Exposure to the leaf litter microbiome of healthy adults protects seedlings from pathogen damage.
Identifieur interne : 000140 ( Main/Exploration ); précédent : 000139; suivant : 000141Exposure to the leaf litter microbiome of healthy adults protects seedlings from pathogen damage.
Auteurs : Natalie Christian [États-Unis] ; Edward Allen Herre [États-Unis] ; Luis C. Mejia [États-Unis] ; Keith Clay [États-Unis]Source :
- Proceedings. Biological sciences [ 1471-2954 ] ; 2017.
Descripteurs français
- KwdFr :
- MESH :
- microbiologie : Cacaoyer, Feuilles de plante, Plant.
- Champignons, Microbiote.
English descriptors
- KwdEn :
- MESH :
- microbiology : Cacao, Plant Leaves, Seedlings.
- Fungi, Microbiota.
Abstract
It is increasingly recognized that microbiota affect host health and physiology. However, it is unclear what factors shape microbiome community assembly in nature, and how microbiome assembly can be manipulated to improve host health. All plant leaves host foliar endophytic fungi, which make up a diverse, environmentally acquired fungal microbiota. Here, we experimentally manipulated assembly of the cacao tree (Theobroma cacao) fungal microbiome in nature and tested the effect of assembly outcome on host health. Using next-generation sequencing, as well as culture-based methods coupled with Sanger sequencing, we found that manipulating leaf litter exposure and location within the forest canopy significantly altered microbiome composition in cacao. Exposing cacao seedlings to leaf litter from healthy conspecific adults enriched the seedling microbiome with Colletotrichum tropicale, a fungal endophyte known to enhance pathogen resistance of cacao seedlings by upregulating host defensive pathways. As a result, seedlings exposed to healthy conspecific litter experienced reduced pathogen damage. Our results link processes that affect the assembly and composition of microbiome communities to their functional consequences for host success, and have broad implications for understanding plant-microbe interactions. Deliberate manipulation of the plant-fungal microbiome also has potentially important applications for cacao production and other agricultural systems in general.
DOI: 10.1098/rspb.2017.0641
PubMed: 28679727
PubMed Central: PMC5524495
Affiliations:
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Mejia</name><affiliation wicri:level="1"><nlm:affiliation>Smithsonian Tropical Research Institute, Unit 9100 Box 0948, DPO AA 34002-9998, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Smithsonian Tropical Research Institute, Unit 9100 Box 0948, DPO AA 34002-9998</wicri:regionArea><wicri:noRegion>DPO AA 34002-9998</wicri:noRegion></affiliation><affiliation><nlm:affiliation>Institute for Scientific Research and High Technology Services (INDICASAT), Building 219, City of Knowledge, Clayton, Panama, Republic of Panama.</nlm:affiliation><wicri:noCountry code="subField">Republic of Panama</wicri:noCountry></affiliation></author><author><name sortKey="Clay, Keith" sort="Clay, Keith" uniqKey="Clay K" first="Keith" last="Clay">Keith Clay</name><affiliation wicri:level="2"><nlm:affiliation>Evolution, Ecology and Behavior Program, Department of Biology, Indiana University, 1001 East 3rd Street, Bloomington, IN 47405, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Evolution, Ecology and Behavior Program, Department of Biology, Indiana University, 1001 East 3rd Street, Bloomington, IN 47405</wicri:regionArea><placeName><region type="state">Indiana</region></placeName></affiliation></author></analytic><series><title level="j">Proceedings. Biological sciences</title><idno type="eISSN">1471-2954</idno><imprint><date when="2017" type="published">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Cacao (microbiology)</term><term>Fungi (MeSH)</term><term>Microbiota (MeSH)</term><term>Plant Leaves (microbiology)</term><term>Seedlings (microbiology)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Cacaoyer (microbiologie)</term><term>Champignons (MeSH)</term><term>Feuilles de plante (microbiologie)</term><term>Microbiote (MeSH)</term><term>Plant (microbiologie)</term></keywords><keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr"><term>Cacaoyer</term><term>Feuilles de plante</term><term>Plant</term></keywords><keywords scheme="MESH" qualifier="microbiology" xml:lang="en"><term>Cacao</term><term>Plant Leaves</term><term>Seedlings</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Fungi</term><term>Microbiota</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Champignons</term><term>Microbiote</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">It is increasingly recognized that microbiota affect host health and physiology. However, it is unclear what factors shape microbiome community assembly in nature, and how microbiome assembly can be manipulated to improve host health. All plant leaves host foliar endophytic fungi, which make up a diverse, environmentally acquired fungal microbiota. Here, we experimentally manipulated assembly of the cacao tree (<i>Theobroma cacao</i>) fungal microbiome in nature and tested the effect of assembly outcome on host health. Using next-generation sequencing, as well as culture-based methods coupled with Sanger sequencing, we found that manipulating leaf litter exposure and location within the forest canopy significantly altered microbiome composition in cacao. Exposing cacao seedlings to leaf litter from healthy conspecific adults enriched the seedling microbiome with <i>Colletotrichum tropicale</i>, a fungal endophyte known to enhance pathogen resistance of cacao seedlings by upregulating host defensive pathways. As a result, seedlings exposed to healthy conspecific litter experienced reduced pathogen damage. Our results link processes that affect the assembly and composition of microbiome communities to their functional consequences for host success, and have broad implications for understanding plant-microbe interactions. Deliberate manipulation of the plant-fungal microbiome also has potentially important applications for cacao production and other agricultural systems in general.