AP2 transcription factor CBX1 with a specific function in symbiotic exchange of nutrients in mycorrhizal Lotus japonicus.
Identifieur interne : 000750 ( Main/Curation ); précédent : 000749; suivant : 000751AP2 transcription factor CBX1 with a specific function in symbiotic exchange of nutrients in mycorrhizal Lotus japonicus.
Auteurs : Li Xue [Allemagne] ; Lompong Klinnawee [Allemagne] ; Yue Zhou [Allemagne] ; Georgios Saridis [Allemagne] ; Vinod Vijayakumar [Allemagne, États-Unis] ; Mathias Brands [Allemagne] ; Peter Dörmann [Allemagne] ; Tamara Gigolashvili [Allemagne] ; Franziska Turck [Allemagne] ; Marcel Bucher [Allemagne]Source :
- Proceedings of the National Academy of Sciences of the United States of America [ 1091-6490 ] ; 2018.
Descripteurs français
- KwdFr :
- Facteurs de transcription (métabolisme), Loteae (génétique), Loteae (microbiologie), Loteae (métabolisme), Mycorhizes (génétique), Mycorhizes (métabolisme), Phosphates (métabolisme), Proton-Translocating ATPases (métabolisme), Protéines de transport du phosphate (métabolisme), Protéines fongiques (métabolisme), Symbiose (génétique).
- MESH :
- génétique : Loteae, Mycorhizes, Symbiose.
- microbiologie : Loteae.
- métabolisme : Facteurs de transcription, Loteae, Mycorhizes, Phosphates, Proton-Translocating ATPases, Protéines de transport du phosphate, Protéines fongiques.
English descriptors
- KwdEn :
- Fungal Proteins (metabolism), Lotus (genetics), Lotus (metabolism), Lotus (microbiology), Mycorrhizae (genetics), Mycorrhizae (metabolism), Phosphate Transport Proteins (metabolism), Phosphates (metabolism), Proton-Translocating ATPases (metabolism), Symbiosis (genetics), Transcription Factors (metabolism).
- MESH :
- chemical , metabolism : Fungal Proteins, Phosphate Transport Proteins, Phosphates, Proton-Translocating ATPases, Transcription Factors.
- genetics : Lotus, Mycorrhizae, Symbiosis.
- metabolism : Lotus, Mycorrhizae.
- microbiology : Lotus.
Abstract
The arbuscular mycorrhizal (AM) symbiosis, a widespread mutualistic association between land plants and fungi, depends on reciprocal exchange of phosphorus driven by proton-coupled phosphate uptake into host plants and carbon supplied to AM fungi by host-dependent sugar and lipid biosynthesis. The molecular mechanisms and cis-regulatory modules underlying the control of phosphate uptake and de novo fatty acid synthesis in AM symbiosis are poorly understood. Here, we show that the AP2 family transcription factor CTTC MOTIF-BINDING TRANSCRIPTION FACTOR1 (CBX1), a WRINKLED1 (WRI1) homolog, directly binds the evolutionary conserved CTTC motif that is enriched in mycorrhiza-regulated genes and activates Lotus japonicus phosphate transporter 4 (LjPT4) in vivo and in vitro. Moreover, the mycorrhiza-inducible gene encoding H+-ATPase (LjHA1), implicated in energizing nutrient uptake at the symbiotic interface across the periarbuscular membrane, is coregulated with LjPT4 by CBX1. Accordingly, CBX1-defective mutants show reduced mycorrhizal colonization. Furthermore, genome-wide-binding profiles, DNA-binding studies, and heterologous expression reveal additional binding of CBX1 to AW box, the consensus DNA-binding motif for WRI1, that is enriched in promoters of glycolysis and fatty acid biosynthesis genes. We show that CBX1 activates expression of lipid metabolic genes including glycerol-3-phosphate acyltransferase RAM2 implicated in acylglycerol biosynthesis. Our finding defines the role of CBX1 as a regulator of host genes involved in phosphate uptake and lipid synthesis through binding to the CTTC/AW molecular module, and supports a model underlying bidirectional exchange of phosphorus and carbon, a fundamental trait in the mutualistic AM symbiosis.
