Fungal Endophytes of Populus trichocarpa Alter Host Phenotype, Gene Expression, and Rhizobiome Composition.
Identifieur interne : 000952 ( Main/Exploration ); précédent : 000951; suivant : 000953Fungal Endophytes of Populus trichocarpa Alter Host Phenotype, Gene Expression, and Rhizobiome Composition.
Auteurs : Hui-Ling Liao [États-Unis] ; Gregory Bonito [États-Unis] ; J Alejandro Rojas [États-Unis] ; Khalid Hameed [États-Unis] ; Steven Wu [États-Unis] ; Christopher W. Schadt [États-Unis] ; Jessy Labbé [États-Unis] ; Gerald A. Tuskan [États-Unis] ; Francis Martin [France] ; Igor V. Grigoriev [États-Unis] ; Rytas Vilgalys [États-Unis]Source :
- Molecular plant-microbe interactions : MPMI [ 0894-0282 ] ; 2019.
Descripteurs français
- KwdFr :
- MESH :
- microbiologie : Populus, Racines de plante.
- physiologie : Champignons, Endophytes.
- Biodiversité, Phénotype, Rhizosphère, Régulation de l'expression des gènes végétaux.
English descriptors
- KwdEn :
- MESH :
- microbiology : Plant Roots, Populus.
- physiology : Endophytes, Fungi.
- Biodiversity, Gene Expression Regulation, Plant, Phenotype, Rhizosphere.
Abstract
Mortierella and Ilyonectria genera include common species of soil fungi that are frequently detected as root endophytes in many plants, including Populus spp. However, the ecological roles of these and other endophytic fungi with respect to plant growth and function are still not well understood. The functional ecology of two key taxa from the P. trichocarpa rhizobiome, M. elongata PMI93 and I. europaea PMI82, was studied by coupling forest soil bioassays with environmental metatranscriptomics. Using soil bioassay experiments amended with fungal inoculants, M. elongata was observed to promote the growth of P. trichocarpa. This response was cultivar independent. In contrast, I. europaea had no visible effect on P. trichocarpa growth. Metatranscriptomic studies revealed that these fungi impacted rhizophytic and endophytic activities in P. trichocarpa and induced shifts in soil and root microbial communities. Differential expression of core genes in P. trichocarpa roots was observed in response to both fungal species. Expression of P. trichocarpa genes for lipid signaling and nutrient uptake were upregulated, and expression of genes associated with gibberellin signaling were altered in plants inoculated with M. elongata, but not I. europaea. Upregulation of genes for growth promotion, downregulation of genes for several leucine-rich repeat receptor kinases, and alteration of expression of genes associated with plant defense responses (e.g., jasmonic acid, salicylic acid, and ethylene signal pathways) also suggest that M. elongata manipulates plant defenses while promoting plant growth.
DOI: 10.1094/MPMI-05-18-0133-R
PubMed: 30699306
Affiliations:
- France, États-Unis
- Arkansas, Californie, Caroline du Nord, Floride, Grand Est, Lorraine (région), Michigan, Tennessee
- Champenoux, East Lansing
- Université d'État du Michigan
Links toward previous steps (curation, corpus...)
