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Albugo-imposed changes to tryptophan-derived antimicrobial metabolite biosynthesis may contribute to suppression of non-host resistance to Phytophthora infestans in Arabidopsis thaliana.

Identifieur interne : 000A67 ( Main/Exploration ); précédent : 000A66; suivant : 000A68

Albugo-imposed changes to tryptophan-derived antimicrobial metabolite biosynthesis may contribute to suppression of non-host resistance to Phytophthora infestans in Arabidopsis thaliana.

Auteurs : David C. Prince [Royaume-Uni] ; Ghanasyam Rallapalli [Royaume-Uni] ; Deyang Xu [Danemark] ; Henk-Jan Schoonbeek [Royaume-Uni] ; Volkan Çevik [Royaume-Uni] ; Shuta Asai [Royaume-Uni, Japon] ; Eric Kemen [Royaume-Uni, Allemagne] ; Neftaly Cruz-Mireles [Royaume-Uni] ; Ariane Kemen [Royaume-Uni, Allemagne] ; Khaoula Belhaj [Royaume-Uni] ; Sebastian Schornack [Royaume-Uni] ; Sophien Kamoun [Royaume-Uni] ; Eric B. Holub [Royaume-Uni] ; Barbara A. Halkier [Danemark] ; Jonathan D G. Jones [Royaume-Uni]

Source :

RBID : pubmed:28320402

Descripteurs français

English descriptors

Abstract

BACKGROUND

Plants are exposed to diverse pathogens and pests, yet most plants are resistant to most plant pathogens. Non-host resistance describes the ability of all members of a plant species to successfully prevent colonization by any given member of a pathogen species. White blister rust caused by Albugo species can overcome non-host resistance and enable secondary infection and reproduction of usually non-virulent pathogens, including the potato late blight pathogen Phytophthora infestans on Arabidopsis thaliana. However, the molecular basis of host defense suppression in this complex plant-microbe interaction is unclear. Here, we investigate specific defense mechanisms in Arabidopsis that are suppressed by Albugo infection.

RESULTS

Gene expression profiling revealed that two species of Albugo upregulate genes associated with tryptophan-derived antimicrobial metabolites in Arabidopsis. Albugo laibachii-infected tissue has altered levels of these metabolites, with lower indol-3-yl methylglucosinolate and higher camalexin accumulation than uninfected tissue. We investigated the contribution of these Albugo-imposed phenotypes to suppression of non-host resistance to P. infestans. Absence of tryptophan-derived antimicrobial compounds enables P. infestans colonization of Arabidopsis, although to a lesser extent than Albugo-infected tissue. A. laibachii also suppresses a subset of genes regulated by salicylic acid; however, salicylic acid plays only a minor role in non-host resistance to P. infestans.

CONCLUSIONS

Albugo sp. alter tryptophan-derived metabolites and suppress elements of the responses to salicylic acid in Arabidopsis. Albugo sp. imposed alterations in tryptophan-derived metabolites may play a role in Arabidopsis non-host resistance to P. infestans. Understanding the basis of non-host resistance to pathogens such as P. infestans could assist in development of strategies to elevate food security.


DOI: 10.1186/s12915-017-0360-z
PubMed: 28320402
PubMed Central: PMC5358052


Affiliations:


