Biocontrol Potential of a Novel Endophytic Bacterium From Mulberry (Morus) Tree.
Identifieur interne : 000083 ( Main/Exploration ); précédent : 000082; suivant : 000084Biocontrol Potential of a Novel Endophytic Bacterium From Mulberry (Morus) Tree.
Auteurs : Sen Xie [République populaire de Chine] ; Marine Vallet [Allemagne] ; Chao Sun [République populaire de Chine] ; Maritta Kunert [Allemagne] ; Anja David [Allemagne] ; Xiancui Zhang [République populaire de Chine] ; Bosheng Chen [République populaire de Chine] ; Xingmeng Lu [République populaire de Chine] ; Wilhelm Boland [Allemagne] ; Yongqi Shao [République populaire de Chine]Source :
- Frontiers in bioengineering and biotechnology [ 2296-4185 ] ; 2019.
Abstract
Mulberry (Morus) is an economically important woody tree that is suitable for use in sericulture as forage and in medicine. However, this broad-leaved tree is facing multiple threats ranging from phytopathogens to insect pests. Here, a Gram-positive, endospore-forming bacterium (ZJU1) was frequently isolated from healthy mulberry plants by screening for foliar endophytes showing antagonism against pathogens and pests. Whole-genome sequencing and annotation resulted in a genome size of 4.06 Mb and classified the bacterium as a novel strain of Bacillus amyloliquefaciens that has rarely been identified from tree leaves. An integrative approach combining traditional natural product chemistry, activity bioassays, and high-resolution mass spectrometry confirmed that strain ZJU1 uses a blend of antimicrobials including peptides and volatile organic compounds to oppose Botrytis cinerea, a major phytopathogenic fungus causing mulberry gray mold disease. We showed that the inoculation of endophyte-free plants with ZJU1 significantly decreased both leaf necrosis and mortality under field conditions. In addition to the direct interactions of endophytes with foliar pathogens, in planta studies suggested that the inoculation of endophytes also induced plant systemic defense, including high expression levels of mulberry disease resistance genes. Moreover, when applied to the generalist herbivore Spodoptera litura, ZJU1 was sufficient to reduce the pest survival rate below 50%. A previously undiscovered crystal toxin (Cry10Aa) could contribute to this insecticidal effect against notorious lepidopteran pests. These unique traits clearly demonstrate that B. amyloliquefaciens ZJU1 is promising for the development of successful strategies for biocontrol applications. The search for new plant-beneficial microbes and engineering microbiomes is therefore of great significance for sustainably improving plant performance.
DOI: 10.3389/fbioe.2019.00488
PubMed: 32039187
PubMed Central: PMC6990687
Affiliations:
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Endophytic Bacterium From Mulberry (<i>Morus</i>) Tree.</title><author><name sortKey="Xie, Sen" sort="Xie, Sen" uniqKey="Xie S" first="Sen" last="Xie">Sen Xie</name><affiliation wicri:level="4"><nlm:affiliation>Institute of Sericulture and Apiculture, College of Animal Sciences, Zhejiang University, Hangzhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Institute of Sericulture and Apiculture, College of Animal Sciences, Zhejiang University, Hangzhou</wicri:regionArea><placeName><settlement type="city">Hangzhou</settlement><region type="province">Zhejiang</region></placeName><orgName type="university">Université de Zhejiang</orgName></affiliation></author><author><name sortKey="Vallet, Marine" sort="Vallet, Marine" uniqKey="Vallet M" first="Marine" last="Vallet">Marine Vallet</name><affiliation wicri:level="1"><nlm:affiliation>Max Planck Fellow Group on Plankton Community Interaction, Max Planck Institute for Chemical Ecology, Jena, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Max Planck Fellow Group on Plankton Community Interaction, Max Planck Institute for Chemical Ecology, Jena</wicri:regionArea><wicri:noRegion>Jena</wicri:noRegion><wicri:noRegion>Jena</wicri:noRegion><wicri:noRegion>Jena</wicri:noRegion></affiliation></author><author><name sortKey="Sun, Chao" sort="Sun, Chao" uniqKey="Sun C" first="Chao" last="Sun">Chao Sun</name><affiliation wicri:level="4"><nlm:affiliation>Analysis Center of Agrobiology and Environmental Sciences, Zhejiang University, Hangzhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Analysis Center of Agrobiology and Environmental Sciences, Zhejiang