Changes in DNA Methylation in Response to 6-Benzylaminopurine Affect Allele-Specific Gene Expression in Populus Tomentosa.
Identifieur interne : 000524 ( Main/Exploration ); précédent : 000523; suivant : 000525Changes in DNA Methylation in Response to 6-Benzylaminopurine Affect Allele-Specific Gene Expression in Populus Tomentosa.
Auteurs : Anran Xuan [République populaire de Chine] ; Yuepeng Song [République populaire de Chine] ; Chenhao Bu [République populaire de Chine] ; Panfei Chen [République populaire de Chine] ; Yousry A. El-Kassaby [Canada] ; Deqiang Zhang [République populaire de Chine]Source :
- International journal of molecular sciences [ 1422-0067 ] ; 2020.
Abstract
Cytokinins play important roles in the growth and development of plants. Physiological and photosynthetic characteristics are common indicators to measure the growth and development in plants. However, few reports have described the molecular mechanisms of physiological and photosynthetic changes in response to cytokinin, particularly in woody plants. DNA methylation is an essential epigenetic modification that dynamically regulates gene expression in response to the external environment. In this study, we examined genome-wide DNA methylation variation and transcriptional variation in poplar (Populus tomentosa) after short-term treatment with the synthetic cytokinin 6-benzylaminopurine (6-BA). We identified 460 significantly differentially methylated regions (DMRs) in response to 6-BA treatment. Transcriptome analysis showed that 339 protein-coding genes, 262 long non-coding RNAs (lncRNAs), and 15,793 24-nt small interfering RNAs (siRNAs) were differentially expressed under 6-BA treatment. Among these, 79% were differentially expressed between alleles in P. tomentosa, and 102,819 allele-specific expression (ASE) loci in 19,200 genes were detected showing differences in ASE levels after 6-BA treatment. Combined DNA methylation and gene expression analysis demonstrated that DNA methylation plays an important role in regulating allele-specific gene expression. To further investigate the relationship between these 6-BA-responsive genes and phenotypic variation, we performed SNP analysis of 460 6-BA-responsive DMRs via re-sequencing using a natural population of P. tomentosa, and we identified 206 SNPs that were significantly associated with growth and wood properties. Association analysis indicated that 53% of loci with allele-specific expression had primarily dominant effects on poplar traits. Our comprehensive analyses of P. tomentosa DNA methylation and the regulation of allele-specific gene expression suggest that DNA methylation is an important regulator of imbalanced expression between allelic loci.
DOI: 10.3390/ijms21062117
PubMed: 32204454
PubMed Central: PMC7139286
Affiliations:
- Canada, République populaire de Chine
- Colombie-Britannique
- Pékin, Vancouver
- Université de la Colombie-Britannique
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Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>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.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>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</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Chen, Panfei" sort="Chen, Panfei" uniqKey="Chen P" first="Panfei" last="Chen">Panfei Chen</name><affiliation wicri:level="1"><nlm:affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>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.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>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</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="El Kassaby, Yousry A" sort="El Kassaby, Yousry A" uniqKey="El Kassaby Y" first="Yousry A" last="El-Kassaby">Yousry A. El-Kassaby</name><affiliation wicri:level="4"><nlm:affiliation>Department of Forest and Conservation Sciences, Faculty of Forestry, Forest Sciences Centre, University of British Columbia, Vancouver, BC V6T 1Z4, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Department of Forest and Conservation Sciences, Faculty of Forestry, Forest Sciences Centre, University of British Columbia, Vancouver, BC V6T 1Z4</wicri:regionArea><orgName type="university">Université de la Colombie-Britannique</orgName><placeName><settlement type="city">Vancouver</settlement><region type="state">Colombie-Britannique </region></placeName></affiliation></author><author><name sortKey="Zhang, Deqiang" sort="Zhang, Deqiang" uniqKey="Zhang D" first="Deqiang" last="Zhang">Deqiang Zhang</name><affiliation wicri:level="1"><nlm:affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>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.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>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</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author></analytic><series><title level="j">International journal of molecular sciences</title><idno type="eISSN">1422-0067</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Cytokinins play important roles in the growth and development of plants. Physiological and photosynthetic characteristics are common indicators to measure the growth and development in plants. However, few reports have described the molecular mechanisms of physiological and photosynthetic changes in response to cytokinin, particularly in woody plants. DNA methylation is an essential epigenetic modification that dynamically regulates gene expression in response to the external environment. In this study, we examined genome-wide DNA methylation variation and transcriptional variation in poplar (<i>Populus tomentosa</i>) after short-term treatment with the synthetic cytokinin 6-benzylaminopurine (6-BA). We identified 460 significantly differentially methylated regions (DMRs) in response to 6-BA treatment. Transcriptome analysis showed that 339 protein-coding genes, 262 long non-coding RNAs (lncRNAs), and 15,793 24-nt small interfering RNAs (siRNAs) were differentially expressed under 6-BA