Synergistic anti-oomycete effect of melatonin with a biofungicide against oomycetic black shank disease.
Identifieur interne : 000658 ( Main/Exploration ); précédent : 000657; suivant : 000659Synergistic anti-oomycete effect of melatonin with a biofungicide against oomycetic black shank disease.
Auteurs : Shumin Zhang [République populaire de Chine] ; Sen Liu [République populaire de Chine] ; Jiankui Zhang [République populaire de Chine] ; Russel J. Reiter [États-Unis] ; Ying Wang [République populaire de Chine] ; Dan Qiu [République populaire de Chine] ; Xiumei Luo [République populaire de Chine] ; A Rehman Khalid [République populaire de Chine] ; Hanyan Wang [République populaire de Chine] ; Li Feng [République populaire de Chine] ; Zhenghong Lin [République populaire de Chine] ; Maozhi Ren [République populaire de Chine]Source :
- Journal of pineal research [ 1600-079X ] ; 2018.
Descripteurs français
- KwdFr :
- MESH :
- croissance et développement : Phytophthora.
- effets des médicaments et des substances chimiques : Résistance aux substances.
- génétique : Phytophthora.
- microbiologie : Maladies des plantes.
- pharmacologie : Acides sulfiniques, Fongicides industriels, Mélatonine.
English descriptors
- KwdEn :
- MESH :
- chemical , pharmacology : Fungicides, Industrial, Melatonin, Sulfinic Acids.
- drug effects : Drug Resistance.
- genetics : Phytophthora.
- growth & development : Phytophthora.
- microbiology : Plant Diseases.
Abstract
Human health, food safety, and agriculture have been threatened by oomycetic diseases caused by notorious pathogenic oomycetes. Chemical oomyceticides are the main approaches in control of pathogenic oomycetes. However, the overused chemical oomyceticides have resulted in serious environmental pollution and drug resistance. The eco-friendly bio-oomyceticides are required for sustainable development through screening synergistic drug combinations. In this study, Phytophthora nicotianae (P. nicotianae), as one of the most destructive oomycetic diseases in agriculture, was used as a model system to screen the novel bio-oomyceticides based on drug combination. The results showed that treatment of melatonin or ethylicin (IUPAC Name: 1-ethylsulfonylsulfanylethane) alone displayed similar phenotypes such as the inhibition of the hyphal growth, reduction of the cell viability, and suppression of the virulence of P. nicotianae. Importantly, melatonin and ethylicin shared the same targets of interfering with the amino acid metabolism, overexpressing apoptosis-inducing factor, and dysregulating the virulence-related genes. Furthermore, strong synergism against P. nicotianae was induced by combining melatonin with ethylicin. Under treatment of the combination of melatonin and ethylicin, the expression of genes associated with amino acid, the apoptosis-inducing factor, and the virulence-related genes was much more significantly dysregulated than that of single drug treatment. Thus, the tobacco black shank caused by P. nicotianae can be successfully controlled using the combination of melatonin and ethylicin. These observations suggest that the synergistic effect based on the combination of melatonin and ethylicin is an eco-friendly alternative for the control of the destructive oomycetic diseases.
