Endophyte-Promoted Phosphorus Solubilization in Populus.
Identifieur interne : 000431 ( Main/Exploration ); précédent : 000430; suivant : 000432Endophyte-Promoted Phosphorus Solubilization in Populus.
Auteurs : Tamas Varga [États-Unis] ; Kim K. Hixson [États-Unis] ; Amir H. Ahkami [États-Unis] ; Andrew W. Sher [États-Unis] ; Morgan E. Barnes [États-Unis] ; Rosalie K. Chu [États-Unis] ; Anil K. Battu [États-Unis] ; Carrie D. Nicora [États-Unis] ; Tanya E. Winkler [États-Unis] ; Loren R. Reno [États-Unis] ; Sirine C. Fakra [États-Unis] ; Olga Antipova [États-Unis] ; Dilworth Y. Parkinson [États-Unis] ; Jackson R. Hall [États-Unis] ; Sharon L. Doty [États-Unis]Source :
- Frontiers in plant science [ 1664-462X ] ; 2020.
Abstract
Phosphorus is one of the essential nutrients for plant growth, but it may be relatively unavailable to plants because of its chemistry. In soil, the majority of phosphorus is present in the form of a phosphate, usually as metal complexes making it bound to minerals or organic matter. Therefore, inorganic phosphate solubilization is an important process of plant growth promotion by plant associated bacteria and fungi. Non-nodulating plant species have been shown to thrive in low-nutrient environments, in some instances by relying on plant associated microorganisms called endophytes. These microorganisms live within the plant and help supply nutrients for the plant. Despite their potential enormous environmental importance, there are a limited number of studies looking at the direct molecular impact of phosphate solubilizing endophytic bacteria on the host plant. In this work, we studied the impact of two endophyte strains of wild poplar (Populus trichocarpa) that solubilize phosphate. Using a combination of x-ray imaging, spectroscopy methods, and proteomics, we report direct evidence of endophyte-promoted phosphorus uptake in poplar. We found that the solubilized phosphate may react and become insoluble once inside plant tissue, suggesting that endophytes may aid in the re-release of phosphate. Using synchrotron x-ray fluorescence spectromicroscopy, we visualized the nutrient phosphorus inside poplar roots inoculated by the selected endophytes and found the phosphorus in both forms of organic and inorganic phosphates inside the root. Tomography-based root imaging revealed a markedly different root biomass and root architecture for poplar samples inoculated with the phosphate solubilizing bacteria strains. Proteomics characterization on poplar roots coupled with protein network analysis revealed novel proteins and metabolic pathways with possible involvement in endophyte enriched phosphorus uptake. These findings suggest an important role of endophytes for phosphorus acquisition and provide a deeper understanding of the critical symbiotic associations between poplar and the endophytic bacteria.
DOI: 10.3389/fpls.2020.567918
PubMed: 33193494
PubMed Central: PMC7609660
Affiliations:
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Hixson</name><affiliation wicri:level="2"><nlm:affiliation>Environmental Molecular Sciences Laboratory, Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Environmental Molecular Sciences Laboratory, Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA</wicri:regionArea><placeName><region type="state">Washington (État)</region></placeName></affiliation></author><author><name sortKey="Ahkami, Amir H" sort="Ahkami, Amir H" uniqKey="Ahkami A" first="Amir H" last="Ahkami">Amir H. Ahkami</name><affiliation wicri:level="2"><nlm:affiliation>Environmental Molecular Sciences Laboratory, Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Environmental Molecular Sciences Laboratory, Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA</wicri:regionArea><placeName><region type="state">Washington (État)</region></placeName></affiliation></author><author><name sortKey="Sher, Andrew W" sort="Sher, Andrew W" uniqKey="Sher A" first="Andrew W" last="Sher">Andrew W. Sher</name><affiliation wicri:level="4"><nlm:affiliation>School of Environmental and Forest Sciences, College of the Environment, University of Washington, Seattle, WA, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>School of Environmental and Forest Sciences, College of the Environment, University of Washington, Seattle, WA</wicri:regionArea><placeName><region type="state">Washington (État)</region><settlement