DOI: 10.1073/pnas.1812275115
PubMed: 30209216
PubMed Central: PMC6166803
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Xue</name><affiliation wicri:level="1"><nlm:affiliation>Botanical Institute, Cologne Biocenter, Cluster of Excellence on Plant Sciences, University of Cologne, D-50674 Cologne, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Botanical Institute, Cologne Biocenter, Cluster of Excellence on Plant Sciences, University of Cologne, D-50674 Cologne</wicri:regionArea></affiliation></author><author><name sortKey="Klinnawee, Lompong" sort="Klinnawee, Lompong" uniqKey="Klinnawee L" first="Lompong" last="Klinnawee">Lompong Klinnawee</name><affiliation wicri:level="1"><nlm:affiliation>Botanical Institute, Cologne Biocenter, Cluster of Excellence on Plant Sciences, University of Cologne, D-50674 Cologne, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Botanical Institute, Cologne Biocenter, Cluster of Excellence on Plant Sciences, University of Cologne, D-50674 Cologne</wicri:regionArea></affiliation></author><author><name sortKey="Zhou, Yue" sort="Zhou, Yue" uniqKey="Zhou Y" first="Yue" last="Zhou">Yue Zhou</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Developmental Biology, Max Planck Institute for Plant Breeding Research, D-50829 Cologne, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Plant Developmental Biology, Max Planck Institute for Plant Breeding Research, D-50829 Cologne</wicri:regionArea></affiliation></author><author><name sortKey="Saridis, Georgios" sort="Saridis, Georgios" uniqKey="Saridis G" first="Georgios" last="Saridis">Georgios Saridis</name><affiliation wicri:level="1"><nlm:affiliation>Botanical Institute, Cologne Biocenter, Cluster of Excellence on Plant Sciences, University of Cologne, D-50674 Cologne, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Botanical Institute, Cologne Biocenter, Cluster of Excellence on Plant Sciences, University of Cologne, D-50674 Cologne</wicri:regionArea></affiliation></author><author><name sortKey="Vijayakumar, Vinod" sort="Vijayakumar, Vinod" uniqKey="Vijayakumar V" first="Vinod" last="Vijayakumar">Vinod Vijayakumar</name><affiliation wicri:level="1"><nlm:affiliation>Botanical Institute, Cologne Biocenter, Cluster of Excellence on Plant Sciences, University of Cologne, D-50674 Cologne, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Botanical Institute, Cologne Biocenter, Cluster of Excellence on Plant Sciences, University of Cologne, D-50674 Cologne</wicri:regionArea></affiliation><affiliation wicri:level="2"><nlm:affiliation>Department of Plant Pathology, The Ohio State University, Columbus, OH 43210.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Ohio</region></placeName><wicri:cityArea>Department of Plant Pathology, The Ohio State University, Columbus</wicri:cityArea></affiliation></author><author><name sortKey="Brands, Mathias" sort="Brands, Mathias" uniqKey="Brands M" first="Mathias" last="Brands">Mathias Brands</name><affiliation wicri:level="1"><nlm:affiliation>Department of Molecular Biotechnology, Institute of Molecular Physiology and Biotechnology of Plants, University of Bonn, 53115 Bonn, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Molecular Biotechnology, Institute of Molecular Physiology and Biotechnology of Plants, University of Bonn, 53115 Bonn</wicri:regionArea></affiliation></author><author><name sortKey="Dormann, Peter" sort="Dormann, Peter" uniqKey="Dormann P" first="Peter" last="Dörmann">Peter Dörmann</name><affiliation wicri:level="1"><nlm:affiliation>Department of Molecular Biotechnology, Institute of Molecular Physiology and Biotechnology of Plants, University of Bonn, 53115 Bonn, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Molecular Biotechnology, Institute of Molecular Physiology and Biotechnology of Plants, University of Bonn, 53115 Bonn</wicri:regionArea></affiliation></author><author><name sortKey="Gigolashvili, Tamara" sort="Gigolashvili, Tamara" uniqKey="Gigolashvili T" first="Tamara" last="Gigolashvili">Tamara Gigolashvili</name><affiliation wicri:level="1"><nlm:affiliation>Botanical Institute, Cologne Biocenter, Cluster of Excellence on Plant Sciences, University of Cologne, D-50674 Cologne, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Botanical Institute, Cologne Biocenter, Cluster of Excellence on Plant Sciences, University of Cologne, D-50674 Cologne</wicri:regionArea></affiliation></author><author><name sortKey="Turck, Franziska" sort="Turck, Franziska" uniqKey="Turck