Serveur d'exploration sur la glutarédoxine

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Thioredoxin and Glutaredoxin Systems Required for Oxidative Stress Resistance, Fungicide Sensitivity, and Virulence of Alternaria alternata.

Identifieur interne : 000202 ( Main/Exploration ); précédent : 000201; suivant : 000203

Thioredoxin and Glutaredoxin Systems Required for Oxidative Stress Resistance, Fungicide Sensitivity, and Virulence of Alternaria alternata.

Auteurs : Haijie Ma [République populaire de Chine] ; Mingshuang Wang [République populaire de Chine] ; Yunpeng Gai [République populaire de Chine] ; Huilan Fu [République populaire de Chine] ; Bin Zhang [République populaire de Chine] ; Ruoxin Ruan [République populaire de Chine] ; Kuang-Ren Chung [Taïwan] ; Hongye Li [Taïwan, République populaire de Chine]

Source :

RBID : pubmed:29752269

Descripteurs français

English descriptors

Abstract

This study determined the function of thioredoxin and glutaredoxin systems in the phytopathogenic fungus Alternaria alternata via analyzing mutants obtained from the targeted deletion of genes encoding thioredoxin peroxidase (Tsa1), thioredoxin reductase (Trr1), and glutathione reductase (Glr1). Trr1 and Glr1, but not Tsa1, are required for growth and conidiation. The reduced growth and conidiation seen in the Trr1 or Glr1 deletion mutant can be restored by glutathione. Deletion mutants showing growth inhibition by oxidants are defective for H2O2 detoxification and induce smaller lesions on citrus leaves. Trr1 and Glr1, but not Tsa1, also contribute to NaCl resistance. Glr1 is required for sorbitol resistance and is responsible for resistance to mancozeb and boscalid but not chlorothalonil fungicides, a novel phenotype that has not been reported in fungi. Trr1 is required for resistance to boscalid and chlorothalonil fungicides but confers susceptibility to mancozeb. The Tsa1 deletion mutant displays wild-type sensitivity to the tested fungicides. The expression of Tsa1 and Trr1 is regulated by the oxidative stress responsive regulators Yap1, Hog1, and Skn7. The expression of Tsa1, but not Trr1, is also regulated indirectly by the NADPH oxidase. The results indicate that the capability to resist oxidative stress is required for virulence of A. alternataIMPORTANCE The thioredoxin and glutaredoxin systems are important thiol antioxidant systems in cells, and knowledge of these two systems in the plant-pathogenic fungus A. alternata is useful for finding new strategies to reduce the virulence of this pathogen. In this study, we demonstrated that thiol antioxidant system-related genes (Tsa1, Trr1, and Glr1) are required for H2O2 detoxification and virulence in A. alternata Moreover, deletion of Trr1 results in hypersensitivity to the fungicides chlorothalonil and boscalid, and Glr1 deletion mutants are highly sensitive to mancozeb, which is the fungicide mostly used in citrus fields. Therefore, our findings demonstrate that the ability to detoxify reactive oxygen species (ROS) plays a critical role in pathogenesis on citrus and provide novel insights into the physiological functions of thiol-containing systems in fungicide sensitivity for A. alternata.

