The BORDER family of negative transcription elongation factors regulates flowering time in Arabidopsis
Transcription initiation has long been considered a primary regulatory step in gene expression. Recent work, however, shows that downstream events, such as transcription elongation, can also play important roles.1–3 A well-characterized example from animals is promoter-proximal pausing, where transc...
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Published in | Current biology Vol. 31; no. 23; pp. 5377 - 5384.e5 |
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Main Authors | , , , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
England
Elsevier Inc
06.12.2021
Elsevier |
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Online Access | Get full text |
ISSN | 0960-9822 1879-0445 1879-0445 |
DOI | 10.1016/j.cub.2021.09.074 |
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Abstract | Transcription initiation has long been considered a primary regulatory step in gene expression. Recent work, however, shows that downstream events, such as transcription elongation, can also play important roles.1–3 A well-characterized example from animals is promoter-proximal pausing, where transcriptionally engaged Pol II accumulates 30–50 bp downstream of the transcription start site (TSS) and is thought to enable rapid gene activation.2 Plants do not make widespread use of promoter-proximal pausing; however, in a phenomenon known as 3′ pausing, a significant increase in Pol II is observed near the transcript end site (TES) of many genes.4–6 Previous work has shown that 3′ pausing is promoted by the BORDER (BDR) family of negative transcription elongation factors. Here we show that BDR proteins play key roles in gene repression. Consistent with BDR proteins acting to slow or pause elongating Pol II, BDR-repressed genes are characterized by high levels of Pol II occupancy, yet low levels of mRNA. The BDR proteins physically interact with FPA,7 one of approximately two dozen genes collectively referred to as the autonomous floral-promotion pathway,8 which are necessary for the repression of the flowering time gene FLOWERING LOCUS C (FLC).9–11 In early-flowering strains, FLC expression is repressed by repressive histone modifications, such as histone H3 lysine 27 trimethylation (H3K27me3), thereby allowing the plants to flower early. These results suggest that the repression of transcription elongation by BDR proteins may allow for the temporary pausing of transcription or facilitate the long-term repression of genes by repressive histone modifications.
•BDR proteins repress expression of the floral repressor, FLC•BDR proteins physically interact with the autonomous pathway protein FPA•BDR-repressed genes have high levels of Pol II occupancy, despite low mRNA levels•Gene repression by BDR may involve the inhibition of transcription elongation
Yu et al. show that genes repressed by the BDR family of negative transcription elongation factors have high levels of Pol II occupancy, despite relatively low steady-state RNA levels. In this way, BDR proteins may allow for the later resumption of transcription or facilitate the long-term repression of genes by repressive histone modifications. |
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AbstractList | Transcription initiation has long been considered a primary regulatory step in gene expression. Recent work, however, shows that downstream events, such as transcription elongation, can also play important roles.1, 2, 3 A well-characterized example from animals is promoter-proximal pausing, where transcriptionally engaged Pol II accumulates 30–50 bp downstream of the transcription start site (TSS) and is thought to enable rapid gene activation.2 Plants do not make widespread use of promoter-proximal pausing; however, in a phenomenon known as 3′ pausing, a significant increase in Pol II is observed near the transcript end site (TES) of many genes.4, 5, 6 Previous work has shown that 3′ pausing is promoted by the BORDER (BDR) family of negative transcription elongation factors. Here we show that BDR proteins play key roles in gene repression. Consistent with BDR proteins acting to slow or pause elongating Pol II, BDR-repressed genes are characterized by high levels of Pol II occupancy, yet low levels of mRNA. The BDR proteins physically interact with FPA,7 one of approximately two dozen genes collectively referred to as the autonomous