TATA and paused promoters active in differentiated tissues have distinct expression characteristics

Abstract Core promoter types differ in the extent to which RNA polymerase II (Pol II) pauses after initiation, but how this affects their tissue‐specific gene expression characteristics is not well understood. While promoters with Pol II pausing elements are active throughout development, TATA promo...

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Main Authors: Vivekanandan Ramalingam, Malini Natarajan, Jeff Johnston, Julia Zeitlinger
Format: Article
Language:English
Published: Springer Nature 2021-02-01
Series:Molecular Systems Biology
Subjects:
Online Access:https://doi.org/10.15252/msb.20209866
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author Vivekanandan Ramalingam
Malini Natarajan
Jeff Johnston
Julia Zeitlinger
author_facet Vivekanandan Ramalingam
Malini Natarajan
Jeff Johnston
Julia Zeitlinger
author_sort Vivekanandan Ramalingam
collection DOAJ
description Abstract Core promoter types differ in the extent to which RNA polymerase II (Pol II) pauses after initiation, but how this affects their tissue‐specific gene expression characteristics is not well understood. While promoters with Pol II pausing elements are active throughout development, TATA promoters are highly active in differentiated tissues. We therefore used a genomics approach on late‐stage Drosophila embryos to analyze the properties of promoter types. Using tissue‐specific Pol II ChIP‐seq, we found that paused promoters have high levels of paused Pol II throughout the embryo, even in tissues where the gene is not expressed, while TATA promoters only show Pol II occupancy when the gene is active. The promoter types are associated with different chromatin accessibility in ATAC‐seq data and have different expression characteristics in single‐cell RNA‐seq data. The two promoter types may therefore be optimized for different properties: paused promoters show more consistent expression when active, while TATA promoters have lower background expression when inactive. We propose that tissue‐specific genes have evolved to use two different strategies for their differential expression across tissues.
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spelling doaj-art-f26a8cfb54b147fd97bbef5f3d2ae4382025-08-20T03:46:37ZengSpringer NatureMolecular Systems Biology1744-42922021-02-0117211210.15252/msb.20209866TATA and paused promoters active in differentiated tissues have distinct expression characteristicsVivekanandan Ramalingam0Malini Natarajan1Jeff Johnston2Julia Zeitlinger3Stowers Institute for Medical ResearchStowers Institute for Medical ResearchStowers Institute for Medical ResearchStowers Institute for Medical ResearchAbstract Core promoter types differ in the extent to which RNA polymerase II (Pol II) pauses after initiation, but how this affects their tissue‐specific gene expression characteristics is not well understood. While promoters with Pol II pausing elements are active throughout development, TATA promoters are highly active in differentiated tissues. We therefore used a genomics approach on late‐stage Drosophila embryos to analyze the properties of promoter types. Using tissue‐specific Pol II ChIP‐seq, we found that paused promoters have high levels of paused Pol II throughout the embryo, even in tissues where the gene is not expressed, while TATA promoters only show Pol II occupancy when the gene is active. The promoter types are associated with different chromatin accessibility in ATAC‐seq data and have different expression characteristics in single‐cell RNA‐seq data. The two promoter types may therefore be optimized for different properties: paused promoters show more consistent expression when active, while TATA promoters have lower background expression when inactive. We propose that tissue‐specific genes have evolved to use two different strategies for their differential expression across tissues.https://doi.org/10.15252/msb.20209866effector genesgene expression noisePol II pausingscRNA‐seqTATA promoter
spellingShingle Vivekanandan Ramalingam
Malini Natarajan
Jeff Johnston
Julia Zeitlinger
TATA and paused promoters active in differentiated tissues have distinct expression characteristics
Molecular Systems Biology
effector genes
gene expression noise
Pol II pausing
scRNA‐seq
TATA promoter
title TATA and paused promoters active in differentiated tissues have distinct expression characteristics
title_full TATA and paused promoters active in differentiated tissues have distinct expression characteristics
title_fullStr TATA and paused promoters active in differentiated tissues have distinct expression characteristics
title_full_unstemmed TATA and paused promoters active in differentiated tissues have distinct expression characteristics
title_short TATA and paused promoters active in differentiated tissues have distinct expression characteristics
title_sort tata and paused promoters active in differentiated tissues have distinct expression characteristics
topic effector genes
gene expression noise
Pol II pausing
scRNA‐seq
TATA promoter
url https://doi.org/10.15252/msb.20209866
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