DOI: 10.1111/jpi.12492
PubMed: 29575191
Affiliations:
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Sciences, Chongqing University, Chongqing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>School of Life Sciences, Chongqing University, Chongqing</wicri:regionArea><wicri:noRegion>Chongqing</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Hanyan" sort="Wang, Hanyan" uniqKey="Wang H" first="Hanyan" last="Wang">Hanyan Wang</name><affiliation wicri:level="1"><nlm:affiliation>School of Basic Medical Sciences, North Sichuan Medical College, Nanchong, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>School of Basic Medical Sciences, North Sichuan Medical College, Nanchong</wicri:regionArea><wicri:noRegion>Nanchong</wicri:noRegion></affiliation></author><author><name sortKey="Feng, Li" sort="Feng, Li" uniqKey="Feng L" first="Li" last="Feng">Li Feng</name><affiliation wicri:level="1"><nlm:affiliation>School of Life Sciences, Chongqing University, Chongqing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>School of Life Sciences, Chongqing University, Chongqing</wicri:regionArea><wicri:noRegion>Chongqing</wicri:noRegion></affiliation></author><author><name sortKey="Lin, Zhenghong" sort="Lin, Zhenghong" uniqKey="Lin Z" first="Zhenghong" last="Lin">Zhenghong Lin</name><affiliation wicri:level="1"><nlm:affiliation>School of Life Sciences, Chongqing University, Chongqing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>School of Life Sciences, Chongqing University, Chongqing</wicri:regionArea><wicri:noRegion>Chongqing</wicri:noRegion></affiliation></author><author><name sortKey="Ren, Maozhi" sort="Ren, Maozhi" uniqKey="Ren M" first="Maozhi" last="Ren">Maozhi Ren</name><affiliation wicri:level="1"><nlm:affiliation>School of Life Sciences, Chongqing University, Chongqing, China.</nlm:affiliation><country xml:lang="fr">République 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first="Shumin" last="Zhang">Shumin Zhang</name><affiliation wicri:level="1"><nlm:affiliation>School of Life Sciences, Chongqing University, Chongqing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>School of Life Sciences, Chongqing University, Chongqing</wicri:regionArea><wicri:noRegion>Chongqing</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>School of Basic Medical Sciences, North Sichuan Medical College, Nanchong, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>School of Basic Medical Sciences, North Sichuan Medical College, Nanchong</wicri:regionArea><wicri:noRegion>Nanchong</wicri:noRegion></affiliation></author><author><name sortKey="Liu, Sen" sort="Liu, Sen" uniqKey="Liu S" first="Sen" last="Liu">Sen Liu</name><affiliation wicri:level="1"><nlm:affiliation>College of Agronomy and Biotechnology, Southwest University, Chongqing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Agronomy and Biotechnology, Southwest University, Chongqing</wicri:regionArea><wicri:noRegion>Chongqing</wicri:noRegion></affiliation></author><author><name sortKey="Zhang, Jiankui" sort="Zhang, Jiankui" uniqKey="Zhang J" first="Jiankui" last="Zhang">Jiankui Zhang</name><affiliation wicri:level="1"><nlm:affiliation>College of Agronomy and Biotechnology, Southwest University, Chongqing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Agronomy and Biotechnology, Southwest University, Chongqing</wicri:regionArea><wicri:noRegion>Chongqing</wicri:noRegion></affiliation></author><author><name sortKey="Reiter, Russel J" sort="Reiter, Russel J" uniqKey="Reiter R" first="Russel J" last="Reiter">Russel J. Reiter</name><affiliation wicri:level="2"><nlm:affiliation>Department of Cellular and Structure Biology, UT Health, San Antonio, TX, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Cellular and Structure Biology, UT Health, San Antonio, TX</wicri:regionArea><placeName><region type="state">Texas</region></placeName></affiliation></author><author><name sortKey="Wang, Ying" sort="Wang, Ying" uniqKey="Wang Y" first="Ying" last="Wang">Ying Wang</name><affiliation wicri:level="1"><nlm:affiliation>School of Life Sciences, Chongqing University, Chongqing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>School of Life Sciences, Chongqing University, Chongqing</wicri:regionArea><wicri:noRegion>Chongqing</wicri:noRegion></affiliation></author><author><name sortKey="Qiu, Dan" sort="Qiu, Dan" uniqKey="Qiu D" first="Dan" last="Qiu">Dan Qiu</name><affiliation wicri:level="1"><nlm:affiliation>School of Life Sciences, Chongqing University, Chongqing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>School of Life Sciences, Chongqing University, Chongqing</wicri:regionArea><wicri:noRegion>Chongqing</wicri:noRegion></affiliation></author><author><name sortKey="Luo, Xiumei" sort="Luo, Xiumei" uniqKey="Luo X" first="Xiumei" last="Luo">Xiumei Luo</name><affiliation wicri:level="1"><nlm:affiliation>School of Life Sciences, Chongqing University, Chongqing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>School of Life Sciences, Chongqing University, Chongqing</wicri:regionArea><wicri:noRegion>Chongqing</wicri:noRegion></affiliation></author><author><name