Le document en format XML
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Liao</name><affiliation wicri:level="2"><nlm:affiliation>1 North Florida Research and Education Center, University of Florida, 155 Research Road, Quincy, FL 32351, U.S.A.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>1 North Florida Research and Education Center, University of Florida, 155 Research Road, Quincy, FL 32351</wicri:regionArea><placeName><region type="state">Floride</region></placeName></affiliation></author><author><name sortKey="Bonito, Gregory" sort="Bonito, Gregory" uniqKey="Bonito G" first="Gregory" last="Bonito">Gregory Bonito</name><affiliation wicri:level="4"><nlm:affiliation>2 Department of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, MI 48824, U.S.A.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>2 Department of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, MI 48824</wicri:regionArea><placeName><region type="state">Michigan</region><settlement type="city">East Lansing</settlement></placeName><orgName type="university">Université d'État du Michigan</orgName></affiliation></author><author><name sortKey="Rojas, J Alejandro" sort="Rojas, J Alejandro" uniqKey="Rojas J" first="J Alejandro" last="Rojas">J Alejandro Rojas</name><affiliation wicri:level="2"><nlm:affiliation>3 Department of Biology, Duke University, Durham, NC, U.S.A.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>3 Department of Biology, Duke University, Durham, NC</wicri:regionArea><placeName><region type="state">Caroline du Nord</region></placeName></affiliation><affiliation wicri:level="2"><nlm:affiliation>4 Plant Pathology Department, University of Arkansas, 211 PTSC-Fayetteville, AR 72701, U.S.A.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>4 Plant Pathology Department, University of Arkansas, 211 PTSC-Fayetteville, AR 72701</wicri:regionArea><placeName><region type="state">Arkansas</region></placeName></affiliation></author><author><name sortKey="Hameed, Khalid" sort="Hameed, Khalid" uniqKey="Hameed K" first="Khalid" last="Hameed">Khalid Hameed</name><affiliation wicri:level="2"><nlm:affiliation>3 Department of Biology, Duke University, Durham, NC, U.S.A.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>3 Department of Biology, Duke University, Durham, NC</wicri:regionArea><placeName><region type="state">Caroline du Nord</region></placeName></affiliation></author><author><name sortKey="Wu, Steven" sort="Wu, Steven" uniqKey="Wu S" first="Steven" last="Wu">Steven Wu</name><affiliation wicri:level="2"><nlm:affiliation>5 Independent Researcher, Davis, CA, U.S.A.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>5 Independent Researcher, Davis, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Schadt, Christopher W" sort="Schadt, Christopher W" uniqKey="Schadt C" first="Christopher W" last="Schadt">Christopher W. Schadt</name><affiliation wicri:level="2"><nlm:affiliation>6 Oak Ridge National Laboratory, 1 Bethel Valley Road, Oak Ridge, TN 37830, U.S.A.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>6 Oak Ridge National Laboratory, 1 Bethel Valley Road, Oak Ridge, TN 37830</wicri:regionArea><placeName><region type="state">Tennessee</region></placeName></affiliation></author><author><name sortKey="Labbe, Jessy" sort="Labbe, Jessy" uniqKey="Labbe J" first="Jessy" last="Labbé">Jessy Labbé</name><affiliation wicri:level="2"><nlm:affiliation>6 Oak Ridge National Laboratory, 1 Bethel Valley Road, Oak Ridge, TN 37830, U.S.A.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>6 Oak Ridge National Laboratory, 1 Bethel Valley Road, Oak Ridge, TN 37830</wicri:regionArea><placeName><region type="state">Tennessee</region></placeName></affiliation></author><author><name sortKey="Tuskan, Gerald A" sort="Tuskan, Gerald A" uniqKey="Tuskan G" first="Gerald A" last="Tuskan">Gerald A. Tuskan</name><affiliation wicri:level="2"><nlm:affiliation>6 Oak Ridge National Laboratory, 1 Bethel Valley Road, Oak Ridge, TN 37830, U.S.A.