treatment. Among these, 79% were differentially expressed between alleles in <i>P</i>. <i>tomentosa</i>, and 102,819 allele-specific expression (ASE) loci in 19,200 genes were detected showing differences in ASE levels after 6-BA treatment. Combined DNA methylation and gene expression analysis demonstrated that DNA methylation plays an important role in regulating allele-specific gene expression. To further investigate the relationship between these 6-BA-responsive genes and phenotypic variation, we performed SNP analysis of 460 6-BA-responsive DMRs via re-sequencing using a natural population of <i>P. tomentosa,</i> and we identified 206 SNPs that were significantly associated with growth and wood properties. Association analysis indicated that 53% of loci with allele-specific expression had primarily dominant effects on poplar traits. Our comprehensive analyses of <i>P. tomentosa</i> DNA methylation and the regulation of allele-specific gene expression suggest that DNA methylation is an important regulator of imbalanced expression between allelic loci.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">32204454</PMID><DateRevised><Year>2020</Year><Month>04</Month><Day>11</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">1422-0067</ISSN><JournalIssue CitedMedium="Internet"><Volume>21</Volume><Issue>6</Issue><PubDate><Year>2020</Year><Month>Mar</Month><Day>19</Day></PubDate></JournalIssue><Title>International journal of molecular sciences</Title><ISOAbbreviation>Int J Mol Sci</ISOAbbreviation></Journal><ArticleTitle>Changes in DNA Methylation in Response to 6-Benzylaminopurine Affect Allele-Specific Gene Expression in <i>Populus Tomentosa</i>.</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">E2117</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.3390/ijms21062117</ELocationID><Abstract><AbstractText>Cytokinins play important roles in the growth and development of plants. Physiological and photosynthetic characteristics are common indicators to measure the growth and development in plants. However, few reports have described the molecular mechanisms of physiological and photosynthetic changes in response to cytokinin, particularly in woody plants. DNA methylation is an essential epigenetic modification that dynamically regulates gene expression in response to the external environment. In this study, we examined genome-wide DNA methylation variation and transcriptional variation in poplar (<i>Populus tomentosa</i>) after short-term treatment with the synthetic cytokinin 6-benzylaminopurine (6-BA). We identified 460 significantly differentially methylated regions (DMRs) in response to 6-BA treatment. Transcriptome analysis showed that 339 protein-coding genes, 262 long non-coding RNAs (lncRNAs), and 15,793 24-nt small interfering RNAs (siRNAs) were differentially expressed under 6-BA treatment. Among these, 79% were differentially expressed between alleles in <i>P</i>. <i>tomentosa</i>, and 102,819 allele-specific expression (ASE) loci in 19,200 genes were detected showing differences in ASE levels after 6-BA treatment. Combined DNA methylation and gene expression analysis demonstrated that DNA methylation plays an important role in regulating allele-specific gene expression. To further investigate the relationship between these 6-BA-responsive genes and phenotypic variation, we performed SNP analysis of 460 6-BA-responsive DMRs via re-sequencing using a natural population of <i>P. tomentosa,</i> and we identified 206 SNPs that were significantly associated with growth and wood properties. Association analysis indicated that 53% of loci with allele-specific expression had primarily dominant effects on poplar traits. Our comprehensive analyses of <i>P. tomentosa</i> DNA methylation and the regulation of allele-specific gene expression suggest that DNA methylation is an important regulator of imbalanced expression between allelic loci.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Xuan</LastName><ForeName>Anran</ForeName><Initials>A</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.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>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>Song</LastName><ForeName>Yuepeng</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.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>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>Bu</LastName><ForeName>Chenhao</ForeName><Initials>C</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.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>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>Panfei</ForeName><Initials>P</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.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>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>El-Kassaby</LastName><ForeName>Yousry A</ForeName><Initials>YA</Initials><AffiliationInfo><Affiliation>Department of Forest and Conservation Sciences, Faculty of Forestry, Forest Sciences Centre, University of British Columbia, Vancouver, BC V6T 1Z4, Canada.</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.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>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></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>2017ZY04</GrantID><Agency>the Fundamental Research Funds for the Central Universities</Agency><Country></Country></Grant><Grant><GrantID>31670333 and 31872671</GrantID><Agency>the Project of the National Natural Science Foundation of China</Agency><Country></Country></Grant><Grant><GrantID>B20050</GrantID><Agency>the 111 Project</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>03</Month><Day>19</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Int J Mol Sci</MedlineTA><NlmUniqueID>101092791</NlmUniqueID><ISSNLinking>1422-0067</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">6-BA</Keyword><Keyword MajorTopicYN="N">DNA methylation</Keyword><Keyword MajorTopicYN="N">allele specific 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