A Medicago truncatula SWEET transporter implicated in arbuscule maintenance during arbuscular mycorrhizal symbiosis.
Identifieur interne : 000445 ( Main/Corpus ); précédent : 000444; suivant : 000446A Medicago truncatula SWEET transporter implicated in arbuscule maintenance during arbuscular mycorrhizal symbiosis.
Auteurs : Jianyong An ; Tian Zeng ; Chuanya Ji ; Sanne De Graaf ; Zijun Zheng ; Ting Ting Xiao ; Xiuxin Deng ; Shunyuan Xiao ; Ton Bisseling ; Erik Limpens ; Zhiyong PanSource :
- The New phytologist [ 1469-8137 ] ; 2019.
English descriptors
- KwdEn :
- Alleles (MeSH), Gene Expression Regulation, Plant (MeSH), Genes, Dominant (MeSH), Glucose (metabolism), Green Fluorescent Proteins (metabolism), Medicago truncatula (genetics), Medicago truncatula (metabolism), Medicago truncatula (microbiology), Membrane Transport Proteins (metabolism), Membranes (metabolism), Models, Biological (MeSH), Mutagenesis, Insertional (genetics), Mycelium (growth & development), Mycorrhizae (cytology), Mycorrhizae (growth & development), Mycorrhizae (physiology), Plant Proteins (genetics), Plant Proteins (metabolism), Symbiosis (MeSH).
- MESH :
- chemical , genetics : Plant Proteins.
- chemical , metabolism : Glucose, Green Fluorescent Proteins, Membrane Transport Proteins, Plant Proteins.
- cytology : Mycorrhizae.
- genetics : Medicago truncatula, Mutagenesis, Insertional.
- growth & development : Mycelium, Mycorrhizae.
- metabolism : Medicago truncatula, Membranes.
- microbiology : Medicago truncatula.
- physiology : Mycorrhizae.
- Alleles, Gene Expression Regulation, Plant, Genes, Dominant, Models, Biological, Symbiosis.
Abstract
Plants form a mutualistic symbiosis with arbuscular mycorrhizal (AM) fungi, which facilitates the acquisition of scarce minerals from the soil. In return, the host plants provide sugars and lipids to its fungal partner. However, the mechanism by which the AM fungi obtain sugars from the plant has remained elusive. In this study we investigated the role of potential SWEET family sugar exporters in AM symbiosis in Medicago truncatula. We show that M. truncatula SWEET1b transporter is strongly upregulated in arbuscule-containing cells compared to roots and localizes to the peri-arbuscular membrane, across which nutrient exchange takes place. Heterologous expression of MtSWEET1b in a yeast hexose transport mutant showed that it mainly transports glucose. Overexpression of MtSWEET1b in M. truncatula roots promoted the growth of intraradical mycelium during AM symbiosis. Surprisingly, two independent Mtsweet1b mutants, which are predicted to produce truncated protein variants impaired in glucose transport, exhibited no significant defects in AM symbiosis. However, arbuscule-specific overexpression of MtSWEET1bY57A/G58D , which are considered to act in a dominant-negative manner, resulted in enhanced collapse of arbuscules. Taken together, our results reveal a (redundant) role for MtSWEET1b in the transport of glucose across the peri-arbuscular membrane to maintain arbuscules for a healthy mutually beneficial symbiosis.