floral-promotion pathway,8 which are necessary for the repression of the flowering time gene FLOWERING LOCUS C (FLC).9, 10, 11 In early-flowering strains, FLC expression is repressed by repressive histone modifications, such as histone H3 lysine 27 trimethylation (H3K27me3), thereby allowing the plants to flower early. These results suggest that the repression of transcription elongation by BDR proteins may allow for the temporary pausing of transcription or facilitate the long-term repression of genes by repressive histone modifications. Transcription initiation has long been considered a primary regulatory step in gene expression. Recent work, however, shows that downstream events, such as transcription elongation, can also play important roles.1-3 A well-characterized example from animals is promoter-proximal pausing, where transcriptionally engaged Pol II accumulates 30-50 bp downstream of the transcription start site (TSS) and is thought to enable rapid gene activation.2 Plants do not make widespread use of promoter-proximal pausing; however, in a phenomenon known as 3' pausing, a significant increase in Pol II is observed near the transcript end site (TES) of many genes.4-6 Previous work has shown that 3' pausing is promoted by the BORDER (BDR) family of negative transcription elongation factors. Here we show that BDR proteins play key roles in gene repression. Consistent with BDR proteins acting to slow or pause elongating Pol II, BDR-repressed genes are characterized by high levels of Pol II occupancy, yet low levels of mRNA. The BDR proteins physically interact with FPA,7 one of approximately two dozen genes collectively referred to as the autonomous floral-promotion pathway,8 which are necessary for the repression of the flowering time gene FLOWERING LOCUS C (FLC).9-11 In early-flowering strains, FLC expression is repressed by repressive histone modifications, such as histone H3 lysine 27 trimethylation (H3K27me3), thereby allowing the plants to flower early. These results suggest that the repression of transcription elongation by BDR proteins may allow for the temporary pausing of transcription or facilitate the long-term repression of genes by repressive histone modifications.Transcription initiation has long been considered a primary regulatory step in gene expression. Recent work, however, shows that downstream events, such as transcription elongation, can also play important roles.1-3 A well-characterized example from animals is promoter-proximal pausing, where transcriptionally engaged Pol II accumulates 30-50 bp downstream of the transcription start site (TSS) and is thought to enable rapid gene activation.2 Plants do not make widespread use of promoter-proximal pausing; however, in a phenomenon known as 3' pausing, a significant increase in Pol II is observed near the transcript end site (TES) of many genes.4-6 Previous work has shown that 3' pausing is promoted by the BORDER (BDR) family of negative transcription elongation factors. Here we show that BDR proteins play key roles in gene repression. Consistent with BDR proteins acting to slow or pause elongating Pol II, BDR-repressed genes are characterized by high levels of Pol II occupancy, yet low levels of mRNA. The BDR proteins physically interact with FPA,7 one of approximately two dozen genes collectively referred to as the autonomous floral-promotion pathway,8 which are necessary for the repression of the flowering time gene FLOWERING LOCUS C (FLC).9-11 In early-flowering strains, FLC expression is repressed by repressive histone modifications, such as histone H3 lysine 27 trimethylation (H3K27me3), thereby allowing the plants to flower early. These results suggest that the repression of transcription elongation by BDR proteins may allow for the temporary pausing of transcription or facilitate the long-term repression of genes by repressive histone modifications. Transcription initiation has long been considered a primary regulatory step in gene expression. Recent work, however, shows that downstream events, such as transcription elongation, can also play important roles.1-3 A well-characterized example from animals is promoter-proximal pausing, where transcriptionally engaged Pol II accumulates 30-50 bp downstream of the transcription start site (TSS) and is thought to enable rapid gene activation.2 Plants do not make widespread use of promoter-proximal pausing; however, in a phenomenon known as 3' pausing, a significant