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Gibberellins interfere with symbiosis signaling and gene expression and alter colonization by arbuscular mycorrhizal fungi in Lotus japonicus.

Identifieur interne : 001612 ( Main/Curation ); précédent : 001611; suivant : 001613

Gibberellins interfere with symbiosis signaling and gene expression and alter colonization by arbuscular mycorrhizal fungi in Lotus japonicus.

Auteurs : Naoya Takeda [Japon] ; Yoshihiro Handa ; Syusaku Tsuzuki ; Mikiko Kojima ; Hitoshi Sakakibara ; Masayoshi Kawaguchi

Source :

RBID : pubmed:25527715

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English descriptors

Abstract

Arbuscular mycorrhiza is a mutualistic plant-fungus interaction that confers great advantages for plant growth. Arbuscular mycorrhizal (AM) fungi enter the host root and form symbiotic structures that facilitate nutrient supplies between the symbionts. The gibberellins (GAs) are phytohormones known to inhibit AM fungal infection. However, our transcriptome analysis and phytohormone quantification revealed GA accumulation in the roots of Lotus japonicus infected with AM fungi, suggesting that de novo GA synthesis plays a role in arbuscular mycorrhiza development. We found pleiotropic effects of GAs on the AM fungal infection. In particular, the morphology of AM fungal colonization was drastically altered by the status of GA signaling in the host root. Exogenous GA treatment inhibited AM hyphal entry into the host root and suppressed the expression of Reduced Arbuscular Mycorrhization1 (RAM1) and RAM2 homologs that function in hyphal entry and arbuscule formation. On the other hand, inhibition of GA biosynthesis or suppression of GA signaling also affected arbuscular mycorrhiza development in the host root. Low-GA conditions suppressed arbuscular mycorrhiza-induced subtilisin-like serine protease1 (SbtM1) expression that is required for AM fungal colonization and reduced hyphal branching in the host root. The reduced hyphal branching and SbtM1 expression caused by the inhibition of GA biosynthesis were recovered by GA treatment, supporting the theory that insufficient GA signaling causes the inhibitory effects on arbuscular mycorrhiza development. Most studies have focused on the negative role of GA signaling, whereas our study demonstrates that GA signaling also positively interacts with symbiotic responses and promotes AM colonization of the host root.

DOI: 10.1104/pp.114.247700
PubMed: 25527715
PubMed Central: PMC4326748

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Yoshihiro Handa
<affiliation>
<nlm:affiliation>Division of Symbiotic Systems, National Institute for Basic Biology, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., Y.H., M.Ka.);Department of Basic Biology, Graduate University for Advanced Studies, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., S.T., M.Ka.); andPlant Productivity Systems Research Group, RIKEN Center for Sustainable Resource Science, Tsurumi, Yokohama 230-0045, Japan (M.Ko., H.S.).</nlm:affiliation>
<wicri:noCountry code="subField">H.S.).</wicri:noCountry>
</affiliation>
Syusaku Tsuzuki
<affiliation>
<nlm:affiliation>Division of Symbiotic Systems, National Institute for Basic Biology, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., Y.H., M.Ka.);Department of Basic Biology, Graduate University for Advanced Studies, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., S.T., M.Ka.); andPlant Productivity Systems Research Group, RIKEN Center for Sustainable Resource Science, Tsurumi, Yokohama 230-0045, Japan (M.Ko., H.S.).</nlm:affiliation>
<wicri:noCountry code="subField">H.S.).</wicri:noCountry>
</affiliation>
Mikiko Kojima
<affiliation>
<nlm:affiliation>Division of Symbiotic Systems, National Institute for Basic Biology, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., Y.H., M.Ka.);Department of Basic Biology, Graduate University for Advanced Studies, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., S.T., M.Ka.); andPlant Productivity Systems Research Group, RIKEN Center for Sustainable Resource Science, Tsurumi, Yokohama 230-0045, Japan (M.Ko., H.S.).</nlm:affiliation>
<wicri:noCountry code="subField">H.S.).</wicri:noCountry>
</affiliation>
Hitoshi Sakakibara
<affiliation>
<nlm:affiliation>Division of Symbiotic Systems, National Institute for Basic Biology, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., Y.H., M.Ka.);Department of Basic Biology, Graduate University for Advanced Studies, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., S.T., M.Ka.); andPlant Productivity Systems Research Group, RIKEN Center for Sustainable Resource Science, Tsurumi, Yokohama 230-0045, Japan (M.Ko., H.S.).</nlm:affiliation>
<wicri:noCountry code="subField">H.S.).</wicri:noCountry>
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Masayoshi Kawaguchi
<affiliation>
<nlm:affiliation>Division of Symbiotic Systems, National Institute for Basic Biology, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., Y.H., M.Ka.);Department of Basic Biology, Graduate University for Advanced Studies, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., S.T., M.Ka.); andPlant Productivity Systems Research Group, RIKEN Center for Sustainable Resource Science, Tsurumi, Yokohama 230-0045, Japan (M.Ko., H.S.).</nlm:affiliation>
<wicri:noCountry code="subField">H.S.).</wicri:noCountry>
</affiliation>

