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The characterization of six auxin-induced tomato GH3 genes uncovers a member, SlGH3.4, strongly responsive to arbuscular mycorrhizal symbiosis.

Identifieur interne : 001371 ( Main/Exploration ); précédent : 001370; suivant : 001372

The characterization of six auxin-induced tomato GH3 genes uncovers a member, SlGH3.4, strongly responsive to arbuscular mycorrhizal symbiosis.

Auteurs : Dehua Liao ; Xiao Chen ; Aiqun Chen [République populaire de Chine] ; Huimin Wang [République populaire de Chine] ; Jianjian Liu [République populaire de Chine] ; Junli Liu [République populaire de Chine] ; Mian Gu [République populaire de Chine] ; Shubin Sun [République populaire de Chine] ; Guohua Xu [République populaire de Chine]

Source :

RBID : pubmed:25535196

Descripteurs français

English descriptors

Abstract

In plants, the GH3 gene family is widely considered to be involved in a broad range of plant physiological processes, through modulation of hormonal homeostasis. Multiple GH3 genes have been functionally characterized in several plant species; however, to date, limited works to study the GH3 genes in tomato have been reported. Here, we characterize the expression and regulatory profiles of six tomato GH3 genes, SlGH3.2, SlGH3.3, SlGH3.4, SlGH3.7, SlGH3.9 and SlGH3.15, in response to different phytohormone applications and arbuscular mycorrhizal (AM) fungal colonization. All six GH3 genes showed inducible responses to external IAA, and three members were significantly up-regulated in response to AM symbiosis. In particular, SlGH3.4, the transcripts of which were barely detectable under normal growth conditions, was strongly activated in the IAA-treated and AM fungal-colonized roots. A comparison of the SlGH3.4 expression in wild-type plants and M161, a mutant with a defect in AM symbiosis, confirmed that SlGH3.4 expression is highly correlated to mycorrhizal colonization. Histochemical staining demonstrated that a 2,258 bp SlGH3.4 promoter fragment could drive β-glucuronidase (GUS) expression strongly in root tips, steles and cortical cells of IAA-treated roots, but predominantly in the fungal-colonized cells of mycorrhizal roots. A truncated 654 bp promoter failed to direct GUS expression in IAA-treated roots, but maintained the symbiosis-induced activity in mycorrhizal roots. In summary, our results suggest that a mycorrhizal signaling pathway that is at least partially independent of the auxin signaling pathway has evolved for the co-regulation of the auxin- and mycorrhiza-activated GH3 genes in plants.