F" first="Franziska" last="Turck">Franziska Turck</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Developmental Biology, Max Planck Institute for Plant Breeding Research, D-50829 Cologne, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Plant Developmental Biology, Max Planck Institute for Plant Breeding Research, D-50829 Cologne</wicri:regionArea></affiliation></author><author><name sortKey="Bucher, Marcel" sort="Bucher, Marcel" uniqKey="Bucher M" first="Marcel" last="Bucher">Marcel Bucher</name><affiliation wicri:level="1"><nlm:affiliation>Botanical Institute, Cologne Biocenter, Cluster of Excellence on Plant Sciences, University of Cologne, D-50674 Cologne, Germany; m.bucher@uni-koeln.de.</nlm:affiliation><country wicri:rule="url">Allemagne</country><wicri:regionArea>Botanical Institute, Cologne Biocenter, Cluster of Excellence on Plant Sciences, University of Cologne, D-50674 Cologne</wicri:regionArea></affiliation></author></analytic><series><title level="j">Proceedings of the National Academy of Sciences of the United States of America</title><idno type="eISSN">1091-6490</idno><imprint><date when="2018" type="published">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Fungal Proteins (metabolism)</term><term>Lotus (genetics)</term><term>Lotus (metabolism)</term><term>Lotus (microbiology)</term><term>Mycorrhizae (genetics)</term><term>Mycorrhizae (metabolism)</term><term>Phosphate Transport Proteins (metabolism)</term><term>Phosphates (metabolism)</term><term>Proton-Translocating ATPases (metabolism)</term><term>Symbiosis (genetics)</term><term>Transcription Factors (metabolism)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Facteurs de transcription (métabolisme)</term><term>Loteae (génétique)</term><term>Loteae (microbiologie)</term><term>Loteae (métabolisme)</term><term>Mycorhizes (génétique)</term><term>Mycorhizes (métabolisme)</term><term>Phosphates (métabolisme)</term><term>Proton-Translocating ATPases (métabolisme)</term><term>Protéines de transport du phosphate (métabolisme)</term><term>Protéines fongiques (métabolisme)</term><term>Symbiose (génétique)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Fungal Proteins</term><term>Phosphate Transport Proteins</term><term>Phosphates</term><term>Proton-Translocating ATPases</term><term>Transcription Factors</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Lotus</term><term>Mycorrhizae</term><term>Symbiosis</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Loteae</term><term>Mycorhizes</term><term>Symbiose</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Lotus</term><term>Mycorrhizae</term></keywords><keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr"><term>Loteae</term></keywords><keywords scheme="MESH" qualifier="microbiology" xml:lang="en"><term>Lotus</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Facteurs de transcription</term><term>Loteae</term><term>Mycorhizes</term><term>Phosphates</term><term>Proton-Translocating ATPases</term><term>Protéines de transport du phosphate</term><term>Protéines fongiques</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">The arbuscular mycorrhizal (AM) symbiosis, a widespread mutualistic association between land plants and fungi, depends on reciprocal exchange of phosphorus driven by proton-coupled phosphate uptake into host plants and carbon supplied to AM fungi by host-dependent sugar and lipid biosynthesis. The molecular mechanisms and <i>cis</i>-regulatory modules underlying the control of phosphate uptake and de novo fatty acid synthesis in AM symbiosis are poorly understood. Here, we show that the AP2 family transcription factor CTTC MOTIF-BINDING TRANSCRIPTION FACTOR1 (CBX1), a WRINKLED1 (WRI1) homolog, directly binds the evolutionary conserved CTTC motif that is enriched in mycorrhiza-regulated genes and activates <i>Lotus japonicus</i> phosphate transporter 4 (<i>LjPT4</i>) in vivo and in vitro. Moreover, the mycorrhiza-inducible gene encoding H<sup>+</sup>-ATPase (<i>LjHA1</i>), implicated in energizing nutrient uptake at the symbiotic interface across the periarbuscular membrane, is coregulated with <i>LjPT4</i> by CBX1. Accordingly, <i>CBX1</i>-defective mutants show reduced mycorrhizal colonization. Furthermore, genome-wide-binding profiles, DNA-binding studies, and heterologous expression reveal additional binding of CBX1 to AW box, the consensus DNA-binding motif for WRI1, that is enriched in promoters of glycolysis and fatty acid biosynthesis genes. We show that CBX1 activates expression of lipid metabolic genes including glycerol-3-phosphate acyltransferase <i>RAM2</i> implicated in acylglycerol biosynthesis. Our finding defines the role of CBX1 as a regulator of host genes involved in phosphate uptake and lipid synthesis through binding to the CTTC/AW molecular module, and supports a model underlying bidirectional exchange of phosphorus and carbon, a fundamental trait in the mutualistic AM symbiosis.