Relatively rare root endophytic bacteria drive plant resource allocation patterns and tissue nutrient concentration in unpredictable ways.
Identifieur interne : 000735 ( Main/Exploration ); précédent : 000734; suivant : 000736Relatively rare root endophytic bacteria drive plant resource allocation patterns and tissue nutrient concentration in unpredictable ways.
Auteurs : Jeremiah A. Henning [États-Unis] ; David J. Weston [États-Unis] ; Dale A. Pelletier [États-Unis] ; Collin M. Timm [États-Unis] ; Sara S. Jawdy [États-Unis] ; Aimée T. Classen [États-Unis]Source :
- American journal of botany [ 1537-2197 ] ; 2019.
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English descriptors
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- MESH :
Abstract
PREMISE
Plant endophytic bacterial strains can influence plant traits such as leaf area and root length. Yet, the influence of more complex bacterial communities in regulating overall plant phenotype is less explored. Here, in two complementary experiments, we tested whether we can predict plant phenotype response to changes in microbial community composition.
METHODS
In the first study, we inoculated a single genotype of Populus deltoides with individual root endophytic bacteria and measured plant phenotype. Next, data from this single inoculation were used to predict phenotypic traits after mixed three-strain community inoculations, which we tested in the second experiment.
RESULTS
By itself, each bacterial endophyte significantly but weakly altered plant phenotype relative to noninoculated plants. In a mixture, bacterial strain Burkholderia BT03, constituted at least 98% of community relative abundance. Yet, plant resource allocation and tissue nutrient concentrations were disproportionately influenced by Pseudomonas sp. GM17, GM30, and GM41. We found a 10% increase in leaf mass fraction and an 11% decrease in root mass fraction when replacing Pseudomonas GM17 with GM41 in communities containing both Pseudomonas GM30 and Burkholderia BT03.
CONCLUSIONS
Our results indicate that interactions among endophytic bacteria may drive plant phenotype over the contribution of each strain individually. Additionally, we have shown that low-abundance strains contribute to plant phenotype challenging the assumption that the dominant strains will drive plant function.
DOI: 10.1002/ajb2.1373
PubMed: 31657872
Affiliations:
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Henning</name><affiliation wicri:level="1"><nlm:affiliation>Ecology & Evolutionary Biology, University of Tennessee, 569 Dabney Hall, 1416 Circle Drive, Knoxville, TN, 37996, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Ecology & Evolutionary Biology, University of Tennessee, 569 Dabney Hall, 1416 Circle Drive, Knoxville, TN, 37996</wicri:regionArea><wicri:noRegion>37996</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Ecology, Evolution, and Behavior, University of Minnesota, 140 Gortner Avenue, St. Paul, MN, 55108, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Ecology, Evolution, and Behavior, University of Minnesota, 140 Gortner Avenue, St. Paul, MN, 55108</wicri:regionArea><wicri:noRegion>55108</wicri:noRegion></affiliation></author><author><name sortKey="Weston, David J" sort="Weston, David J" uniqKey="Weston D" first="David J" last="Weston">David J. Weston</name><affiliation wicri:level="2"><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN</wicri:regionArea><placeName><region type="state">Tennessee</region></placeName></affiliation></author><author><name sortKey="Pelletier, Dale A" sort="Pelletier, Dale A" uniqKey="Pelletier D" first="Dale A" last="Pelletier">Dale A. Pelletier</name><affiliation wicri:level="2"><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN</wicri:regionArea><placeName><region type="state">Tennessee</region></placeName></affiliation></author><author><name sortKey="Timm, Collin M" sort="Timm, Collin M" uniqKey="Timm C" first="Collin M" last="Timm">Collin M. Timm</name><affiliation wicri:level="2"><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN</wicri:regionArea><placeName><region type="state">Tennessee</region></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Biosciences, Johns Hopkins University Applied Physics Laboratory, 11100 Johns Hopkins Road, Laurel, MD, 20723, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Biosciences, Johns Hopkins University Applied Physics Laboratory, 11100 Johns Hopkins Road, Laurel, MD, 20723</wicri:regionArea><wicri:noRegion>20723</wicri:noRegion></affiliation></author><author><name sortKey="Jawdy, Sara S" sort="Jawdy, Sara S" uniqKey="Jawdy S" first="Sara S" last="Jawdy">Sara S. Jawdy</name><affiliation wicri:level="2"><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN</wicri:regionArea><placeName><region type="state">Tennessee</region></placeName></affiliation></author><author><name sortKey="Classen, Aimee T" sort="Classen, Aimee T" uniqKey="Classen A" first="Aimée T" last="Classen">Aimée T. Classen</name><affiliation wicri:level="1"><nlm:affiliation>Ecology & Evolutionary Biology, University of Tennessee, 569 Dabney