Chitotetraose activates the fungal-dependent endosymbiotic signaling pathway in actinorhizal plant species.
Identifieur interne : 000301 ( Main/Corpus ); précédent : 000300; suivant : 000302Chitotetraose activates the fungal-dependent endosymbiotic signaling pathway in actinorhizal plant species.
Auteurs : Mireille Chabaud ; Joëlle Fournier ; Lukas Brichet ; Iltaf Abdou-Pavy ; Leandro Imanishi ; Laurent Brottier ; Elodie Pirolles ; Valérie Hocher ; Claudine Franche ; Didier Bogusz ; Luis G. Wall ; Sergio Svistoonoff ; Hassen Gherbi ; David G. BarkerSource :
- PloS one [ 1932-6203 ] ; 2019.
English descriptors
- KwdEn :
- Fabaceae (genetics), Fabaceae (growth & development), Fabaceae (microbiology), Fagales (genetics), Fagales (growth & development), Fagales (microbiology), Frankia (genetics), Frankia (growth & development), Frankia (metabolism), Mycorrhizae (growth & development), Mycorrhizae (metabolism), Nitrogen Fixation (genetics), Oligosaccharides (genetics), Plant Root Nodulation (genetics), Plant Roots (genetics), Plant Roots (growth & development), Plant Roots (microbiology), Signal Transduction (genetics), Symbiosis (genetics).
- MESH :
- chemical , genetics : Oligosaccharides.
- genetics : Fabaceae, Fagales, Frankia, Nitrogen Fixation, Plant Root Nodulation, Plant Roots, Signal Transduction, Symbiosis.
- growth & development : Fabaceae, Fagales, Frankia, Mycorrhizae, Plant Roots.
- metabolism : Frankia, Mycorrhizae.
- microbiology : Fabaceae, Fagales, Plant Roots.
Abstract
Mutualistic plant-microbe associations are widespread in natural ecosystems and have made major contributions throughout the evolutionary history of terrestrial plants. Amongst the most remarkable of these are the so-called root endosymbioses, resulting from the intracellular colonization of host tissues by either arbuscular mycorrhizal (AM) fungi or nitrogen-fixing bacteria that both provide key nutrients to the host in exchange for energy-rich photosynthates. Actinorhizal host plants, members of the Eurosid 1 clade, are able to associate with both AM fungi and nitrogen-fixing actinomycetes known as Frankia. Currently, little is known about the molecular signaling that allows these plants to recognize their fungal and bacterial partners. In this article, we describe the use of an in vivo Ca2+ reporter to identify symbiotic signaling responses to AM fungi in roots of both Casuarina glauca and Discaria trinervis, actinorhizal species with contrasting modes of Frankia colonization. This approach has revealed that, for both actinorhizal hosts, the short-chain chitin oligomer chitotetraose is able to mimic AM fungal exudates in activating the conserved symbiosis signaling pathway (CSSP) in epidermal root cells targeted by AM fungi. These results mirror findings in other AM host plants including legumes and the monocot rice. In addition, we show that chitotetraose is a more efficient elicitor of CSSP activation compared to AM fungal lipo-chitooligosaccharides. These findings reinforce the likely role of short-chain chitin oligomers during the initial stages of the AM association, and are discussed in relation to both our current knowledge about molecular signaling during Frankia recognition as well as the different microsymbiont root colonization mechanisms employed by actinorhizal hosts.