DOI: 10.1111/nph.15975
PubMed: 31148173
Links to Exploration step
pubmed:31148173Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">A Medicago truncatula SWEET transporter implicated in arbuscule maintenance during arbuscular mycorrhizal symbiosis.</title><author><name sortKey="An, Jianyong" sort="An, Jianyong" uniqKey="An J" first="Jianyong" last="An">Jianyong An</name><affiliation><nlm:affiliation>Key Laboratory of Horticultural Plant Biology (Ministry of Education), Key Laboratory of Horticultural Crop Biology and Genetic Improvement (Central Region, Ministry of Agriculture), College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, 430070, China.</nlm:affiliation></affiliation></author><author><name sortKey="Zeng, Tian" sort="Zeng, Tian" uniqKey="Zeng T" first="Tian" last="Zeng">Tian Zeng</name><affiliation><nlm:affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University & Research, Droevendaalsesteeg 1, 6708 PB, Wageningen, the Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Ji, Chuanya" sort="Ji, Chuanya" uniqKey="Ji C" first="Chuanya" last="Ji">Chuanya Ji</name><affiliation><nlm:affiliation>Key Laboratory of Horticultural Plant Biology (Ministry of Education), Key Laboratory of Horticultural Crop Biology and Genetic Improvement (Central Region, Ministry of Agriculture), College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, 430070, China.</nlm:affiliation></affiliation></author><author><name sortKey="De Graaf, Sanne" sort="De Graaf, Sanne" uniqKey="De Graaf S" first="Sanne" last="De Graaf">Sanne De Graaf</name><affiliation><nlm:affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University & Research, Droevendaalsesteeg 1, 6708 PB, Wageningen, the Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Zheng, Zijun" sort="Zheng, Zijun" uniqKey="Zheng Z" first="Zijun" last="Zheng">Zijun Zheng</name><affiliation><nlm:affiliation>Key Laboratory of Horticultural Plant Biology (Ministry of Education), Key Laboratory of Horticultural Crop Biology and Genetic Improvement (Central Region, Ministry of Agriculture), College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, 430070, China.</nlm:affiliation></affiliation></author><author><name sortKey="Xiao, Ting Ting" sort="Xiao, Ting Ting" uniqKey="Xiao T" first="Ting Ting" last="Xiao">Ting Ting Xiao</name><affiliation><nlm:affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University & Research, Droevendaalsesteeg 1, 6708 PB, Wageningen, the Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Deng, Xiuxin" sort="Deng, Xiuxin" uniqKey="Deng X" first="Xiuxin" last="Deng">Xiuxin Deng</name><affiliation><nlm:affiliation>Key Laboratory of Horticultural Plant Biology (Ministry of Education), Key Laboratory of Horticultural Crop Biology and Genetic Improvement (Central Region, Ministry of Agriculture), College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, 430070, China.</nlm:affiliation></affiliation></author><author><name sortKey="Xiao, Shunyuan" sort="Xiao, Shunyuan" uniqKey="Xiao S" first="Shunyuan" last="Xiao">Shunyuan Xiao</name><affiliation><nlm:affiliation>Key Laboratory of Horticultural Plant Biology (Ministry of Education), Key Laboratory of Horticultural Crop Biology and Genetic Improvement (Central Region, Ministry of Agriculture), College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, 430070, China.</nlm:affiliation></affiliation><affiliation><nlm:affiliation>Institute for Bioscience and Biotechnology Research & Department of Plant Sciences and Landscape Architecture, University of Maryland College Park, Rockville, MD, 20850, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Bisseling, Ton" sort="Bisseling, Ton" uniqKey="Bisseling T" first="Ton" last="Bisseling">Ton Bisseling</name><affiliation><nlm:affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University & Research, Droevendaalsesteeg 1, 6708 PB, Wageningen, the Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Limpens, Erik" sort="Limpens, Erik" uniqKey="Limpens E" first="Erik" last="Limpens">Erik Limpens</name><affiliation><nlm:affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University & Research, Droevendaalsesteeg 1, 6708 PB, Wageningen, the Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Pan, Zhiyong" sort="Pan, Zhiyong" uniqKey="Pan Z" first="Zhiyong" last="Pan">Zhiyong Pan</name><affiliation><nlm:affiliation>Key Laboratory of Horticultural Plant Biology (Ministry of Education), Key Laboratory of Horticultural Crop Biology and Genetic Improvement (Central Region, Ministry of Agriculture), College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, 430070, China.