Genome Wide Binding Site Analysis Reveals Transcriptional Coactivation of Cytokinin-Responsive Genes by DELLA Proteins
The ability of plants to provide a plastic response to environmental cues relies on the connectivity between signaling pathways. DELLA proteins act as hubs that relay environmental information to the multiple transcriptional circuits that control growth and development through physical interaction w...
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creator | Marín-de la Rosa, Nora Pfeiffer, Anne Hill, Kristine Locascio, Antonella Bhalerao, Rishikesh P Miskolczi, Pal Grønlund, Anne L Wanchoo-Kohli, Aakriti Thomas, Stephen G Bennett, Malcolm J Lohmann, Jan U Blázquez, Miguel A Alabadí, David |
description | The ability of plants to provide a plastic response to environmental cues relies on the connectivity between signaling pathways. DELLA proteins act as hubs that relay environmental information to the multiple transcriptional circuits that control growth and development through physical interaction with transcription factors from different families. We have analyzed the presence of one DELLA protein at the Arabidopsis genome by chromatin immunoprecipitation coupled to large-scale sequencing and we find that it binds at the promoters of multiple genes. Enrichment analysis shows a strong preference for cis elements recognized by specific transcription factor families. In particular, we demonstrate that DELLA proteins are recruited by type-B ARABIDOPSIS RESPONSE REGULATORS (ARR) to the promoters of cytokinin-regulated genes, where they act as transcriptional co-activators. The biological relevance of this mechanism is underpinned by the necessity of simultaneous presence of DELLAs and ARRs to restrict root meristem growth and to promote photomorphogenesis. |
doi_str_mv | 10.1371/journal.pgen.1005337 |
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DELLA proteins act as hubs that relay environmental information to the multiple transcriptional circuits that control growth and development through physical interaction with transcription factors from different families. We have analyzed the presence of one DELLA protein at the Arabidopsis genome by chromatin immunoprecipitation coupled to large-scale sequencing and we find that it binds at the promoters of multiple genes. Enrichment analysis shows a strong preference for cis elements recognized by specific transcription factor families. In particular, we demonstrate that DELLA proteins are recruited by type-B ARABIDOPSIS RESPONSE REGULATORS (ARR) to the promoters of cytokinin-regulated genes, where they act as transcriptional co-activators. The biological relevance of this mechanism is underpinned by the necessity of simultaneous presence of DELLAs and ARRs to restrict root meristem growth and to promote photomorphogenesis.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1005337</identifier><identifier>PMID: 26134422</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Arabidopsis - embryology ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Base Sequence ; Binding Sites - genetics ; Chromatin Immunoprecipitation ; Councils ; Cytokinins - metabolism ; DNA, Plant - genetics ; DNA-Binding Proteins - metabolism ; Gene expression ; Gene Expression Regulation, Plant ; Genetics ; Genetik ; Genomes ; Plant Development - physiology ; Plant Roots - growth & development ; Promoter Regions, Genetic - genetics ; Proteins ; Repressor Proteins - genetics ; Repressor Proteins - metabolism ; Scholarships & fellowships ; Seeds ; Sequence Analysis, DNA ; Signal Transduction ; Transcription factors ; Transcription Factors - metabolism ; Transcriptional Activation - genetics</subject><ispartof>PLoS genetics, 2015-07, Vol.11 (7), p.e1005337-e1005337</ispartof><rights>2015 Marín-de la Rosa et al 2015 Marín-de la Rosa et al</rights><rights>2015 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Marín-de la Rosa N, Pfeiffer A, Hill K, Locascio A, Bhalerao RP, Miskolczi P, et al. (2015) Genome Wide Binding Site Analysis Reveals Transcriptional Coactivation of Cytokinin-Responsive Genes by DELLA Proteins. 