseases (genetics), Plant Diseases (immunology), Plant Diseases (microbiology), Plant Immunity (MeSH), Polymorphism, Genetic (genetics), Soybeans (genetics), Soybeans (physiology), Virulence (MeSH), Virulence Factors (metabolism).
MESH :
- chemical , metabolism : Virulence Factors.
- genetics : Phytophthora, Plant Diseases, Polymorphism, Genetic, Soybeans.
- immunology : Plant Diseases.
- microbiology : Plant Diseases.
- physiology : Phytophthora, Soybeans.
- Acclimatization, Genotype, Plant Immunity, Virulence.

Abstract

Filamentous pathogens, such as fungi and oomycetes, secrete avirulence (AVR) effectors that trigger plant immune responses and provide striking examples of host adaptations. Avr effector genes display different types of allelic variations, including deletions, epigenetic silencing and sequence polymorphisms, to avoid detection. However, how effector sequence polymorphisms enable pathogens to dodge host immune surveillance remains largely unknown. PsAvr3c is a Phytophthora AVR gene that is recognized by soybean carrying Rps3c. PsAvr3c natural alleles display a rich diversity of single nucleotide polymorphisms in field isolates. We combined both site-directed mutagenesis and population sequence surveys to identify a serine substitution of glycine at position 174 in PsAvr3c that resulted in evasion of Rps3c-mediated soybean immunity. The S174G substitution did not affect the nuclear localization of PsAvr3c in planta, which is required to activate Rps3c, but it significantly impaired the binding affinity of PsAvr3c with a previously identified spliceosome-associated protein GmSKRPs. Silencing GmSKRPs specifically impaired PsAvr3c-triggered cell death in Rps3c soybean. This study uncovered a plant Phytophthora pathogen that adapted to a resistant plant through a key amino acid mutation and subsequently reduced the binding affinity with a plant immune regulator to evade host resistance.

DOI: 10.1111/nph.15414
PubMed: 30169906

Affiliations:

République populaire de Chine

Links toward previous steps (curation, corpus...)

to stream Main, to step Corpus: 000676
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Le document en format XML

