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Changes in chromatin accessibility between Arabidopsis stem cells and mesophyll cells illuminate cell type‐specific transcription factor networks
Summary Cell differentiation is driven by changes in the activity of transcription factors (TFs) and subsequent alterations in transcription. To study this process, differences in TF binding between cell types can be deduced by probing chromatin accessibility. We used cell type‐specific nuclear puri...
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Published in: | The Plant journal : for cell and molecular biology 2018-04, Vol.94 (2), p.215-231 |
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description | Summary
Cell differentiation is driven by changes in the activity of transcription factors (TFs) and subsequent alterations in transcription. To study this process, differences in TF binding between cell types can be deduced by probing chromatin accessibility. We used cell type‐specific nuclear purification followed by the assay for transposase‐accessible chromatin (ATAC‐seq) to delineate differences in chromatin accessibility and TF regulatory networks between stem cells of the shoot apical meristem (SAM) and differentiated leaf mesophyll cells in Arabidopsis thaliana. Chromatin accessibility profiles of SAM stem cells and leaf mesophyll cells were very similar at a qualitative level, yet thousands of regions having quantitatively different chromatin accessibility were also identified. Analysis of the genomic regions preferentially accessible in each cell type identified hundreds of overrepresented TF‐binding motifs, highlighting sets of TFs that are probably important for each cell type. Within these sets, we found evidence for extensive co‐regulation of target genes by multiple TFs that are preferentially expressed in each cell type. Interestingly, the TFs within each of these cell type‐enriched sets also showed evidence of extensively co‐regulating each other. We further found that preferentially accessible chromatin regions in mesophyll cells tended to also be substantially accessible in the stem cells, whereas the converse was not true. This observation suggests that the generally higher accessibility of regulatory elements in stem cells might contribute to their developmental plasticity. This work demonstrates the utility of cell type‐specific chromatin accessibility profiling for the rapid development of testable models of regulatory control differences between cell types.
Significance Statement
Differences in transcription factor (TF) activity between plant cells of different types remain largely unexplored. We used cell type‐specific nuclear purification followed by chromatin accessibility assays to delineate TF networks in stem cells of the shoot apical meristem and differentiated leaf mesophyll cells in Arabidopsis thaliana, providing insight into how the transcriptomes of these cell types are established and maintained. |
doi_str_mv | 10.1111/tpj.13882 |
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Cell differentiation is driven by changes in the activity of transcription factors (TFs) and subsequent alterations in transcription. To study this process, differences in TF binding between cell types can be deduced by probing chromatin accessibility. We used cell type‐specific nuclear purification followed by the assay for transposase‐accessible chromatin (ATAC‐seq) to delineate differences in chromatin accessibility and TF regulatory networks between stem cells of the shoot apical meristem (SAM) and differentiated leaf mesophyll cells in Arabidopsis thaliana. Chromatin accessibility profiles of SAM stem cells and leaf mesophyll cells were very similar at a qualitative level, yet thousands of regions having quantitatively different chromatin accessibility were also identified. Analysis of the genomic regions preferentially accessible in each cell type identified hundreds of overrepresented TF‐binding motifs, highlighting sets of TFs that are probably important for each cell type. Within these sets, we found evidence for extensive co‐regulation of target genes by multiple TFs that are preferentially expressed in each cell type. Interestingly, the TFs within each of these cell type‐enriched sets also showed evidence of extensively co‐regulating each other. We further found that preferentially accessible chromatin regions in mesophyll cells tended to also be substantially accessible in the stem cells, whereas the converse was not true. This observation suggests that the generally higher accessibility of regulatory elements in stem cells might contribute to their developmental plasticity. This work demonstrates the utility of cell type‐specific chromatin accessibility profiling for the rapid development of testable models of regulatory control differences between cell types.