type="city">Seattle</settlement></placeName><orgName type="university">Université de Washington</orgName></affiliation></author><author><name sortKey="Barnes, Morgan E" sort="Barnes, Morgan E" uniqKey="Barnes M" first="Morgan E" last="Barnes">Morgan E. Barnes</name><affiliation wicri:level="2"><nlm:affiliation>Environmental Systems Graduate Group, University of California, Merced, Merced, CA, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Environmental Systems Graduate Group, University of California, Merced, Merced, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Chu, Rosalie K" sort="Chu, Rosalie K" uniqKey="Chu R" first="Rosalie K" last="Chu">Rosalie K. Chu</name><affiliation wicri:level="2"><nlm:affiliation>Environmental Molecular Sciences Laboratory, Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Environmental Molecular Sciences Laboratory, Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA</wicri:regionArea><placeName><region type="state">Washington (État)</region></placeName></affiliation></author><author><name sortKey="Battu, Anil K" sort="Battu, Anil K" uniqKey="Battu A" first="Anil K" last="Battu">Anil K. Battu</name><affiliation wicri:level="2"><nlm:affiliation>Environmental Molecular Sciences Laboratory, Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Environmental Molecular Sciences Laboratory, Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA</wicri:regionArea><placeName><region type="state">Washington (État)</region></placeName></affiliation></author><author><name sortKey="Nicora, Carrie D" sort="Nicora, Carrie D" uniqKey="Nicora C" first="Carrie D" last="Nicora">Carrie D. Nicora</name><affiliation wicri:level="2"><nlm:affiliation>Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA</wicri:regionArea><placeName><region type="state">Washington (État)</region></placeName></affiliation></author><author><name sortKey="Winkler, Tanya E" sort="Winkler, Tanya E" uniqKey="Winkler T" first="Tanya E" last="Winkler">Tanya E. Winkler</name><affiliation wicri:level="2"><nlm:affiliation>Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA</wicri:regionArea><placeName><region type="state">Washington (État)</region></placeName></affiliation></author><author><name sortKey="Reno, Loren R" sort="Reno, Loren R" uniqKey="Reno L" first="Loren R" last="Reno">Loren R. Reno</name><affiliation wicri:level="2"><nlm:affiliation>Environmental Molecular Sciences Laboratory, Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Environmental Molecular Sciences Laboratory, Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA</wicri:regionArea><placeName><region type="state">Washington (État)</region></placeName></affiliation></author><author><name sortKey="Fakra, Sirine C" sort="Fakra, Sirine C" uniqKey="Fakra S" first="Sirine C" last="Fakra">Sirine C. Fakra</name><affiliation wicri:level="2"><nlm:affiliation>Advanced Light Source, Lawrence Berkeley National Laboratory, Berkeley, CA, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Advanced Light Source, Lawrence Berkeley National Laboratory, Berkeley, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Antipova, Olga" sort="Antipova, Olga" uniqKey="Antipova O" first="Olga" last="Antipova">Olga Antipova</name><affiliation wicri:level="2"><nlm:affiliation>Advanced Photon Source, Argonne National Laboratory, Lemont, IL, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Advanced Photon Source, Argonne National Laboratory, Lemont, IL</wicri:regionArea><placeName><region type="state">Illinois</region></placeName></affiliation></author><author><name sortKey="Parkinson, Dilworth Y" sort="Parkinson, Dilworth Y" uniqKey="Parkinson D" first="Dilworth Y" last="Parkinson">Dilworth Y. Parkinson</name><affiliation wicri:level="2"><nlm:affiliation>Advanced Light Source, Lawrence Berkeley National Laboratory, Berkeley, CA, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Advanced Light Source, Lawrence Berkeley National Laboratory, Berkeley, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Hall, Jackson R" sort="Hall, Jackson R" uniqKey="Hall J" first="Jackson R" last="Hall">Jackson R. Hall</name><affiliation wicri:level="4"><nlm:affiliation>School of Environmental and Forest Sciences, College of the Environment, University of Washington, Seattle, WA, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>School of Environmental and Forest Sciences, College of