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<author><name sortKey="Dong, Suomeng" sort="Dong, Suomeng" uniqKey="Dong S" first="Suomeng" last="Dong">Suomeng Dong</name>
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<sourceDesc><biblStruct><analytic><title xml:lang="en">Natural allelic variations provide insights into host adaptation of Phytophthora avirulence effector PsAvr3c.</title>
<author><name sortKey="Huang, Jie" sort="Huang, Jie" uniqKey="Huang J" first="Jie" last="Huang">Jie Huang</name>
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<affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, 210095, China.</nlm:affiliation>
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<author><name sortKey="Chen, Ling" sort="Chen, Ling" uniqKey="Chen L" first="Ling" last="Chen">Ling Chen</name>
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<country xml:lang="fr">République populaire de Chine</country>
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<author><name sortKey="Yang, Jin" sort="Yang, Jin" uniqKey="Yang J" first="Jin" last="Yang">Jin Yang</name>
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<country xml:lang="fr">République populaire de Chine</country>
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<author><name sortKey="Zhang, Bai Yu" sort="Zhang, Bai Yu" uniqKey="Zhang B" first="Bai Yu" last="Zhang">Bai Yu Zhang</name>
<affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, 210095, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, 210095</wicri:regionArea>
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</affiliation>
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<author><name sortKey="Yang, Bo" sort="Yang, Bo" uniqKey="Yang B" first="Bo" last="Yang">Bo Yang</name>
<affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, 210095, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, 210095</wicri:regionArea>
<wicri:noRegion>210095</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Waletich, Justin Reed" sort="Waletich, Justin Reed" uniqKey="Waletich J" first="Justin Reed" last="Waletich">Justin Reed Waletich</name>
<affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, 210095, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, 210095</wicri:regionArea>
<wicri:noRegion>210095</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Yin, Weixiao" sort="Yin, Weixiao" uniqKey="Yin W" first="Weixiao" last="Yin">Weixiao Yin</name>
<affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, 210095, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, 210095</wicri:regionArea>
<wicri:noRegion>210095</wicri:noRegion>
</affiliation>
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<author><name sortKey="Zheng, Xiaobo" sort="Zheng, Xiaobo" uniqKey="Zheng X" first="Xiaobo" last="Zheng">Xiaobo Zheng</name>
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<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, 210095</wicri:regionArea>
<wicri:noRegion>210095</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, 210095, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, 210095</wicri:regionArea>
<wicri:noRegion>210095</wicri:noRegion>
</affiliation>
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<author><name sortKey="Wang, Yuanchao" sort="Wang, Yuanchao" uniqKey="Wang Y" first="Yuanchao" last="Wang">Yuanchao Wang</name>
<affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, 210095, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
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<affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, 210095, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, 210095</wicri:regionArea>
<wicri:noRegion>210095</wicri:noRegion>
</affiliation>
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<author><name sortKey="Dong, Suomeng" sort="Dong, Suomeng" uniqKey="Dong S" first="Suomeng" last="Dong">Suomeng Dong</name>
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<profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Acclimatization (MeSH)</term>
<term>Genotype (MeSH)</term>
<term>Phytophthora (genetics)</term>
<term>Phytophthora (physiology)</term>
<term>Plant Diseases (genetics)</term>
<term>Plant Diseases (immunology)</term>
<term>Plant Diseases (microbiology)</term>
<term>Plant Immunity (MeSH)</term>
<term>Polymorphism, Genetic (genetics)</term>
<term>Soybeans (genetics)</term>
<term>Soybeans (physiology)</term>
<term>Virulence (MeSH)</term>
<term>Virulence Factors (metabolism)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr"><term>Acclimatation (MeSH)</term>
<term>Facteurs de virulence (métabolisme)</term>
<term>Génotype (MeSH)</term>
<term>Immunité des plantes (MeSH)</term>
<term>Maladies des plantes (génétique)</term>
<term>Maladies des plantes (immunologie)</term>
<term>Maladies des plantes (microbiologie)</term>
<term>Phytophthora (génétique)</term>
<term>Phytophthora (physiologie)</term>
<term>Polymorphisme génétique (génétique)</term>
<term>Soja (génétique)</term>
<term>Soja (physiologie)</term>
<term>Virulence (MeSH)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Virulence Factors</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Phytophthora</term>
<term>Plant Diseases</term>
<term>Polymorphism, Genetic</term>
<term>Soybeans</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Maladies des plantes</term>
<term>Phytophthora</term>
<term>Polymorphisme génétique</term>
<term>Soja</term>
</keywords>
<keywords scheme="MESH" qualifier="immunologie" xml:lang="fr"><term>Maladies des plantes</term>
</keywords>
<keywords scheme="MESH" qualifier="immunology" xml:lang="en"><term>Plant Diseases</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr"><term>Maladies des plantes</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en"><term>Plant Diseases</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Facteurs de virulence</term>
</keywords>
<keywords scheme="MESH" qualifier="physiologie" xml:lang="fr"><term>Phytophthora</term>