DOI: 10.1128/AEM.00086-18
PubMed: 29752269
PubMed Central: PMC6029089


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Le document en format XML

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<name sortKey="Fu, Huilan" sort="Fu, Huilan" uniqKey="Fu H" first="Huilan" last="Fu">Huilan Fu</name>
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<name sortKey="Zhang, Bin" sort="Zhang, Bin" uniqKey="Zhang B" first="Bin" last="Zhang">Bin Zhang</name>
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<keywords scheme="KwdEn" xml:lang="en">
<term>Alternaria (drug effects)</term>
<term>Alternaria (genetics)</term>
<term>Antifungal Agents (pharmacology)</term>
<term>Biphenyl Compounds (pharmacology)</term>
<term>Citrus (microbiology)</term>
<term>Drug Resistance, Fungal (genetics)</term>
<term>Gene Deletion (MeSH)</term>
<term>Gene Expression Regulation, Fungal (MeSH)</term>
<term>Glutaredoxins (genetics)</term>
<term>Glutaredoxins (metabolism)</term>
<term>Glutathione Reductase (genetics)</term>
<term>Glutathione Reductase (metabolism)</term>
<term>Hydrogen Peroxide (metabolism)</term>
<term>Maneb (pharmacology)</term>
<term>NADPH Oxidases (metabolism)</term>
<term>Niacinamide (analogs & derivatives)</term>
<term>Niacinamide (pharmacology)</term>
<term>Nitriles (pharmacology)</term>
<term>Oxidative Stress (MeSH)</term>
<term>Peroxiredoxins (genetics)</term>
<term>Peroxiredoxins (metabolism)</term>
<term>Plant Leaves (microbiology)</term>
<term>Reactive Oxygen Species (metabolism)</term>
<term>Sulfhydryl Compounds (metabolism)</term>
<term>Thioredoxin-Disulfide Reductase (genetics)</term>
<term>Thioredoxin-Disulfide Reductase (metabolism)</term>
<term>Thioredoxins (genetics)</term>
<term>Thioredoxins (metabolism)</term>
<term>Zineb (pharmacology)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Alternaria (effets des médicaments et des substances chimiques)</term>
<term>Alternaria (génétique)</term>
<term>Antifongiques (pharmacologie)</term>
<term>Citrus (microbiologie)</term>
<term>Délétion de gène (MeSH)</term>
<term>Dérivés du biphényle (pharmacologie)</term>
<term>Espèces réactives de l'oxygène (métabolisme)</term>
<term>Feuilles de plante (microbiologie)</term>
<term>Glutarédoxines (génétique)</term>
<term>Glutarédoxines (métabolisme)</term>
<term>Glutathione reductase (génétique)</term>
<term>Glutathione reductase (métabolisme)</term>
<term>Manèbe (pharmacologie)</term>
<term>NADPH oxidase (métabolisme)</term>
<term>Nicotinamide (analogues et dérivés)</term>
<term>Nicotinamide (pharmacologie)</term>
<term>Nitriles (pharmacologie)</term>
<term>Peroxirédoxines (génétique)</term>
<term>Peroxirédoxines (métabolisme)</term>
<term>Peroxyde d'hydrogène (métabolisme)</term>
<term>Régulation de l'expression des gènes fongiques (MeSH)</term>
<term>Résistance des champignons aux médicaments (génétique)</term>
<term>Stress oxydatif (MeSH)</term>
<term>Thiols (métabolisme)</term>
<term>Thioredoxin-disulfide reductase (génétique)</term>
<term>Thioredoxin-disulfide reductase (métabolisme)</term>
<term>Thiorédoxines (génétique)</term>
<term>Thiorédoxines (métabolisme)</term>
<term>Zinèbe (pharmacologie)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="analogs & derivatives" xml:lang="en">
<term>Niacinamide</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en">
<term>Glutaredoxins</term>
<term>Glutathione Reductase</term>
<term>Peroxiredoxins</term>
<term>Thioredoxin-Disulfide Reductase</term>
<term>Thioredoxins</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Glutaredoxins</term>
<term>Glutathione Reductase</term>
<term>Hydrogen Peroxide</term>
<term>NADPH Oxidases</term>
<term>Peroxiredoxins</term>
<term>Reactive Oxygen Species</term>
<term>Sulfhydryl Compounds</term>
<term>Thioredoxin-Disulfide Reductase</term>
<term>Thioredoxins</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en">
<term>Antifungal Agents</term>
<term>Biphenyl Compounds</term>
<term>Maneb</term>
<term>Niacinamide</term>
<term>Nitriles</term>
<term>Zineb</term>
</keywords>