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<name sortKey="Handa, Yoshihiro" sort="Handa, Yoshihiro" uniqKey="Handa Y" first="Yoshihiro" last="Handa">Yoshihiro Handa</name>
<affiliation>
<nlm:affiliation>Division of Symbiotic Systems, National Institute for Basic Biology, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., Y.H., M.Ka.);Department of Basic Biology, Graduate University for Advanced Studies, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., S.T., M.Ka.); andPlant Productivity Systems Research Group, RIKEN Center for Sustainable Resource Science, Tsurumi, Yokohama 230-0045, Japan (M.Ko., H.S.).</nlm:affiliation>
<wicri:noCountry code="subField">H.S.).</wicri:noCountry>
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<nlm:affiliation>Division of Symbiotic Systems, National Institute for Basic Biology, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., Y.H., M.Ka.);Department of Basic Biology, Graduate University for Advanced Studies, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., S.T., M.Ka.); andPlant Productivity Systems Research Group, RIKEN Center for Sustainable Resource Science, Tsurumi, Yokohama 230-0045, Japan (M.Ko., H.S.).</nlm:affiliation>
<wicri:noCountry code="subField">H.S.).</wicri:noCountry>
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<nlm:affiliation>Division of Symbiotic Systems, National Institute for Basic Biology, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., Y.H., M.Ka.);Department of Basic Biology, Graduate University for Advanced Studies, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., S.T., M.Ka.); andPlant Productivity Systems Research Group, RIKEN Center for Sustainable Resource Science, Tsurumi, Yokohama 230-0045, Japan (M.Ko., H.S.).</nlm:affiliation>
<wicri:noCountry code="subField">H.S.).</wicri:noCountry>
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<nlm:affiliation>Division of Symbiotic Systems, National Institute for Basic Biology, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., Y.H., M.Ka.);Department of Basic Biology, Graduate University for Advanced Studies, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., S.T., M.Ka.); andPlant Productivity Systems Research Group, RIKEN Center for Sustainable Resource Science, Tsurumi, Yokohama 230-0045, Japan (M.Ko., H.S.).</nlm:affiliation>
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<name sortKey="Kawaguchi, Masayoshi" sort="Kawaguchi, Masayoshi" uniqKey="Kawaguchi M" first="Masayoshi" last="Kawaguchi">Masayoshi Kawaguchi</name>
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<nlm:affiliation>Division of Symbiotic Systems, National Institute for Basic Biology, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., Y.H., M.Ka.);Department of Basic Biology, Graduate University for Advanced Studies, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., S.T., M.Ka.); andPlant Productivity Systems Research Group, RIKEN Center for Sustainable Resource Science, Tsurumi, Yokohama 230-0045, Japan (M.Ko., H.S.).</nlm:affiliation>
<wicri:noCountry code="subField">H.S.).</wicri:noCountry>
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<series>
<title level="j">Plant physiology</title>
<idno type="eISSN">1532-2548</idno>
<imprint>
<date when="2015" type="published">2015</date>
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<textClass>
<keywords scheme="KwdEn" xml:lang="en">
<term>Biosynthetic Pathways (genetics)</term>
<term>Colony Count, Microbial (MeSH)</term>
<term>Gene Expression Regulation, Plant (drug effects)</term>
<term>Genes, Plant (MeSH)</term>
<term>Gibberellins (biosynthesis)</term>
<term>Gibberellins (metabolism)</term>
<term>Gibberellins (pharmacology)</term>
<term>Glomeromycota (drug effects)</term>
<term>Glomeromycota (growth & development)</term>
<term>Glomeromycota (physiology)</term>
<term>Hyphae (drug effects)</term>
<term>Lotus (drug effects)</term>
<term>Lotus (genetics)</term>
<term>Lotus (microbiology)</term>
<term>Models, Biological (MeSH)</term>
<term>Mycorrhizae (drug effects)</term>
<term>Mycorrhizae (growth & development)</term>
<term>Mycorrhizae (physiology)</term>
<term>Organ Specificity (genetics)</term>
<term>Plant Growth Regulators (metabolism)</term>
<term>Plant Roots (genetics)</term>
<term>Plant Roots (microbiology)</term>
<term>Signal Transduction (drug effects)</term>
<term>Signal Transduction (genetics)</term>
<term>Symbiosis (drug effects)</term>
<term>Symbiosis (genetics)</term>
<term>Up-Regulation (genetics)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Facteur de croissance végétal (métabolisme)</term>
<term>Gibbérellines (biosynthèse)</term>
<term>Gibbérellines (métabolisme)</term>
<term>Gibbérellines (pharmacologie)</term>
<term>Glomeromycota (croissance et développement)</term>
<term>Glomeromycota (effets des médicaments et des substances chimiques)</term>
