Pervasive effects of a dominant foliar endophytic fungus on host genetic and phenotypic expression in a tropical tree.
Identifieur interne : 002112 ( Main/Exploration ); précédent : 002111; suivant : 002113Pervasive effects of a dominant foliar endophytic fungus on host genetic and phenotypic expression in a tropical tree.
Auteurs : Luis C. Mejía [États-Unis] ; Edward A. Herre [États-Unis] ; Jed P. Sparks [États-Unis] ; Klaus Winter [États-Unis] ; Milton N. García [États-Unis] ; Sunshine A. Van Bael [États-Unis] ; Joseph Stitt [États-Unis] ; Zi Shi [États-Unis] ; Yufan Zhang [États-Unis] ; Mark J. Guiltinan [États-Unis] ; Siela N. Maximova [États-Unis]Source :
- Frontiers in microbiology [ 1664-302X ] ; 2014.
Abstract
It is increasingly recognized that macro-organisms (corals, insects, plants, vertebrates) consist of both host tissues and multiple microbial symbionts that play essential roles in their host's ecological and evolutionary success. Consequently, identifying benefits and costs of symbioses, as well as mechanisms underlying them are research priorities. All plants surveyed under natural conditions harbor foliar endophytic fungi (FEF) in their leaf tissues, often at high densities. Despite producing no visible effects on their hosts, experiments have nonetheless shown that FEF reduce pathogen and herbivore damage. Here, combining results from three genomic, and two physiological experiments, we demonstrate pervasive genetic and phenotypic effects of the apparently asymptomatic endophytes on their hosts. Specifically, inoculation of endophyte-free (E-) Theobroma cacao leaves with Colletotrichum tropicale (E+), the dominant FEF species in healthy T. cacao, induces consistent changes in the expression of hundreds of host genes, including many with known defensive functions. Further, E+ plants exhibited increased lignin and cellulose content, reduced maximum rates of photosynthesis (Amax), and enrichment of nitrogen-15 and carbon-13 isotopes. These phenotypic changes observed in E+ plants correspond to changes in expression of specific functional genes in related pathways. Moreover, a cacao gene (Tc00g04254) highly up-regulated by C. tropicale also confers resistance to pathogen damage in the absence of endophytes or their products in host tissues. Thus, the benefits of increased pathogen resistance in E+ plants are derived in part from up-regulation of intrinsic host defense responses, and appear to be offset by potential costs including reduced photosynthesis, altered host nitrogen metabolism, and endophyte heterotrophy of host tissues. Similar effects are likely in most plant-endophyte interactions, and should be recognized in the design and interpretation of genetic and phenotypic studies of plants.
DOI: 10.3389/fmicb.2014.00479
PubMed: 25309519
PubMed Central: PMC4162356
Affiliations:
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García</name><affiliation wicri:level="1"><nlm:affiliation>Smithsonian Tropical Research Institute Unit 9100, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Smithsonian Tropical Research Institute Unit 9100</wicri:regionArea></affiliation></author><author><name sortKey="Van Bael, Sunshine A" sort="Van Bael, Sunshine A" uniqKey="Van Bael S" first="Sunshine A" last="Van Bael">Sunshine A. Van Bael</name><affiliation wicri:level="2"><nlm:affiliation>Smithsonian Tropical Research Institute Unit 9100, USA ; Department of Ecology and Evolutionary Biology, Tulane University New Orleans, LA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Smithsonian Tropical Research Institute Unit 9100, USA ; Department of Ecology and Evolutionary Biology, Tulane University New Orleans, LA</wicri:regionArea><placeName><region type="state">Louisiane</region></placeName></affiliation></author><author><name sortKey="Stitt, Joseph" sort="Stitt, Joseph" uniqKey="Stitt J" first="Joseph" last="Stitt">Joseph Stitt</name><affiliation wicri:level="2"><nlm:affiliation>Social, Life and Engineering Sciences Imaging Center, Materials Research Institute University Park, PA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Social, Life and Engineering Sciences Imaging Center, Materials Research Institute University Park, PA</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Shi, Zi" sort="Shi, Zi" uniqKey="Shi Z" first="Zi" last="Shi">Zi Shi</name><affiliation wicri:level="2"><nlm:affiliation>Department of Plant Science and The Huck Institutes of the Life Sciences, The Pennsylvania State University University Park, PA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Plant Science and The Huck Institutes of the Life Sciences, The Pennsylvania State University University Park, PA</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Zhang, Yufan" sort="Zhang, Yufan" uniqKey="Zhang Y" first="Yufan" last="Zhang">Yufan Zhang</name><affiliation wicri:level="2"><nlm:affiliation>Department of Plant Science and The Huck Institutes of the Life Sciences, The Pennsylvania State University University Park, PA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Plant Science and The Huck Institutes of the Life Sciences, The Pennsylvania State University University Park, PA</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Guiltinan, Mark J" sort="Guiltinan, Mark J" uniqKey="Guiltinan M" first="Mark J" last="Guiltinan">Mark J. Guiltinan</name><affiliation wicri:level="2"><nlm:affiliation>Department of Plant Science and The Huck Institutes of the Life Sciences, The Pennsylvania State University University Park, PA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Plant