DOI: 10.1371/journal.pone.0223149
PubMed: 31600251
PubMed Central: PMC6786586
Links to Exploration step
pubmed:31600251Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Chitotetraose activates the fungal-dependent endosymbiotic signaling pathway in actinorhizal plant species.</title><author><name sortKey="Chabaud, Mireille" sort="Chabaud, Mireille" uniqKey="Chabaud M" first="Mireille" last="Chabaud">Mireille Chabaud</name><affiliation><nlm:affiliation>Laboratory of Plant-Microbe Interactions (INRA/CNRS/University of Toulouse), Castanet-Tolosan, France.</nlm:affiliation></affiliation></author><author><name sortKey="Fournier, Joelle" sort="Fournier, Joelle" uniqKey="Fournier J" first="Joëlle" last="Fournier">Joëlle Fournier</name><affiliation><nlm:affiliation>Laboratory of Plant-Microbe Interactions (INRA/CNRS/University of Toulouse), Castanet-Tolosan, France.</nlm:affiliation></affiliation></author><author><name sortKey="Brichet, Lukas" sort="Brichet, Lukas" uniqKey="Brichet L" first="Lukas" last="Brichet">Lukas Brichet</name><affiliation><nlm:affiliation>Laboratory of Plant-Microbe Interactions (INRA/CNRS/University of Toulouse), Castanet-Tolosan, France.</nlm:affiliation></affiliation></author><author><name sortKey="Abdou Pavy, Iltaf" sort="Abdou Pavy, Iltaf" uniqKey="Abdou Pavy I" first="Iltaf" last="Abdou-Pavy">Iltaf Abdou-Pavy</name><affiliation><nlm:affiliation>Laboratory of Plant-Microbe Interactions (INRA/CNRS/University of Toulouse), Castanet-Tolosan, France.</nlm:affiliation></affiliation></author><author><name sortKey="Imanishi, Leandro" sort="Imanishi, Leandro" uniqKey="Imanishi L" first="Leandro" last="Imanishi">Leandro Imanishi</name><affiliation><nlm:affiliation>Laboratory of Biochemistry, Microbiology and Soil Biological Interactions, Department of Science and Technology, National University of Quilmes, CONICET, Bernal, Argentina.</nlm:affiliation></affiliation></author><author><name sortKey="Brottier, Laurent" sort="Brottier, Laurent" uniqKey="Brottier L" first="Laurent" last="Brottier">Laurent Brottier</name><affiliation><nlm:affiliation>Laboratory of Tropical and Mediterranean Symbioses (IRD/INRA/CIRAD/University of Montpellier/Supagro), Montpellier, France.</nlm:affiliation></affiliation></author><author><name sortKey="Pirolles, Elodie" sort="Pirolles, Elodie" uniqKey="Pirolles E" first="Elodie" last="Pirolles">Elodie Pirolles</name><affiliation><nlm:affiliation>Laboratory of Tropical and Mediterranean Symbioses (IRD/INRA/CIRAD/University of Montpellier/Supagro), Montpellier, France.</nlm:affiliation></affiliation></author><author><name sortKey="Hocher, Valerie" sort="Hocher, Valerie" uniqKey="Hocher V" first="Valérie" last="Hocher">Valérie Hocher</name><affiliation><nlm:affiliation>Laboratory of Tropical and Mediterranean Symbioses (IRD/INRA/CIRAD/University of Montpellier/Supagro), Montpellier, France.</nlm:affiliation></affiliation></author><author><name sortKey="Franche, Claudine" sort="Franche, Claudine" uniqKey="Franche C" first="Claudine" last="Franche">Claudine Franche</name><affiliation><nlm:affiliation>Plant Diversity, Adaptation and Development (IRD/University of Montpellier), Montpellier, France.</nlm:affiliation></affiliation></author><author><name sortKey="Bogusz, Didier" sort="Bogusz, Didier" uniqKey="Bogusz D" first="Didier" last="Bogusz">Didier Bogusz</name><affiliation><nlm:affiliation>Plant Diversity, Adaptation and Development (IRD/University of Montpellier), Montpellier, France.</nlm:affiliation></affiliation></author><author><name sortKey="Wall, Luis G" sort="Wall, Luis G" uniqKey="Wall L" first="Luis G" last="Wall">Luis G. 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Barker</name><affiliation><nlm:affiliation>Laboratory of Plant-Microbe Interactions (INRA/CNRS/University of Toulouse), Castanet-Tolosan, France.</nlm:affiliation></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2019">2019</date><idno type="RBID">pubmed:31600251</idno><idno type="pmid">31600251</idno><idno type="doi">10.1371/journal.pone.0223149</idno><idno type="pmc">PMC6786586</idno><idno type="wicri:Area/Main/Corpus">000301</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000301</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Chitotetraose activates the fungal-dependent endosymbiotic signaling pathway in actinorhizal plant species.