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">30209216</PMID><DateCompleted><Year>2018</Year><Month>10</Month><Day>22</Day></DateCompleted><DateRevised><Year>2018</Year><Month>12</Month><Day>02</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1091-6490</ISSN><JournalIssue CitedMedium="Internet"><Volume>115</Volume><Issue>39</Issue><PubDate><Year>2018</Year><Month>09</Month><Day>25</Day></PubDate></JournalIssue><Title>Proceedings of the National Academy of Sciences of the United States of America</Title><ISOAbbreviation>Proc Natl Acad Sci U S A</ISOAbbreviation></Journal><ArticleTitle>AP2 transcription factor CBX1 with a specific function in symbiotic exchange of nutrients in mycorrhizal <i>Lotus japonicus</i>.</ArticleTitle><Pagination><MedlinePgn>E9239-E9246</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1073/pnas.1812275115</ELocationID><Abstract><AbstractText>The arbuscular mycorrhizal (AM) symbiosis, a widespread mutualistic association between land plants and fungi, depends on reciprocal exchange of phosphorus driven by proton-coupled phosphate uptake into host plants and carbon supplied to AM fungi by host-dependent sugar and lipid biosynthesis. The molecular mechanisms and <i>cis</i>-regulatory modules underlying the control of phosphate uptake and de novo fatty acid synthesis in AM symbiosis are poorly understood. Here, we show that the AP2 family transcription factor CTTC MOTIF-BINDING TRANSCRIPTION FACTOR1 (CBX1), a WRINKLED1 (WRI1) homolog, directly binds the evolutionary conserved CTTC motif that is enriched in mycorrhiza-regulated genes and activates <i>Lotus japonicus</i> phosphate transporter 4 (<i>LjPT4</i>) in vivo and in vitro. Moreover, the mycorrhiza-inducible gene encoding H<sup>+</sup>-ATPase (<i>LjHA1</i>), implicated in energizing nutrient uptake at the symbiotic interface across the periarbuscular membrane, is coregulated with <i>LjPT4</i> by CBX1. Accordingly, <i>CBX1</i>-defective mutants show reduced mycorrhizal colonization. Furthermore, genome-wide-binding profiles, DNA-binding studies, and heterologous expression reveal additional binding of CBX1 to AW box, the consensus DNA-binding motif for WRI1, that is enriched in promoters of glycolysis and fatty acid biosynthesis genes. We show that CBX1 activates expression of lipid metabolic genes including glycerol-3-phosphate acyltransferase <i>RAM2</i> implicated in acylglycerol biosynthesis. Our finding defines the role of CBX1 as a regulator of host genes involved in phosphate uptake and lipid synthesis through binding to the CTTC/AW molecular module, and supports a model underlying bidirectional exchange of phosphorus and carbon, a fundamental trait in the mutualistic AM symbiosis.</AbstractText><CopyrightInformation>Copyright © 2018 the Author(s). Published by PNAS.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Xue</LastName><ForeName>Li</ForeName><Initials>L</Initials><Identifier Source="ORCID">0000-0002-9367-0155</Identifier><AffiliationInfo><Affiliation>Botanical Institute, Cologne Biocenter, Cluster of Excellence on Plant Sciences, University of Cologne, D-50674 Cologne, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Klinnawee</LastName><ForeName>Lompong</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Botanical Institute, Cologne Biocenter, Cluster of Excellence on Plant Sciences, University of Cologne, D-50674 Cologne, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhou</LastName><ForeName>Yue</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Department of Plant Developmental Biology, Max Planck Institute for Plant Breeding Research, D-50829 Cologne, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Saridis</LastName><ForeName>Georgios</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Botanical Institute, Cologne Biocenter, Cluster of Excellence on Plant Sciences, University of Cologne, D-50674 Cologne, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Vijayakumar</LastName><ForeName>Vinod</ForeName><Initials>V</Initials><AffiliationInfo><Affiliation>Botanical Institute, Cologne Biocenter, Cluster of Excellence on Plant Sciences, University of Cologne, D-50674 Cologne, Germany.