<keywords scheme="MESH" qualifier="analogues et dérivés" xml:lang="fr">
<term>Nicotinamide</term>
</keywords>
<keywords scheme="MESH" qualifier="drug effects" xml:lang="en">
<term>Alternaria</term>
</keywords>
<keywords scheme="MESH" qualifier="effets des médicaments et des substances chimiques" xml:lang="fr">
<term>Alternaria</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Alternaria</term>
<term>Drug Resistance, Fungal</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Alternaria</term>
<term>Glutarédoxines</term>
<term>Glutathione reductase</term>
<term>Peroxirédoxines</term>
<term>Résistance des champignons aux médicaments</term>
<term>Thioredoxin-disulfide reductase</term>
<term>Thiorédoxines</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr">
<term>Citrus</term>
<term>Feuilles de plante</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Citrus</term>
<term>Plant Leaves</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Espèces réactives de l'oxygène</term>
<term>Glutarédoxines</term>
<term>Glutathione reductase</term>
<term>NADPH oxidase</term>
<term>Peroxirédoxines</term>
<term>Peroxyde d'hydrogène</term>
<term>Thiols</term>
<term>Thioredoxin-disulfide reductase</term>
<term>Thiorédoxines</term>
</keywords>
<keywords scheme="MESH" qualifier="pharmacologie" xml:lang="fr">
<term>Antifongiques</term>
<term>Dérivés du biphényle</term>
<term>Manèbe</term>
<term>Nicotinamide</term>
<term>Nitriles</term>
<term>Zinèbe</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Gene Deletion</term>
<term>Gene Expression Regulation, Fungal</term>
<term>Oxidative Stress</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Délétion de gène</term>
<term>Régulation de l'expression des gènes fongiques</term>
<term>Stress oxydatif</term>
</keywords>
</textClass>
</profileDesc>
</teiHeader>
<front>
<div type="abstract" xml:lang="en">This study determined the function of thioredoxin and glutaredoxin systems in the phytopathogenic fungus
<i>Alternaria alternata</i>
via analyzing mutants obtained from the targeted deletion of genes encoding thioredoxin peroxidase (
<i>Tsa1</i>
), thioredoxin reductase (
<i>Trr1</i>
), and glutathione reductase (
<i>Glr1</i>
).
<i>Trr1</i>
and
<i>Glr1</i>
, but not
<i>Tsa1</i>
, are required for growth and conidiation. The reduced growth and conidiation seen in the
<i>Trr1</i>
or
<i>Glr1</i>
deletion mutant can be restored by glutathione. Deletion mutants showing growth inhibition by oxidants are defective for H
<sub>2</sub>
O
<sub>2</sub>
detoxification and induce smaller lesions on citrus leaves.
<i>Trr1</i>
and
<i>Glr1</i>
, but not
<i>Tsa1</i>
, also contribute to NaCl resistance.
<i>Glr1</i>
is required for sorbitol resistance and is responsible for resistance to mancozeb and boscalid but not chlorothalonil fungicides, a novel phenotype that has not been reported in fungi.
<i>Trr1</i>
is required for resistance to boscalid and chlorothalonil fungicides but confers susceptibility to mancozeb. The
<i>Tsa1</i>
deletion mutant displays wild-type sensitivity to the tested fungicides. The expression of
<i>Tsa1</i>
and
<i>Trr1</i>
is regulated by the oxidative stress responsive regulators Yap1, Hog1, and Skn7. The expression of
<i>Tsa1</i>
, but not
<i>Trr1</i>
, is also regulated indirectly by the NADPH oxidase. The results indicate that the capability to resist oxidative stress is required for virulence of
<i>A. alternata</i>
<b>IMPORTANCE</b>
The thioredoxin and glutaredoxin systems are important thiol antioxidant systems in cells, and knowledge of these two systems in the plant-pathogenic fungus
<i>A. alternata</i>
is useful for finding new strategies to reduce the virulence of this pathogen. In this study, we demonstrated that thiol antioxidant system-related genes (
<i>Tsa1</i>
,
<i>Trr1</i>
, and
<i>Glr1</i>
) are required for H
<sub>2</sub>
O
<sub>2</sub>
detoxification and virulence in
<i>A. alternata</i>
Moreover, deletion of
<i>Trr1</i>
results in hypersensitivity to the fungicides chlorothalonil and boscalid, and