Significance Statement
Differences in transcription factor (TF) activity between plant cells of different types remain largely unexplored. We used cell type‐specific nuclear purification followed by chromatin accessibility assays to delineate TF networks in stem cells of the shoot apical meristem and differentiated leaf mesophyll cells in Arabidopsis thaliana, providing insight into how the transcriptomes of these cell types are established and maintained.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/tpj.13882</identifier><identifier>PMID: 29513366</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Accessibility ; Arabidopsis - cytology ; Arabidopsis - metabolism ; Arabidopsis Proteins - physiology ; Arabidopsis thaliana ; ATAC‐seq ; Binding ; Cell differentiation ; Chromatin ; Chromatin - metabolism ; Developmental plasticity ; Differentiation (biology) ; Gene expression ; Gene Expression Regulation, Plant ; Gene regulation ; INTACT ; Leaves ; Meristem - cytology ; Meristem - metabolism ; Mesophyll ; Mesophyll Cells - metabolism ; Plant Leaves - cytology ; Plant Leaves - metabolism ; Plant Shoots - cytology ; Plant Shoots - metabolism ; Purification ; Regulatory sequences ; shoot meristem ; stem cell ; Stem cells ; Stem Cells - metabolism ; T cell receptors ; transcription factor ; Transcription factors ; Transcription Factors - physiology ; Transposase</subject><ispartof>The Plant journal : for cell and molecular biology, 2018-04, Vol.94 (2), p.215-231</ispartof><rights>2018 The Authors The Plant Journal © 2018 John Wiley & Sons Ltd</rights><rights>2018 The Authors The Plant Journal © 2018 John Wiley & Sons Ltd.</rights><rights>Copyright © 2018 John Wiley & Sons Ltd and the Society for Experimental Biology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4542-1eb02c5a4b9e5dd2c7c3b42fa9053f52354d6e781ed10fa9898ecd25f9e939b23</citedby><cites>FETCH-LOGICAL-c4542-1eb02c5a4b9e5dd2c7c3b42fa9053f52354d6e781ed10fa9898ecd25f9e939b23</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29513366$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Sijacic, Paja</creatorcontrib><creatorcontrib>Bajic, Marko</creatorcontrib><creatorcontrib>McKinney, Elizabeth C.</creatorcontrib><creatorcontrib>Meagher, Richard B.</creatorcontrib><creatorcontrib>Deal, Roger B.</creatorcontrib><title>Changes in chromatin accessibility between Arabidopsis stem cells and mesophyll cells illuminate cell type‐specific transcription factor networks</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>Summary
Cell differentiation is driven by changes in the activity of transcription factors (TFs) and subsequent alterations in transcription. To study this process, differences in TF binding between cell types can be deduced by probing chromatin accessibility. We used cell type‐specific nuclear purification followed by the assay for transposase‐accessible chromatin (ATAC‐seq) to delineate differences in chromatin accessibility and TF regulatory networks between stem cells of the shoot apical meristem (SAM) and differentiated leaf mesophyll cells in Arabidopsis thaliana. Chromatin accessibility profiles of SAM stem cells and leaf mesophyll cells were very similar at a qualitative level, yet thousands of regions having quantitatively different chromatin accessibility were also identified. Analysis of the genomic regions preferentially accessible in each cell type identified hundreds of overrepresented TF‐binding motifs, highlighting sets of TFs that are probably important for each cell type. Within these sets, we found evidence for extensive co‐regulation of target genes by multiple TFs that are preferentially expressed in each cell type. Interestingly, the TFs within each of these cell type‐enriched sets also showed evidence of extensively co‐regulating each other. We further found that preferentially accessible chromatin regions in mesophyll cells tended to also be substantially accessible in the stem cells, whereas the converse was not true. This observation suggests that the generally higher accessibility of regulatory elements in stem cells might contribute to their developmental plasticity. This work demonstrates the utility of cell type‐specific chromatin accessibility profiling for the rapid development of testable models of regulatory control differences between cell types.