University, Hangzhou</wicri:regionArea><placeName><settlement type="city">Hangzhou</settlement><region type="province">Zhejiang</region></placeName><orgName type="university">Université de Zhejiang</orgName></affiliation></author><author><name sortKey="Kunert, Maritta" sort="Kunert, Maritta" uniqKey="Kunert M" first="Maritta" last="Kunert">Maritta Kunert</name><affiliation wicri:level="1"><nlm:affiliation>Department of Natural Product Biosynthesis, Max Planck Institute for Chemical Ecology, Jena, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Natural Product Biosynthesis, Max Planck Institute for Chemical Ecology, Jena</wicri:regionArea><wicri:noRegion>Jena</wicri:noRegion><wicri:noRegion>Jena</wicri:noRegion><wicri:noRegion>Jena</wicri:noRegion></affiliation></author><author><name sortKey="David, Anja" sort="David, Anja" uniqKey="David A" first="Anja" last="David">Anja David</name><affiliation wicri:level="1"><nlm:affiliation>Department of Natural Product Biosynthesis, Max Planck Institute for Chemical Ecology, Jena, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Natural Product Biosynthesis, Max Planck Institute for Chemical Ecology, Jena</wicri:regionArea><wicri:noRegion>Jena</wicri:noRegion><wicri:noRegion>Jena</wicri:noRegion><wicri:noRegion>Jena</wicri:noRegion></affiliation></author><author><name sortKey="Zhang, Xiancui" sort="Zhang, Xiancui" uniqKey="Zhang X" first="Xiancui" last="Zhang">Xiancui Zhang</name><affiliation wicri:level="4"><nlm:affiliation>Institute of Sericulture and Apiculture, College of Animal Sciences, Zhejiang University, Hangzhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Institute of Sericulture and Apiculture, College of Animal Sciences, Zhejiang University, Hangzhou</wicri:regionArea><placeName><settlement type="city">Hangzhou</settlement><region type="province">Zhejiang</region></placeName><orgName type="university">Université de Zhejiang</orgName></affiliation></author><author><name sortKey="Chen, Bosheng" sort="Chen, Bosheng" uniqKey="Chen B" first="Bosheng" last="Chen">Bosheng Chen</name><affiliation wicri:level="4"><nlm:affiliation>Institute of Sericulture and Apiculture, College of Animal Sciences, Zhejiang University, Hangzhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Institute of Sericulture and Apiculture, College of Animal Sciences, Zhejiang University, Hangzhou</wicri:regionArea><placeName><settlement type="city">Hangzhou</settlement><region type="province">Zhejiang</region></placeName><orgName type="university">Université de Zhejiang</orgName></affiliation></author><author><name sortKey="Lu, Xingmeng" sort="Lu, Xingmeng" uniqKey="Lu X" first="Xingmeng" last="Lu">Xingmeng Lu</name><affiliation wicri:level="4"><nlm:affiliation>Institute of Sericulture and Apiculture, College of Animal Sciences, Zhejiang University, Hangzhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Institute of Sericulture and Apiculture, College of Animal Sciences, Zhejiang University, Hangzhou</wicri:regionArea><placeName><settlement type="city">Hangzhou</settlement><region type="province">Zhejiang</region></placeName><orgName type="university">Université de Zhejiang</orgName></affiliation></author><author><name sortKey="Boland, Wilhelm" sort="Boland, Wilhelm" uniqKey="Boland W" first="Wilhelm" last="Boland">Wilhelm Boland</name><affiliation wicri:level="1"><nlm:affiliation>Department of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology, Jena, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology, Jena</wicri:regionArea><wicri:noRegion>Jena</wicri:noRegion><wicri:noRegion>Jena</wicri:noRegion><wicri:noRegion>Jena</wicri:noRegion></affiliation></author><author><name sortKey="Shao, Yongqi" sort="Shao, Yongqi" uniqKey="Shao Y" first="Yongqi" last="Shao">Yongqi Shao</name><affiliation wicri:level="4"><nlm:affiliation>Institute of Sericulture and Apiculture, College of Animal Sciences, Zhejiang University, Hangzhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Institute of Sericulture and Apiculture, College of Animal Sciences, Zhejiang University, Hangzhou</wicri:regionArea><placeName><settlement type="city">Hangzhou</settlement><region type="province">Zhejiang</region></placeName><orgName type="university">Université de Zhejiang</orgName></affiliation><affiliation wicri:level="3"><nlm:affiliation>Key Laboratory for Molecular Animal Nutrition, Ministry of Education, Hangzhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory for Molecular Animal Nutrition, Ministry of Education, Hangzhou</wicri:regionArea><placeName><settlement type="city">Hangzhou</settlement><region type="province">Zhejiang</region></placeName></affiliation></author></analytic><series><title level="j">Frontiers in bioengineering and biotechnology</title><idno type="ISSN">2296-4185</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Mulberry (<i>Morus</i>) is an economically important woody tree that is suitable for use in sericulture as forage and in medicine. However, this broad-leaved tree is facing multiple threats ranging from phytopathogens to insect pests. Here, a Gram-positive, endospore-forming bacterium (ZJU1) was frequently isolated from healthy mulberry plants by screening for foliar endophytes showing antagonism against pathogens and pests. Whole-genome sequencing and annotation resulted in a genome size of 4.06 Mb and classified the bacterium as a novel strain of <i>Bacillus amyloliquefaciens</i> that has rarely been identified from tree leaves. An integrative approach combining traditional natural product chemistry, activity bioassays, and high-resolution mass spectrometry confirmed that strain ZJU1 uses a blend of antimicrobials including peptides and volatile organic compounds to oppose <i>Botrytis cinerea</i>, a major phytopathogenic fungus causing mulberry gray mold disease. We showed that the inoculation of endophyte-free plants with ZJU1 significantly decreased both leaf necrosis and mortality under field conditions. In addition to the direct interactions of endophytes with foliar pathogens, <i>in planta</i> studies suggested that the inoculation of endophytes also induced plant systemic defense, including high expression levels of mulberry disease resistance genes. Moreover, when applied to the generalist herbivore <i>Spodoptera litura</i>, ZJU1 was sufficient to reduce the pest survival rate below 50%. A previously undiscovered crystal toxin (Cry10Aa) could contribute to this insecticidal effect against notorious lepidopteran pests. These unique traits clearly demonstrate that <i>B. amyloliquefaciens</i> ZJU1 is promising for the development of successful strategies for biocontrol applications. The search for new plant-beneficial microbes and engineering microbiomes is therefore of great significance for sustainably improving plant performance.</div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">32039187</PMID><DateRevised><Year>2020</Year><Month>09</Month><Day>28</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">2296-4185</ISSN><JournalIssue CitedMedium="Print"><Volume>7</Volume><PubDate><Year>2019</Year></PubDate></JournalIssue><Title>Frontiers in bioengineering and biotechnology</Title><ISOAbbreviation>Front Bioeng Biotechnol</ISOAbbreviation></Journal><ArticleTitle>Biocontrol Potential of a Novel Endophytic Bacterium From Mulberry (<i>Morus</i>) Tree.</ArticleTitle><Pagination><MedlinePgn>488</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.3389/fbioe.2019.00488</ELocationID><Abstract><AbstractText>Mulberry (<i>Morus</i>) is an economically important woody tree that is suitable for use in sericulture as forage and in medicine. However, this broad-leaved tree is facing multiple threats ranging from phytopathogens to insect pests. Here, a Gram-positive, endospore-forming bacterium (ZJU1) was frequently isolated from healthy mulberry plants by screening for foliar endophytes showing antagonism against pathogens and pests. Whole-genome sequencing and annotation resulted in a genome size of 4.06 Mb and classified the bacterium as a novel strain of <i>Bacillus amyloliquefaciens</i> that has rarely been identified from tree leaves. An integrative approach combining traditional natural product chemistry, activity bioassays, and high-resolution mass spectrometry confirmed that strain ZJU1 uses a blend of antimicrobials including peptides and volatile organic compounds to oppose <i>Botrytis cinerea</i>, a major phytopathogenic fungus causing mulberry gray mold disease. We showed that the inoculation of endophyte-free plants with ZJU1 significantly decreased both leaf necrosis and mortality under field conditions. In addition to the direct interactions of endophytes with foliar pathogens, <i>in planta</i> studies suggested that the inoculation of endophytes also induced plant systemic defense, including high expression levels of mulberry disease resistance genes. Moreover, when applied to the generalist herbivore <i>Spodoptera litura</i>, ZJU1 was sufficient to reduce the pest survival rate below 50%. A previously undiscovered crystal toxin (Cry10Aa) could contribute to this insecticidal effect against notorious lepidopteran pests. These unique traits clearly demonstrate that <i>B. amyloliquefaciens</i> ZJU1 is promising for the development of successful strategies for biocontrol applications. The search for new plant-beneficial microbes and engineering microbiomes is therefore of great significance for sustainably improving plant performance.