<i>Glr1</i>
deletion mutants are highly sensitive to mancozeb, which is the fungicide mostly used in citrus fields. Therefore, our findings demonstrate that the ability to detoxify reactive oxygen species (ROS) plays a critical role in pathogenesis on citrus and provide novel insights into the physiological functions of thiol-containing systems in fungicide sensitivity for
<i>A. alternata</i>
.</div>
</front>
</TEI>
<pubmed>
<MedlineCitation Status="MEDLINE" Owner="NLM">
<PMID Version="1">29752269</PMID>
<DateCompleted>
<Year>2019</Year>
<Month>10</Month>
<Day>07</Day>
</DateCompleted>
<DateRevised>
<Year>2019</Year>
<Month>10</Month>
<Day>07</Day>
</DateRevised>
<Article PubModel="Electronic-Print">
<Journal>
<ISSN IssnType="Electronic">1098-5336</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>84</Volume>
<Issue>14</Issue>
<PubDate>
<Year>2018</Year>
<Month>07</Month>
<Day>15</Day>
</PubDate>
</JournalIssue>
<Title>Applied and environmental microbiology</Title>
<ISOAbbreviation>Appl Environ Microbiol</ISOAbbreviation>
</Journal>
<ArticleTitle>Thioredoxin and Glutaredoxin Systems Required for Oxidative Stress Resistance, Fungicide Sensitivity, and Virulence of Alternaria alternata.</ArticleTitle>
<ELocationID EIdType="pii" ValidYN="Y">e00086-18</ELocationID>
<ELocationID EIdType="doi" ValidYN="Y">10.1128/AEM.00086-18</ELocationID>
<Abstract>
<AbstractText>This study determined the function of thioredoxin and glutaredoxin systems in the phytopathogenic fungus
<i>Alternaria alternata</i>
via analyzing mutants obtained from the targeted deletion of genes encoding thioredoxin peroxidase (
<i>Tsa1</i>
), thioredoxin reductase (
<i>Trr1</i>
), and glutathione reductase (
<i>Glr1</i>
).
<i>Trr1</i>
and
<i>Glr1</i>
, but not
<i>Tsa1</i>
, are required for growth and conidiation. The reduced growth and conidiation seen in the
<i>Trr1</i>
or
<i>Glr1</i>
deletion mutant can be restored by glutathione. Deletion mutants showing growth inhibition by oxidants are defective for H
<sub>2</sub>
O
<sub>2</sub>
detoxification and induce smaller lesions on citrus leaves.
<i>Trr1</i>
and
<i>Glr1</i>
, but not
<i>Tsa1</i>
, also contribute to NaCl resistance.
<i>Glr1</i>
is required for sorbitol resistance and is responsible for resistance to mancozeb and boscalid but not chlorothalonil fungicides, a novel phenotype that has not been reported in fungi.
<i>Trr1</i>
is required for resistance to boscalid and chlorothalonil fungicides but confers susceptibility to mancozeb. The
<i>Tsa1</i>
deletion mutant displays wild-type sensitivity to the tested fungicides. The expression of
<i>Tsa1</i>
and
<i>Trr1</i>
is regulated by the oxidative stress responsive regulators Yap1, Hog1, and Skn7. The expression of
<i>Tsa1</i>
, but not
<i>Trr1</i>
, is also regulated indirectly by the NADPH oxidase. The results indicate that the capability to resist oxidative stress is required for virulence of
<i>A. alternata</i>
<b>IMPORTANCE</b>
The thioredoxin and glutaredoxin systems are important thiol antioxidant systems in cells, and knowledge of these two systems in the plant-pathogenic fungus
<i>A. alternata</i>
is useful for finding new strategies to reduce the virulence of this pathogen. In this study, we demonstrated that thiol antioxidant system-related genes (
<i>Tsa1</i>
,
<i>Trr1</i>
, and
<i>Glr1</i>
) are required for H
<sub>2</sub>
O
<sub>2</sub>
detoxification and virulence in
<i>A. alternata</i>
Moreover, deletion of
<i>Trr1</i>
results in hypersensitivity to the fungicides chlorothalonil and boscalid, and
<i>Glr1</i>
deletion mutants are highly sensitive to mancozeb, which is the fungicide mostly used in citrus fields. Therefore, our findings demonstrate that the ability to detoxify reactive oxygen species (ROS) plays a critical role in pathogenesis on citrus and provide novel insights into the physiological functions of thiol-containing systems in fungicide sensitivity for
<i>A. alternata</i>
.</AbstractText>