<term>Glomeromycota (physiologie)</term>
<term>Gènes de plante (MeSH)</term>
<term>Hyphae (effets des médicaments et des substances chimiques)</term>
<term>Loteae (effets des médicaments et des substances chimiques)</term>
<term>Loteae (génétique)</term>
<term>Loteae (microbiologie)</term>
<term>Modèles biologiques (MeSH)</term>
<term>Mycorhizes (croissance et développement)</term>
<term>Mycorhizes (effets des médicaments et des substances chimiques)</term>
<term>Mycorhizes (physiologie)</term>
<term>Numération de colonies microbiennes (MeSH)</term>
<term>Racines de plante (génétique)</term>
<term>Racines de plante (microbiologie)</term>
<term>Régulation de l'expression des gènes végétaux (effets des médicaments et des substances chimiques)</term>
<term>Régulation positive (génétique)</term>
<term>Spécificité d'organe (génétique)</term>
<term>Symbiose (effets des médicaments et des substances chimiques)</term>
<term>Symbiose (génétique)</term>
<term>Transduction du signal (effets des médicaments et des substances chimiques)</term>
<term>Transduction du signal (génétique)</term>
<term>Voies de biosynthèse (génétique)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="biosynthesis" xml:lang="en">
<term>Gibberellins</term>
</keywords>
<keywords scheme="MESH" qualifier="biosynthèse" xml:lang="fr">
<term>Gibbérellines</term>
</keywords>
<keywords scheme="MESH" qualifier="croissance et développement" xml:lang="fr">
<term>Glomeromycota</term>
<term>Mycorhizes</term>
</keywords>
<keywords scheme="MESH" qualifier="drug effects" xml:lang="en">
<term>Gene Expression Regulation, Plant</term>
<term>Glomeromycota</term>
<term>Hyphae</term>
<term>Lotus</term>
<term>Mycorrhizae</term>
<term>Signal Transduction</term>
<term>Symbiosis</term>
</keywords>
<keywords scheme="MESH" qualifier="effets des médicaments et des substances chimiques" xml:lang="fr">
<term>Glomeromycota</term>
<term>Hyphae</term>
<term>Loteae</term>
<term>Mycorhizes</term>
<term>Régulation de l'expression des gènes végétaux</term>
<term>Symbiose</term>
<term>Transduction du signal</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Biosynthetic Pathways</term>
<term>Lotus</term>
<term>Organ Specificity</term>
<term>Plant Roots</term>
<term>Signal Transduction</term>
<term>Symbiosis</term>
<term>Up-Regulation</term>
</keywords>
<keywords scheme="MESH" qualifier="growth & development" xml:lang="en">
<term>Glomeromycota</term>
<term>Mycorrhizae</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Loteae</term>
<term>Racines de plante</term>
<term>Régulation positive</term>
<term>Spécificité d'organe</term>
<term>Symbiose</term>
<term>Transduction du signal</term>
<term>Voies de biosynthèse</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Gibberellins</term>
<term>Plant Growth Regulators</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr">
<term>Loteae</term>
<term>Racines de plante</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Lotus</term>
<term>Plant Roots</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Facteur de croissance végétal</term>
<term>Gibbérellines</term>
</keywords>
<keywords scheme="MESH" qualifier="pharmacologie" xml:lang="fr">
<term>Gibbérellines</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en">
<term>Gibberellins</term>
</keywords>
<keywords scheme="MESH" qualifier="physiologie" xml:lang="fr">
<term>Glomeromycota</term>
<term>Mycorhizes</term>
</keywords>
<keywords scheme="MESH" qualifier="physiology" xml:lang="en">
<term>Glomeromycota</term>
<term>Mycorrhizae</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Colony Count, Microbial</term>
<term>Genes, Plant</term>
<term>Models, Biological</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Gènes de plante</term>
<term>Modèles biologiques</term>
<term>Numération de colonies microbiennes</term>
</keywords>
</textClass>
</profileDesc>
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<front>
<div type="abstract" xml:lang="en">Arbuscular mycorrhiza is a mutualistic plant-fungus interaction that confers great advantages for plant growth. Arbuscular mycorrhizal (AM) fungi enter the host root and form symbiotic structures that facilitate nutrient supplies between the symbionts. The gibberellins (GAs) are phytohormones known to inhibit AM fungal infection. However, our transcriptome analysis and phytohormone quantification revealed GA accumulation in the roots of Lotus japonicus infected with AM fungi, suggesting that de novo GA synthesis plays a role in arbuscular mycorrhiza development. We found pleiotropic effects of GAs on the AM fungal infection. In particular, the morphology of AM fungal colonization was drastically altered by the status of GA signaling in the host root. Exogenous GA treatment inhibited AM hyphal entry into the host root and suppressed the expression of Reduced Arbuscular Mycorrhization1 (RAM1) and