</nlm:affiliation></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2019">2019</date><idno type="RBID">pubmed:31148173</idno><idno type="pmid">31148173</idno><idno type="doi">10.1111/nph.15975</idno><idno type="wicri:Area/Main/Corpus">000445</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000445</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">A Medicago truncatula SWEET transporter implicated in arbuscule maintenance during arbuscular mycorrhizal symbiosis.</title><author><name sortKey="An, Jianyong" sort="An, Jianyong" uniqKey="An J" first="Jianyong" last="An">Jianyong An</name><affiliation><nlm:affiliation>Key Laboratory of Horticultural Plant Biology (Ministry of Education), Key Laboratory of Horticultural Crop Biology and Genetic Improvement (Central Region, Ministry of Agriculture), College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, 430070, China.</nlm:affiliation></affiliation></author><author><name sortKey="Zeng, Tian" sort="Zeng, Tian" uniqKey="Zeng T" first="Tian" last="Zeng">Tian Zeng</name><affiliation><nlm:affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University & Research, Droevendaalsesteeg 1, 6708 PB, Wageningen, the Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Ji, Chuanya" sort="Ji, Chuanya" uniqKey="Ji C" first="Chuanya" last="Ji">Chuanya Ji</name><affiliation><nlm:affiliation>Key Laboratory of Horticultural Plant Biology (Ministry of Education), Key Laboratory of Horticultural Crop Biology and Genetic Improvement (Central Region, Ministry of Agriculture), College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, 430070, China.</nlm:affiliation></affiliation></author><author><name sortKey="De Graaf, Sanne" sort="De Graaf, Sanne" uniqKey="De Graaf S" first="Sanne" last="De Graaf">Sanne De Graaf</name><affiliation><nlm:affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University & Research, Droevendaalsesteeg 1, 6708 PB, Wageningen, the Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Zheng, Zijun" sort="Zheng, Zijun" uniqKey="Zheng Z" first="Zijun" last="Zheng">Zijun Zheng</name><affiliation><nlm:affiliation>Key Laboratory of Horticultural Plant Biology (Ministry of Education), Key Laboratory of Horticultural Crop Biology and Genetic Improvement (Central Region, Ministry of Agriculture), College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, 430070, China.</nlm:affiliation></affiliation></author><author><name sortKey="Xiao, Ting Ting" sort="Xiao, Ting Ting" uniqKey="Xiao T" first="Ting Ting" last="Xiao">Ting Ting Xiao</name><affiliation><nlm:affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University & Research, Droevendaalsesteeg 1, 6708 PB, Wageningen, the Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Deng, Xiuxin" sort="Deng, Xiuxin" uniqKey="Deng X" first="Xiuxin" last="Deng">Xiuxin Deng</name><affiliation><nlm:affiliation>Key Laboratory of Horticultural Plant Biology (Ministry of Education), Key Laboratory of Horticultural Crop Biology and Genetic Improvement (Central Region, Ministry of Agriculture), College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, 430070, China.</nlm:affiliation></affiliation></author><author><name sortKey="Xiao, Shunyuan" sort="Xiao, Shunyuan" uniqKey="Xiao S" first="Shunyuan" last="Xiao">Shunyuan Xiao</name><affiliation><nlm:affiliation>Key Laboratory of Horticultural Plant Biology (Ministry of Education), Key Laboratory of Horticultural Crop Biology and Genetic Improvement (Central Region, Ministry of Agriculture), College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, 430070, China.</nlm:affiliation></affiliation><affiliation><nlm:affiliation>Institute for Bioscience and Biotechnology Research & Department of Plant Sciences and Landscape Architecture, University of Maryland College Park, Rockville, MD, 20850, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Bisseling, Ton" sort="Bisseling, Ton" uniqKey="Bisseling T" first="Ton" last="Bisseling">Ton Bisseling</name><affiliation><nlm:affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University & Research, Droevendaalsesteeg 1, 6708 PB, Wageningen, the Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Limpens, Erik" sort="Limpens, Erik" uniqKey="Limpens E" first="Erik" last="Limpens">Erik Limpens</name><affiliation><nlm:affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University & Research, Droevendaalsesteeg 1, 6708 PB, Wageningen, the Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Pan, Zhiyong" sort="Pan, Zhiyong" uniqKey="Pan Z" first="Zhiyong" last="Pan">Zhiyong Pan</name><affiliation><nlm:affiliation>Key Laboratory of Horticultural Plant Biology (Ministry of Education), Key Laboratory of Horticultural Crop Biology and Genetic Improvement (Central Region, Ministry of Agriculture), College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, 430070, China.