Science and The Huck Institutes of the Life Sciences, The Pennsylvania State University University Park, PA</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Maximova, Siela N" sort="Maximova, Siela N" uniqKey="Maximova S" first="Siela N" last="Maximova">Siela N. Maximova</name><affiliation wicri:level="2"><nlm:affiliation>Department of Plant Science and The Huck Institutes of the Life Sciences, The Pennsylvania State University University Park, PA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Plant Science and The Huck Institutes of the Life Sciences, The Pennsylvania State University University Park, PA</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author></analytic><series><title level="j">Frontiers in microbiology</title><idno type="ISSN">1664-302X</idno><imprint><date when="2014" type="published">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">It is increasingly recognized that macro-organisms (corals, insects, plants, vertebrates) consist of both host tissues and multiple microbial symbionts that play essential roles in their host's ecological and evolutionary success. Consequently, identifying benefits and costs of symbioses, as well as mechanisms underlying them are research priorities. All plants surveyed under natural conditions harbor foliar endophytic fungi (FEF) in their leaf tissues, often at high densities. Despite producing no visible effects on their hosts, experiments have nonetheless shown that FEF reduce pathogen and herbivore damage. Here, combining results from three genomic, and two physiological experiments, we demonstrate pervasive genetic and phenotypic effects of the apparently asymptomatic endophytes on their hosts. Specifically, inoculation of endophyte-free (E-) Theobroma cacao leaves with Colletotrichum tropicale (E+), the dominant FEF species in healthy T. cacao, induces consistent changes in the expression of hundreds of host genes, including many with known defensive functions. Further, E+ plants exhibited increased lignin and cellulose content, reduced maximum rates of photosynthesis (Amax), and enrichment of nitrogen-15 and carbon-13 isotopes. These phenotypic changes observed in E+ plants correspond to changes in expression of specific functional genes in related pathways. Moreover, a cacao gene (Tc00g04254) highly up-regulated by C. tropicale also confers resistance to pathogen damage in the absence of endophytes or their products in host tissues. Thus, the benefits of increased pathogen resistance in E+ plants are derived in part from up-regulation of intrinsic host defense responses, and appear to be offset by potential costs including reduced photosynthesis, altered host nitrogen metabolism, and endophyte heterotrophy of host tissues. Similar effects are likely in most plant-endophyte interactions, and should be recognized in the design and interpretation of genetic and phenotypic studies of plants. </div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">25309519</PMID><DateCompleted><Year>2014</Year><Month>10</Month><Day>13</Day></DateCompleted><DateRevised><Year>2020</Year><Month>09</Month><Day>30</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">1664-302X</ISSN><JournalIssue CitedMedium="Print"><Volume>5</Volume><PubDate><Year>2014</Year></PubDate></JournalIssue><Title>Frontiers in microbiology</Title><ISOAbbreviation>Front Microbiol</ISOAbbreviation></Journal><ArticleTitle>Pervasive effects of a dominant foliar endophytic fungus on host genetic and phenotypic expression in a tropical tree.</ArticleTitle><Pagination><MedlinePgn>479</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.3389/fmicb.2014.00479</ELocationID><Abstract><AbstractText>It is increasingly recognized that macro-organisms (corals, insects, plants, vertebrates) consist of both host tissues and multiple microbial symbionts that play essential roles in their host's ecological and evolutionary success. Consequently, identifying benefits and costs of symbioses, as well as mechanisms underlying them are research priorities. All plants surveyed under natural conditions harbor foliar endophytic fungi (FEF) in their leaf tissues, often at high densities. Despite producing no visible effects on their hosts, experiments have nonetheless shown that FEF reduce pathogen and herbivore damage. Here, combining results from three genomic, and two physiological experiments, we demonstrate pervasive genetic and phenotypic effects of the apparently asymptomatic endophytes on their hosts. Specifically, inoculation of endophyte-free (E-) Theobroma cacao leaves with Colletotrichum tropicale (E+), the dominant FEF species in healthy T. cacao, induces consistent changes in the expression of hundreds of host genes, including many with known defensive functions. Further, E+ plants exhibited increased lignin and cellulose content, reduced maximum rates of photosynthesis (Amax), and enrichment of nitrogen-15 and carbon-13 isotopes. These phenotypic changes observed in E+ plants correspond to changes in expression of specific functional genes in related pathways. Moreover, a cacao gene (Tc00g04254) highly up-regulated by C. tropicale also confers resistance to pathogen damage in the absence of endophytes or their products in host tissues. Thus, the benefits of increased pathogen resistance in E+ plants are derived in part from up-regulation of intrinsic host defense responses, and appear to be offset by potential costs including reduced photosynthesis, altered host nitrogen metabolism, and endophyte heterotrophy of host tissues. Similar effects