Serveur d'exploration Phytophthora

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A Phytophthora Effector Suppresses Trans-Kingdom RNAi to Promote Disease Susceptibility.

Identifieur interne : 000597 ( Main/Exploration ); précédent : 000596; suivant : 000598

A Phytophthora Effector Suppresses Trans-Kingdom RNAi to Promote Disease Susceptibility.

Auteurs : Yingnan Hou [États-Unis] ; Yi Zhai [États-Unis] ; Li Feng [République populaire de Chine] ; Hana Z. Karimi [États-Unis] ; Brian D. Rutter [États-Unis] ; Liping Zeng [États-Unis] ; Du Seok Choi [États-Unis] ; Bailong Zhang [États-Unis] ; Weifeng Gu [États-Unis] ; Xuemei Chen [États-Unis] ; Wenwu Ye [République populaire de Chine] ; Roger W. Innes [États-Unis] ; Jixian Zhai [République populaire de Chine] ; Wenbo Ma [États-Unis]

Source :

RBID : pubmed:30595554

Descripteurs français

English descriptors

Abstract

RNA silencing (RNAi) has a well-established role in anti-viral immunity in plants. The destructive eukaryotic pathogen Phytophthora encodes suppressors of RNAi (PSRs), which enhance plant susceptibility. However, the role of small RNAs in defense against eukaryotic pathogens is unclear. Here, we show that Phytophthora infection of Arabidopsis leads to increased production of a diverse pool of secondary small interfering RNAs (siRNAs). Instead of regulating endogenous plant genes, these siRNAs are found in extracellular vesicles and likely silence target genes in Phytophthora during natural infection. Introduction of a plant siRNA in Phytophthora leads to developmental deficiency and abolishes virulence, while Arabidopsis mutants defective in secondary siRNA biogenesis are hypersusceptible. Notably, Phytophthora effector PSR2 specifically inhibits secondary siRNA biogenesis in Arabidopsis and promotes infection. These findings uncover the role of siRNAs as antimicrobial agents against eukaryotic pathogens and highlight a defense/counter-defense arms race centered on trans-kingdom gene silencing between hosts and pathogens.

DOI: 10.1016/j.chom.2018.11.007
PubMed: 30595554


Affiliations:


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Le document en format XML

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<nlm:affiliation>Department of Microbiology and Plant Pathology, University of California, Riverside, Riverside, CA 92521, USA; Center for Plant Cell Biology, University of California, Riverside, Riverside, CA 92521, USA. Electronic address: wenbo.ma@ucr.edu.</nlm:affiliation>
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<name sortKey="Hou, Yingnan" sort="Hou, Yingnan" uniqKey="Hou Y" first="Yingnan" last="Hou">Yingnan Hou</name>
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<nlm:affiliation>Department of Microbiology and Plant Pathology, University of California, Riverside, Riverside, CA 92521, USA; Center for Plant Cell Biology, University of California, Riverside, Riverside, CA 92521, USA.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
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<region type="state">Californie</region>
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<name sortKey="Zhai, Yi" sort="Zhai, Yi" uniqKey="Zhai Y" first="Yi" last="Zhai">Yi Zhai</name>
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<nlm:affiliation>Department of Microbiology and Plant Pathology, University of California, Riverside, Riverside, CA 92521, USA; Center for Plant Cell Biology, University of California, Riverside, Riverside, CA 92521, USA.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
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<region type="state">Californie</region>
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<name sortKey="Feng, Li" sort="Feng, Li" uniqKey="Feng L" first="Li" last="Feng">Li Feng</name>
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<nlm:affiliation>Department of Biology, Indiana University, Bloomington, IN 47405, USA.</nlm:affiliation>
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<wicri:regionArea>Department of Biology, Indiana University, Bloomington, IN 47405</wicri:regionArea>
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<name sortKey="Rutter, Brian D" sort="Rutter, Brian D" uniqKey="Rutter B" first="Brian D" last="Rutter">Brian D. Rutter</name>
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<nlm:affiliation>Department of Biology, Indiana University, Bloomington, IN 47405, USA.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Biology, Indiana University, Bloomington, IN 47405</wicri:regionArea>
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<region type="state">Indiana</region>
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<name sortKey="Zeng, Liping" sort="Zeng, Liping" uniqKey="Zeng L" first="Liping" last="Zeng">Liping Zeng</name>
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<nlm:affiliation>Department of Microbiology and Plant Pathology, University of California, Riverside, Riverside, CA 92521, USA; Center for Plant Cell Biology, University of California, Riverside, Riverside, CA 92521, USA.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Microbiology and Plant Pathology, University of California, Riverside, Riverside, CA 92521, USA; Center for Plant Cell Biology, University of California, Riverside, Riverside, CA 92521</wicri:regionArea>
<placeName>
<region type="state">Californie</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Choi, Du Seok" sort="Choi, Du Seok" uniqKey="Choi D" first="Du Seok" last="Choi">Du Seok Choi</name>
<affiliation wicri:level="2">
<nlm:affiliation>Department of Microbiology and Plant Pathology, University of California, Riverside, Riverside, CA 92521, USA; Center for Plant Cell Biology, University of California, Riverside, Riverside, CA 92521, USA.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Microbiology and Plant Pathology, University of California, Riverside, Riverside, CA 92521, USA; Center for Plant Cell Biology, University of California, Riverside, Riverside, CA 92521</wicri:regionArea>
<placeName>
<region type="state">Californie</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Zhang, Bailong" sort="Zhang, Bailong" uniqKey="Zhang B" first="Bailong" last="Zhang">Bailong Zhang</name>
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<nlm:affiliation>Center for Plant Cell Biology, University of California, Riverside, Riverside, CA 92521, USA; Department of Botany and Plant Science, University of California, Riverside, Riverside, CA 92521, USA.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
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<region type="state">Californie</region>
</placeName>
</affiliation>
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<author>
<name sortKey="Gu, Weifeng" sort="Gu, Weifeng" uniqKey="Gu W" first="Weifeng" last="Gu">Weifeng Gu</name>