DOI: 10.1093/pcp/pcu212
PubMed: 25535196


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<term>Chromosomes, Plant (genetics)</term>
<term>Gene Expression Regulation, Plant (drug effects)</term>
<term>Genes, Plant (MeSH)</term>
<term>Glucuronidase (metabolism)</term>
<term>Indoleacetic Acids (pharmacology)</term>
<term>Lycopersicon esculentum (drug effects)</term>
<term>Lycopersicon esculentum (genetics)</term>
<term>Lycopersicon esculentum (microbiology)</term>
<term>Mutation (genetics)</term>
<term>Mycorrhizae (drug effects)</term>
<term>Mycorrhizae (physiology)</term>
<term>Phylogeny (MeSH)</term>
<term>Plant Growth Regulators (pharmacology)</term>
<term>Plant Proteins (genetics)</term>
<term>Plant Proteins (metabolism)</term>
<term>Plant Roots (drug effects)</term>
<term>Plant Roots (genetics)</term>
<term>Plant Roots (microbiology)</term>
<term>Promoter Regions, Genetic (genetics)</term>
<term>Real-Time Polymerase Chain Reaction (MeSH)</term>
<term>Symbiosis (drug effects)</term>
<term>Symbiosis (genetics)</term>
<term>Time Factors (MeSH)</term>
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<term>Chromosomes de plante (génétique)</term>
<term>Facteur de croissance végétal (pharmacologie)</term>
<term>Facteurs temps (MeSH)</term>
<term>Glucuronidase (métabolisme)</term>
<term>Gènes de plante (MeSH)</term>
<term>Lycopersicon esculentum (effets des médicaments et des substances chimiques)</term>
<term>Lycopersicon esculentum (génétique)</term>
<term>Lycopersicon esculentum (microbiologie)</term>
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<term>Mycorhizes (effets des médicaments et des substances chimiques)</term>
<term>Mycorhizes (physiologie)</term>
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<term>Protéines végétales (métabolisme)</term>
<term>Racines de plante (effets des médicaments et des substances chimiques)</term>
<term>Racines de plante (génétique)</term>
<term>Racines de plante (microbiologie)</term>
<term>Réaction de polymérisation en chaine en temps réel (MeSH)</term>
<term>Régions promotrices (génétique) (génétique)</term>
<term>Régulation de l'expression des gènes végétaux (effets des médicaments et des substances chimiques)</term>
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<term>Symbiose (génétique)</term>
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<term>Plant Proteins</term>
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<term>Plant Roots</term>
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<term>Racines de plante</term>
<term>Régulation de l'expression des gènes végétaux</term>
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<term>Mutation</term>
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<term>Protéines végétales</term>
<term>Racines de plante</term>
<term>Régions promotrices (génétique)</term>
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<term>Racines de plante</term>
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<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Lycopersicon esculentum</term>
<term>Plant Roots</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
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<term>Protéines végétales</term>
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<keywords scheme="MESH" qualifier="pharmacologie" xml:lang="fr">
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<term>Facteur de croissance végétal</term>
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<keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en">
<term>Indoleacetic Acids</term>
<term>Plant Growth Regulators</term>
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<term>Mycorrhizae</term>
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<term>Phylogeny</term>
<term>Real-Time Polymerase Chain Reaction</term>
<term>Time Factors</term>
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<keywords scheme="MESH" xml:lang="fr">
<term>Facteurs temps</term>
<term>Gènes de plante</term>
<term>Phylogenèse</term>
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<div type="abstract" xml:lang="en">In plants, the GH3 gene family is widely considered to be involved in a broad range of plant physiological processes, through modulation of hormonal homeostasis. Multiple GH3 genes have been functionally characterized in several plant species; however, to date, limited works to study the GH3 genes in tomato have been reported. Here, we characterize the expression and regulatory profiles of six tomato GH3 genes, SlGH3.2, SlGH3.3, SlGH3.4, SlGH3.7, SlGH3.9 and SlGH3.15, in response to different phytohormone applications and arbuscular mycorrhizal (AM) fungal colonization. All six GH3 genes showed inducible responses to external IAA, and three members were significantly up-regulated in response to AM symbiosis. In particular, SlGH3.4, the transcripts of which were barely detectable under normal