<CopyrightInformation>Copyright © 2018 American Society for Microbiology.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Ma</LastName>
<ForeName>Haijie</ForeName>
<Initials>H</Initials>
<AffiliationInfo>
<Affiliation>Institute of Biotechnology, Zhejiang University, Hangzhou, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Hangzhou, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Wang</LastName>
<ForeName>Mingshuang</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Institute of Biotechnology, Zhejiang University, Hangzhou, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Hangzhou, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Gai</LastName>
<ForeName>Yunpeng</ForeName>
<Initials>Y</Initials>
<AffiliationInfo>
<Affiliation>Institute of Biotechnology, Zhejiang University, Hangzhou, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Hangzhou, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Fu</LastName>
<ForeName>Huilan</ForeName>
<Initials>H</Initials>
<AffiliationInfo>
<Affiliation>Institute of Biotechnology, Zhejiang University, Hangzhou, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Hangzhou, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Zhang</LastName>
<ForeName>Bin</ForeName>
<Initials>B</Initials>
<AffiliationInfo>
<Affiliation>Institute of Biotechnology, Zhejiang University, Hangzhou, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Hangzhou, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Ruan</LastName>
<ForeName>Ruoxin</ForeName>
<Initials>R</Initials>
<AffiliationInfo>
<Affiliation>Institute of Biotechnology, Zhejiang University, Hangzhou, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Hangzhou, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Chung</LastName>
<ForeName>Kuang-Ren</ForeName>
<Initials>KR</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Pathology, College of Agriculture and Natural Resources, National Chung-Hsing University, Taichung, Taiwan krchung@nchu.edu.tw hyli@zju.edu.cn.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Li</LastName>
<ForeName>Hongye</ForeName>
<Initials>H</Initials>
<AffiliationInfo>
<Affiliation>Institute of Biotechnology, Zhejiang University, Hangzhou, China krchung@nchu.edu.tw hyli@zju.edu.cn.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Hangzhou, China.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList>
<PublicationType UI="D016428">Journal Article</PublicationType>
<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2018</Year>
<Month>07</Month>
<Day>02</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>United States</Country>
<MedlineTA>Appl Environ Microbiol</MedlineTA>
<NlmUniqueID>7605801</NlmUniqueID>
<ISSNLinking>0099-2240</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D000935">Antifungal Agents</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D001713">Biphenyl Compounds</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D054477">Glutaredoxins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D009570">Nitriles</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D017382">Reactive Oxygen Species</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D013438">Sulfhydryl Compounds</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>12427-38-2</RegistryNumber>
<NameOfSubstance UI="D008344">Maneb</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>25X51I8RD4</RegistryNumber>
<NameOfSubstance UI="D009536">Niacinamide</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>32MS8ZRD1V</RegistryNumber>
<NameOfSubstance UI="C550088">2-chloro-N-(4-chlorobiphenyl-2-yl)nicotinamide</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>52500-60-4</RegistryNumber>
<NameOfSubstance UI="D013879">Thioredoxins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>BBX060AN9V</RegistryNumber>
<NameOfSubstance UI="D006861">Hydrogen Peroxide</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>EC 1.11.1.15</RegistryNumber>
<NameOfSubstance UI="D054464">Peroxiredoxins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>EC 1.6.3.-</RegistryNumber>