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<name sortKey="Kemen, Ariane" sort="Kemen, Ariane" uniqKey="Kemen A" first="Ariane" last="Kemen">Ariane Kemen</name>
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<nlm:affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH, United Kingdom.</nlm:affiliation>
<country xml:lang="fr">Royaume-Uni</country>
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<affiliation wicri:level="4">
<nlm:affiliation>Sainsbury Laboratory, University of Cambridge, Cambridge, UK.</nlm:affiliation>
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<region type="country">Angleterre</region>
<region type="région" nuts="1">Angleterre de l'Est</region>
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<author>
<name sortKey="Kamoun, Sophien" sort="Kamoun, Sophien" uniqKey="Kamoun S" first="Sophien" last="Kamoun">Sophien Kamoun</name>
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<nlm:affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH, United Kingdom.</nlm:affiliation>
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<author>
<name sortKey="Holub, Eric B" sort="Holub, Eric B" uniqKey="Holub E" first="Eric B" last="Holub">Eric B. Holub</name>
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<nlm:affiliation>School of Life Sciences, Warwick Crop Centre, University of Warwick, Wellesbourne, UK.</nlm:affiliation>
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<wicri:regionArea>School of Life Sciences, Warwick Crop Centre, University of Warwick, Wellesbourne</wicri:regionArea>
<wicri:noRegion>Wellesbourne</wicri:noRegion>
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</author>
<author>
<name sortKey="Halkier, Barbara A" sort="Halkier, Barbara A" uniqKey="Halkier B" first="Barbara A" last="Halkier">Barbara A. Halkier</name>
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<nlm:affiliation>DynaMo Center, Department of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen, 40 Thorvaldsensvej, DK-1871, Frederiksberg C, Denmark.</nlm:affiliation>
<country xml:lang="fr">Danemark</country>
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<author>
<name sortKey="Jones, Jonathan D G" sort="Jones, Jonathan D G" uniqKey="Jones J" first="Jonathan D G" last="Jones">Jonathan D G. Jones</name>
<affiliation wicri:level="1">
<nlm:affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH, United Kingdom. jonathan.jones@tsl.ac.uk.</nlm:affiliation>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea>The Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH</wicri:regionArea>
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<series>
<title level="j">BMC biology</title>
<idno type="eISSN">1741-7007</idno>
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<date when="2017" type="published">2017</date>
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<keywords scheme="KwdEn" xml:lang="en">
<term>Anti-Infective Agents (metabolism)</term>
<term>Arabidopsis (drug effects)</term>
<term>Arabidopsis (genetics)</term>
<term>Arabidopsis (immunology)</term>
<term>Arabidopsis (microbiology)</term>
<term>Biomass (MeSH)</term>
<term>Biosynthetic Pathways (drug effects)</term>
<term>Biosynthetic Pathways (genetics)</term>
<term>Brassica (microbiology)</term>
<term>Disease Resistance (drug effects)</term>
<term>Disease Resistance (immunology)</term>
<term>Disease Susceptibility (MeSH)</term>
<term>Gene Expression Profiling (MeSH)</term>
<term>Gene Expression Regulation, Plant (drug effects)</term>
<term>Gene Ontology (MeSH)</term>
<term>Genes, Plant (MeSH)</term>
<term>Glucosinolates (metabolism)</term>
<term>Indoles (metabolism)</term>
<term>Metabolic Networks and Pathways (drug effects)</term>
<term>Mutation (genetics)</term>
<term>Phytophthora infestans (physiology)</term>
<term>Plant Diseases (immunology)</term>
<term>Plant Diseases (microbiology)</term>
<term>Plant Immunity (drug effects)</term>
<term>Plant Leaves (drug effects)</term>
<term>Plant Leaves (microbiology)</term>
<term>Reproducibility of Results (MeSH)</term>
<term>Salicylic Acid (pharmacology)</term>
<term>Signal Transduction (drug effects)</term>
<term>Thiazoles (metabolism)</term>
<term>Tryptophan (metabolism)</term>
<term>Up-Regulation (drug effects)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Acide salicylique (pharmacologie)</term>
<term>Analyse de profil d'expression de gènes (MeSH)</term>
<term>Anti-infectieux (métabolisme)</term>
<term>Arabidopsis (effets des médicaments et des substances chimiques)</term>
<term>Arabidopsis (génétique)</term>
<term>Arabidopsis (immunologie)</term>
<term>Arabidopsis (microbiologie)</term>
<term>Biomasse (MeSH)</term>
<term>Brassica (microbiologie)</term>
<term>Feuilles de plante (effets des médicaments et des substances chimiques)</term>
<term>Feuilles de plante (microbiologie)</term>
<term>Gene Ontology (MeSH)</term>
<term>Glucosinolates (métabolisme)</term>