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The biological relevance of this mechanism is underpinned by the necessity of simultaneous presence of DELLAs and ARRs to restrict root meristem growth and to promote photomorphogenesis.</description><subject>Arabidopsis - embryology</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Base Sequence</subject><subject>Binding Sites - genetics</subject><subject>Chromatin Immunoprecipitation</subject><subject>Councils</subject><subject>Cytokinins - metabolism</subject><subject>DNA, Plant - genetics</subject><subject>DNA-Binding Proteins - metabolism</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant</subject><subject>Genetics</subject><subject>Genetik</subject><subject>Genomes</subject><subject>Plant Development - physiology</subject><subject>Plant Roots - growth & development</subject><subject>Promoter Regions, Genetic - genetics</subject><subject>Proteins</subject><subject>Repressor Proteins - genetics</subject><subject>Repressor Proteins - metabolism</subject><subject>Scholarships & fellowships</subject><subject>Seeds</subject><subject>Sequence Analysis, DNA</subject><subject>Signal Transduction</subject><subject>Transcription factors</subject><subject>Transcription Factors - metabolism</subject><subject>Transcriptional Activation - genetics</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>D8T</sourceid><sourceid>DOA</sourceid><recordid>eNpVklFv0zAQxyMEYmPwDRD4kZcUO3bi5AWplG1MqgQaQzxajn0uLqkd7CSo334O7ab16Wzf_36-O_2z7C3BC0I5-bj1Y3CyW_QbcAuCcUkpf5adk7KkOWeYPX9yPstexbjFmJZ1w19mZ0VFKGNFcZ5N1-D8DtAvqwF9tk5bt0E_7ABomeD7aCO6hQlkF9FdkC6qYPvB-pRDKy_VYCc5X5E3aLUf_B_rrMtvIfbeRTsBSniIqN2jL5fr9RJ9D34A6-Lr7IVJTHhzjBfZz6vLu9XXfP3t-ma1XOeqpNWQ84qYsjXKaF5RoyvOKsMLiYuy1ZwVrSp4A2lIwzEpVKEpk7gmlZJQqwITTi-y9wdu3_kojiuLgnDMaNoiq5Pi5qDQXm5FH-xOhr3w0or_Dz5shAyDVR0IQxTUtGaNVg0zJZe8TBcmFYem1a1MrPzAiv-gH9sTWuzGVoY5iAiCc8Lm7j4duxvbHWgFbgiyOyk7zTj7W2z8JBirmxrPgA9HQPB_R4iD2NmooOukAz-mOauGNVVZUZak7CBVwccYwDx-Q7CYDfWwHTEbShwNlcrePW3xsejBQfQeJpXMWw</recordid><startdate>20150701</startdate><enddate>20150701</enddate><creator>Marín-de la Rosa, Nora</creator><creator>Pfeiffer, Anne</creator><creator>Hill, Kristine</creator><creator>Locascio, Antonella</creator><creator>Bhalerao, Rishikesh P</creator><creator>Miskolczi, Pal</creator><creator>Grønlund, Anne L</creator><creator>Wanchoo-Kohli, Aakriti</creator><creator>Thomas, Stephen G</creator><creator>Bennett, Malcolm J</creator><creator>Lohmann, Jan U</creator><creator>Blázquez, Miguel A</creator><creator>Alabadí, David</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>7X8</scope><scope>5PM</scope><scope>ADTPV</scope><scope>AOWAS</scope><scope>D8T</scope><scope>ZZAVC</scope><scope>DOA</scope></search><sort><creationdate>20150701</creationdate><title>Genome Wide Binding Site Analysis Reveals Transcriptional Coactivation of Cytokinin-Responsive Genes by DELLA Proteins</title><author>Marín-de la Rosa, Nora ; Pfeiffer, Anne ; Hill, Kristine ; Locascio, Antonella ; Bhalerao, Rishikesh P ; Miskolczi, Pal ; Grønlund, Anne L ; Wanchoo-Kohli, Aakriti ; Thomas, Stephen G ; Bennett, Malcolm J ; Lohmann, Jan U ; Blázquez, Miguel A ; Alabadí, David</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c536t-761f5bfcfd763fd6746f72a025bd742bc279e553f7012c2d34a0816cae8c20173</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Arabidopsis - embryology</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Base Sequence</topic><topic>Binding Sites - genetics</topic><topic>Chromatin Immunoprecipitation</topic><topic>Councils</topic><topic>Cytokinins - metabolism</topic><topic>DNA, Plant - genetics</topic><topic>DNA-Binding Proteins - metabolism</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Plant</topic><topic>Genetics</topic><topic>Genetik</topic><topic>Genomes</topic><topic>Plant Development - physiology</topic><topic>Plant Roots - growth & development</topic><topic>Promoter Regions, Genetic - genetics</topic><topic>Proteins</topic><topic>Repressor Proteins - genetics</topic><topic>Repressor Proteins - metabolism</topic><topic>Scholarships & fellowships</topic><topic>Seeds</topic><topic>Sequence Analysis, DNA</topic><topic>Signal Transduction</topic><topic>Transcription factors</topic><topic>Transcription Factors - metabolism</topic><topic>Transcriptional Activation - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Marín-de la Rosa, Nora</creatorcontrib><creatorcontrib>Pfeiffer, Anne</creatorcontrib><creatorcontrib>Hill, Kristine</creatorcontrib><creatorcontrib>Locascio, Antonella</creatorcontrib><creatorcontrib>Bhalerao, Rishikesh P</creatorcontrib><creatorcontrib>Miskolczi, Pal</creatorcontrib><creatorcontrib>Grønlund, Anne L</creatorcontrib><creatorcontrib>Wanchoo-Kohli, Aakriti</creatorcontrib><creatorcontrib>Thomas, Stephen G</creatorcontrib><creatorcontrib>Bennett, Malcolm J</creatorcontrib><creatorcontrib>Lohmann, Jan U</creatorcontrib><creatorcontrib>Blázquez, Miguel A</creatorcontrib><creatorcontrib>Alabadí, David</creatorcontrib><creatorcontrib>Sveriges lantbruksuniversitet</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>SwePub</collection><collection>SwePub Articles</collection><collection>SWEPUB Freely available online</collection><collection>SwePub Articles full text</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Marín-de la Rosa, Nora</au><au>Pfeiffer, Anne</au><au>Hill, Kristine</au><au>Locascio, Antonella</au><au>Bhalerao, Rishikesh P</au><au>Miskolczi, Pal</au><au>Grønlund, Anne L</au><au>Wanchoo-Kohli, Aakriti</au><au>Thomas, Stephen G</au><au>Bennett, Malcolm J</au><au>Lohmann, Jan U</au><au>Blázquez, Miguel A</au><au>Alabadí, David</au><au>Yu, Hao</au><aucorp>Sveriges lantbruksuniversitet</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genome Wide Binding Site Analysis Reveals Transcriptional Coactivation of Cytokinin-Responsive Genes by DELLA Proteins</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2015-07-01</date><risdate>2015</risdate><volume>11</volume><issue>7</issue><spage>e1005337</spage><epage>e1005337</epage><pages>e1005337-e1005337</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>The ability of plants to provide a plastic response to environmental cues relies on the connectivity between signaling pathways. DELLA proteins act as hubs that relay environmental information to the multiple transcriptional circuits that control growth and development through physical interaction with transcription factors from different families. We have analyzed the presence of one DELLA protein at the Arabidopsis genome by chromatin immunoprecipitation coupled to large-scale sequencing and we find that it binds at the promoters of multiple genes. Enrichment analysis shows a strong preference for cis elements recognized by specific transcription factor families. In particular, we demonstrate that DELLA proteins are recruited by type-B ARABIDOPSIS RESPONSE REGULATORS (ARR) to the promoters of cytokinin-regulated genes, where they act as transcriptional co-activators. 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subjects | Arabidopsis - embryology Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Base Sequence Binding Sites - genetics Chromatin Immunoprecipitation Councils Cytokinins - metabolism DNA, Plant - genetics DNA-Binding Proteins - metabolism Gene expression Gene Expression Regulation, Plant Genetics Genetik Genomes Plant Development - physiology Plant Roots - growth & development Promoter Regions, Genetic - genetics Proteins Repressor Proteins - genetics Repressor Proteins - metabolism Scholarships & fellowships Seeds Sequence Analysis, DNA Signal Transduction Transcription factors Transcription Factors - metabolism Transcriptional Activation - genetics |
title | Genome Wide Binding Site Analysis Reveals Transcriptional Coactivation of Cytokinin-Responsive Genes by DELLA Proteins |
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