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>6 Oak Ridge National Laboratory, 1 Bethel Valley Road, Oak Ridge, TN 37830</wicri:regionArea><placeName><region type="state">Tennessee</region></placeName></affiliation></author><author><name sortKey="Martin, Francis" sort="Martin, Francis" uniqKey="Martin F" first="Francis" last="Martin">Francis Martin</name><affiliation wicri:level="3"><nlm:affiliation>7 INRA, UMR 1136 INRA-University of Lorraine, Interactions Arbres/Microorganismes, Laboratory of Excellence ARBRE, INRA-Nancy, 54280, Champenoux, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>7 INRA, UMR 1136 INRA-University of Lorraine, Interactions Arbres/Microorganismes, Laboratory of Excellence ARBRE, INRA-Nancy, 54280, Champenoux</wicri:regionArea><placeName><region type="region" nuts="2">Grand Est</region><region type="old region" nuts="2">Lorraine (région)</region><settlement type="city">Champenoux</settlement></placeName></affiliation></author><author><name sortKey="Grigoriev, Igor V" sort="Grigoriev, Igor V" uniqKey="Grigoriev I" first="Igor V" last="Grigoriev">Igor V. Grigoriev</name><affiliation wicri:level="2"><nlm:affiliation>8 U.S. Department of Energy Joint Genome Institute and Department of Plant and Microbial Biology, University of California Berkeley, 2800 Mitchell Drive, Walnut Creek, CA 94598, U.S.A.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>8 U.S. Department of Energy Joint Genome Institute and Department of Plant and Microbial Biology, University of California Berkeley, 2800 Mitchell Drive, Walnut Creek, CA 94598</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Vilgalys, Rytas" sort="Vilgalys, Rytas" uniqKey="Vilgalys R" first="Rytas" last="Vilgalys">Rytas Vilgalys</name><affiliation wicri:level="2"><nlm:affiliation>3 Department of Biology, Duke University, Durham, NC, U.S.A.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>3 Department of Biology, Duke University, Durham, NC</wicri:regionArea><placeName><region type="state">Caroline du Nord</region></placeName></affiliation></author></analytic><series><title level="j">Molecular plant-microbe interactions : MPMI</title><idno type="ISSN">0894-0282</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Biodiversity (MeSH)</term><term>Endophytes (physiology)</term><term>Fungi (physiology)</term><term>Gene Expression Regulation, Plant (MeSH)</term><term>Phenotype (MeSH)</term><term>Plant Roots (microbiology)</term><term>Populus (microbiology)</term><term>Rhizosphere (MeSH)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Biodiversité (MeSH)</term><term>Champignons (physiologie)</term><term>Endophytes (physiologie)</term><term>Phénotype (MeSH)</term><term>Populus (microbiologie)</term><term>Racines de plante (microbiologie)</term><term>Rhizosphère (MeSH)</term><term>Régulation de l'expression des gènes végétaux (MeSH)</term></keywords><keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr"><term>Populus</term><term>Racines de plante</term></keywords><keywords scheme="MESH" qualifier="microbiology" xml:lang="en"><term>Plant Roots</term><term>Populus</term></keywords><keywords scheme="MESH" qualifier="physiologie" xml:lang="fr"><term>Champignons</term><term>Endophytes</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Endophytes</term><term>Fungi</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Biodiversity</term><term>Gene Expression Regulation, Plant</term><term>Phenotype</term><term>Rhizosphere</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Biodiversité</term><term>Phénotype</term><term>Rhizosphère</term><term>Régulation de l'expression des gènes végétaux</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><i>Mortierella</i> and <i>Ilyonectria</i> genera include common species of soil fungi that are frequently detected as root endophytes in many plants, including <i>Populus</i> spp. However, the ecological roles of these and other endophytic fungi with respect to plant growth and function are still not well understood. The functional ecology of two key taxa from the <i>P. trichocarpa</i> rhizobiome, <i>M. elongata</i> PMI93 and <i>I. europaea</i> PMI82, was studied by coupling forest soil bioassays with environmental metatranscriptomics. Using soil bioassay experiments amended with fungal inoculants, <i>M. elongata</i> was observed to promote the growth of <i>P. trichocarpa</i>. This response was cultivar independent. In contrast, <i>I. europaea</i> had no visible effect on <i>P. trichocarpa</i> growth. Metatranscriptomic studies revealed that these fungi impacted rhizophytic and endophytic activities in <i>P. trichocarpa</i> and induced shifts in soil and root microbial communities. Differential expression of core genes in <i>P. trichocarpa</i> roots was observed in response to both fungal species. Expression of <i>P. trichocarpa</i> genes for lipid signaling and nutrient uptake were upregulated, and expression of genes associated with gibberellin signaling were altered in plants inoculated with <i>M. elongata</i>, but not <i>I. europaea</i>. Upregulation of genes for growth promotion, downregulation of genes for several leucine-rich repeat receptor kinases, and alteration of expression of genes associated with plant defense responses (e.g., jasmonic acid, salicylic acid, and ethylene signal pathways) also suggest that <i>M. elongata</i> manipulates plant defenses while promoting plant growth.