<term>Gènes de plante (MeSH)</term>
<term>Immunité des plantes (effets des médicaments et des substances chimiques)</term>
<term>Indoles (métabolisme)</term>
<term>Maladies des plantes (immunologie)</term>
<term>Maladies des plantes (microbiologie)</term>
<term>Mutation (génétique)</term>
<term>Phytophthora infestans (physiologie)</term>
<term>Prédisposition aux maladies (MeSH)</term>
<term>Reproductibilité des résultats (MeSH)</term>
<term>Régulation de l'expression des gènes végétaux (effets des médicaments et des substances chimiques)</term>
<term>Régulation positive (effets des médicaments et des substances chimiques)</term>
<term>Résistance à la maladie (effets des médicaments et des substances chimiques)</term>
<term>Résistance à la maladie (immunologie)</term>
<term>Thiazoles (métabolisme)</term>
<term>Transduction du signal (effets des médicaments et des substances chimiques)</term>
<term>Tryptophane (métabolisme)</term>
<term>Voies de biosynthèse (effets des médicaments et des substances chimiques)</term>
<term>Voies de biosynthèse (génétique)</term>
<term>Voies et réseaux métaboliques (effets des médicaments et des substances chimiques)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Anti-Infective Agents</term>
<term>Glucosinolates</term>
<term>Indoles</term>
<term>Thiazoles</term>
<term>Tryptophan</term>
</keywords>
<keywords scheme="MESH" qualifier="drug effects" xml:lang="en">
<term>Arabidopsis</term>
<term>Biosynthetic Pathways</term>
<term>Disease Resistance</term>
<term>Gene Expression Regulation, Plant</term>
<term>Metabolic Networks and Pathways</term>
<term>Plant Immunity</term>
<term>Plant Leaves</term>
<term>Signal Transduction</term>
<term>Up-Regulation</term>
</keywords>
<keywords scheme="MESH" qualifier="effets des médicaments et des substances chimiques" xml:lang="fr">
<term>Arabidopsis</term>
<term>Feuilles de plante</term>
<term>Immunité des plantes</term>
<term>Régulation de l'expression des gènes végétaux</term>
<term>Régulation positive</term>
<term>Résistance à la maladie</term>
<term>Transduction du signal</term>
<term>Voies de biosynthèse</term>
<term>Voies et réseaux métaboliques</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Arabidopsis</term>
<term>Biosynthetic Pathways</term>
<term>Mutation</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Arabidopsis</term>
<term>Mutation</term>
<term>Voies de biosynthèse</term>
</keywords>
<keywords scheme="MESH" qualifier="immunologie" xml:lang="fr">
<term>Arabidopsis</term>
<term>Maladies des plantes</term>
<term>Résistance à la maladie</term>
</keywords>
<keywords scheme="MESH" qualifier="immunology" xml:lang="en">
<term>Arabidopsis</term>
<term>Disease Resistance</term>
<term>Plant Diseases</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr">
<term>Arabidopsis</term>
<term>Brassica</term>
<term>Feuilles de plante</term>
<term>Maladies des plantes</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Arabidopsis</term>
<term>Brassica</term>
<term>Plant Diseases</term>
<term>Plant Leaves</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Anti-infectieux</term>
<term>Glucosinolates</term>
<term>Indoles</term>
<term>Thiazoles</term>
<term>Tryptophane</term>
</keywords>
<keywords scheme="MESH" qualifier="pharmacologie" xml:lang="fr">
<term>Acide salicylique</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en">
<term>Salicylic Acid</term>
</keywords>
<keywords scheme="MESH" qualifier="physiologie" xml:lang="fr">
<term>Phytophthora infestans</term>
</keywords>
<keywords scheme="MESH" qualifier="physiology" xml:lang="en">
<term>Phytophthora infestans</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Biomass</term>
<term>Disease Susceptibility</term>
<term>Gene Expression Profiling</term>
<term>Gene Ontology</term>
<term>Genes, Plant</term>
<term>Reproducibility of Results</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Analyse de profil d'expression de gènes</term>
<term>Biomasse</term>
<term>Gene Ontology</term>
<term>Gènes de plante</term>
<term>Prédisposition aux maladies</term>
<term>Reproductibilité des résultats</term>
</keywords>
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<front>
<div type="abstract" xml:lang="en">
<p>
<b>BACKGROUND</b>
</p>
<p>Plants are exposed to diverse pathogens and pests, yet most plants are resistant to most plant pathogens. Non-host resistance describes the ability of all members of a plant species to successfully prevent colonization by any given member of a pathogen species. White blister rust caused by Albugo species can overcome non-host resistance and enable secondary infection and reproduction of usually non-virulent pathogens, including the potato late blight pathogen Phytophthora infestans on Arabidopsis thaliana. However, the molecular basis of host defense suppression in this complex plant-microbe interaction is unclear. Here, we investigate specific defense mechanisms in Arabidopsis that are suppressed by Albugo infection.</p>