increase in Pol II is observed near the transcript end site (TES) of many genes.4-6 Previous work has shown that 3' pausing is promoted by the BORDER (BDR) family of negative transcription elongation factors. Here we show that BDR proteins play key roles in gene repression. Consistent with BDR proteins acting to slow or pause elongating Pol II, BDR-repressed genes are characterized by high levels of Pol II occupancy, yet low levels of mRNA. The BDR proteins physically interact with FPA,7 one of approximately two dozen genes collectively referred to as the autonomous floral-promotion pathway,8 which are necessary for the repression of the flowering time gene FLOWERING LOCUS C (FLC).9-11 In early-flowering strains, FLC expression is repressed by repressive histone modifications, such as histone H3 lysine 27 trimethylation (H3K27me3), thereby allowing the plants to flower early. These results suggest that the repression of transcription elongation by BDR proteins may allow for the temporary pausing of transcription or facilitate the long-term repression of genes by repressive histone modifications. Transcription initiation has long been considered a primary regulatory step in gene expression. Recent work, however, shows that downstream events, such as transcription elongation, can also play important roles. A well-characterized example from animals is promoter-proximal pausing, where transcriptionally engaged Pol II accumulates 30-50 bp downstream of the transcription start site (TSS) and is thought to enable rapid gene activation. Plants do not make widespread use of promoter-proximal pausing; however, in a phenomenon known as 3' pausing, a significant increase in Pol II is observed near the transcript end site (TES) of many genes. Previous work has shown that 3' pausing is promoted by the BORDER (BDR) family of negative transcription elongation factors. Here we show that BDR proteins play key roles in gene repression. Consistent with BDR proteins acting to slow or pause elongating Pol II, BDR-repressed genes are characterized by high levels of Pol II occupancy, yet low levels of mRNA. The BDR proteins physically interact with FPA, one of approximately two dozen genes collectively referred to as the autonomous floral-promotion pathway, which are necessary for the repression of the flowering time gene FLOWERING LOCUS C (FLC). In early-flowering strains, FLC expression is repressed by repressive histone modifications, such as histone H3 lysine 27 trimethylation (H3K27me3), thereby allowing the plants to flower early. These results suggest that the repression of transcription elongation by BDR proteins may allow for the temporary pausing of transcription or facilitate the long-term repression of genes by repressive histone modifications. Transcription initiation has long been considered a primary regulatory step in gene expression. Recent work, however, shows that downstream events, such as transcription elongation, can also play important roles.1–3 A well-characterized example from animals is promoter-proximal pausing, where transcriptionally engaged Pol II accumulates 30–50 bp downstream of the transcription start site (TSS) and is thought to enable rapid gene activation.2 Plants do not make widespread use of promoter-proximal pausing; however, in a phenomenon known as 3′ pausing, a significant increase in Pol II is observed near the transcript end site (TES) of many genes.4–6 Previous work has shown that 3′ pausing is promoted by the BORDER (BDR) family of negative transcription elongation factors. Here we show that BDR proteins play key roles in gene repression. Consistent with BDR proteins acting to slow or pause elongating Pol II, BDR-repressed genes are characterized by high levels of Pol II occupancy, yet low levels of mRNA. The BDR proteins physically interact with FPA,7 one of approximately two dozen genes collectively referred to as the autonomous floral-promotion pathway,8 which are necessary for the repression of the flowering time gene FLOWERING LOCUS C (FLC).9–11 In early-flowering strains, FLC expression is repressed by repressive histone modifications, such as histone H3 lysine 27 trimethylation (H3K27me3), thereby allowing the plants to flower early. These results suggest that the repression of transcription elongation by BDR proteins may allow for the temporary pausing of transcription or facilitate the long-term repression of genes by repressive histone modifications. •BDR proteins repress expression of the floral repressor, FLC•BDR proteins physically interact with the autonomous pathway protein FPA•BDR-repressed genes have high levels of Pol II occupancy, despite low mRNA levels•Gene repression by BDR may involve the inhibition of transcription elongation Yu et al. show that genes repressed by the BDR family of negative transcription elongation factors have high levels of Pol II occupancy, despite relatively low steady-state RNA levels. In this way, BDR proteins may allow for the later resumption of transcription or facilitate the long-term repression of genes by repressive histone modifications. |