<term>Soja</term>
</keywords>
<keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Phytophthora</term>
<term>Soybeans</term>
</keywords>
<keywords scheme="MESH" xml:lang="en"><term>Acclimatization</term>
<term>Genotype</term>
<term>Plant Immunity</term>
<term>Virulence</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr"><term>Acclimatation</term>
<term>Génotype</term>
<term>Immunité des plantes</term>
<term>Virulence</term>
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<front><div type="abstract" xml:lang="en">Filamentous pathogens, such as fungi and oomycetes, secrete avirulence (AVR) effectors that trigger plant immune responses and provide striking examples of host adaptations. Avr effector genes display different types of allelic variations, including deletions, epigenetic silencing and sequence polymorphisms, to avoid detection. However, how effector sequence polymorphisms enable pathogens to dodge host immune surveillance remains largely unknown. PsAvr3c is a Phytophthora AVR gene that is recognized by soybean carrying Rps3c. PsAvr3c natural alleles display a rich diversity of single nucleotide polymorphisms in field isolates. We combined both site-directed mutagenesis and population sequence surveys to identify a serine substitution of glycine at position 174 in PsAvr3c that resulted in evasion of Rps3c-mediated soybean immunity. The S174G substitution did not affect the nuclear localization of PsAvr3c in planta, which is required to activate Rps3c, but it significantly impaired the binding affinity of PsAvr3c with a previously identified spliceosome-associated protein GmSKRPs. Silencing GmSKRPs specifically impaired PsAvr3c-triggered cell death in Rps3c soybean. This study uncovered a plant Phytophthora pathogen that adapted to a resistant plant through a key amino acid mutation and subsequently reduced the binding affinity with a plant immune regulator to evade host resistance.</div>
</front>
</TEI>
<pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">30169906</PMID>
<DateCompleted><Year>2020</Year>
<Month>02</Month>
<Day>18</Day>
</DateCompleted>
<DateRevised><Year>2020</Year>
<Month>09</Month>
<Day>30</Day>
</DateRevised>
<Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1469-8137</ISSN>
<JournalIssue CitedMedium="Internet"><Volume>221</Volume>
<Issue>2</Issue>
<PubDate><Year>2019</Year>
<Month>01</Month>
</PubDate>
</JournalIssue>
<Title>The New phytologist</Title>
<ISOAbbreviation>New Phytol</ISOAbbreviation>
</Journal>
<ArticleTitle>Natural allelic variations provide insights into host adaptation of Phytophthora avirulence effector PsAvr3c.</ArticleTitle>
<Pagination><MedlinePgn>1010-1022</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1111/nph.15414</ELocationID>
<Abstract><AbstractText>Filamentous pathogens, such as fungi and oomycetes, secrete avirulence (AVR) effectors that trigger plant immune responses and provide striking examples of host adaptations. Avr effector genes display different types of allelic variations, including deletions, epigenetic silencing and sequence polymorphisms, to avoid detection. However, how effector sequence polymorphisms enable pathogens to dodge host immune surveillance remains largely unknown. PsAvr3c is a Phytophthora AVR gene that is recognized by soybean carrying Rps3c. PsAvr3c natural alleles display a rich diversity of single nucleotide polymorphisms in field isolates. We combined both site-directed mutagenesis and population sequence surveys to identify a serine substitution of glycine at position 174 in PsAvr3c that resulted in evasion of Rps3c-mediated soybean immunity. The S174G substitution did not affect the nuclear localization of PsAvr3c in planta, which is required to activate Rps3c, but it significantly impaired the binding affinity of PsAvr3c with a previously identified spliceosome-associated protein GmSKRPs. Silencing GmSKRPs specifically impaired PsAvr3c-triggered cell death in Rps3c soybean. This study uncovered a plant Phytophthora pathogen that adapted to a resistant plant through a key amino acid mutation and subsequently reduced the binding affinity with a plant immune regulator to evade host resistance.</AbstractText>
<CopyrightInformation>© 2018 The Authors. New Phytologist © 2018 New Phytologist Trust.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Huang</LastName>
<ForeName>Jie</ForeName>
<Initials>J</Initials>
<Identifier Source="ORCID">0000-0002-6657-8740</Identifier>
<AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, 210095, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Chen</LastName>
<ForeName>Ling</ForeName>
<Initials>L</Initials>
<AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Lu</LastName>
<ForeName>Xinyu</ForeName>
<Initials>X</Initials>
<AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Peng</LastName>
<ForeName>Qian</ForeName>
<Initials>Q</Initials>
<AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Zhang</LastName>
<ForeName>Ying</ForeName>
<Initials>Y</Initials>
<AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Yang</LastName>
<ForeName>Jin</ForeName>
<Initials>J</Initials>
<AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Zhang</LastName>
<ForeName>Bai Yu</ForeName>
<Initials>BY</Initials>
<AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Yang</LastName>
<ForeName>Bo</ForeName>
<Initials>B</Initials>
<AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Waletich</LastName>
<ForeName>Justin Reed</ForeName>
<Initials>JR</Initials>
<AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Yin</LastName>
<ForeName>Weixiao</ForeName>
<Initials>W</Initials>
<AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Zheng</LastName>
<ForeName>Xiaobo</ForeName>
<Initials>X</Initials>
<AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, 210095, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Wang</LastName>
<ForeName>Yuanchao</ForeName>
<Initials>Y</Initials>