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<nlm:affiliation>Department of Cell Biology and Neuroscience, University of California, Riverside, Riverside, CA 92521, USA.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Cell Biology and Neuroscience, University of California, Riverside, Riverside, CA 92521</wicri:regionArea>
<placeName>
<region type="state">Californie</region>
</placeName>
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<author>
<name sortKey="Chen, Xuemei" sort="Chen, Xuemei" uniqKey="Chen X" first="Xuemei" last="Chen">Xuemei Chen</name>
<affiliation wicri:level="2">
<nlm:affiliation>Center for Plant Cell Biology, University of California, Riverside, Riverside, CA 92521, USA; Department of Botany and Plant Science, University of California, Riverside, Riverside, CA 92521, USA.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
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<region type="state">Californie</region>
</placeName>
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<author>
<name sortKey="Ye, Wenwu" sort="Ye, Wenwu" uniqKey="Ye W" first="Wenwu" last="Ye">Wenwu Ye</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>Nanjing 210095</wicri:noRegion>
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<name sortKey="Innes, Roger W" sort="Innes, Roger W" uniqKey="Innes R" first="Roger W" last="Innes">Roger W. Innes</name>
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<nlm:affiliation>Department of Biology, Indiana University, Bloomington, IN 47405, USA.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Biology, Indiana University, Bloomington, IN 47405</wicri:regionArea>
<placeName>
<region type="state">Indiana</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Zhai, Jixian" sort="Zhai, Jixian" uniqKey="Zhai J" first="Jixian" last="Zhai">Jixian Zhai</name>
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<nlm:affiliation>Institute of Plant and Food Science, Department of Biology, Southern University of Science and Technology, Shenzhen 518055, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Institute of Plant and Food Science, Department of Biology, Southern University of Science and Technology, Shenzhen 518055</wicri:regionArea>
<placeName>
<settlement type="city">Shenzhen</settlement>
<region type="province">Guangdong</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Ma, Wenbo" sort="Ma, Wenbo" uniqKey="Ma W" first="Wenbo" last="Ma">Wenbo Ma</name>
<affiliation wicri:level="2">
<nlm:affiliation>Department of Microbiology and Plant Pathology, University of California, Riverside, Riverside, CA 92521, USA; Center for Plant Cell Biology, University of California, Riverside, Riverside, CA 92521, USA. Electronic address: wenbo.ma@ucr.edu.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
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<placeName>
<region type="state">Californie</region>
</placeName>
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</analytic>
<series>
<title level="j">Cell host & microbe</title>
<idno type="eISSN">1934-6069</idno>
<imprint>
<date when="2019" type="published">2019</date>
</imprint>
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<textClass>
<keywords scheme="KwdEn" xml:lang="en">
<term>Arabidopsis (genetics)</term>
<term>Arabidopsis (immunology)</term>
<term>Arabidopsis (microbiology)</term>
<term>Arabidopsis Proteins (genetics)</term>
<term>Disease Susceptibility (microbiology)</term>
<term>Gene Expression Regulation, Plant (MeSH)</term>
<term>Gene Silencing (MeSH)</term>
<term>Genes, Reporter (genetics)</term>
<term>Host-Pathogen Interactions (genetics)</term>
<term>Host-Pathogen Interactions (immunology)</term>
<term>MicroRNAs (genetics)</term>
<term>MicroRNAs (immunology)</term>
<term>Phosphoprotein Phosphatases (antagonists & inhibitors)</term>
<term>Phosphoprotein Phosphatases (metabolism)</term>
<term>Phytophthora (metabolism)</term>
<term>Phytophthora (pathogenicity)</term>
<term>Plant Diseases (immunology)</term>
<term>Plant Diseases (microbiology)</term>
<term>Plant Immunity (genetics)</term>
<term>Plant Immunity (immunology)</term>
<term>Plant Leaves (immunology)</term>
<term>Plant Leaves (microbiology)</term>
<term>RNA Interference (immunology)</term>
<term>RNA, Small Interfering (biosynthesis)</term>
<term>RNA, Small Interfering (drug effects)</term>
<term>RNA, Small Interfering (genetics)</term>
<term>RNA-Binding Proteins (genetics)</term>
<term>RNA-Binding Proteins (metabolism)</term>
<term>Tobacco (MeSH)</term>
<term>Verticillium (MeSH)</term>
<term>Virulence (MeSH)</term>
<term>Virulence Factors (genetics)</term>
<term>Virulence Factors (metabolism)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Arabidopsis (génétique)</term>
<term>Arabidopsis (immunologie)</term>
<term>Arabidopsis (microbiologie)</term>
<term>Extinction de l'expression des gènes (MeSH)</term>