sortKey="Khalid, A Rehman" sort="Khalid, A Rehman" uniqKey="Khalid A" first="A Rehman" last="Khalid">A Rehman Khalid</name><affiliation wicri:level="1"><nlm:affiliation>School of Life Sciences, Chongqing University, Chongqing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>School of Life Sciences, Chongqing University, Chongqing</wicri:regionArea><wicri:noRegion>Chongqing</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Hanyan" sort="Wang, Hanyan" uniqKey="Wang H" first="Hanyan" last="Wang">Hanyan Wang</name><affiliation wicri:level="1"><nlm:affiliation>School of Basic Medical Sciences, North Sichuan Medical College, Nanchong, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>School of Basic Medical Sciences, North Sichuan Medical College, Nanchong</wicri:regionArea><wicri:noRegion>Nanchong</wicri:noRegion></affiliation></author><author><name sortKey="Feng, Li" sort="Feng, Li" uniqKey="Feng L" first="Li" last="Feng">Li Feng</name><affiliation wicri:level="1"><nlm:affiliation>School of Life Sciences, Chongqing University, Chongqing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>School of Life Sciences, Chongqing University, Chongqing</wicri:regionArea><wicri:noRegion>Chongqing</wicri:noRegion></affiliation></author><author><name sortKey="Lin, Zhenghong" sort="Lin, Zhenghong" uniqKey="Lin Z" first="Zhenghong" last="Lin">Zhenghong Lin</name><affiliation wicri:level="1"><nlm:affiliation>School of Life Sciences, Chongqing University, Chongqing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>School of Life Sciences, Chongqing University, Chongqing</wicri:regionArea><wicri:noRegion>Chongqing</wicri:noRegion></affiliation></author><author><name sortKey="Ren, Maozhi" sort="Ren, Maozhi" uniqKey="Ren M" first="Maozhi" last="Ren">Maozhi Ren</name><affiliation wicri:level="1"><nlm:affiliation>School of Life Sciences, Chongqing University, Chongqing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>School of Life Sciences, Chongqing University, Chongqing</wicri:regionArea><wicri:noRegion>Chongqing</wicri:noRegion></affiliation></author></analytic><series><title level="j">Journal of pineal research</title><idno type="eISSN">1600-079X</idno><imprint><date when="2018" type="published">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Drug Resistance (drug effects)</term><term>Fungicides, Industrial (pharmacology)</term><term>Melatonin (pharmacology)</term><term>Phytophthora (genetics)</term><term>Phytophthora (growth & development)</term><term>Plant Diseases (microbiology)</term><term>Sulfinic Acids (pharmacology)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Acides sulfiniques (pharmacologie)</term><term>Fongicides industriels (pharmacologie)</term><term>Maladies des plantes (microbiologie)</term><term>Mélatonine (pharmacologie)</term><term>Phytophthora (croissance et développement)</term><term>Phytophthora (génétique)</term><term>Résistance aux substances (effets des médicaments et des substances chimiques)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en"><term>Fungicides, Industrial</term><term>Melatonin</term><term>Sulfinic Acids</term></keywords><keywords scheme="MESH" qualifier="croissance et développement" xml:lang="fr"><term>Phytophthora</term></keywords><keywords scheme="MESH" qualifier="drug effects" xml:lang="en"><term>Drug Resistance</term></keywords><keywords scheme="MESH" qualifier="effets des médicaments et des substances chimiques" xml:lang="fr"><term>Résistance aux substances</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Phytophthora</term></keywords><keywords scheme="MESH" qualifier="growth & development" xml:lang="en"><term>Phytophthora</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Phytophthora</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="pharmacologie" xml:lang="fr"><term>Acides sulfiniques</term><term>Fongicides industriels</term><term>Mélatonine</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Human health, food safety, and agriculture have been threatened by oomycetic diseases caused by notorious pathogenic oomycetes. Chemical oomyceticides are the main approaches in control of pathogenic oomycetes. However, the overused chemical oomyceticides have resulted in serious environmental pollution and drug resistance. The eco-friendly bio-oomyceticides are required for sustainable development through screening synergistic drug combinations. In this study, Phytophthora nicotianae (P. nicotianae), as one of the most destructive oomycetic diseases in agriculture, was used as a model system to screen the novel bio-oomyceticides based on drug combination. The results showed that treatment of melatonin or ethylicin (IUPAC Name: 1-ethylsulfonylsulfanylethane) alone displayed similar phenotypes such as the inhibition of the hyphal growth, reduction of the cell viability, and suppression of the virulence of P. nicotianae. Importantly, melatonin and ethylicin shared the same targets of interfering with the amino acid metabolism, overexpressing apoptosis-inducing factor, and dysregulating the virulence-related genes. Furthermore, strong synergism against P. nicotianae was induced by combining melatonin with ethylicin. Under treatment of the combination of melatonin and ethylicin, the expression of genes associated with amino acid, the apoptosis-inducing factor, and the virulence-related genes was much more significantly dysregulated than that of single drug treatment. Thus, the tobacco black shank caused by P. nicotianae can be successfully controlled using the combination of melatonin and ethylicin. These observations suggest that the synergistic effect based on the combination of melatonin and ethylicin is an eco-friendly alternative for the control of the destructive oomycetic diseases.