<Identifier Source="ORCID">0000-0001-5803-5343</Identifier>
<AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, 210095, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Dong</LastName>
<ForeName>Suomeng</ForeName>
<Initials>S</Initials>
<Identifier Source="ORCID">0000-0002-9623-6776</Identifier>
<AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing, 210095, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<GrantList CompleteYN="Y"><Grant><GrantID>31721004</GrantID>
<Agency>National Natural Science Foundation of China</Agency>
<Country>International</Country>
</Grant>
<Grant><GrantID>31772144</GrantID>
<Agency>National Natural Science Foundation of China</Agency>
<Country>International</Country>
</Grant>
<Grant><GrantID>151025</GrantID>
<Agency>Fok Ying Tong Education Foundation</Agency>
<Country>International</Country>
</Grant>
</GrantList>
<PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType>
<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic"><Year>2018</Year>
<Month>08</Month>
<Day>31</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo><Country>England</Country>
<MedlineTA>New Phytol</MedlineTA>
<NlmUniqueID>9882884</NlmUniqueID>
<ISSNLinking>0028-646X</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList><Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D037521">Virulence Factors</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList><MeshHeading><DescriptorName UI="D000064" MajorTopicYN="N">Acclimatization</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D005838" MajorTopicYN="N">Genotype</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D010838" MajorTopicYN="N">Phytophthora</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D010935" MajorTopicYN="N">Plant Diseases</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000276" MajorTopicYN="Y">immunology</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D057865" MajorTopicYN="Y">Plant Immunity</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D011110" MajorTopicYN="N">Polymorphism, Genetic</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D013025" MajorTopicYN="N">Soybeans</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D014774" MajorTopicYN="N">Virulence</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D037521" MajorTopicYN="N">Virulence Factors</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">Phytophthora
</Keyword>
<Keyword MajorTopicYN="Y">Rps3c
</Keyword>
<Keyword MajorTopicYN="Y">PsAvr3c</Keyword>
<Keyword MajorTopicYN="Y">allelic variations</Keyword>
<Keyword MajorTopicYN="Y">avirulence effector</Keyword>
<Keyword MajorTopicYN="Y">coevolution</Keyword>
<Keyword MajorTopicYN="Y">soybean</Keyword>
</KeywordList>
</MedlineCitation>
<PubmedData><History><PubMedPubDate PubStatus="received"><Year>2018</Year>
<Month>03</Month>
<Day>28</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted"><Year>2018</Year>
<Month>07</Month>
<Day>26</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="pubmed"><Year>2018</Year>
<Month>9</Month>
<Day>1</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="medline"><Year>2020</Year>
<Month>2</Month>
<Day>19</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez"><Year>2018</Year>
<Month>9</Month>
<Day>1</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
</History>
<PublicationStatus>ppublish</PublicationStatus>
<ArticleIdList><ArticleId IdType="pubmed">30169906</ArticleId>
<ArticleId IdType="doi">10.1111/nph.15414</ArticleId>
</ArticleIdList>
</PubmedData>
</pubmed>
<affiliations><list><country><li>République populaire de Chine</li>
</country>
</list>
<tree><country name="République populaire de Chine"><noRegion><name sortKey="Huang, Jie" sort="Huang, Jie" uniqKey="Huang J" first="Jie" last="Huang">Jie Huang</name>
</noRegion>
<name sortKey="Chen, Ling" sort="Chen, Ling" uniqKey="Chen L" first="Ling" last="Chen">Ling Chen</name>
<name sortKey="Dong, Suomeng" sort="Dong, Suomeng" uniqKey="Dong S" first="Suomeng" last="Dong">Suomeng Dong</name>
<name sortKey="Dong, Suomeng" sort="Dong, Suomeng" uniqKey="Dong S" first="Suomeng" last="Dong">Suomeng Dong</name>
<name sortKey="Huang, Jie" sort="Huang, Jie" uniqKey="Huang J" first="Jie" last="Huang">Jie Huang</name>
<name sortKey="Lu, Xinyu" sort="Lu, Xinyu" uniqKey="Lu X" first="Xinyu" last="Lu">Xinyu Lu</name>
<name sortKey="Peng, Qian" sort="Peng, Qian" uniqKey="Peng Q" first="Qian" last="Peng">Qian Peng</name>
<name sortKey="Waletich, Justin Reed" sort="Waletich, Justin Reed" uniqKey="Waletich J" first="Justin Reed" last="Waletich">Justin Reed Waletich</name>
<name sortKey="Wang, Yuanchao" sort="Wang, Yuanchao" uniqKey="Wang Y" first="Yuanchao" last="Wang">Yuanchao Wang</name>
<name sortKey="Wang, Yuanchao" sort="Wang, Yuanchao" uniqKey="Wang Y" first="Yuanchao" last="Wang">Yuanchao Wang</name>
<name sortKey="Yang, Bo" sort="Yang, Bo" uniqKey="Yang B" first="Bo" last="Yang">Bo Yang</name>
<name sortKey="Yang, Jin" sort="Yang, Jin" uniqKey="Yang J" first="Jin" last="Yang">Jin Yang</name>
<name sortKey="Yin, Weixiao" sort="Yin, Weixiao" uniqKey="Yin W" first="Weixiao" last="Yin">Weixiao Yin</name>
<name sortKey="Zhang, Bai Yu" sort="Zhang, Bai Yu" uniqKey="Zhang B" first="Bai Yu" last="Zhang">Bai Yu Zhang</name>
<name sortKey="Zhang, Ying" sort="Zhang, Ying" uniqKey="Zhang Y" first="Ying" last="Zhang">Ying Zhang</name>
<name sortKey="Zheng, Xiaobo" sort="Zheng, Xiaobo" uniqKey="Zheng X" first="Xiaobo" last="Zheng">Xiaobo Zheng</name>
<name sortKey="Zheng, Xiaobo" sort="Zheng, Xiaobo" uniqKey="Zheng X" first="Xiaobo" last="Zheng">Xiaobo Zheng</name>
</country>
</tree>
</affiliations>
</record>

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Natural allelic variations provide insights into host adaptation of Phytophthora avirulence effector PsAvr3c.

Natural allelic variations provide insights into host adaptation of Phytophthora avirulence effector PsAvr3c.

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