</div>
<div type="abstract" xml:lang="en">
<p>
<b>RESULTS</b>
</p>
<p>Gene expression profiling revealed that two species of Albugo upregulate genes associated with tryptophan-derived antimicrobial metabolites in Arabidopsis. Albugo laibachii-infected tissue has altered levels of these metabolites, with lower indol-3-yl methylglucosinolate and higher camalexin accumulation than uninfected tissue. We investigated the contribution of these Albugo-imposed phenotypes to suppression of non-host resistance to P. infestans. Absence of tryptophan-derived antimicrobial compounds enables P. infestans colonization of Arabidopsis, although to a lesser extent than Albugo-infected tissue. A. laibachii also suppresses a subset of genes regulated by salicylic acid; however, salicylic acid plays only a minor role in non-host resistance to P. infestans.</p>
</div>
<div type="abstract" xml:lang="en">
<p>
<b>CONCLUSIONS</b>
</p>
<p>Albugo sp. alter tryptophan-derived metabolites and suppress elements of the responses to salicylic acid in Arabidopsis. Albugo sp. imposed alterations in tryptophan-derived metabolites may play a role in Arabidopsis non-host resistance to P. infestans. Understanding the basis of non-host resistance to pathogens such as P. infestans could assist in development of strategies to elevate food security.</p>
</div>
</front>
</TEI>
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<PMID Version="1">28320402</PMID>
<DateCompleted>
<Year>2017</Year>
<Month>10</Month>
<Day>16</Day>
</DateCompleted>
<DateRevised>
<Year>2018</Year>
<Month>11</Month>
<Day>13</Day>
</DateRevised>
<Article PubModel="Electronic">
<Journal>
<ISSN IssnType="Electronic">1741-7007</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>15</Volume>
<Issue>1</Issue>
<PubDate>
<Year>2017</Year>
<Month>03</Month>
<Day>20</Day>
</PubDate>
</JournalIssue>
<Title>BMC biology</Title>
<ISOAbbreviation>BMC Biol</ISOAbbreviation>
</Journal>
<ArticleTitle>Albugo-imposed changes to tryptophan-derived antimicrobial metabolite biosynthesis may contribute to suppression of non-host resistance to Phytophthora infestans in Arabidopsis thaliana.</ArticleTitle>
<Pagination>
<MedlinePgn>20</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1186/s12915-017-0360-z</ELocationID>
<Abstract>
<AbstractText Label="BACKGROUND">Plants are exposed to diverse pathogens and pests, yet most plants are resistant to most plant pathogens. Non-host resistance describes the ability of all members of a plant species to successfully prevent colonization by any given member of a pathogen species. White blister rust caused by Albugo species can overcome non-host resistance and enable secondary infection and reproduction of usually non-virulent pathogens, including the potato late blight pathogen Phytophthora infestans on Arabidopsis thaliana. However, the molecular basis of host defense suppression in this complex plant-microbe interaction is unclear. Here, we investigate specific defense mechanisms in Arabidopsis that are suppressed by Albugo infection.</AbstractText>
<AbstractText Label="RESULTS">Gene expression profiling revealed that two species of Albugo upregulate genes associated with tryptophan-derived antimicrobial metabolites in Arabidopsis. Albugo laibachii-infected tissue has altered levels of these metabolites, with lower indol-3-yl methylglucosinolate and higher camalexin accumulation than uninfected tissue. We investigated the contribution of these Albugo-imposed phenotypes to suppression of non-host resistance to P. infestans. Absence of tryptophan-derived antimicrobial compounds enables P. infestans colonization of Arabidopsis, although to a lesser extent than Albugo-infected tissue. A. laibachii also suppresses a subset of genes regulated by salicylic acid; however, salicylic acid plays only a minor role in non-host resistance to P. infestans.</AbstractText>
<AbstractText Label="CONCLUSIONS">Albugo sp. alter tryptophan-derived metabolites and suppress elements of the responses to salicylic acid in Arabidopsis. Albugo sp. imposed alterations in tryptophan-derived metabolites may play a role in Arabidopsis non-host resistance to P. infestans. Understanding the basis of non-host resistance to pathogens such as P. infestans could assist in development of strategies to elevate food security.</AbstractText>
</Abstract>
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<LastName>Prince</LastName>
<ForeName>David C</ForeName>
<Initials>DC</Initials>
<AffiliationInfo>
<Affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH, United Kingdom.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Rallapalli</LastName>
<ForeName>Ghanasyam</ForeName>
<Initials>G</Initials>
<AffiliationInfo>
<Affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH, United Kingdom.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Norwich Medical School, University of East Anglia, Norwich Research Park, Norwich, UK.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Xu</LastName>
<ForeName>Deyang</ForeName>
<Initials>D</Initials>
<AffiliationInfo>
<Affiliation>DynaMo Center, Department of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen, 40 Thorvaldsensvej, DK-1871, Frederiksberg C, Denmark.</Affiliation>
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<ForeName>Henk-Jan</ForeName>
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<Affiliation>Department of Crop Genetics, John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK.</Affiliation>
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<ForeName>Volkan</ForeName>
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</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Biology and Biochemistry, University of Bath, Bath, UK.</Affiliation>
</AffiliationInfo>
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<ForeName>Shuta</ForeName>
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<AffiliationInfo>
<Affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH, United Kingdom.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Plant Immunity Research Group, Center for Sustainable Resource Science, RIKEN Yokohama Institute, Yokohama, Japan.</Affiliation>
</AffiliationInfo>
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<AffiliationInfo>
<Affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH, United Kingdom.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Max Planck Research Group Fungal Biodiversity, Max Planck Institute for Plant Breeding Research, Cologne, Germany.</Affiliation>
</AffiliationInfo>
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<LastName>Cruz-Mireles</LastName>
<ForeName>Neftaly</ForeName>
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<AffiliationInfo>
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<LastName>Belhaj</LastName>
<ForeName>Khaoula</ForeName>
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<AffiliationInfo>
<Affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Schornack</LastName>
<ForeName>Sebastian</ForeName>
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<AffiliationInfo>
<Affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH, United Kingdom.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Sainsbury Laboratory, University of Cambridge, Cambridge, UK.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Kamoun</LastName>
<ForeName>Sophien</ForeName>
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<Affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH, United Kingdom.</Affiliation>
</AffiliationInfo>
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<Affiliation>School of Life Sciences, Warwick Crop Centre, University of Warwick, Wellesbourne, UK.</Affiliation>
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<ForeName>Barbara A</ForeName>
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<Affiliation>DynaMo Center, Department of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen, 40 Thorvaldsensvej, DK-1871, Frederiksberg C, Denmark.</Affiliation>
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<GrantID>BB/G042960/1</GrantID>
<Agency>Biotechnology and Biological Sciences Research Council</Agency>
<Country>United Kingdom</Country>
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<Month>03</Month>
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<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
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<DescriptorName UI="D001937" MajorTopicYN="N">Brassica</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
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<MeshHeading>
<DescriptorName UI="D060467" MajorTopicYN="N">Disease Resistance</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
<QualifierName UI="Q000276" MajorTopicYN="Y">immunology</QualifierName>
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<MeshHeading>
<DescriptorName UI="D004198" MajorTopicYN="N">Disease Susceptibility</DescriptorName>
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<MeshHeading>
<DescriptorName UI="D020869" MajorTopicYN="N">Gene Expression Profiling</DescriptorName>
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<MeshHeading>
<DescriptorName UI="D018506" MajorTopicYN="N">Gene Expression Regulation, Plant</DescriptorName>
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<DescriptorName UI="D063990" MajorTopicYN="N">Gene Ontology</DescriptorName>
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<DescriptorName UI="D017343" MajorTopicYN="N">Genes, Plant</DescriptorName>
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<MeshHeading>
<DescriptorName UI="D005961" MajorTopicYN="N">Glucosinolates</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
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