Significance Statement
Differences in transcription factor (TF) activity between plant cells of different types remain largely unexplored. We used cell type‐specific nuclear purification followed by chromatin accessibility assays to delineate TF networks in stem cells of the shoot apical meristem and differentiated leaf mesophyll cells in Arabidopsis thaliana, providing insight into how the transcriptomes of these cell types are established and maintained.</description><subject>Accessibility</subject><subject>Arabidopsis - cytology</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - physiology</subject><subject>Arabidopsis thaliana</subject><subject>ATAC‐seq</subject><subject>Binding</subject><subject>Cell differentiation</subject><subject>Chromatin</subject><subject>Chromatin - metabolism</subject><subject>Developmental plasticity</subject><subject>Differentiation (biology)</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant</subject><subject>Gene regulation</subject><subject>INTACT</subject><subject>Leaves</subject><subject>Meristem - cytology</subject><subject>Meristem - metabolism</subject><subject>Mesophyll</subject><subject>Mesophyll Cells - metabolism</subject><subject>Plant Leaves - cytology</subject><subject>Plant Leaves - metabolism</subject><subject>Plant Shoots - cytology</subject><subject>Plant Shoots - metabolism</subject><subject>Purification</subject><subject>Regulatory sequences</subject><subject>shoot meristem</subject><subject>stem cell</subject><subject>Stem cells</subject><subject>Stem Cells - metabolism</subject><subject>T cell receptors</subject><subject>transcription factor</subject><subject>Transcription factors</subject><subject>Transcription Factors - physiology</subject><subject>Transposase</subject><issn>0960-7412</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><recordid>eNp1kc1qFEEUhQsxmEl04QtIgRuz6KR-e7qXYdCoBHQRwV1TXX3bqbG7qq1bTeidjxDwDX0SK5mJC8G7uZfDx7kHDiEvOTvneS7StDvnsqrEE7ListSF5PLrU7JidcmKteLimJwg7hjja1mqZ-RY1JpLWZYr8muzNf4bIHWe2m0Mo0n5MtYComvd4NJCW0i3AJ5eRtO6LkzokGKCkVoYBqTGd3QEDNN2GYaD5oZhHp03CR4EmpYJfv-8wwms652lKRqPNropueBpb2wKkfr8J8Tv-Jwc9WZAeHHYp-TLu7c3m_fF9aerD5vL68IqrUTBoWXCaqPaGnTXCbu2slWiNzXTstdCatWVsK44dJxltaorsJ3QfQ21rFshT8mbve8Uw48ZMDWjw_u4xkOYsRGM85LLmvOMvv4H3YU5-pwuU4IpxZWuMnW2p2wMiBH6ZopuNHFpOGvum2pyU81DU5l9dXCc2xG6v-RjNRm42AO3boDl_07NzeePe8s_8P6h7w</recordid><startdate>201804</startdate><enddate>201804</enddate><creator>Sijacic, Paja</creator><creator>Bajic, Marko</creator><creator>McKinney, Elizabeth C.</creator><creator>Meagher, Richard B.</creator><creator>Deal, Roger B.</creator><general>Blackwell Publishing Ltd</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QO</scope><scope>7QP</scope><scope>7QR</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>201804</creationdate><title>Changes in chromatin accessibility between Arabidopsis stem cells and mesophyll cells illuminate cell type‐specific transcription factor networks</title><author>Sijacic, Paja ; Bajic, Marko ; McKinney, Elizabeth C. ; Meagher, Richard B. ; Deal, Roger B.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4542-1eb02c5a4b9e5dd2c7c3b42fa9053f52354d6e781ed10fa9898ecd25f9e939b23</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Accessibility</topic><topic>Arabidopsis - cytology</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis Proteins - physiology</topic><topic>Arabidopsis thaliana</topic><topic>ATAC‐seq</topic><topic>Binding</topic><topic>Cell differentiation</topic><topic>Chromatin</topic><topic>Chromatin - metabolism</topic><topic>Developmental plasticity</topic><topic>Differentiation (biology)</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Plant</topic><topic>Gene regulation</topic><topic>INTACT</topic><topic>Leaves</topic><topic>Meristem - cytology</topic><topic>Meristem - metabolism</topic><topic>Mesophyll</topic><topic>Mesophyll Cells - metabolism</topic><topic>Plant Leaves - cytology</topic><topic>Plant Leaves - metabolism</topic><topic>Plant Shoots - cytology</topic><topic>Plant Shoots - metabolism</topic><topic>Purification</topic><topic>Regulatory sequences</topic><topic>shoot meristem</topic><topic>stem cell</topic><topic>Stem cells</topic><topic>Stem Cells - metabolism</topic><topic>T cell receptors</topic><topic>transcription factor</topic><topic>Transcription factors</topic><topic>Transcription Factors - physiology</topic><topic>Transposase</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sijacic, Paja</creatorcontrib><creatorcontrib>Bajic, Marko</creatorcontrib><creatorcontrib>McKinney, Elizabeth C.