RAM2 homologs that function in hyphal entry and arbuscule formation. On the other hand, inhibition of GA biosynthesis or suppression of GA signaling also affected arbuscular mycorrhiza development in the host root. Low-GA conditions suppressed arbuscular mycorrhiza-induced subtilisin-like serine protease1 (SbtM1) expression that is required for AM fungal colonization and reduced hyphal branching in the host root. The reduced hyphal branching and SbtM1 expression caused by the inhibition of GA biosynthesis were recovered by GA treatment, supporting the theory that insufficient GA signaling causes the inhibitory effects on arbuscular mycorrhiza development. Most studies have focused on the negative role of GA signaling, whereas our study demonstrates that GA signaling also positively interacts with symbiotic responses and promotes AM colonization of the host root. </div>
</front>
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<Month>10</Month>
<Day>06</Day>
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<Year>2018</Year>
<Month>12</Month>
<Day>02</Day>
</DateRevised>
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<ISSN IssnType="Electronic">1532-2548</ISSN>
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<Volume>167</Volume>
<Issue>2</Issue>
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<Month>Feb</Month>
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<Title>Plant physiology</Title>
<ISOAbbreviation>Plant Physiol</ISOAbbreviation>
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<ArticleTitle>Gibberellins interfere with symbiosis signaling and gene expression and alter colonization by arbuscular mycorrhizal fungi in Lotus japonicus.</ArticleTitle>
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<Abstract>
<AbstractText>Arbuscular mycorrhiza is a mutualistic plant-fungus interaction that confers great advantages for plant growth. Arbuscular mycorrhizal (AM) fungi enter the host root and form symbiotic structures that facilitate nutrient supplies between the symbionts. The gibberellins (GAs) are phytohormones known to inhibit AM fungal infection. However, our transcriptome analysis and phytohormone quantification revealed GA accumulation in the roots of Lotus japonicus infected with AM fungi, suggesting that de novo GA synthesis plays a role in arbuscular mycorrhiza development. We found pleiotropic effects of GAs on the AM fungal infection. In particular, the morphology of AM fungal colonization was drastically altered by the status of GA signaling in the host root. Exogenous GA treatment inhibited AM hyphal entry into the host root and suppressed the expression of Reduced Arbuscular Mycorrhization1 (RAM1) and RAM2 homologs that function in hyphal entry and arbuscule formation. On the other hand, inhibition of GA biosynthesis or suppression of GA signaling also affected arbuscular mycorrhiza development in the host root. Low-GA conditions suppressed arbuscular mycorrhiza-induced subtilisin-like serine protease1 (SbtM1) expression that is required for AM fungal colonization and reduced hyphal branching in the host root. The reduced hyphal branching and SbtM1 expression caused by the inhibition of GA biosynthesis were recovered by GA treatment, supporting the theory that insufficient GA signaling causes the inhibitory effects on arbuscular mycorrhiza development. Most studies have focused on the negative role of GA signaling, whereas our study demonstrates that GA signaling also positively interacts with symbiotic responses and promotes AM colonization of the host root. </AbstractText>
<CopyrightInformation>© 2015 American Society of Plant Biologists. All Rights Reserved.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Takeda</LastName>
<ForeName>Naoya</ForeName>
<Initials>N</Initials>
<AffiliationInfo>
<Affiliation>Division of Symbiotic Systems, National Institute for Basic Biology, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., Y.H., M.Ka.);Department of Basic Biology, Graduate University for Advanced Studies, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., S.T., M.Ka.); andPlant Productivity Systems Research Group, RIKEN Center for Sustainable Resource Science, Tsurumi, Yokohama 230-0045, Japan (M.Ko., H.S.) takedan@nibb.ac.jp.</Affiliation>
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<Author ValidYN="Y">
<LastName>Handa</LastName>
<ForeName>Yoshihiro</ForeName>
<Initials>Y</Initials>
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<Affiliation>Division of Symbiotic Systems, National Institute for Basic Biology, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., Y.H., M.Ka.);Department of Basic Biology, Graduate University for Advanced Studies, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., S.T., M.Ka.); andPlant Productivity Systems Research Group, RIKEN Center for Sustainable Resource Science, Tsurumi, Yokohama 230-0045, Japan (M.Ko., H.S.).</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Tsuzuki</LastName>