Hall, 1416 Circle Drive, Knoxville, TN, 37996, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Ecology & Evolutionary Biology, University of Tennessee, 569 Dabney Hall, 1416 Circle Drive, Knoxville, TN, 37996</wicri:regionArea><wicri:noRegion>37996</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>The Rubenstein School of Environment & Natural Resources, University of Vermont, Burlington, VT, 05405, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>The Rubenstein School of Environment & Natural Resources, University of Vermont, Burlington, VT, 05405</wicri:regionArea><wicri:noRegion>05405</wicri:noRegion></affiliation></author></analytic><series><title level="j">American journal of botany</title><idno type="eISSN">1537-2197</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Bacteria (MeSH)</term><term>Endophytes (MeSH)</term><term>Nutrients (MeSH)</term><term>Plant Roots (MeSH)</term><term>Populus (MeSH)</term><term>Resource Allocation (MeSH)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Allocation des ressources (MeSH)</term><term>Bactéries (MeSH)</term><term>Endophytes (MeSH)</term><term>Nutriments (MeSH)</term><term>Populus (MeSH)</term><term>Racines de plante (MeSH)</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Bacteria</term><term>Endophytes</term><term>Nutrients</term><term>Plant Roots</term><term>Populus</term><term>Resource Allocation</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Allocation des ressources</term><term>Bactéries</term><term>Endophytes</term><term>Nutriments</term><term>Populus</term><term>Racines de plante</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p><b>PREMISE</b></p><p>Plant endophytic bacterial strains can influence plant traits such as leaf area and root length. Yet, the influence of more complex bacterial communities in regulating overall plant phenotype is less explored. Here, in two complementary experiments, we tested whether we can predict plant phenotype response to changes in microbial community composition.</p></div><div type="abstract" xml:lang="en"><p><b>METHODS</b></p><p>In the first study, we inoculated a single genotype of Populus deltoides with individual root endophytic bacteria and measured plant phenotype. Next, data from this single inoculation were used to predict phenotypic traits after mixed three-strain community inoculations, which we tested in the second experiment.</p></div><div type="abstract" xml:lang="en"><p><b>RESULTS</b></p><p>By itself, each bacterial endophyte significantly but weakly altered plant phenotype relative to noninoculated plants. In a mixture, bacterial strain Burkholderia BT03, constituted at least 98% of community relative abundance. Yet, plant resource allocation and tissue nutrient concentrations were disproportionately influenced by Pseudomonas sp. GM17, GM30, and GM41. We found a 10% increase in leaf mass fraction and an 11% decrease in root mass fraction when replacing Pseudomonas GM17 with GM41 in communities containing both Pseudomonas GM30 and Burkholderia BT03.</p></div><div type="abstract" xml:lang="en"><p><b>CONCLUSIONS</b></p><p>Our results indicate that interactions among endophytic bacteria may drive plant phenotype over the contribution of each strain individually. Additionally, we have shown that low-abundance strains contribute to plant phenotype challenging the assumption that the dominant strains will drive plant function.</p></div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" IndexingMethod="Automated" Owner="NLM"><PMID Version="1">31657872</PMID><DateCompleted><Year>2020</Year><Month>03</Month><Day>18</Day></DateCompleted><DateRevised><Year>2020</Year><Month>03</Month><Day>18</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1537-2197</ISSN><JournalIssue CitedMedium="Internet"><Volume>106</Volume><Issue>11</Issue><PubDate><Year>2019</Year><Month>11</Month></PubDate></JournalIssue><Title>American journal of botany</Title><ISOAbbreviation>Am J Bot</ISOAbbreviation></Journal><ArticleTitle>Relatively rare root endophytic bacteria drive plant resource allocation patterns and tissue nutrient concentration in unpredictable ways.</ArticleTitle><Pagination><MedlinePgn>1423-1434</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1002/ajb2.1373</ELocationID><Abstract><AbstractText Label="PREMISE">Plant endophytic bacterial strains can influence plant traits such as leaf area and root length. Yet, the influence of more complex bacterial communities in regulating overall plant phenotype is less explored. Here, in two complementary experiments, we tested whether we can predict plant phenotype response to changes in microbial community composition.</AbstractText><AbstractText Label="METHODS">In the first study, we inoculated a single genotype of Populus deltoides with individual root endophytic bacteria and measured plant phenotype. Next, data from this single inoculation were used to predict phenotypic traits after mixed three-strain community inoculations, which we tested in the second experiment.