the Environment, University of Washington, Seattle, WA</wicri:regionArea><placeName><region type="state">Washington (État)</region><settlement type="city">Seattle</settlement></placeName><orgName type="university">Université de Washington</orgName></affiliation></author><author><name sortKey="Doty, Sharon L" sort="Doty, Sharon L" uniqKey="Doty S" first="Sharon L" last="Doty">Sharon L. Doty</name><affiliation wicri:level="4"><nlm:affiliation>School of Environmental and Forest Sciences, College of the Environment, University of Washington, Seattle, WA, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>School of Environmental and Forest Sciences, College of the Environment, University of Washington, Seattle, WA</wicri:regionArea><placeName><region type="state">Washington (État)</region><settlement type="city">Seattle</settlement></placeName><orgName type="university">Université de Washington</orgName></affiliation></author></analytic><series><title level="j">Frontiers in plant science</title><idno type="ISSN">1664-462X</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Phosphorus is one of the essential nutrients for plant growth, but it may be relatively unavailable to plants because of its chemistry. In soil, the majority of phosphorus is present in the form of a phosphate, usually as metal complexes making it bound to minerals or organic matter. Therefore, inorganic phosphate solubilization is an important process of plant growth promotion by plant associated bacteria and fungi. Non-nodulating plant species have been shown to thrive in low-nutrient environments, in some instances by relying on plant associated microorganisms called endophytes. These microorganisms live within the plant and help supply nutrients for the plant. Despite their potential enormous environmental importance, there are a limited number of studies looking at the direct molecular impact of phosphate solubilizing endophytic bacteria on the host plant. In this work, we studied the impact of two endophyte strains of wild poplar (<i>Populus trichocarpa</i>) that solubilize phosphate. Using a combination of x-ray imaging, spectroscopy methods, and proteomics, we report direct evidence of endophyte-promoted phosphorus uptake in poplar. We found that the solubilized phosphate may react and become insoluble once inside plant tissue, suggesting that endophytes may aid in the re-release of phosphate. Using synchrotron x-ray fluorescence spectromicroscopy, we visualized the nutrient phosphorus inside poplar roots inoculated by the selected endophytes and found the phosphorus in both forms of organic and inorganic phosphates inside the root. Tomography-based root imaging revealed a markedly different root biomass and root architecture for poplar samples inoculated with the phosphate solubilizing bacteria strains. Proteomics characterization on poplar roots coupled with protein network analysis revealed novel proteins and metabolic pathways with possible involvement in endophyte enriched phosphorus uptake. These findings suggest an important role of endophytes for phosphorus acquisition and provide a deeper understanding of the critical symbiotic associations between poplar and the endophytic bacteria.</div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">33193494</PMID><DateRevised><Year>2020</Year><Month>11</Month><Day>17</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">1664-462X</ISSN><JournalIssue CitedMedium="Print"><Volume>11</Volume><PubDate><Year>2020</Year></PubDate></JournalIssue><Title>Frontiers in plant science</Title><ISOAbbreviation>Front Plant Sci</ISOAbbreviation></Journal><ArticleTitle>Endophyte-Promoted Phosphorus Solubilization in <i>Populus</i>.</ArticleTitle><Pagination><MedlinePgn>567918</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.3389/fpls.2020.567918</ELocationID><Abstract><AbstractText>Phosphorus is one of the essential nutrients for plant growth, but it may be relatively unavailable to plants because of its chemistry. In soil, the majority of phosphorus is present in the form of a phosphate, usually as metal complexes making it bound to minerals or organic matter. Therefore, inorganic phosphate solubilization is an important process of plant growth promotion by plant associated bacteria and fungi. Non-nodulating plant species have been shown to thrive in low-nutrient environments, in some instances