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" IndexingMethod="Curated" Owner="NLM"><PMID Version="1">30699306</PMID><DateCompleted><Year>2019</Year><Month>07</Month><Day>30</Day></DateCompleted><DateRevised><Year>2019</Year><Month>07</Month><Day>30</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Print">0894-0282</ISSN><JournalIssue CitedMedium="Print"><Volume>32</Volume><Issue>7</Issue><PubDate><Year>2019</Year><Month>Jul</Month></PubDate></JournalIssue><Title>Molecular plant-microbe interactions : MPMI</Title><ISOAbbreviation>Mol Plant Microbe Interact</ISOAbbreviation></Journal><ArticleTitle>Fungal Endophytes of <i>Populus trichocarpa</i> Alter Host Phenotype, Gene Expression, and Rhizobiome Composition.</ArticleTitle><Pagination><MedlinePgn>853-864</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1094/MPMI-05-18-0133-R</ELocationID><Abstract><AbstractText><i>Mortierella</i> and <i>Ilyonectria</i> genera include common species of soil fungi that are frequently detected as root endophytes in many plants, including <i>Populus</i> spp. However, the ecological roles of these and other endophytic fungi with respect to plant growth and function are still not well understood. The functional ecology of two key taxa from the <i>P. trichocarpa</i> rhizobiome, <i>M. elongata</i> PMI93 and <i>I. europaea</i> PMI82, was studied by coupling forest soil bioassays with environmental metatranscriptomics. Using soil bioassay experiments amended with fungal inoculants, <i>M. elongata</i> was observed to promote the growth of <i>P. trichocarpa</i>. This response was cultivar independent. In contrast, <i>I. europaea</i> had no visible effect on <i>P. trichocarpa</i> growth. Metatranscriptomic studies revealed that these fungi impacted rhizophytic and endophytic activities in <i>P. trichocarpa</i> and induced shifts in soil and root microbial communities. Differential expression of core genes in <i>P. trichocarpa</i> roots was observed in response to both fungal species. Expression of <i>P. trichocarpa</i> genes for lipid signaling and nutrient uptake were upregulated, and expression of genes associated with gibberellin signaling were altered in plants inoculated with <i>M. elongata</i>, but not <i>I. europaea</i>. Upregulation of genes for growth promotion, downregulation of genes for several leucine-rich repeat receptor kinases, and alteration of expression of genes associated with plant defense responses (e.g., jasmonic acid, salicylic acid, and ethylene signal pathways) also suggest that <i>M. elongata</i> manipulates plant defenses while promoting plant growth.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Liao</LastName><ForeName>Hui-Ling</ForeName><Initials>HL</Initials><Identifier Source="ORCID">http://orcid.org/0000-0002-1648-3444</Identifier><AffiliationInfo><Affiliation>1 North Florida Research and Education Center, University of Florida, 155 Research Road, Quincy, FL 32351, U.S.A.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bonito</LastName><ForeName>Gregory</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>2 Department of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, MI 48824, U.S.A.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Rojas</LastName><ForeName>J Alejandro</ForeName><Initials>JA</Initials><Identifier Source="ORCID">http://orcid.org/0000-0001-5492-5963</Identifier><AffiliationInfo><Affiliation>3 Department of Biology, Duke University, Durham, NC, U.S.A.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>4 Plant Pathology Department, University of Arkansas, 211 PTSC-Fayetteville, AR 72701, U.S.A.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hameed</LastName><ForeName>Khalid</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>3 Department of Biology, Duke University, Durham, NC, U.S.A.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wu</LastName><ForeName>Steven</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>5 Independent Researcher, Davis, CA, U.S.A.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Schadt</LastName><ForeName>Christopher W</ForeName><Initials>CW</Initials><AffiliationInfo><Affiliation>6 Oak Ridge National Laboratory, 1 Bethel Valley Road, Oak Ridge, TN 37830, U.S.A.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Labbé</LastName><ForeName>Jessy</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>6 Oak Ridge National Laboratory, 1 Bethel Valley Road, Oak Ridge, TN 37830, U.S.A.