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Association genetics and transcriptome analysis reveal a gibberellin-responsive pathway involved in regulating photosynthesis.

Identifieur interne : 001997 ( Main/Exploration ); précédent : 001996; suivant : 001998

Association genetics and transcriptome analysis reveal a gibberellin-responsive pathway involved in regulating photosynthesis.

Auteurs : Jianbo Xie [République populaire de Chine] ; Jiaxing Tian [République populaire de Chine] ; Qingzhang Du [République populaire de Chine] ; Jinhui Chen [République populaire de Chine] ; Ying Li [République populaire de Chine] ; Xiaohui Yang [République populaire de Chine] ; Bailian Li [États-Unis] ; Deqiang Zhang [République populaire de Chine]

Source :

RBID : pubmed:27091876

Descripteurs français

English descriptors

Abstract

Gibberellins (GAs) regulate a wide range of important processes in plant growth and development, including photosynthesis. However, the mechanism by which GAs regulate photosynthesis remains to be understood. Here, we used multi-gene association to investigate the effect of genes in the GA-responsive pathway, as constructed by RNA sequencing, on photosynthesis, growth, and wood property traits, in a population of 435 Populus tomentosa By analyzing changes in the transcriptome following GA treatment, we identified many key photosynthetic genes, in agreement with the observed increase in measurements of photosynthesis. Regulatory motif enrichment analysis revealed that 37 differentially expressed genes related to photosynthesis shared two essential GA-related cis-regulatory elements, the GA response element and the pyrimidine box. Thus, we constructed a GA-responsive pathway consisting of 47 genes involved in regulating photosynthesis, including GID1, RGA, GID2, MYBGa, and 37 photosynthetic differentially expressed genes. Single nucleotide polymorphism (SNP)-based association analysis showed that 142 SNPs, representing 40 candidate genes in this pathway, were significantly associated with photosynthesis, growth, and wood property traits. Epistasis analysis uncovered interactions between 310 SNP-SNP pairs from 37 genes in this pathway, revealing possible genetic interactions. Moreover, a structural gene-gene matrix based on a time-course of transcript abundances provided a better understanding of the multi-gene pathway affecting photosynthesis. The results imply a functional role for these genes in mediating photosynthesis, growth, and wood properties, demonstrating the potential of combining transcriptome-based regulatory pathway construction and genetic association approaches to detect the complex genetic networks underlying quantitative traits.

DOI: 10.1093/jxb/erw151
PubMed: 27091876


Affiliations:


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<term>Gene Expression Profiling (MeSH)</term>
<term>Gene Expression Regulation, Plant (MeSH)</term>
<term>Gibberellins (metabolism)</term>
<term>Photosynthesis (genetics)</term>
<term>Plant Proteins (genetics)</term>
<term>Plant Proteins (metabolism)</term>
<term>Polymorphism, Single Nucleotide (MeSH)</term>
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<term>Populus (metabolism)</term>
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<term>Analyse de profil d'expression de gènes (MeSH)</term>
<term>Gibbérellines (métabolisme)</term>
<term>Photosynthèse (génétique)</term>
<term>Polymorphisme de nucléotide simple (MeSH)</term>
<term>Populus (croissance et développement)</term>
<term>Populus (génétique)</term>
<term>Populus (métabolisme)</term>
<term>Protéines végétales (génétique)</term>
<term>Protéines végétales (métabolisme)</term>
<term>Régulation de l'expression des gènes végétaux (MeSH)</term>
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<term>Plant Proteins</term>
</keywords>
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<term>Gibberellins</term>
<term>Plant Proteins</term>
</keywords>
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<term>Populus</term>
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<term>Photosynthesis</term>
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<div type="abstract" xml:lang="en">Gibberellins (GAs) regulate a wide range of important processes in plant growth and development, including photosynthesis. However, the mechanism by which GAs regulate photosynthesis remains to be understood. Here, we used multi-gene association to investigate the effect of genes in the GA-responsive pathway, as constructed by RNA sequencing, on photosynthesis, growth, and wood property traits, in a population of 435 Populus tomentosa By analyzing changes in the transcriptome following GA treatment, we identified many key photosynthetic genes, in agreement with the observed increase in measurements of photosynthesis. Regulatory motif enrichment analysis revealed that 37 differentially expressed genes related to photosynthesis shared two essential GA-related cis-regulatory elements, the GA response element and the pyrimidine box. Thus, we constructed a GA-responsive pathway consisting of 47 genes involved in regulating photosynthesis, including GID1, RGA, GID2, MYBGa, and 37 photosynthetic differentially expressed genes. Single nucleotide polymorphism (SNP)-based association analysis showed that 142 SNPs, representing 40 candidate genes in this pathway, were significantly associated with photosynthesis, growth, and wood property traits. Epistasis analysis uncovered interactions between 310 SNP-SNP pairs from 37 genes in this pathway, revealing possible genetic interactions. Moreover, a structural gene-gene matrix based on a time-course of transcript abundances provided a better understanding of the multi-gene pathway affecting photosynthesis. The results imply a functional role for these genes in mediating photosynthesis, growth, and wood properties, demonstrating the potential of combining transcriptome-based regulatory pathway construction and genetic association approaches to detect the complex genetic networks underlying quantitative traits.</div>
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<Abstract>
<AbstractText>Gibberellins (GAs) regulate a wide range of important processes in plant growth and development, including photosynthesis. However, the mechanism by which GAs regulate photosynthesis remains to be understood. Here, we used multi-gene association to investigate the effect of genes in the GA-responsive pathway, as constructed by RNA sequencing, on photosynthesis, growth, and wood property traits, in a population of 435 Populus tomentosa By analyzing changes in the transcriptome following GA treatment, we identified many key photosynthetic genes, in agreement with the observed increase in measurements of photosynthesis. Regulatory motif enrichment analysis revealed that 37 differentially expressed genes related to photosynthesis shared two essential GA-related cis-regulatory elements, the GA response element and the pyrimidine box. Thus, we constructed a GA-responsive pathway consisting of 47 genes involved in regulating photosynthesis, including GID1, RGA, GID2, MYBGa, and 37 photosynthetic differentially expressed genes. Single nucleotide polymorphism (SNP)-based association analysis showed that 142 SNPs, representing 40 candidate genes in this pathway, were significantly associated with photosynthesis, growth, and wood property traits. Epistasis analysis uncovered interactions between 310 SNP-SNP pairs from 37 genes in this pathway, revealing possible genetic interactions. Moreover, a structural gene-gene matrix based on a time-course of transcript abundances provided a better understanding of the multi-gene pathway affecting photosynthesis. The results imply a functional role for these genes in mediating photosynthesis, growth, and wood properties, demonstrating the potential of combining transcriptome-based regulatory pathway construction and genetic association approaches to detect the complex genetic networks underlying quantitative traits.</AbstractText>
<CopyrightInformation>© The Author 2016. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Xie</LastName>
<ForeName>Jianbo</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Tian</LastName>
<ForeName>Jiaxing</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Du</LastName>
<ForeName>Qingzhang</ForeName>
<Initials>Q</Initials>
<AffiliationInfo>
<Affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Chen</LastName>
<ForeName>Jinhui</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Li</LastName>
<ForeName>Ying</ForeName>
<Initials>Y</Initials>
<AffiliationInfo>
<Affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Yang</LastName>
<ForeName>Xiaohui</ForeName>
<Initials>X</Initials>
<AffiliationInfo>
<Affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Li</LastName>
<ForeName>Bailian</ForeName>
<Initials>B</Initials>
<AffiliationInfo>
<Affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China Department of Forestry, North Carolina State University, Raleigh, NC 27695-8203, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Zhang</LastName>
<ForeName>Deqiang</ForeName>
<Initials>D</Initials>
<AffiliationInfo>
<Affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China DeqiangZhang@bjfu.edu.cn.</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>2016</Year>
<Month>04</Month>
<Day>18</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>England</Country>
<MedlineTA>J Exp Bot</MedlineTA>
<NlmUniqueID>9882906</NlmUniqueID>
<ISSNLinking>0022-0957</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D005875">Gibberellins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D020869" MajorTopicYN="N">Gene Expression Profiling</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018506" MajorTopicYN="Y">Gene Expression Regulation, Plant</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D005875" MajorTopicYN="N">Gibberellins</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010788" MajorTopicYN="N">Photosynthesis</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D020641" MajorTopicYN="Y">Polymorphism, Single Nucleotide</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D032107" MajorTopicYN="N">Populus</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000254" MajorTopicYN="N">growth & development</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="Y">Association genetics</Keyword>
<Keyword MajorTopicYN="Y">Populus tomentosa</Keyword>
<Keyword MajorTopicYN="Y">epistatic interactions</Keyword>
<Keyword MajorTopicYN="Y">gibberellins</Keyword>
<Keyword MajorTopicYN="Y">photosynthesis pathway</Keyword>
<Keyword MajorTopicYN="Y">transcriptome.</Keyword>
</KeywordList>
</MedlineCitation>
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<PubMedPubDate PubStatus="entrez">
<Year>2016</Year>
<Month>4</Month>
<Day>20</Day>
<Hour>6</Hour>
<Minute>0</Minute>
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<PubMedPubDate PubStatus="pubmed">
<Year>2016</Year>
<Month>4</Month>
<Day>20</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="medline">
<Year>2017</Year>
<Month>12</Month>
<Day>21</Day>
<Hour>6</Hour>
<Minute>0</Minute>
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</History>
<PublicationStatus>ppublish</PublicationStatus>
<ArticleIdList>
<ArticleId IdType="pubmed">27091876</ArticleId>
<ArticleId IdType="pii">erw151</ArticleId>
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</pubmed>
<affiliations>
<list>
<country>
<li>République populaire de Chine</li>
<li>États-Unis</li>
</country>
<region>
<li>Caroline du Nord</li>
</region>
<settlement>
<li>Pékin</li>
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<country name="République populaire de Chine">
<noRegion>
<name sortKey="Xie, Jianbo" sort="Xie, Jianbo" uniqKey="Xie J" first="Jianbo" last="Xie">Jianbo Xie</name>
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<name sortKey="Chen, Jinhui" sort="Chen, Jinhui" uniqKey="Chen J" first="Jinhui" last="Chen">Jinhui Chen</name>
<name sortKey="Du, Qingzhang" sort="Du, Qingzhang" uniqKey="Du Q" first="Qingzhang" last="Du">Qingzhang Du</name>
<name sortKey="Li, Ying" sort="Li, Ying" uniqKey="Li Y" first="Ying" last="Li">Ying Li</name>
<name sortKey="Tian, Jiaxing" sort="Tian, Jiaxing" uniqKey="Tian J" first="Jiaxing" last="Tian">Jiaxing Tian</name>
<name sortKey="Yang, Xiaohui" sort="Yang, Xiaohui" uniqKey="Yang X" first="Xiaohui" last="Yang">Xiaohui Yang</name>
<name sortKey="Zhang, Deqiang" sort="Zhang, Deqiang" uniqKey="Zhang D" first="Deqiang" last="Zhang">Deqiang Zhang</name>
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<name sortKey="Li, Bailian" sort="Li, Bailian" uniqKey="Li B" first="Bailian" last="Li">Bailian Li</name>
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