<term>Facteurs de virulence (génétique)</term>
<term>Facteurs de virulence (métabolisme)</term>
<term>Feuilles de plante (immunologie)</term>
<term>Feuilles de plante (microbiologie)</term>
<term>Gènes rapporteurs (génétique)</term>
<term>Immunité des plantes (génétique)</term>
<term>Immunité des plantes (immunologie)</term>
<term>Interactions hôte-pathogène (génétique)</term>
<term>Interactions hôte-pathogène (immunologie)</term>
<term>Interférence par ARN (immunologie)</term>
<term>Maladies des plantes (immunologie)</term>
<term>Maladies des plantes (microbiologie)</term>
<term>Petit ARN interférent (biosynthèse)</term>
<term>Petit ARN interférent (effets des médicaments et des substances chimiques)</term>
<term>Petit ARN interférent (génétique)</term>
<term>Phosphoprotein Phosphatases (antagonistes et inhibiteurs)</term>
<term>Phosphoprotein Phosphatases (métabolisme)</term>
<term>Phytophthora (métabolisme)</term>
<term>Phytophthora (pathogénicité)</term>
<term>Protéines d'Arabidopsis (génétique)</term>
<term>Protéines de liaison à l'ARN (génétique)</term>
<term>Protéines de liaison à l'ARN (métabolisme)</term>
<term>Prédisposition aux maladies (microbiologie)</term>
<term>Régulation de l'expression des gènes végétaux (MeSH)</term>
<term>Tabac (MeSH)</term>
<term>Verticillium (MeSH)</term>
<term>Virulence (MeSH)</term>
<term>microARN (génétique)</term>
<term>microARN (immunologie)</term>
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<term>Phosphoprotein Phosphatases</term>
</keywords>
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<term>RNA, Small Interfering</term>
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<term>RNA, Small Interfering</term>
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<term>Arabidopsis Proteins</term>
<term>MicroRNAs</term>
<term>RNA, Small Interfering</term>
<term>RNA-Binding Proteins</term>
<term>Virulence Factors</term>
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<term>Phosphoprotein Phosphatases</term>
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<term>Petit ARN interférent</term>
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<term>Arabidopsis</term>
<term>Genes, Reporter</term>
<term>Host-Pathogen Interactions</term>
<term>Plant Immunity</term>
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<term>Arabidopsis</term>
<term>Facteurs de virulence</term>
<term>Gènes rapporteurs</term>
<term>Immunité des plantes</term>
<term>Interactions hôte-pathogène</term>
<term>Petit ARN interférent</term>
<term>Protéines d'Arabidopsis</term>
<term>Protéines de liaison à l'ARN</term>
<term>microARN</term>
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<term>Arabidopsis</term>
<term>Feuilles de plante</term>
<term>Immunité des plantes</term>
<term>Interactions hôte-pathogène</term>
<term>Interférence par ARN</term>
<term>Maladies des plantes</term>
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<term>Arabidopsis</term>
<term>Host-Pathogen Interactions</term>
<term>MicroRNAs</term>
<term>Plant Diseases</term>
<term>Plant Immunity</term>
<term>Plant Leaves</term>
<term>RNA Interference</term>
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<term>Phosphoprotein Phosphatases</term>
<term>Phytophthora</term>
<term>RNA-Binding Proteins</term>
<term>Virulence Factors</term>
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<term>Arabidopsis</term>
<term>Feuilles de plante</term>
<term>Maladies des plantes</term>
<term>Prédisposition aux maladies</term>
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<term>Arabidopsis</term>
<term>Disease Susceptibility</term>
<term>Plant Diseases</term>
<term>Plant Leaves</term>
</keywords>
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<term>Facteurs de virulence</term>
<term>Phosphoprotein Phosphatases</term>
<term>Phytophthora</term>
<term>Protéines de liaison à l'ARN</term>
</keywords>
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<term>Phytophthora</term>
</keywords>
<keywords scheme="MESH" qualifier="pathogénicité" xml:lang="fr">
<term>Phytophthora</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Gene Expression Regulation, Plant</term>
<term>Gene Silencing</term>
<term>Tobacco</term>
<term>Verticillium</term>
<term>Virulence</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Extinction de l'expression des gènes</term>
<term>Régulation de l'expression des gènes végétaux</term>
<term>Tabac</term>
<term>Verticillium</term>
<term>Virulence</term>