<NameOfSubstance UI="D019255">NADPH Oxidases</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>EC 1.8.1.7</RegistryNumber>
<NameOfSubstance UI="D005980">Glutathione Reductase</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>EC 1.8.1.9</RegistryNumber>
<NameOfSubstance UI="D013880">Thioredoxin-Disulfide Reductase</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>J718M71A7A</RegistryNumber>
<NameOfSubstance UI="C005806">tetrachloroisophthalonitrile</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>R0HY55EB9E</RegistryNumber>
<NameOfSubstance UI="C013099">mancozeb</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>X1FSB1OZPT</RegistryNumber>
<NameOfSubstance UI="D015038">Zineb</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D000528" MajorTopicYN="N">Alternaria</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="Y">drug effects</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D000935" MajorTopicYN="N">Antifungal Agents</DescriptorName>
<QualifierName UI="Q000494" MajorTopicYN="N">pharmacology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D001713" MajorTopicYN="N">Biphenyl Compounds</DescriptorName>
<QualifierName UI="Q000494" MajorTopicYN="N">pharmacology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D002957" MajorTopicYN="N">Citrus</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D025141" MajorTopicYN="N">Drug Resistance, Fungal</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D017353" MajorTopicYN="N">Gene Deletion</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D015966" MajorTopicYN="N">Gene Expression Regulation, Fungal</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D054477" MajorTopicYN="N">Glutaredoxins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D005980" MajorTopicYN="N">Glutathione Reductase</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D006861" MajorTopicYN="N">Hydrogen Peroxide</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D008344" MajorTopicYN="N">Maneb</DescriptorName>
<QualifierName UI="Q000494" MajorTopicYN="N">pharmacology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D019255" MajorTopicYN="N">NADPH Oxidases</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D009536" MajorTopicYN="N">Niacinamide</DescriptorName>
<QualifierName UI="Q000031" MajorTopicYN="N">analogs & derivatives</QualifierName>
<QualifierName UI="Q000494" MajorTopicYN="N">pharmacology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D009570" MajorTopicYN="N">Nitriles</DescriptorName>
<QualifierName UI="Q000494" MajorTopicYN="N">pharmacology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018384" MajorTopicYN="Y">Oxidative Stress</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D054464" MajorTopicYN="N">Peroxiredoxins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018515" MajorTopicYN="N">Plant Leaves</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D017382" MajorTopicYN="N">Reactive Oxygen Species</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D013438" MajorTopicYN="N">Sulfhydryl Compounds</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D013880" MajorTopicYN="N">Thioredoxin-Disulfide Reductase</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D013879" MajorTopicYN="N">Thioredoxins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D015038" MajorTopicYN="N">Zineb</DescriptorName>
<QualifierName UI="Q000494" MajorTopicYN="N">pharmacology</QualifierName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="Y">Alternaria alternata</Keyword>
<Keyword MajorTopicYN="Y">fungicide resistance</Keyword>
<Keyword MajorTopicYN="Y">glutaredoxin</Keyword>
<Keyword MajorTopicYN="Y">oxidative stress resistance</Keyword>
<Keyword MajorTopicYN="Y">thioredoxin</Keyword>
<Keyword MajorTopicYN="Y">virulence</Keyword>
</KeywordList>
</MedlineCitation>
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<Year>2018</Year>
<Month>01</Month>
<Day>12</Day>
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<Month>05</Month>
<Day>04</Day>
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