</AbstractText><CopyrightInformation>Copyright © 2020 Xie, Vallet, Sun, Kunert, David, Zhang, Chen, Lu, Boland and Shao.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Xie</LastName><ForeName>Sen</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Institute of Sericulture and Apiculture, College of Animal Sciences, Zhejiang University, Hangzhou, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Vallet</LastName><ForeName>Marine</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Max Planck Fellow Group on Plankton Community Interaction, Max Planck Institute for Chemical Ecology, Jena, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sun</LastName><ForeName>Chao</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Analysis Center of Agrobiology and Environmental Sciences, Zhejiang University, Hangzhou, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kunert</LastName><ForeName>Maritta</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Department of Natural Product Biosynthesis, Max Planck Institute for Chemical Ecology, Jena, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>David</LastName><ForeName>Anja</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Natural Product Biosynthesis, Max Planck Institute for Chemical Ecology, Jena, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Xiancui</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Institute of Sericulture and Apiculture, College of Animal Sciences, Zhejiang University, Hangzhou, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Chen</LastName><ForeName>Bosheng</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>Institute of Sericulture and Apiculture, College of Animal Sciences, Zhejiang University, Hangzhou, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lu</LastName><ForeName>Xingmeng</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Institute of Sericulture and Apiculture, College of Animal Sciences, Zhejiang University, Hangzhou, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Boland</LastName><ForeName>Wilhelm</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>Department of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology, Jena, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Shao</LastName><ForeName>Yongqi</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Institute of Sericulture and Apiculture, College of Animal Sciences, Zhejiang University, Hangzhou, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Key Laboratory for Molecular Animal Nutrition, Ministry of Education, Hangzhou, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><DataBankList CompleteYN="Y"><DataBank><DataBankName>Dryad</DataBankName><AccessionNumberList><AccessionNumber>10.5061/dryad.0rxwdbrv4</AccessionNumber></AccessionNumberList></DataBank></DataBankList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>01</Month><Day>23</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Front Bioeng Biotechnol</MedlineTA><NlmUniqueID>101632513</NlmUniqueID><ISSNLinking>2296-4185</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">endophyte</Keyword><Keyword MajorTopicYN="N">fungal pathogen</Keyword><Keyword MajorTopicYN="N">lepidopteran pest</Keyword><Keyword MajorTopicYN="N">mulberry</Keyword><Keyword MajorTopicYN="N">symbiosis</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>09</Month><Day>26</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2019</Year><Month>12</Month><Day>30</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>2</Month><Day>11</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>2</Month><Day>11</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>2</Month><Day>11</Day><Hour>6</Hour><Minute>1</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32039187</ArticleId><ArticleId 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