</nlm:affiliation></affiliation></author></analytic><series><title level="j">The New phytologist</title><idno type="eISSN">1469-8137</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Alleles (MeSH)</term><term>Gene Expression Regulation, Plant (MeSH)</term><term>Genes, Dominant (MeSH)</term><term>Glucose (metabolism)</term><term>Green Fluorescent Proteins (metabolism)</term><term>Medicago truncatula (genetics)</term><term>Medicago truncatula (metabolism)</term><term>Medicago truncatula (microbiology)</term><term>Membrane Transport Proteins (metabolism)</term><term>Membranes (metabolism)</term><term>Models, Biological (MeSH)</term><term>Mutagenesis, Insertional (genetics)</term><term>Mycelium (growth & development)</term><term>Mycorrhizae (cytology)</term><term>Mycorrhizae (growth & development)</term><term>Mycorrhizae (physiology)</term><term>Plant Proteins (genetics)</term><term>Plant Proteins (metabolism)</term><term>Symbiosis (MeSH)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Plant Proteins</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Glucose</term><term>Green Fluorescent Proteins</term><term>Membrane Transport Proteins</term><term>Plant Proteins</term></keywords><keywords scheme="MESH" qualifier="cytology" xml:lang="en"><term>Mycorrhizae</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Medicago truncatula</term><term>Mutagenesis, Insertional</term></keywords><keywords scheme="MESH" qualifier="growth & development" xml:lang="en"><term>Mycelium</term><term>Mycorrhizae</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Medicago truncatula</term><term>Membranes</term></keywords><keywords scheme="MESH" qualifier="microbiology" xml:lang="en"><term>Medicago truncatula</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Mycorrhizae</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Alleles</term><term>Gene Expression Regulation, Plant</term><term>Genes, Dominant</term><term>Models, Biological</term><term>Symbiosis</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Plants form a mutualistic symbiosis with arbuscular mycorrhizal (AM) fungi, which facilitates the acquisition of scarce minerals from the soil. In return, the host plants provide sugars and lipids to its fungal partner. However, the mechanism by which the AM fungi obtain sugars from the plant has remained elusive. In this study we investigated the role of potential SWEET family sugar exporters in AM symbiosis in Medicago truncatula. We show that M. truncatula SWEET1b transporter is strongly upregulated in arbuscule-containing cells compared to roots and localizes to the peri-arbuscular membrane, across which nutrient exchange takes place. Heterologous expression of MtSWEET1b in a yeast hexose transport mutant showed that it mainly transports glucose. Overexpression of MtSWEET1b in M. truncatula roots promoted the growth of intraradical mycelium during AM symbiosis. Surprisingly, two independent Mtsweet1b mutants, which are predicted to produce truncated protein variants impaired in glucose transport, exhibited no significant defects in AM symbiosis. However, arbuscule-specific overexpression of MtSWEET1b<sup>Y57A/G58D</sup> , which are considered to act in a dominant-negative manner, resulted in enhanced collapse of arbuscules. Taken together, our results reveal a (redundant) role for MtSWEET1b in the transport of glucose across the peri-arbuscular membrane to maintain arbuscules for a healthy mutually beneficial symbiosis.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">31148173</PMID><DateCompleted><Year>2020</Year><Month>05</Month><Day>04</Day></DateCompleted><DateRevised><Year>2020</Year><Month>09</Month><Day>30</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1469-8137</ISSN><JournalIssue CitedMedium="Internet"><Volume>224</Volume><Issue>1</Issue><PubDate><Year>2019</Year><Month>10</Month></PubDate></JournalIssue><Title>The New phytologist</Title><ISOAbbreviation>New Phytol</ISOAbbreviation></Journal><ArticleTitle>A Medicago truncatula SWEET transporter implicated in arbuscule maintenance during arbuscular mycorrhizal symbiosis.