growth conditions, was strongly activated in the IAA-treated and AM fungal-colonized roots. A comparison of the SlGH3.4 expression in wild-type plants and M161, a mutant with a defect in AM symbiosis, confirmed that SlGH3.4 expression is highly correlated to mycorrhizal colonization. Histochemical staining demonstrated that a 2,258 bp SlGH3.4 promoter fragment could drive β-glucuronidase (GUS) expression strongly in root tips, steles and cortical cells of IAA-treated roots, but predominantly in the fungal-colonized cells of mycorrhizal roots. A truncated 654 bp promoter failed to direct GUS expression in IAA-treated roots, but maintained the symbiosis-induced activity in mycorrhizal roots. In summary, our results suggest that a mycorrhizal signaling pathway that is at least partially independent of the auxin signaling pathway has evolved for the co-regulation of the auxin- and mycorrhiza-activated GH3 genes in plants. </div>
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<ELocationID EIdType="doi" ValidYN="Y">10.1093/pcp/pcu212</ELocationID>
<Abstract>
<AbstractText>In plants, the GH3 gene family is widely considered to be involved in a broad range of plant physiological processes, through modulation of hormonal homeostasis. Multiple GH3 genes have been functionally characterized in several plant species; however, to date, limited works to study the GH3 genes in tomato have been reported. Here, we characterize the expression and regulatory profiles of six tomato GH3 genes, SlGH3.2, SlGH3.3, SlGH3.4, SlGH3.7, SlGH3.9 and SlGH3.15, in response to different phytohormone applications and arbuscular mycorrhizal (AM) fungal colonization. All six GH3 genes showed inducible responses to external IAA, and three members were significantly up-regulated in response to AM symbiosis. In particular, SlGH3.4, the transcripts of which were barely detectable under normal growth conditions, was strongly activated in the IAA-treated and AM fungal-colonized roots. A comparison of the SlGH3.4 expression in wild-type plants and M161, a mutant with a defect in AM symbiosis, confirmed that SlGH3.4 expression is highly correlated to mycorrhizal colonization. Histochemical staining demonstrated that a 2,258 bp SlGH3.4 promoter fragment could drive β-glucuronidase (GUS) expression strongly in root tips, steles and cortical cells of IAA-treated roots, but predominantly in the fungal-colonized cells of mycorrhizal roots. A truncated 654 bp promoter failed to direct GUS expression in IAA-treated roots, but maintained the symbiosis-induced activity in mycorrhizal roots. In summary, our results suggest that a mycorrhizal signaling pathway that is at least partially independent of the auxin signaling pathway has evolved for the co-regulation of the auxin- and mycorrhiza-activated GH3 genes in plants. </AbstractText>
<CopyrightInformation>© The Author 2014. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: journals.permissions@oup.com.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Liao</LastName>
<ForeName>Dehua</ForeName>
<Initials>D</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, 210095, China These authors contributed equally to this work.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Chen</LastName>
<ForeName>Xiao</ForeName>
<Initials>X</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, 210095, China These authors contributed equally to this work.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Chen</LastName>
<ForeName>Aiqun</ForeName>
<Initials>A</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, 210095, China chenaq8@njau.edu.cn.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Wang</LastName>
<ForeName>Huimin</ForeName>
<Initials>H</Initials>
<AffiliationInfo>
<Affiliation>MOA Key Laboratory of Plant Nutrition and Fertilization in Lower-Middle Reaches of the Yangtze River, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Liu</LastName>
<ForeName>Jianjian</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>MOA Key Laboratory of Plant Nutrition and Fertilization in Lower-Middle Reaches of the Yangtze River, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Liu</LastName>
<ForeName>Junli</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>MOA Key Laboratory of Plant Nutrition and Fertilization in Lower-Middle Reaches of the Yangtze River, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Gu</LastName>
<ForeName>Mian</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>MOA Key Laboratory of Plant Nutrition and Fertilization in Lower-Middle Reaches of the Yangtze River, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Sun</LastName>
<ForeName>Shubin</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Xu</LastName>
<ForeName>Guohua</ForeName>