</title><author><name sortKey="Chabaud, Mireille" sort="Chabaud, Mireille" uniqKey="Chabaud M" first="Mireille" last="Chabaud">Mireille Chabaud</name><affiliation><nlm:affiliation>Laboratory of Plant-Microbe Interactions (INRA/CNRS/University of Toulouse), Castanet-Tolosan, France.</nlm:affiliation></affiliation></author><author><name sortKey="Fournier, Joelle" sort="Fournier, Joelle" uniqKey="Fournier J" first="Joëlle" last="Fournier">Joëlle Fournier</name><affiliation><nlm:affiliation>Laboratory of Plant-Microbe Interactions (INRA/CNRS/University of Toulouse), Castanet-Tolosan, France.</nlm:affiliation></affiliation></author><author><name sortKey="Brichet, Lukas" sort="Brichet, Lukas" uniqKey="Brichet L" first="Lukas" last="Brichet">Lukas Brichet</name><affiliation><nlm:affiliation>Laboratory of Plant-Microbe Interactions (INRA/CNRS/University of Toulouse), Castanet-Tolosan, France.</nlm:affiliation></affiliation></author><author><name sortKey="Abdou Pavy, Iltaf" sort="Abdou Pavy, Iltaf" uniqKey="Abdou Pavy I" first="Iltaf" last="Abdou-Pavy">Iltaf Abdou-Pavy</name><affiliation><nlm:affiliation>Laboratory of Plant-Microbe Interactions (INRA/CNRS/University of Toulouse), Castanet-Tolosan, France.</nlm:affiliation></affiliation></author><author><name sortKey="Imanishi, Leandro" sort="Imanishi, Leandro" uniqKey="Imanishi L" first="Leandro" last="Imanishi">Leandro Imanishi</name><affiliation><nlm:affiliation>Laboratory of Biochemistry, Microbiology and Soil Biological Interactions, Department of Science and Technology, National University of Quilmes, CONICET, Bernal, Argentina.</nlm:affiliation></affiliation></author><author><name sortKey="Brottier, Laurent" sort="Brottier, Laurent" uniqKey="Brottier L" first="Laurent" last="Brottier">Laurent Brottier</name><affiliation><nlm:affiliation>Laboratory of Tropical and Mediterranean Symbioses (IRD/INRA/CIRAD/University of Montpellier/Supagro), Montpellier, France.</nlm:affiliation></affiliation></author><author><name sortKey="Pirolles, Elodie" sort="Pirolles, Elodie" uniqKey="Pirolles E" first="Elodie" last="Pirolles">Elodie Pirolles</name><affiliation><nlm:affiliation>Laboratory of Tropical and Mediterranean Symbioses (IRD/INRA/CIRAD/University of Montpellier/Supagro), Montpellier, France.</nlm:affiliation></affiliation></author><author><name sortKey="Hocher, Valerie" sort="Hocher, Valerie" uniqKey="Hocher V" first="Valérie" last="Hocher">Valérie Hocher</name><affiliation><nlm:affiliation>Laboratory of Tropical and Mediterranean Symbioses (IRD/INRA/CIRAD/University of Montpellier/Supagro), Montpellier, France.</nlm:affiliation></affiliation></author><author><name sortKey="Franche, Claudine" sort="Franche, Claudine" uniqKey="Franche C" first="Claudine" last="Franche">Claudine Franche</name><affiliation><nlm:affiliation>Plant Diversity, Adaptation and Development (IRD/University of Montpellier), Montpellier, France.</nlm:affiliation></affiliation></author><author><name sortKey="Bogusz, Didier" sort="Bogusz, Didier" uniqKey="Bogusz D" first="Didier" last="Bogusz">Didier Bogusz</name><affiliation><nlm:affiliation>Plant Diversity, Adaptation and Development (IRD/University of Montpellier), Montpellier, France.</nlm:affiliation></affiliation></author><author><name sortKey="Wall, Luis G" sort="Wall, Luis G" uniqKey="Wall L" first="Luis G" last="Wall">Luis G. Wall</name><affiliation><nlm:affiliation>Laboratory of Biochemistry, Microbiology and Soil Biological Interactions, Department of Science and Technology, National University of Quilmes, CONICET, Bernal, Argentina.</nlm:affiliation></affiliation></author><author><name sortKey="Svistoonoff, Sergio" sort="Svistoonoff, Sergio" uniqKey="Svistoonoff S" first="Sergio" last="Svistoonoff">Sergio Svistoonoff</name><affiliation><nlm:affiliation>Laboratory of Tropical and Mediterranean Symbioses (IRD/INRA/CIRAD/University of Montpellier/Supagro), Montpellier, France.</nlm:affiliation></affiliation></author><author><name sortKey="Gherbi, Hassen" sort="Gherbi, Hassen" uniqKey="Gherbi H" first="Hassen" last="Gherbi">Hassen Gherbi</name><affiliation><nlm:affiliation>Laboratory of Tropical and Mediterranean Symbioses (IRD/INRA/CIRAD/University of Montpellier/Supagro), Montpellier, France.