</ArticleTitle><Pagination><MedlinePgn>396-408</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1111/nph.15975</ELocationID><Abstract><AbstractText>Plants form a mutualistic symbiosis with arbuscular mycorrhizal (AM) fungi, which facilitates the acquisition of scarce minerals from the soil. In return, the host plants provide sugars and lipids to its fungal partner. However, the mechanism by which the AM fungi obtain sugars from the plant has remained elusive. In this study we investigated the role of potential SWEET family sugar exporters in AM symbiosis in Medicago truncatula. We show that M. truncatula SWEET1b transporter is strongly upregulated in arbuscule-containing cells compared to roots and localizes to the peri-arbuscular membrane, across which nutrient exchange takes place. Heterologous expression of MtSWEET1b in a yeast hexose transport mutant showed that it mainly transports glucose. Overexpression of MtSWEET1b in M. truncatula roots promoted the growth of intraradical mycelium during AM symbiosis. Surprisingly, two independent Mtsweet1b mutants, which are predicted to produce truncated protein variants impaired in glucose transport, exhibited no significant defects in AM symbiosis. However, arbuscule-specific overexpression of MtSWEET1b<sup>Y57A/G58D</sup> , which are considered to act in a dominant-negative manner, resulted in enhanced collapse of arbuscules. Taken together, our results reveal a (redundant) role for MtSWEET1b in the transport of glucose across the peri-arbuscular membrane to maintain arbuscules for a healthy mutually beneficial symbiosis.</AbstractText><CopyrightInformation>© 2019 The Authors. New Phytologist © 2019 New Phytologist Trust.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>An</LastName><ForeName>Jianyong</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Key Laboratory of Horticultural Plant Biology (Ministry of Education), Key Laboratory of Horticultural Crop Biology and Genetic Improvement (Central Region, Ministry of Agriculture), College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, 430070, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zeng</LastName><ForeName>Tian</ForeName><Initials>T</Initials><AffiliationInfo><Affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University & Research, Droevendaalsesteeg 1, 6708 PB, Wageningen, the Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ji</LastName><ForeName>Chuanya</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Key Laboratory of Horticultural Plant Biology (Ministry of Education), Key Laboratory of Horticultural Crop Biology and Genetic Improvement (Central Region, Ministry of Agriculture), College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, 430070, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>de Graaf</LastName><ForeName>Sanne</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University & Research, Droevendaalsesteeg 1, 6708 PB, Wageningen, the Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zheng</LastName><ForeName>Zijun</ForeName><Initials>Z</Initials><AffiliationInfo><Affiliation>Key Laboratory of Horticultural Plant Biology (Ministry of Education), Key Laboratory of Horticultural Crop Biology and Genetic Improvement (Central Region, Ministry of Agriculture), College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, 430070, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Xiao</LastName><ForeName>Ting Ting</ForeName><Initials>TT</Initials><AffiliationInfo><Affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University & Research, Droevendaalsesteeg 1, 6708 PB, Wageningen, the Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Deng</LastName><ForeName>Xiuxin</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Key Laboratory of Horticultural Plant Biology (Ministry of Education), Key Laboratory of Horticultural Crop Biology and Genetic Improvement (Central Region, Ministry of Agriculture), College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, 430070, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Xiao</LastName><ForeName>Shunyuan</ForeName><Initials>S</Initials><Identifier Source="ORCID">0000-0003-1348-4879</Identifier><AffiliationInfo><Affiliation>Key Laboratory of Horticultural Plant Biology (Ministry of Education), Key Laboratory of Horticultural Crop Biology and Genetic Improvement (Central Region, Ministry of Agriculture), College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, 