</creatorcontrib><creatorcontrib>Meagher, Richard B.</creatorcontrib><creatorcontrib>Deal, Roger B.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>The Plant journal : for cell and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sijacic, Paja</au><au>Bajic, Marko</au><au>McKinney, Elizabeth C.</au><au>Meagher, Richard B.</au><au>Deal, Roger B.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Changes in chromatin accessibility between Arabidopsis stem cells and mesophyll cells illuminate cell type‐specific transcription factor networks</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2018-04</date><risdate>2018</risdate><volume>94</volume><issue>2</issue><spage>215</spage><epage>231</epage><pages>215-231</pages><issn>0960-7412</issn><eissn>1365-313X</eissn><abstract>Summary
Cell differentiation is driven by changes in the activity of transcription factors (TFs) and subsequent alterations in transcription. To study this process, differences in TF binding between cell types can be deduced by probing chromatin accessibility. We used cell type‐specific nuclear purification followed by the assay for transposase‐accessible chromatin (ATAC‐seq) to delineate differences in chromatin accessibility and TF regulatory networks between stem cells of the shoot apical meristem (SAM) and differentiated leaf mesophyll cells in Arabidopsis thaliana. Chromatin accessibility profiles of SAM stem cells and leaf mesophyll cells were very similar at a qualitative level, yet thousands of regions having quantitatively different chromatin accessibility were also identified. Analysis of the genomic regions preferentially accessible in each cell type identified hundreds of overrepresented TF‐binding motifs, highlighting sets of TFs that are probably important for each cell type. Within these sets, we found evidence for extensive co‐regulation of target genes by multiple TFs that are preferentially expressed in each cell type. Interestingly, the TFs within each of these cell type‐enriched sets also showed evidence of extensively co‐regulating each other. We further found that preferentially accessible chromatin regions in mesophyll cells tended to also be substantially accessible in the stem cells, whereas the converse was not true. This observation suggests that the generally higher accessibility of regulatory elements in stem cells might contribute to their developmental plasticity. This work demonstrates the utility of cell type‐specific chromatin accessibility profiling for the rapid development of testable models of regulatory control differences between cell types.
Significance Statement
Differences in transcription factor (TF) activity between plant cells of different types remain largely unexplored. We used cell type‐specific nuclear purification followed by chromatin accessibility assays to delineate TF networks in stem cells of the shoot apical meristem and differentiated leaf mesophyll cells in Arabidopsis thaliana, providing insight into how the transcriptomes of these cell types are established and maintained.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>29513366</pmid><doi>10.1111/tpj.13882</doi><tpages>17</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Accessibility Arabidopsis - cytology Arabidopsis - metabolism Arabidopsis Proteins - physiology Arabidopsis thaliana ATAC‐seq Binding Cell differentiation Chromatin Chromatin - metabolism Developmental plasticity Differentiation (biology) Gene expression Gene Expression Regulation, Plant Gene regulation INTACT Leaves Meristem - cytology Meristem - metabolism Mesophyll Mesophyll Cells - metabolism Plant Leaves - cytology Plant Leaves - metabolism Plant Shoots - cytology Plant Shoots - metabolism Purification Regulatory sequences shoot meristem stem cell Stem cells Stem Cells - metabolism T cell receptors transcription factor Transcription factors Transcription Factors - physiology Transposase |
title | Changes in chromatin accessibility between Arabidopsis stem cells and mesophyll cells illuminate cell type‐specific transcription factor networks |
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