<ForeName>Syusaku</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>Division of Symbiotic Systems, National Institute for Basic Biology, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., Y.H., M.Ka.);Department of Basic Biology, Graduate University for Advanced Studies, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., S.T., M.Ka.); andPlant Productivity Systems Research Group, RIKEN Center for Sustainable Resource Science, Tsurumi, Yokohama 230-0045, Japan (M.Ko., H.S.).</Affiliation>
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<LastName>Kojima</LastName>
<ForeName>Mikiko</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Division of Symbiotic Systems, National Institute for Basic Biology, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., Y.H., M.Ka.);Department of Basic Biology, Graduate University for Advanced Studies, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., S.T., M.Ka.); andPlant Productivity Systems Research Group, RIKEN Center for Sustainable Resource Science, Tsurumi, Yokohama 230-0045, Japan (M.Ko., H.S.).</Affiliation>
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<LastName>Sakakibara</LastName>
<ForeName>Hitoshi</ForeName>
<Initials>H</Initials>
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<Affiliation>Division of Symbiotic Systems, National Institute for Basic Biology, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., Y.H., M.Ka.);Department of Basic Biology, Graduate University for Advanced Studies, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., S.T., M.Ka.); andPlant Productivity Systems Research Group, RIKEN Center for Sustainable Resource Science, Tsurumi, Yokohama 230-0045, Japan (M.Ko., H.S.).</Affiliation>
</AffiliationInfo>
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<Author ValidYN="Y">
<LastName>Kawaguchi</LastName>
<ForeName>Masayoshi</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Division of Symbiotic Systems, National Institute for Basic Biology, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., Y.H., M.Ka.);Department of Basic Biology, Graduate University for Advanced Studies, Myodaiji, Okazaki, Aichi 444-8585, Japan (N.T., S.T., M.Ka.); andPlant Productivity Systems Research Group, RIKEN Center for Sustainable Resource Science, Tsurumi, Yokohama 230-0045, Japan (M.Ko., H.S.).</Affiliation>
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<Language>eng</Language>
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<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
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<ArticleDate DateType="Electronic">
<Year>2014</Year>
<Month>12</Month>
<Day>19</Day>
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<Country>United States</Country>
<MedlineTA>Plant Physiol</MedlineTA>
<NlmUniqueID>0401224</NlmUniqueID>
<ISSNLinking>0032-0889</ISSNLinking>
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<MeshHeading>
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<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D015169" MajorTopicYN="N">Colony Count, Microbial</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018506" MajorTopicYN="Y">Gene Expression Regulation, Plant</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
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<MeshHeading>
<DescriptorName UI="D005875" MajorTopicYN="N">Gibberellins</DescriptorName>
<QualifierName UI="Q000096" MajorTopicYN="N">biosynthesis</QualifierName>
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<MeshHeading>
<DescriptorName UI="D055137" MajorTopicYN="N">Glomeromycota</DescriptorName>
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<MeshHeading>
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<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
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</MeshHeading>
<MeshHeading>
<DescriptorName UI="D038821" MajorTopicYN="N">Mycorrhizae</DescriptorName>
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<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
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<DescriptorName UI="D009928" MajorTopicYN="N">Organ Specificity</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
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<DescriptorName UI="D010937" MajorTopicYN="N">Plant Growth Regulators</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018517" MajorTopicYN="N">Plant Roots</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D015398" MajorTopicYN="N">Signal Transduction</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D013559" MajorTopicYN="Y">Symbiosis</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
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