430070, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Institute for Bioscience and Biotechnology Research & Department of Plant Sciences and Landscape Architecture, University of Maryland College Park, Rockville, MD, 20850, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bisseling</LastName><ForeName>Ton</ForeName><Initials>T</Initials><Identifier Source="ORCID">0000-0001-5494-8786</Identifier><AffiliationInfo><Affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University & Research, Droevendaalsesteeg 1, 6708 PB, Wageningen, the Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Limpens</LastName><ForeName>Erik</ForeName><Initials>E</Initials><Identifier Source="ORCID">0000-0002-9668-4085</Identifier><AffiliationInfo><Affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University & Research, Droevendaalsesteeg 1, 6708 PB, Wageningen, the Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Pan</LastName><ForeName>Zhiyong</ForeName><Initials>Z</Initials><Identifier Source="ORCID">0000-0002-0018-4298</Identifier><AffiliationInfo><Affiliation>Key Laboratory of Horticultural Plant Biology (Ministry of Education), Key Laboratory of Horticultural Crop Biology and Genetic Improvement (Central Region, Ministry of Agriculture), College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, 430070, China.</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>07</Month><Day>03</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>New Phytol</MedlineTA><NlmUniqueID>9882884</NlmUniqueID><ISSNLinking>0028-646X</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D026901">Membrane Transport Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>147336-22-9</RegistryNumber><NameOfSubstance UI="D049452">Green Fluorescent Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>IY9XDZ35W2</RegistryNumber><NameOfSubstance UI="D005947">Glucose</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000483" MajorTopicYN="N">Alleles</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D018506" MajorTopicYN="N">Gene Expression Regulation, Plant</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D005799" MajorTopicYN="N">Genes, Dominant</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D005947" MajorTopicYN="N">Glucose</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D049452" MajorTopicYN="N">Green Fluorescent Proteins</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D046913" MajorTopicYN="N">Medicago truncatula</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName><QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D026901" MajorTopicYN="N">Membrane Transport Proteins</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D008566" MajorTopicYN="N">Membranes</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D008954" MajorTopicYN="N">Models, Biological</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D016254" MajorTopicYN="N">Mutagenesis, Insertional</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D025282" MajorTopicYN="N">Mycelium</DescriptorName><QualifierName UI="Q000254" MajorTopicYN="N">growth & development</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D038821" MajorTopicYN="N">Mycorrhizae</DescriptorName><QualifierName UI="Q000166" MajorTopicYN="N">cytology</QualifierName><QualifierName UI="Q000254" MajorTopicYN="N">growth & development</QualifierName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D013559" MajorTopicYN="Y">Symbiosis</DescriptorName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">Medicago truncatula
</Keyword><Keyword MajorTopicYN="Y">SWEET
</Keyword><Keyword MajorTopicYN="Y">arbuscular mycorrhiza (AM)</Keyword><Keyword MajorTopicYN="Y">glucose</Keyword><Keyword MajorTopicYN="Y">sugar export</Keyword><Keyword MajorTopicYN="Y">symbiosis</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>02</Month><Day>14</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2019</Year><Month>05</Month><Day>27</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2019</Year><Month>5</Month><Day>31</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>5</Month><Day>6</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2019</Year><Month>6</Month><Day>1</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">31148173</ArticleId><ArticleId IdType="doi">10.1111/nph.15975</ArticleId></ArticleIdList><ReferenceList><Title>References</Title><Reference><Citation>Bago B, Pfeffer PE, Abubaker J, Jun J, Allen JW, Brouillette J, Douds DD, Lammers PJ, Shachar-Hill Y. 2003. 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