Modulation of transcription burst amplitude underpins dosage compensation in the Drosophila embryo

Summary: Dosage compensation, the balancing of X-linked gene expression between sexes and to the autosomes, is critical to an organism’s fitness and survival. In Drosophila, dosage compensation involves hypertranscription of the male X chromosome. Here, we use quantitative live imaging and modeling...

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Main Authors: Lauren Forbes Beadle, Hongpeng Zhou, Magnus Rattray, Hilary L. Ashe
Format: Article
Language:English
Published: Elsevier 2023-04-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124723003935
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author Lauren Forbes Beadle
Hongpeng Zhou
Magnus Rattray
Hilary L. Ashe
author_facet Lauren Forbes Beadle
Hongpeng Zhou
Magnus Rattray
Hilary L. Ashe
author_sort Lauren Forbes Beadle
collection DOAJ
description Summary: Dosage compensation, the balancing of X-linked gene expression between sexes and to the autosomes, is critical to an organism’s fitness and survival. In Drosophila, dosage compensation involves hypertranscription of the male X chromosome. Here, we use quantitative live imaging and modeling at single-cell resolution to study X chromosome dosage compensation in Drosophila. We show that the four X chromosome genes studied undergo transcriptional bursting in male and female embryos. Mechanistically, our data reveal that transcriptional upregulation of male X chromosome genes is primarily mediated by a higher RNA polymerase II initiation rate and burst amplitude across the expression domain. In contrast, burst frequency is spatially modulated in nuclei within the expression domain in response to different transcription factor concentrations to tune the transcriptional response. Together, these data show how the local and global regulation of distinct burst parameters can establish the complex transcriptional outputs underpinning developmental patterning.
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spelling doaj.art-11b317e5b51240e388482d81b8ca4dcd2023-04-15T05:52:30ZengElsevierCell Reports2211-12472023-04-01424112382Modulation of transcription burst amplitude underpins dosage compensation in the Drosophila embryoLauren Forbes Beadle0Hongpeng Zhou1Magnus Rattray2Hilary L. Ashe3Faculty of Biology, Medicine and Health, University of Manchester, Manchester M13 9PT, UKFaculty of Biology, Medicine and Health, University of Manchester, Manchester M13 9PT, UKFaculty of Biology, Medicine and Health, University of Manchester, Manchester M13 9PT, UK; Corresponding authorFaculty of Biology, Medicine and Health, University of Manchester, Manchester M13 9PT, UK; Corresponding authorSummary: Dosage compensation, the balancing of X-linked gene expression between sexes and to the autosomes, is critical to an organism’s fitness and survival. In Drosophila, dosage compensation involves hypertranscription of the male X chromosome. Here, we use quantitative live imaging and modeling at single-cell resolution to study X chromosome dosage compensation in Drosophila. We show that the four X chromosome genes studied undergo transcriptional bursting in male and female embryos. Mechanistically, our data reveal that transcriptional upregulation of male X chromosome genes is primarily mediated by a higher RNA polymerase II initiation rate and burst amplitude across the expression domain. In contrast, burst frequency is spatially modulated in nuclei within the expression domain in response to different transcription factor concentrations to tune the transcriptional response. Together, these data show how the local and global regulation of distinct burst parameters can establish the complex transcriptional outputs underpinning developmental patterning.http://www.sciencedirect.com/science/article/pii/S2211124723003935CP: Molecular biology
spellingShingle Lauren Forbes Beadle
Hongpeng Zhou
Magnus Rattray
Hilary L. Ashe
Modulation of transcription burst amplitude underpins dosage compensation in the Drosophila embryo
Cell Reports
CP: Molecular biology
title Modulation of transcription burst amplitude underpins dosage compensation in the Drosophila embryo
title_full Modulation of transcription burst amplitude underpins dosage compensation in the Drosophila embryo
title_fullStr Modulation of transcription burst amplitude underpins dosage compensation in the Drosophila embryo
title_full_unstemmed Modulation of transcription burst amplitude underpins dosage compensation in the Drosophila embryo
title_short Modulation of transcription burst amplitude underpins dosage compensation in the Drosophila embryo
title_sort modulation of transcription burst amplitude underpins dosage compensation in the drosophila embryo
topic CP: Molecular biology
url http://www.sciencedirect.com/science/article/pii/S2211124723003935
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