</nlm:affiliation></affiliation></author><author><name sortKey="Barker, David G" sort="Barker, David G" uniqKey="Barker D" first="David G" last="Barker">David G. Barker</name><affiliation><nlm:affiliation>Laboratory of Plant-Microbe Interactions (INRA/CNRS/University of Toulouse), Castanet-Tolosan, France.</nlm:affiliation></affiliation></author></analytic><series><title level="j">PloS one</title><idno type="eISSN">1932-6203</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Fabaceae (genetics)</term><term>Fabaceae (growth & development)</term><term>Fabaceae (microbiology)</term><term>Fagales (genetics)</term><term>Fagales (growth & development)</term><term>Fagales (microbiology)</term><term>Frankia (genetics)</term><term>Frankia (growth & development)</term><term>Frankia (metabolism)</term><term>Mycorrhizae (growth & development)</term><term>Mycorrhizae (metabolism)</term><term>Nitrogen Fixation (genetics)</term><term>Oligosaccharides (genetics)</term><term>Plant Root Nodulation (genetics)</term><term>Plant Roots (genetics)</term><term>Plant Roots (growth & development)</term><term>Plant Roots (microbiology)</term><term>Signal Transduction (genetics)</term><term>Symbiosis (genetics)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Oligosaccharides</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Fabaceae</term><term>Fagales</term><term>Frankia</term><term>Nitrogen Fixation</term><term>Plant Root Nodulation</term><term>Plant Roots</term><term>Signal Transduction</term><term>Symbiosis</term></keywords><keywords scheme="MESH" qualifier="growth & development" xml:lang="en"><term>Fabaceae</term><term>Fagales</term><term>Frankia</term><term>Mycorrhizae</term><term>Plant Roots</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Frankia</term><term>Mycorrhizae</term></keywords><keywords scheme="MESH" qualifier="microbiology" xml:lang="en"><term>Fabaceae</term><term>Fagales</term><term>Plant Roots</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Mutualistic plant-microbe associations are widespread in natural ecosystems and have made major contributions throughout the evolutionary history of terrestrial plants. Amongst the most remarkable of these are the so-called root endosymbioses, resulting from the intracellular colonization of host tissues by either arbuscular mycorrhizal (AM) fungi or nitrogen-fixing bacteria that both provide key nutrients to the host in exchange for energy-rich photosynthates. Actinorhizal host plants, members of the Eurosid 1 clade, are able to associate with both AM fungi and nitrogen-fixing actinomycetes known as Frankia. Currently, little is known about the molecular signaling that allows these plants to recognize their fungal and bacterial partners. In this article, we describe the use of an in vivo Ca2+ reporter to identify symbiotic signaling responses to AM fungi in roots of both Casuarina glauca and Discaria trinervis, actinorhizal species with contrasting modes of Frankia colonization. This approach has revealed that, for both actinorhizal hosts, the short-chain chitin oligomer chitotetraose is able to mimic AM fungal exudates in activating the conserved symbiosis signaling pathway (CSSP) in epidermal root cells targeted by AM fungi. These results mirror findings in other AM host plants including legumes and the monocot rice. In addition, we show that chitotetraose is a more efficient elicitor of CSSP activation compared to AM fungal lipo-chitooligosaccharides. These findings reinforce the likely role of short-chain chitin oligomers during the initial stages of the AM association, and are discussed in relation to both our current knowledge about molecular signaling during Frankia recognition as well as the different microsymbiont root colonization mechanisms employed by actinorhizal hosts.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">31600251</PMID><DateCompleted><Year>2020</Year><Month>03</Month><Day>12</Day></DateCompleted><DateRevised><Year>2020</Year><Month>03</Month><Day>12</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Electronic">1932-6203</ISSN><JournalIssue CitedMedium="Internet"><Volume>14</Volume><Issue>10</Issue><PubDate><Year>2019</Year></PubDate></JournalIssue><Title>PloS one</Title><ISOAbbreviation>PLoS One</ISOAbbreviation></Journal><ArticleTitle>Chitotetraose activates the fungal-dependent endosymbiotic signaling pathway in actinorhizal plant species.