Author | Michaels, Scott D. Wang, Xingjun Xu, Feifei Trinidad, Jonathan C. Li, Ke Martin, Pascal G.P. Zhang, Yixiang Huang, Jie Thum, Karen E. Yu, Xuhong Zhao, ShuZhen Gu, Yangnan |
Author_xml | – sequence: 1 givenname: Xuhong surname: Yu fullname: Yu, Xuhong email: xuhongy@gmail.com organization: Department of Biology, Indiana University, 915 East Third Street, Bloomington, IN 47405, USA – sequence: 2 givenname: Pascal G.P. orcidid: 0000-0002-4271-658X surname: Martin fullname: Martin, Pascal G.P. organization: Department of Biology, Indiana University, 915 East Third Street, Bloomington, IN 47405, USA – sequence: 3 givenname: Yixiang surname: Zhang fullname: Zhang, Yixiang organization: Department of Chemistry, Indiana University, Bloomington, IN 47405, USA – sequence: 4 givenname: Jonathan C. surname: Trinidad fullname: Trinidad, Jonathan C. organization: Department of Chemistry, Indiana University, Bloomington, IN 47405, USA – sequence: 5 givenname: Feifei orcidid: 0000-0002-3380-7287 surname: Xu fullname: Xu, Feifei organization: Institute of Nuclear Agricultural Sciences, Key Laboratory for Nuclear Agricultural Sciences of Zhejiang Province and Ministry of Agriculture and Rural Affairs, Zhejiang University, Zijingang Campus, Hangzhou 310058, China – sequence: 6 givenname: Jie surname: Huang fullname: Huang, Jie organization: Center for Genomics and Bioinformatics, Indiana University, 915 East Third Street, Bloomington, IN 47405, USA – sequence: 7 givenname: Karen E. surname: Thum fullname: Thum, Karen E. organization: Department of Biology, Indiana University, 915 East Third Street, Bloomington, IN 47405, USA – sequence: 8 givenname: Ke surname: Li fullname: Li, Ke organization: Department of Biology, Indiana University, 915 East Third Street, Bloomington, IN 47405, USA – sequence: 9 givenname: ShuZhen surname: Zhao fullname: Zhao, ShuZhen organization: Shandong Provincial Key Laboratory of Crop Genetic Improvement, Ecology and Physiology, Biotechnology Research Center, Shandong Academy of Agricultural Sciences, Jinan 250100, China – sequence: 10 givenname: Yangnan orcidid: 0000-0001-5135-0180 surname: Gu fullname: Gu, Yangnan organization: Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA 94720, USA – sequence: 11 givenname: Xingjun surname: Wang fullname: Wang, Xingjun organization: Shandong Provincial Key Laboratory of Crop Genetic Improvement, Ecology and Physiology, Biotechnology Research Center, Shandong Academy of Agricultural Sciences, Jinan 250100, China – sequence: 12 givenname: Scott D. surname: Michaels fullname: Michaels, Scott D. email: michaels@indiana.edu organization: Department of Biology, Indiana University, 915 East Third Street, Bloomington, IN 47405, USA |
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Keywords | transcription elongation BORDER flowering time pausing FLOWERING LOCUS C RNA polymerase II transcription time flowering elongation |
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Snippet | Transcription initiation has long been considered a primary regulatory step in gene expression. Recent work, however, shows that downstream events, such as... |
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SubjectTerms | Animals Arabidopsis Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism BORDER early flowering FLOWERING LOCUS C flowering time Flowers - genetics Flowers - metabolism gene expression histones Histones - metabolism Life Sciences loci lysine pausing RNA polymerase II RNA Polymerase II - genetics RNA Polymerase II - metabolism transcription elongation transcription initiation transcription initiation site Transcription, Genetic Vegetal Biology |
Title | The BORDER family of negative transcription elongation factors regulates flowering time in Arabidopsis |
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