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">29575191</PMID><DateCompleted><Year>2018</Year><Month>11</Month><Day>14</Day></DateCompleted><DateRevised><Year>2018</Year><Month>11</Month><Day>14</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1600-079X</ISSN><JournalIssue CitedMedium="Internet"><Volume>65</Volume><Issue>2</Issue><PubDate><Year>2018</Year><Month>Sep</Month></PubDate></JournalIssue><Title>Journal of pineal research</Title><ISOAbbreviation>J Pineal Res</ISOAbbreviation></Journal><ArticleTitle>Synergistic anti-oomycete effect of melatonin with a biofungicide against oomycetic black shank disease.</ArticleTitle><Pagination><MedlinePgn>e12492</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1111/jpi.12492</ELocationID><Abstract><AbstractText>Human health, food safety, and agriculture have been threatened by oomycetic diseases caused by notorious pathogenic oomycetes. Chemical oomyceticides are the main approaches in control of pathogenic oomycetes. However, the overused chemical oomyceticides have resulted in serious environmental pollution and drug resistance. The eco-friendly bio-oomyceticides are required for sustainable development through screening synergistic drug combinations. In this study, Phytophthora nicotianae (P. nicotianae), as one of the most destructive oomycetic diseases in agriculture, was used as a model system to screen the novel bio-oomyceticides based on drug combination. The results showed that treatment of melatonin or ethylicin (IUPAC Name: 1-ethylsulfonylsulfanylethane) alone displayed similar phenotypes such as the inhibition of the hyphal growth, reduction of the cell viability, and suppression of the virulence of P. nicotianae. Importantly, melatonin and ethylicin shared the same targets of interfering with the amino acid metabolism, overexpressing apoptosis-inducing factor, and dysregulating the virulence-related genes. Furthermore, strong synergism against P. nicotianae was induced by combining melatonin with ethylicin. Under treatment of the combination of melatonin and ethylicin, the expression of genes associated with amino acid, the apoptosis-inducing factor, and the virulence-related genes was much more significantly dysregulated than that of single drug treatment. Thus, the tobacco black shank caused by P. nicotianae can be successfully controlled using the combination of melatonin and ethylicin. These observations suggest that the synergistic effect based on the combination of melatonin and ethylicin is an eco-friendly alternative for the control of the destructive oomycetic diseases.</AbstractText><CopyrightInformation>© 2018 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Shumin</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>School of Life Sciences, Chongqing University, Chongqing, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>School of Basic Medical Sciences, North Sichuan Medical College, Nanchong, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Sen</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>College of Agronomy and Biotechnology, Southwest University, Chongqing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Jiankui</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>College of Agronomy and Biotechnology, Southwest University, Chongqing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Reiter</LastName><ForeName>Russel J</ForeName><Initials>RJ</Initials><AffiliationInfo><Affiliation>Department of Cellular and Structure Biology, UT Health, San Antonio, TX, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Ying</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>School of Life Sciences, Chongqing University, Chongqing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Qiu</LastName><ForeName>Dan</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>School of Life Sciences, Chongqing University, Chongqing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Luo</LastName><ForeName>Xiumei</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>School of Life Sciences, Chongqing University, Chongqing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Khalid</LastName><ForeName>A Rehman</ForeName><Initials>AR</Initials><AffiliationInfo><Affiliation>School of Life Sciences, Chongqing