</ArticleTitle><Pagination><MedlinePgn>e0223149</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1371/journal.pone.0223149</ELocationID><Abstract><AbstractText>Mutualistic plant-microbe associations are widespread in natural ecosystems and have made major contributions throughout the evolutionary history of terrestrial plants. Amongst the most remarkable of these are the so-called root endosymbioses, resulting from the intracellular colonization of host tissues by either arbuscular mycorrhizal (AM) fungi or nitrogen-fixing bacteria that both provide key nutrients to the host in exchange for energy-rich photosynthates. Actinorhizal host plants, members of the Eurosid 1 clade, are able to associate with both AM fungi and nitrogen-fixing actinomycetes known as Frankia. Currently, little is known about the molecular signaling that allows these plants to recognize their fungal and bacterial partners. In this article, we describe the use of an in vivo Ca2+ reporter to identify symbiotic signaling responses to AM fungi in roots of both Casuarina glauca and Discaria trinervis, actinorhizal species with contrasting modes of Frankia colonization. This approach has revealed that, for both actinorhizal hosts, the short-chain chitin oligomer chitotetraose is able to mimic AM fungal exudates in activating the conserved symbiosis signaling pathway (CSSP) in epidermal root cells targeted by AM fungi. These results mirror findings in other AM host plants including legumes and the monocot rice. In addition, we show that chitotetraose is a more efficient elicitor of CSSP activation compared to AM fungal lipo-chitooligosaccharides. These findings reinforce the likely role of short-chain chitin oligomers during the initial stages of the AM association, and are discussed in relation to both our current knowledge about molecular signaling during Frankia recognition as well as the different microsymbiont root colonization mechanisms employed by actinorhizal hosts.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Chabaud</LastName><ForeName>Mireille</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Laboratory of Plant-Microbe Interactions (INRA/CNRS/University of Toulouse), Castanet-Tolosan, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Fournier</LastName><ForeName>Joëlle</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Laboratory of Plant-Microbe Interactions (INRA/CNRS/University of Toulouse), Castanet-Tolosan, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Brichet</LastName><ForeName>Lukas</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Laboratory of Plant-Microbe Interactions (INRA/CNRS/University of Toulouse), Castanet-Tolosan, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Abdou-Pavy</LastName><ForeName>Iltaf</ForeName><Initials>I</Initials><AffiliationInfo><Affiliation>Laboratory of Plant-Microbe Interactions (INRA/CNRS/University of Toulouse), Castanet-Tolosan, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Imanishi</LastName><ForeName>Leandro</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Laboratory of Biochemistry, Microbiology and Soil Biological Interactions, Department of Science and Technology, National University of Quilmes, CONICET, Bernal, Argentina.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Brottier</LastName><ForeName>Laurent</ForeName><Initials>L</Initials><Identifier Source="ORCID">0000-0002-8584-2199</Identifier><AffiliationInfo><Affiliation>Laboratory of Tropical and Mediterranean Symbioses (IRD/INRA/CIRAD/University of Montpellier/Supagro), Montpellier, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Pirolles</LastName><ForeName>Elodie</ForeName><Initials>E</Initials><AffiliationInfo><Affiliation>Laboratory of Tropical and Mediterranean Symbioses (IRD/INRA/CIRAD/University of Montpellier/Supagro), Montpellier, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hocher</LastName><ForeName>Valérie</ForeName><Initials>V</Initials><AffiliationInfo><Affiliation>Laboratory of Tropical and Mediterranean Symbioses (IRD/INRA/CIRAD/University of