</AbstractText><AbstractText Label="RESULTS">By itself, each bacterial endophyte significantly but weakly altered plant phenotype relative to noninoculated plants. In a mixture, bacterial strain Burkholderia BT03, constituted at least 98% of community relative abundance. Yet, plant resource allocation and tissue nutrient concentrations were disproportionately influenced by Pseudomonas sp. GM17, GM30, and GM41. We found a 10% increase in leaf mass fraction and an 11% decrease in root mass fraction when replacing Pseudomonas GM17 with GM41 in communities containing both Pseudomonas GM30 and Burkholderia BT03.</AbstractText><AbstractText Label="CONCLUSIONS">Our results indicate that interactions among endophytic bacteria may drive plant phenotype over the contribution of each strain individually. Additionally, we have shown that low-abundance strains contribute to plant phenotype challenging the assumption that the dominant strains will drive plant function.</AbstractText><CopyrightInformation>© 2019 Botanical Society of America.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Henning</LastName><ForeName>Jeremiah A</ForeName><Initials>JA</Initials><Identifier Source="ORCID">0000-0002-2214-4895</Identifier><AffiliationInfo><Affiliation>Ecology & Evolutionary Biology, University of Tennessee, 569 Dabney Hall, 1416 Circle Drive, Knoxville, TN, 37996, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Ecology, Evolution, and Behavior, University of Minnesota, 140 Gortner Avenue, St. Paul, MN, 55108, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Weston</LastName><ForeName>David J</ForeName><Initials>DJ</Initials><AffiliationInfo><Affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Pelletier</LastName><ForeName>Dale A</ForeName><Initials>DA</Initials><AffiliationInfo><Affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Timm</LastName><ForeName>Collin M</ForeName><Initials>CM</Initials><AffiliationInfo><Affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Biosciences, Johns Hopkins University Applied Physics Laboratory, 11100 Johns Hopkins Road, Laurel, MD, 20723, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jawdy</LastName><ForeName>Sara S</ForeName><Initials>SS</Initials><AffiliationInfo><Affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Classen</LastName><ForeName>Aimée T</ForeName><Initials>AT</Initials><AffiliationInfo><Affiliation>Ecology & Evolutionary Biology, University of Tennessee, 569 Dabney Hall, 1416 Circle Drive, Knoxville, TN, 37996, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>The Rubenstein School of Environment & Natural Resources, University of Vermont, Burlington, VT, 05405, USA.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><Agency>Office of Science</Agency><Country>International</Country></Grant><Grant><Agency>Biological and Environmental Research</Agency><Country>International</Country></Grant><Grant><GrantID>DE-AC05-00OR22725</GrantID><Agency>U.S. Department of Energy</Agency><Country>International</Country></Grant><Grant><GrantID>DE-SC0010562</GrantID><Agency>University of Tennessee</Agency><Country>International</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType><PublicationType UI="D013486">Research Support, U.S. Gov't, Non-P.H.S.</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>10</Month><Day>28</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Am J Bot</MedlineTA><NlmUniqueID>0370467</NlmUniqueID><ISSNLinking>0002-9122</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D001419" MajorTopicYN="N">Bacteria</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D060026" MajorTopicYN="Y">Endophytes</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D000078622" MajorTopicYN="N">Nutrients</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D018517" MajorTopicYN="N">Plant Roots</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D032107" MajorTopicYN="Y">Populus</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D040841" MajorTopicYN="N">Resource Allocation</DescriptorName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">Burkholderia
</Keyword><Keyword MajorTopicYN="Y">Populus deltoides
</Keyword><Keyword MajorTopicYN="Y">Pseudomonas
</Keyword><Keyword MajorTopicYN="Y">Salicaceae</Keyword><Keyword MajorTopicYN="Y">allocation</Keyword><Keyword MajorTopicYN="Y">bacterial endophytes</Keyword><Keyword MajorTopicYN="Y">constructed communities</Keyword><Keyword MajorTopicYN="Y">mass-ratio hypothesis</Keyword><Keyword MajorTopicYN="Y">plant traits</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>07</Month><Day>09</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2019</Year><Month>09</Month><Day>06</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2019</Year><Month>10</Month><Day>29</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>3</Month><Day>19</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2019</Year><Month>10</Month><Day>29</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">31657872</ArticleId><ArticleId IdType="doi">10.1002/ajb2.1373</ArticleId></ArticleIdList><ReferenceList><Title>LITERATURE CITED</Title><Reference><Citation>Balvanera, P., C. 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