are likely in most plant-endophyte interactions, and should be recognized in the design and interpretation of genetic and phenotypic studies of plants. </AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Mejía</LastName><ForeName>Luis C</ForeName><Initials>LC</Initials><AffiliationInfo><Affiliation>Smithsonian Tropical Research Institute Unit 9100, USA ; Department of Plant Science and The Huck Institutes of the Life Sciences, The Pennsylvania State University University Park, PA, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Herre</LastName><ForeName>Edward A</ForeName><Initials>EA</Initials><AffiliationInfo><Affiliation>Smithsonian Tropical Research Institute Unit 9100, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sparks</LastName><ForeName>Jed P</ForeName><Initials>JP</Initials><AffiliationInfo><Affiliation>Department of Ecology and Evolution, Cornell University Ithaca, NY, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Winter</LastName><ForeName>Klaus</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>Smithsonian Tropical Research Institute Unit 9100, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>García</LastName><ForeName>Milton N</ForeName><Initials>MN</Initials><AffiliationInfo><Affiliation>Smithsonian Tropical Research Institute Unit 9100, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Van Bael</LastName><ForeName>Sunshine A</ForeName><Initials>SA</Initials><AffiliationInfo><Affiliation>Smithsonian Tropical Research Institute Unit 9100, USA ; Department of Ecology and Evolutionary Biology, Tulane University New Orleans, LA, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Stitt</LastName><ForeName>Joseph</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Social, Life and Engineering Sciences Imaging Center, Materials Research Institute University Park, PA, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Shi</LastName><ForeName>Zi</ForeName><Initials>Z</Initials><AffiliationInfo><Affiliation>Department of Plant Science and The Huck Institutes of the Life Sciences, The Pennsylvania State University University Park, PA, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Yufan</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Department of Plant Science and The Huck Institutes of the Life Sciences, The Pennsylvania State University University Park, PA, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Guiltinan</LastName><ForeName>Mark J</ForeName><Initials>MJ</Initials><AffiliationInfo><Affiliation>Department of Plant Science and The Huck Institutes of the Life Sciences, The Pennsylvania State University University Park, PA, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Maximova</LastName><ForeName>Siela N</ForeName><Initials>SN</Initials><AffiliationInfo><Affiliation>Department of Plant Science and The Huck Institutes of the Life Sciences, The Pennsylvania State University University Park, PA, USA.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2014</Year><Month>09</Month><Day>12</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Front Microbiol</MedlineTA><NlmUniqueID>101548977</NlmUniqueID><ISSNLinking>1664-302X</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Arabidopsis</Keyword><Keyword MajorTopicYN="N">Colletotrichum</Keyword><Keyword MajorTopicYN="N">Populus</Keyword><Keyword MajorTopicYN="N">Theobroma</Keyword><Keyword MajorTopicYN="N">fungal endophytes</Keyword><Keyword MajorTopicYN="N">gene expression</Keyword><Keyword MajorTopicYN="N">plant defense</Keyword><Keyword MajorTopicYN="N">symbiosis</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2014</Year><Month>05</Month><Day>12</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2014</Year><Month>08</Month><Day>25</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2014</Year><Month>10</Month><Day>14</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2014</Year><Month>10</Month><Day>14</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2014</Year><Month>10</Month><Day>14</Day><Hour>6</Hour><Minute>1</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">25309519</ArticleId><ArticleId IdType="doi">10.3389/fmicb.2014.00479</ArticleId><ArticleId 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Mejía</name></region><name sortKey="Garcia, Milton N" sort="Garcia, Milton N" uniqKey="Garcia M" first="Milton N" last="García">Milton N. García</name><name sortKey="Guiltinan, Mark J" sort="Guiltinan, Mark J" uniqKey="Guiltinan M" first="Mark J" last="Guiltinan">Mark J. Guiltinan</name><name sortKey="Herre, Edward A" sort="Herre, Edward A" uniqKey="Herre E" first="Edward A" last="Herre">Edward A. Herre</name><name sortKey="Maximova, Siela N" sort="Maximova, Siela N" uniqKey="Maximova S" first="Siela N" last="Maximova">Siela N. Maximova</name><name sortKey="Shi, Zi" sort="Shi, Zi" uniqKey="Shi Z" first="Zi" last="Shi">Zi Shi</name><name sortKey="Sparks, Jed P" sort="Sparks, Jed P" uniqKey="Sparks J" first="Jed P" last="Sparks">Jed P. Sparks</name><name sortKey="Stitt, Joseph" sort="Stitt, Joseph" uniqKey="Stitt J" first="Joseph" last="Stitt">Joseph Stitt</name><name sortKey="Van Bael, Sunshine A" sort="Van Bael, Sunshine A" uniqKey="Van Bael S" first="Sunshine A" last="Van Bael">Sunshine A. Van Bael</name><name sortKey="Winter, Klaus" sort="Winter, Klaus" uniqKey="Winter K" first="Klaus" last="Winter">Klaus Winter</name><name sortKey="Zhang, Yufan" sort="Zhang, Yufan" uniqKey="Zhang Y" first="Yufan" last="Zhang">Yufan Zhang</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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