Montpellier/Supagro), Montpellier, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Franche</LastName><ForeName>Claudine</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Plant Diversity, Adaptation and Development (IRD/University of Montpellier), Montpellier, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bogusz</LastName><ForeName>Didier</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Plant Diversity, Adaptation and Development (IRD/University of Montpellier), Montpellier, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wall</LastName><ForeName>Luis G</ForeName><Initials>LG</Initials><Identifier Source="ORCID">0000-0003-0880-8023</Identifier><AffiliationInfo><Affiliation>Laboratory of Biochemistry, Microbiology and Soil Biological Interactions, Department of Science and Technology, National University of Quilmes, CONICET, Bernal, Argentina.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Svistoonoff</LastName><ForeName>Sergio</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Laboratory of Tropical and Mediterranean Symbioses (IRD/INRA/CIRAD/University of Montpellier/Supagro), Montpellier, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gherbi</LastName><ForeName>Hassen</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Laboratory of Tropical and Mediterranean Symbioses (IRD/INRA/CIRAD/University of Montpellier/Supagro), Montpellier, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Barker</LastName><ForeName>David G</ForeName><Initials>DG</Initials><Identifier Source="ORCID">0000-0001-6361-119X</Identifier><AffiliationInfo><Affiliation>Laboratory of Plant-Microbe Interactions (INRA/CNRS/University of Toulouse), Castanet-Tolosan, France.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>10</Month><Day>10</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>PLoS One</MedlineTA><NlmUniqueID>101285081</NlmUniqueID><ISSNLinking>1932-6203</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D009844">Oligosaccharides</NameOfSubstance></Chemical><Chemical><RegistryNumber>5567-52-2</RegistryNumber><NameOfSubstance UI="C012238">chitotetrose</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D007887" MajorTopicYN="N">Fabaceae</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000254" MajorTopicYN="N">growth & development</QualifierName><QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D000073567" MajorTopicYN="N">Fagales</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName><QualifierName UI="Q000254" MajorTopicYN="N">growth & development</QualifierName><QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D040161" MajorTopicYN="N">Frankia</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName><QualifierName UI="Q000254" MajorTopicYN="N">growth & development</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D038821" MajorTopicYN="N">Mycorrhizae</DescriptorName><QualifierName UI="Q000254" MajorTopicYN="N">growth & development</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D009586" MajorTopicYN="N">Nitrogen Fixation</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D009844" MajorTopicYN="N">Oligosaccharides</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D055170" MajorTopicYN="N">Plant Root Nodulation</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D018517" MajorTopicYN="N">Plant Roots</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000254" MajorTopicYN="N">growth & development</QualifierName><QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D015398" MajorTopicYN="N">Signal Transduction</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D013559" MajorTopicYN="N">Symbiosis</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName></MeshHeading></MeshHeadingList><CoiStatement>The authors have declared that no competing interests exist.</CoiStatement></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>05</Month><Day>29</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2019</Year><Month>09</Month><Day>13</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2019</Year><Month>10</Month><Day>11</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2019</Year><Month>10</Month><Day>11</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>3</Month><Day>13</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">31600251</ArticleId><ArticleId 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