by relying on plant associated microorganisms called endophytes. These microorganisms live within the plant and help supply nutrients for the plant. Despite their potential enormous environmental importance, there are a limited number of studies looking at the direct molecular impact of phosphate solubilizing endophytic bacteria on the host plant. In this work, we studied the impact of two endophyte strains of wild poplar (<i>Populus trichocarpa</i>) that solubilize phosphate. Using a combination of x-ray imaging, spectroscopy methods, and proteomics, we report direct evidence of endophyte-promoted phosphorus uptake in poplar. We found that the solubilized phosphate may react and become insoluble once inside plant tissue, suggesting that endophytes may aid in the re-release of phosphate. Using synchrotron x-ray fluorescence spectromicroscopy, we visualized the nutrient phosphorus inside poplar roots inoculated by the selected endophytes and found the phosphorus in both forms of organic and inorganic phosphates inside the root. Tomography-based root imaging revealed a markedly different root biomass and root architecture for poplar samples inoculated with the phosphate solubilizing bacteria strains. Proteomics characterization on poplar roots coupled with protein network analysis revealed novel proteins and metabolic pathways with possible involvement in endophyte enriched phosphorus uptake. These findings suggest an important role of endophytes for phosphorus acquisition and provide a deeper understanding of the critical symbiotic associations between poplar and the endophytic bacteria.</AbstractText><CopyrightInformation>Copyright © 2020 Varga, Hixson, Ahkami, Sher, Barnes, Chu, Battu, Nicora, Winkler, Reno, Fakra, Antipova, Parkinson, Hall and Doty.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Varga</LastName><ForeName>Tamas</ForeName><Initials>T</Initials><AffiliationInfo><Affiliation>Environmental Molecular Sciences Laboratory, Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA, United States.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hixson</LastName><ForeName>Kim K</ForeName><Initials>KK</Initials><AffiliationInfo><Affiliation>Environmental Molecular Sciences Laboratory, Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA, United States.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ahkami</LastName><ForeName>Amir H</ForeName><Initials>AH</Initials><AffiliationInfo><Affiliation>Environmental Molecular Sciences Laboratory, Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA, United States.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sher</LastName><ForeName>Andrew W</ForeName><Initials>AW</Initials><AffiliationInfo><Affiliation>School of Environmental and Forest Sciences, College of the Environment, University of Washington, Seattle, WA, United States.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Barnes</LastName><ForeName>Morgan E</ForeName><Initials>ME</Initials><AffiliationInfo><Affiliation>Environmental Systems Graduate Group, University of California, Merced, Merced, CA, United States.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Chu</LastName><ForeName>Rosalie K</ForeName><Initials>RK</Initials><AffiliationInfo><Affiliation>Environmental Molecular Sciences Laboratory, Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA, United States.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Battu</LastName><ForeName>Anil K</ForeName><Initials>AK</Initials><AffiliationInfo><Affiliation>Environmental Molecular Sciences Laboratory, Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA, United States.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Nicora</LastName><ForeName>Carrie D</ForeName><Initials>CD</Initials><AffiliationInfo><Affiliation>Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA, United States.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Winkler</LastName><ForeName>Tanya E</ForeName><Initials>TE</Initials><AffiliationInfo><Affiliation>Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA, United States.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Reno</LastName><ForeName>Loren R</ForeName><Initials>LR</Initials><AffiliationInfo><Affiliation>Environmental Molecular Sciences Laboratory, Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA, United States.