<Initials>G</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, 210095, China MOA Key Laboratory of Plant Nutrition and Fertilization in Lower-Middle Reaches of the Yangtze River, Nanjing Agricultural University, Nanjing 210095, 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>2014</Year>
<Month>12</Month>
<Day>21</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>Japan</Country>
<MedlineTA>Plant Cell Physiol</MedlineTA>
<NlmUniqueID>9430925</NlmUniqueID>
<ISSNLinking>0032-0781</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D007210">Indoleacetic Acids</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D010937">Plant Growth Regulators</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>EC 3.2.1.31</RegistryNumber>
<NameOfSubstance UI="D005966">Glucuronidase</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D032461" MajorTopicYN="N">Chromosomes, Plant</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018506" MajorTopicYN="N">Gene Expression Regulation, Plant</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="Y">drug effects</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D017343" MajorTopicYN="Y">Genes, Plant</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D005966" MajorTopicYN="N">Glucuronidase</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D007210" MajorTopicYN="N">Indoleacetic Acids</DescriptorName>
<QualifierName UI="Q000494" MajorTopicYN="Y">pharmacology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018551" MajorTopicYN="N">Lycopersicon esculentum</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D009154" MajorTopicYN="N">Mutation</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D038821" MajorTopicYN="N">Mycorrhizae</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010802" MajorTopicYN="N">Phylogeny</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010937" MajorTopicYN="N">Plant Growth Regulators</DescriptorName>
<QualifierName UI="Q000494" MajorTopicYN="N">pharmacology</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="D018517" MajorTopicYN="N">Plant Roots</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D011401" MajorTopicYN="N">Promoter Regions, Genetic</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D060888" MajorTopicYN="N">Real-Time Polymerase Chain Reaction</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D013559" MajorTopicYN="N">Symbiosis</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="Y">drug effects</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D013997" MajorTopicYN="N">Time Factors</DescriptorName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="N">Arbuscular mycorrhiza</Keyword>
<Keyword MajorTopicYN="N">Auxin</Keyword>
<Keyword MajorTopicYN="N">Expression</Keyword>
<Keyword MajorTopicYN="N">GH3 genes</Keyword>
<Keyword MajorTopicYN="N">GUS reporter</Keyword>
</KeywordList>
</MedlineCitation>
<PubmedData>
<History>
<PubMedPubDate PubStatus="received">
<Year>2014</Year>
<Month>03</Month>
<Day>24</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted">
<Year>2014</Year>
<Month>12</Month>
<Day>16</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez">
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<Month>12</Month>
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<Hour>6</Hour>
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<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="medline">
<Year>2016</Year>
<Month>1</Month>
<Day>12</Day>
<Hour>6</Hour>
<Minute>0</Minute>
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</History>
<PublicationStatus>ppublish</PublicationStatus>
<ArticleIdList>
<ArticleId IdType="pubmed">25535196</ArticleId>
<ArticleId IdType="pii">pcu212</ArticleId>
<ArticleId IdType="doi">10.1093/pcp/pcu212</ArticleId>
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<affiliations>
<list>
<country>
<li>République populaire de Chine</li>
</country>
</list>
<tree>
<noCountry>
<name sortKey="Chen, Xiao" sort="Chen, Xiao" uniqKey="Chen X" first="Xiao" last="Chen">Xiao Chen</name>
<name sortKey="Liao, Dehua" sort="Liao, Dehua" uniqKey="Liao D" first="Dehua" last="Liao">Dehua Liao</name>
</noCountry>
<country name="République populaire de Chine">
<noRegion>
<name sortKey="Chen, Aiqun" sort="Chen, Aiqun" uniqKey="Chen A" first="Aiqun" last="Chen">Aiqun Chen</name>
</noRegion>
<name sortKey="Gu, Mian" sort="Gu, Mian" uniqKey="Gu M" first="Mian" last="Gu">Mian Gu</name>
<name sortKey="Liu, Jianjian" sort="Liu, Jianjian" uniqKey="Liu J" first="Jianjian" last="Liu">Jianjian Liu</name>
<name sortKey="Liu, Junli" sort="Liu, Junli" uniqKey="Liu J" first="Junli" last="Liu">Junli Liu</name>
<name sortKey="Sun, Shubin" sort="Sun, Shubin" uniqKey="Sun S" first="Shubin" last="Sun">Shubin Sun</name>
<name sortKey="Wang, Huimin" sort="Wang, Huimin" uniqKey="Wang H" first="Huimin" last="Wang">Huimin Wang</name>
<name sortKey="Xu, Guohua" sort="Xu, Guohua" uniqKey="Xu G" first="Guohua" last="Xu">Guohua Xu</name>
</country>
</tree>
</affiliations>
</record>

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