University, Chongqing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Hanyan</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>School of Basic Medical Sciences, North Sichuan Medical College, Nanchong, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Feng</LastName><ForeName>Li</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>School of Life Sciences, Chongqing University, Chongqing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lin</LastName><ForeName>Zhenghong</ForeName><Initials>Z</Initials><AffiliationInfo><Affiliation>School of Life Sciences, Chongqing University, Chongqing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ren</LastName><ForeName>Maozhi</ForeName><Initials>M</Initials><Identifier Source="ORCID">http://orcid.org/0000-0002-2379-5315</Identifier><AffiliationInfo><Affiliation>School of Life Sciences, Chongqing University, Chongqing, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2018</Year><Month>04</Month><Day>06</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>J Pineal Res</MedlineTA><NlmUniqueID>8504412</NlmUniqueID><ISSNLinking>0742-3098</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D005659">Fungicides, Industrial</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D013441">Sulfinic Acids</NameOfSubstance></Chemical><Chemical><RegistryNumber>682-91-7</RegistryNumber><NameOfSubstance UI="C578025">ethylicin</NameOfSubstance></Chemical><Chemical><RegistryNumber>JL5DK93RCL</RegistryNumber><NameOfSubstance UI="D008550">Melatonin</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D004351" MajorTopicYN="N">Drug Resistance</DescriptorName><QualifierName UI="Q000187" MajorTopicYN="Y">drug effects</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D005659" MajorTopicYN="N">Fungicides, Industrial</DescriptorName><QualifierName UI="Q000494" MajorTopicYN="Y">pharmacology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D008550" MajorTopicYN="N">Melatonin</DescriptorName><QualifierName UI="Q000494" MajorTopicYN="Y">pharmacology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D010838" MajorTopicYN="N">Phytophthora</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000254" MajorTopicYN="Y">growth & development</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D010935" MajorTopicYN="N">Plant Diseases</DescriptorName><QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D013441" MajorTopicYN="N">Sulfinic Acids</DescriptorName><QualifierName UI="Q000494" MajorTopicYN="Y">pharmacology</QualifierName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">biofungicide</Keyword><Keyword MajorTopicYN="N">drug combination</Keyword><Keyword MajorTopicYN="N">melatonin</Keyword><Keyword MajorTopicYN="N">pathogenic oomycetes</Keyword><Keyword MajorTopicYN="N">synergistic inhibition</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2018</Year><Month>02</Month><Day>10</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2018</Year><Month>03</Month><Day>09</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2018</Year><Month>3</Month><Day>27</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2018</Year><Month>11</Month><Day>15</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2018</Year><Month>3</Month><Day>26</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">29575191</ArticleId><ArticleId IdType="doi">10.1111/jpi.12492</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>République populaire de Chine</li><li>États-Unis</li></country><region><li>Texas</li></region></list><tree><country name="République populaire de Chine"><noRegion><name sortKey="Zhang, Shumin" sort="Zhang, Shumin" uniqKey="Zhang S" first="Shumin" last="Zhang">Shumin Zhang</name></noRegion><name sortKey="Feng, Li" sort="Feng, Li" uniqKey="Feng L" first="Li" last="Feng">Li Feng</name><name sortKey="Khalid, A Rehman" sort="Khalid, A Rehman" uniqKey="Khalid A" first="A Rehman" last="Khalid">A Rehman Khalid</name><name sortKey="Lin, Zhenghong" sort="Lin, Zhenghong" uniqKey="Lin Z" first="Zhenghong" last="Lin">Zhenghong Lin</name><name sortKey="Liu, Sen" sort="Liu, Sen" uniqKey="Liu S" first="Sen" last="Liu">Sen Liu</name><name sortKey="Luo, Xiumei" sort="Luo, Xiumei" uniqKey="Luo X" first="Xiumei" last="Luo">Xiumei Luo</name><name sortKey="Qiu, Dan" sort="Qiu, Dan" uniqKey="Qiu D" first="Dan" last="Qiu">Dan Qiu</name><name sortKey="Ren, Maozhi" sort="Ren, Maozhi" uniqKey="Ren M" first="Maozhi" last="Ren">Maozhi Ren</name><name sortKey="Wang, Hanyan" sort="Wang, Hanyan" uniqKey="Wang H" first="Hanyan" last="Wang">Hanyan Wang</name><name sortKey="Wang, Ying" sort="Wang, Ying" uniqKey="Wang Y" first="Ying" last="Wang">Ying Wang</name><name sortKey="Zhang, Jiankui" sort="Zhang, Jiankui" uniqKey="Zhang J" first="Jiankui" last="Zhang">Jiankui Zhang</name><name sortKey="Zhang, Shumin" sort="Zhang, Shumin" uniqKey="Zhang S" first="Shumin" last="Zhang">Shumin Zhang</name></country><country name="États-Unis"><region name="Texas"><name sortKey="Reiter, Russel J" sort="Reiter, Russel J" uniqKey="Reiter R" first="Russel J" last="Reiter">Russel J. 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