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Fakra</LastName><ForeName>Sirine C</ForeName><Initials>SC</Initials><AffiliationInfo><Affiliation>Advanced Light Source, Lawrence Berkeley National Laboratory, Berkeley, CA, United States.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Antipova</LastName><ForeName>Olga</ForeName><Initials>O</Initials><AffiliationInfo><Affiliation>Advanced Photon Source, Argonne National Laboratory, Lemont, IL, United States.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Parkinson</LastName><ForeName>Dilworth Y</ForeName><Initials>DY</Initials><AffiliationInfo><Affiliation>Advanced Light Source, Lawrence Berkeley National Laboratory, Berkeley, CA, United States.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hall</LastName><ForeName>Jackson R</ForeName><Initials>JR</Initials><AffiliationInfo><Affiliation>School of Environmental and Forest Sciences, College of the Environment, University of Washington, Seattle, WA, United States.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Doty</LastName><ForeName>Sharon L</ForeName><Initials>SL</Initials><AffiliationInfo><Affiliation>School of Environmental and Forest Sciences, College of the Environment, University of Washington, Seattle, WA, United States.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>10</Month><Day>21</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Front Plant Sci</MedlineTA><NlmUniqueID>101568200</NlmUniqueID><ISSNLinking>1664-462X</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Populus</Keyword><Keyword MajorTopicYN="N">endophytes</Keyword><Keyword MajorTopicYN="N">phosphorus</Keyword><Keyword MajorTopicYN="N">poplar</Keyword><Keyword MajorTopicYN="N">solubilization</Keyword><Keyword MajorTopicYN="N">synchrotron x-ray fluorescence</Keyword><Keyword MajorTopicYN="N">x-ray absorption near edge structure</Keyword><Keyword MajorTopicYN="N">x-ray computed tomography</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>06</Month><Day>11</Day></PubMedPubDate><PubMedPubDate 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IdType="pubmed">9449838</ArticleId></ArticleIdList></Reference></ReferenceList></PubmedData></pubmed><affiliations><list><country><li>États-Unis</li></country><region><li>Californie</li><li>Illinois</li><li>Washington (État)</li></region><settlement><li>Seattle</li></settlement><orgName><li>Université de Washington</li></orgName></list><tree><country name="États-Unis"><region name="Washington (État)"><name sortKey="Varga, Tamas" sort="Varga, Tamas" uniqKey="Varga T" first="Tamas" last="Varga">Tamas Varga</name></region><name sortKey="Ahkami, Amir H" sort="Ahkami, Amir H" uniqKey="Ahkami A" first="Amir H" last="Ahkami">Amir H. Ahkami</name><name sortKey="Antipova, Olga" sort="Antipova, Olga" uniqKey="Antipova O" first="Olga" last="Antipova">Olga Antipova</name><name sortKey="Barnes, Morgan E" sort="Barnes, Morgan E" uniqKey="Barnes M" first="Morgan E" last="Barnes">Morgan E. Barnes</name><name sortKey="Battu, Anil K" sort="Battu, Anil K" uniqKey="Battu A" first="Anil K" last="Battu">Anil K. Battu</name><name sortKey="Chu, Rosalie K" sort="Chu, Rosalie K" uniqKey="Chu R" first="Rosalie K" last="Chu">Rosalie K. Chu</name><name sortKey="Doty, Sharon L" sort="Doty, Sharon L" uniqKey="Doty S" first="Sharon L" last="Doty">Sharon L. Doty</name><name sortKey="Fakra, Sirine C" sort="Fakra, Sirine C" uniqKey="Fakra S" first="Sirine C" last="Fakra">Sirine C. Fakra</name><name sortKey="Hall, Jackson R" sort="Hall, Jackson R" uniqKey="Hall J" first="Jackson R" last="Hall">Jackson R. Hall</name><name sortKey="Hixson, Kim K" sort="Hixson, Kim K" uniqKey="Hixson K" first="Kim K" last="Hixson">Kim K. Hixson</name><name sortKey="Nicora, Carrie D" sort="Nicora, Carrie D" uniqKey="Nicora C" first="Carrie D" last="Nicora">Carrie D. Nicora</name><name sortKey="Parkinson, Dilworth Y" sort="Parkinson, Dilworth Y" uniqKey="Parkinson D" first="Dilworth Y" last="Parkinson">Dilworth Y. Parkinson</name><name sortKey="Reno, Loren R" sort="Reno, Loren R" uniqKey="Reno L" first="Loren R" last="Reno">Loren R. Reno</name><name sortKey="Sher, Andrew W" sort="Sher, Andrew W" uniqKey="Sher A" first="Andrew W" last="Sher">Andrew W. Sher</name><name sortKey="Winkler, Tanya E" sort="Winkler, Tanya E" uniqKey="Winkler T" first="Tanya E" last="Winkler">Tanya E. Winkler</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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