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Plant Pathology, The Ohio State University, Columbus, OH 43210.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Brands</LastName><ForeName>Mathias</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Department of Molecular Biotechnology, Institute of Molecular Physiology and Biotechnology of Plants, University of Bonn, 53115 Bonn, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Dörmann</LastName><ForeName>Peter</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>Department of Molecular Biotechnology, Institute of Molecular Physiology and Biotechnology of Plants, University of Bonn, 53115 Bonn, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gigolashvili</LastName><ForeName>Tamara</ForeName><Initials>T</Initials><AffiliationInfo><Affiliation>Botanical Institute, Cologne Biocenter, Cluster of Excellence on Plant Sciences, University of Cologne, D-50674 Cologne, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Turck</LastName><ForeName>Franziska</ForeName><Initials>F</Initials><Identifier Source="ORCID">0000-0002-4982-5949</Identifier><AffiliationInfo><Affiliation>Department of Plant Developmental Biology, Max Planck Institute for Plant Breeding Research, D-50829 Cologne, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bucher</LastName><ForeName>Marcel</ForeName><Initials>M</Initials><Identifier Source="ORCID">0000-0003-1680-9413</Identifier><AffiliationInfo><Affiliation>Botanical Institute, Cologne Biocenter, Cluster of Excellence on Plant Sciences, University of Cologne, D-50674 Cologne, Germany; m.bucher@uni-koeln.de.</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>2018</Year><Month>09</Month><Day>12</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Proc Natl Acad Sci U S A</MedlineTA><NlmUniqueID>7505876</NlmUniqueID><ISSNLinking>0027-8424</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D005656">Fungal Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D028061">Phosphate Transport Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D010710">Phosphates</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D014157">Transcription Factors</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 3.6.3.14</RegistryNumber><NameOfSubstance UI="D006180">Proton-Translocating ATPases</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><CommentsCorrectionsList><CommentsCorrections RefType="CommentIn"><RefSource>Mol Plant. 2018 Dec 3;11(12):1421-1423</RefSource><PMID Version="1">30447333</PMID></CommentsCorrections></CommentsCorrectionsList><MeshHeadingList><MeshHeading><DescriptorName UI="D005656" MajorTopicYN="N">Fungal Proteins</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D000070116" MajorTopicYN="N">Lotus</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName><QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D038821" MajorTopicYN="N">Mycorrhizae</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D028061" MajorTopicYN="N">Phosphate Transport Proteins</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D010710" MajorTopicYN="N">Phosphates</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D006180" MajorTopicYN="N">Proton-Translocating ATPases</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D013559" MajorTopicYN="Y">Symbiosis</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D014157" MajorTopicYN="N">Transcription Factors</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">AP2 transcription factor</Keyword><Keyword MajorTopicYN="Y">CTTC cis-regulatory element</Keyword><Keyword MajorTopicYN="Y">fatty acid biosynthesis</Keyword><Keyword MajorTopicYN="Y">mycorrhizal symbiosis</Keyword><Keyword MajorTopicYN="Y">phosphate transport</Keyword></KeywordList><CoiStatement>The authors declare no conflict of interest.</CoiStatement></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="pubmed"><Year>2018</Year><Month>9</Month><Day>14</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2018</Year><Month>10</Month><Day>23</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2018</Year><Month>9</Month><Day>14</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">30209216</ArticleId><ArticleId IdType="pii">1812275115</ArticleId><ArticleId IdType="doi">10.1073/pnas.1812275115</ArticleId><ArticleId IdType="pmc">PMC6166803</ArticleId></ArticleIdList><ReferenceList><Reference><Citation>Plant J. 2015 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