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" IndexingMethod="Curated" Owner="NLM"><PMID Version="1">28679727</PMID><DateCompleted><Year>2018</Year><Month>02</Month><Day>01</Day></DateCompleted><DateRevised><Year>2019</Year><Month>01</Month><Day>30</Day></DateRevised><Article PubModel="Print"><Journal><ISSN IssnType="Electronic">1471-2954</ISSN><JournalIssue CitedMedium="Internet"><Volume>284</Volume><Issue>1858</Issue><PubDate><Year>2017</Year><Month>Jul</Month><Day>12</Day></PubDate></JournalIssue><Title>Proceedings. Biological sciences</Title><ISOAbbreviation>Proc Biol Sci</ISOAbbreviation></Journal><ArticleTitle>Exposure to the leaf litter microbiome of healthy adults protects seedlings from pathogen damage.</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">20170641</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1098/rspb.2017.0641</ELocationID><Abstract><AbstractText>It is increasingly recognized that microbiota affect host health and physiology. However, it is unclear what factors shape microbiome community assembly in nature, and how microbiome assembly can be manipulated to improve host health. All plant leaves host foliar endophytic fungi, which make up a diverse, environmentally acquired fungal microbiota. Here, we experimentally manipulated assembly of the cacao tree (<i>Theobroma cacao</i>) fungal microbiome in nature and tested the effect of assembly outcome on host health. Using next-generation sequencing, as well as culture-based methods coupled with Sanger sequencing, we found that manipulating leaf litter exposure and location within the forest canopy significantly altered microbiome composition in cacao. Exposing cacao seedlings to leaf litter from healthy conspecific adults enriched the seedling microbiome with <i>Colletotrichum tropicale</i>, a fungal endophyte known to enhance pathogen resistance of cacao seedlings by upregulating host defensive pathways. As a result, seedlings exposed to healthy conspecific litter experienced reduced pathogen damage. Our results link processes that affect the assembly and composition of microbiome communities to their functional consequences for host success, and have broad implications for understanding plant-microbe interactions. Deliberate manipulation of the plant-fungal microbiome also has potentially important applications for cacao production and other agricultural systems in general.</AbstractText><CopyrightInformation>© 2017 The Author(s).</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Christian</LastName><ForeName>Natalie</ForeName><Initials>N</Initials><Identifier Source="ORCID">http://orcid.org/0000-0003-1568-7645</Identifier><AffiliationInfo><Affiliation>Evolution, Ecology and Behavior Program, Department of Biology, Indiana University, 1001 East 3rd Street, Bloomington, IN 47405, USA nschrist@indiana.edu.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Herre</LastName><ForeName>Edward Allen</ForeName><Initials>EA</Initials><AffiliationInfo><Affiliation>Smithsonian Tropical Research Institute, Unit 9100 Box 0948, DPO AA 34002-9998, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mejia</LastName><ForeName>Luis C</ForeName><Initials>LC</Initials><AffiliationInfo><Affiliation>Smithsonian Tropical Research Institute, Unit 9100 Box 0948, DPO AA 34002-9998, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Institute for Scientific Research and High Technology Services (INDICASAT), Building 219, City of Knowledge, Clayton, Panama, Republic of Panama.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Clay</LastName><ForeName>Keith</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>Evolution, Ecology and Behavior Program, Department of Biology, Indiana University, 1001 East 3rd Street, Bloomington, IN 47405, USA.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Proc Biol 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MajorTopicYN="N">Theobroma cacao</Keyword><Keyword MajorTopicYN="N">community assembly</Keyword><Keyword MajorTopicYN="N">foliar endophytic fungi</Keyword><Keyword MajorTopicYN="N">vertical stratification</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2017</Year><Month>03</Month><Day>26</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2017</Year><Month>05</Month><Day>30</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2017</Year><Month>7</Month><Day>7</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2017</Year><Month>7</Month><Day>7</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2018</Year><Month>2</Month><Day>2</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">28679727</ArticleId><ArticleId 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last="Christian">Natalie Christian</name></region><name sortKey="Clay, Keith" sort="Clay, Keith" uniqKey="Clay K" first="Keith" last="Clay">Keith Clay</name><name sortKey="Herre, Edward Allen" sort="Herre, Edward Allen" uniqKey="Herre E" first="Edward Allen" last="Herre">Edward Allen Herre</name><name sortKey="Mejia, Luis C" sort="Mejia, Luis C" uniqKey="Mejia L" first="Luis C" last="Mejia">Luis C. 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