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tuskan</LastName><ForeName>Gerald A</ForeName><Initials>GA</Initials><AffiliationInfo><Affiliation>6 Oak Ridge National Laboratory, 1 Bethel Valley Road, Oak Ridge, TN 37830, U.S.A.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Martin</LastName><ForeName>Francis</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>7 INRA, UMR 1136 INRA-University of Lorraine, Interactions Arbres/Microorganismes, Laboratory of Excellence ARBRE, INRA-Nancy, 54280, Champenoux, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Grigoriev</LastName><ForeName>Igor V</ForeName><Initials>IV</Initials><AffiliationInfo><Affiliation>8 U.S. Department of Energy Joint Genome Institute and Department of Plant and Microbial Biology, University of California Berkeley, 2800 Mitchell Drive, Walnut Creek, CA 94598, U.S.A.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Vilgalys</LastName><ForeName>Rytas</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>3 Department of Biology, Duke University, Durham, NC, U.S.A.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>06</Month><Day>10</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Mol Plant Microbe Interact</MedlineTA><NlmUniqueID>9107902</NlmUniqueID><ISSNLinking>0894-0282</ISSNLinking></MedlineJournalInfo><MeshHeadingList><MeshHeading><DescriptorName UI="D044822" MajorTopicYN="N">Biodiversity</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D060026" MajorTopicYN="Y">Endophytes</DescriptorName><QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D005658" MajorTopicYN="Y">Fungi</DescriptorName><QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D018506" MajorTopicYN="Y">Gene Expression Regulation, Plant</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D010641" MajorTopicYN="N">Phenotype</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D018517" MajorTopicYN="N">Plant Roots</DescriptorName><QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D032107" MajorTopicYN="Y">Populus</DescriptorName><QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D058441" MajorTopicYN="N">Rhizosphere</DescriptorName></MeshHeading></MeshHeadingList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="pubmed"><Year>2019</Year><Month>1</Month><Day>31</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2019</Year><Month>7</Month><Day>31</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2019</Year><Month>1</Month><Day>31</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">30699306</ArticleId><ArticleId IdType="doi">10.1094/MPMI-05-18-0133-R</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>France</li><li>États-Unis</li></country><region><li>Arkansas</li><li>Californie</li><li>Caroline du Nord</li><li>Floride</li><li>Grand Est</li><li>Lorraine (région)</li><li>Michigan</li><li>Tennessee</li></region><settlement><li>Champenoux</li><li>East Lansing</li></settlement><orgName><li>Université d'État du Michigan</li></orgName></list><tree><country name="États-Unis"><region name="Floride"><name sortKey="Liao, Hui Ling" sort="Liao, Hui Ling" uniqKey="Liao H" first="Hui-Ling" last="Liao">Hui-Ling Liao</name></region><name sortKey="Bonito, Gregory" sort="Bonito, Gregory" uniqKey="Bonito G" first="Gregory" last="Bonito">Gregory Bonito</name><name sortKey="Grigoriev, Igor V" sort="Grigoriev, Igor V" uniqKey="Grigoriev I" first="Igor V" last="Grigoriev">Igor V. Grigoriev</name><name sortKey="Hameed, Khalid" sort="Hameed, Khalid" uniqKey="Hameed K" first="Khalid" last="Hameed">Khalid Hameed</name><name sortKey="Labbe, Jessy" sort="Labbe, Jessy" uniqKey="Labbe J" first="Jessy" last="Labbé">Jessy Labbé</name><name sortKey="Rojas, J Alejandro" sort="Rojas, J Alejandro" uniqKey="Rojas J" first="J Alejandro" last="Rojas">J Alejandro Rojas</name><name sortKey="Rojas, J Alejandro" sort="Rojas, J Alejandro" uniqKey="Rojas J" first="J Alejandro" last="Rojas">J Alejandro Rojas</name><name sortKey="Schadt, Christopher W" sort="Schadt, Christopher W" uniqKey="Schadt C" first="Christopher W" last="Schadt">Christopher W. Schadt</name><name sortKey="Tuskan, Gerald A" sort="Tuskan, Gerald A" uniqKey="Tuskan G" first="Gerald A" last="Tuskan">Gerald A. Tuskan</name><name sortKey="Vilgalys, Rytas" sort="Vilgalys, Rytas" uniqKey="Vilgalys R" first="Rytas" last="Vilgalys">Rytas Vilgalys</name><name sortKey="Wu, Steven" sort="Wu, Steven" uniqKey="Wu S" first="Steven" last="Wu">Steven Wu</name></country><country name="France"><region name="Grand Est"><name sortKey="Martin, Francis" sort="Martin, Francis" uniqKey="Martin F" first="Francis" last="Martin">Francis Martin</name></region></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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