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<div type="abstract" xml:lang="en">RNA silencing (RNAi) has a well-established role in anti-viral immunity in plants. The destructive eukaryotic pathogen Phytophthora encodes suppressors of RNAi (PSRs), which enhance plant susceptibility. However, the role of small RNAs in defense against eukaryotic pathogens is unclear. Here, we show that Phytophthora infection of Arabidopsis leads to increased production of a diverse pool of secondary small interfering RNAs (siRNAs). Instead of regulating endogenous plant genes, these siRNAs are found in extracellular vesicles and likely silence target genes in Phytophthora during natural infection. Introduction of a plant siRNA in Phytophthora leads to developmental deficiency and abolishes virulence, while Arabidopsis mutants defective in secondary siRNA biogenesis are hypersusceptible. Notably, Phytophthora effector PSR2 specifically inhibits secondary siRNA biogenesis in Arabidopsis and promotes infection. These findings uncover the role of siRNAs as antimicrobial agents against eukaryotic pathogens and highlight a defense/counter-defense arms race centered on trans-kingdom gene silencing between hosts and pathogens.</div>
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<Year>2019</Year>
<Month>03</Month>
<Day>14</Day>
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<DateRevised>
<Year>2020</Year>
<Month>09</Month>
<Day>30</Day>
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<Month>01</Month>
<Day>09</Day>
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<Title>Cell host & microbe</Title>
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<ArticleTitle>A Phytophthora Effector Suppresses Trans-Kingdom RNAi to Promote Disease Susceptibility.</ArticleTitle>
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<AbstractText>RNA silencing (RNAi) has a well-established role in anti-viral immunity in plants. The destructive eukaryotic pathogen Phytophthora encodes suppressors of RNAi (PSRs), which enhance plant susceptibility. However, the role of small RNAs in defense against eukaryotic pathogens is unclear. Here, we show that Phytophthora infection of Arabidopsis leads to increased production of a diverse pool of secondary small interfering RNAs (siRNAs). Instead of regulating endogenous plant genes, these siRNAs are found in extracellular vesicles and likely silence target genes in Phytophthora during natural infection. Introduction of a plant siRNA in Phytophthora leads to developmental deficiency and abolishes virulence, while Arabidopsis mutants defective in secondary siRNA biogenesis are hypersusceptible. Notably, Phytophthora effector PSR2 specifically inhibits secondary siRNA biogenesis in Arabidopsis and promotes infection. These findings uncover the role of siRNAs as antimicrobial agents against eukaryotic pathogens and highlight a defense/counter-defense arms race centered on trans-kingdom gene silencing between hosts and pathogens.</AbstractText>
<CopyrightInformation>Copyright © 2018 Elsevier Inc. All rights reserved.</CopyrightInformation>
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<LastName>Hou</LastName>
<ForeName>Yingnan</ForeName>
<Initials>Y</Initials>
<AffiliationInfo>
<Affiliation>Department of Microbiology and Plant Pathology, University of California, Riverside, Riverside, CA 92521, USA; Center for Plant Cell Biology, University of California, Riverside, Riverside, CA 92521, USA.</Affiliation>
</AffiliationInfo>
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</AffiliationInfo>
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<LastName>Karimi</LastName>
<ForeName>Hana Z</ForeName>
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<AffiliationInfo>
<Affiliation>Department of Biology, Indiana University, Bloomington, IN 47405, USA.</Affiliation>
</AffiliationInfo>
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<ForeName>Brian D</ForeName>
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<Affiliation>Department of Biology, Indiana University, Bloomington, IN 47405, USA.</Affiliation>
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</AffiliationInfo>
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<Affiliation>Center for Plant Cell Biology, University of California, Riverside, Riverside, CA 92521, USA; Department of Botany and Plant Science, University of California, Riverside, Riverside, CA 92521, USA.</Affiliation>
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<Affiliation>Department of Microbiology and Plant Pathology, University of California, Riverside, Riverside, CA 92521, USA; Center for Plant Cell Biology, University of California, Riverside, Riverside, CA 92521, USA. Electronic address: wenbo.ma@ucr.edu.</Affiliation>
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<Month>12</Month>
<Day>27</Day>
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HfdIndexSelect -h $EXPLOR_AREA/Data/Main/Exploration/RBID.i   -Sk "pubmed:30595554" \
       | HfdSelect -Kh $EXPLOR_AREA/Data/Main/Exploration/biblio.hfd   \
       | NlmPubMed2Wicri -a PhytophthoraV1 

Wicri

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