The miR-430 locus with extreme promoter density forms a transcription body during the minor wave of zygotic genome activation

Yavor Hadzhiev; Lucy Wheatley; Ledean Cooper; Federico Ansaloni; Celina Whalley; Zhelin Chen; Sara Finaurini; Stefano Gustincich; Remo Sanges; Shawn Burgess; Andrew Beggs; Ferenc Müller

doi:10.1016/j.devcel.2022.12.007

The miR-430 locus with extreme promoter density forms a transcription body during the minor wave of zygotic genome activation

Yavor Hadzhiev, Lucy Wheatley, Ledean Cooper, Federico Ansaloni, Celina Whalley, Zhelin Chen, Sara Finaurini, Stefano Gustincich, Remo Sanges, Shawn Burgess, Andrew Beggs, Ferenc Müller^*

^*Corresponding author for this work

Cancer and Genomic Sciences

Research output: Contribution to journal › Article › peer-review

58 Downloads (Pure)

Abstract

In anamniote embryos, the major wave of zygotic genome activation starts during the mid-blastula transition. However, some genes escape global genome repression, are activated substantially earlier, and contribute to the minor wave of genome activation. The mechanisms underlying the minor wave of genome activation are little understood. We explored the genomic organization and cis-regulatory mechanisms of a transcription body, in which the minor wave of genome activation is first detected in zebrafish. We identified the miR-430 cluster as having excessive copy number and the highest density of Pol-II-transcribed promoters in the genome, and this is required for forming the transcription body. However, this transcription body is not essential for, nor does it encompasse, minor wave transcription globally. Instead, distinct minor-wave-specific promoter architecture suggests that promoter-autonomous mechanisms regulate the minor wave of genome activation. The minor-wave-specific features also suggest distinct transcription initiation mechanisms between the minor and major waves of genome activation.

Original language	English
Pages (from-to)	155-170.e8
Number of pages	24
Journal	Developmental Cell
Volume	58
Issue number	2
DOIs	https://doi.org/10.1016/j.devcel.2022.12.007
Publication status	Published - 23 Jan 2023

Bibliographical note

Funding Information:
This work was funded by a Wellcome Trust Investigator Award ( 106955/Z/15/Z ) and funding from the MDS Research Development Fund to F.M. and was supported in part (S.B.) by the Intramural Research Program of the NHGRI ( ZIAHG200386-06 ). We thank Genomics Birmingham for sequencing, the imaging facility of the Technology Hub core, and the BMSU facility at the University of Birmingham. We thank S. Branford and J.-B. Cazier for support from the University of Birmingham BlueBEAR/CaStLeS high performance computing cluster. We also thank A. Jimenez-Gonzalez for embryo injections and P. Balwierz for advice on gene copy-number calculations. We thank M. Lagha for their smiFISH protocol. We thank Darius Balciunas for providing the pDB783:Xla.crygc-attP-Gal4vp16-14UAS:eGFP plasmid.

Publisher Copyright:
© 2022 The Authors

Keywords

core promoter features
minor wave
miR-430
RNA Pol II
transcription body
zygotic genome activation

ASJC Scopus subject areas

Molecular Biology
General Biochemistry,Genetics and Molecular Biology
Developmental Biology
Cell Biology

Access to Document

10.1016/j.devcel.2022.12.007Licence: Creative Commons: Attribution (CC BY)

HadzhievY2023miR430Final published version, 4.41 MBLicence: Creative Commons: Attribution (CC BY)

The core promoter: an unexplored regulatory level of transcription during vertebrate development
Müller, F.
THE WELLCOME TRUST, Imperial College
1/12/15 → 31/10/21
Project: Research

Cite this

Hadzhiev, Y., Wheatley, L., Cooper, L., Ansaloni, F., Whalley, C., Chen, Z., Finaurini, S., Gustincich, S., Sanges, R., Burgess, S., Beggs, A., & Müller, F. (2023). The miR-430 locus with extreme promoter density forms a transcription body during the minor wave of zygotic genome activation. Developmental Cell, 58(2), 155-170.e8. https://doi.org/10.1016/j.devcel.2022.12.007

@article{f6e62f78ab7a4e9d9dde475a7a419ea0,

title = "The miR-430 locus with extreme promoter density forms a transcription body during the minor wave of zygotic genome activation",

abstract = "In anamniote embryos, the major wave of zygotic genome activation starts during the mid-blastula transition. However, some genes escape global genome repression, are activated substantially earlier, and contribute to the minor wave of genome activation. The mechanisms underlying the minor wave of genome activation are little understood. We explored the genomic organization and cis-regulatory mechanisms of a transcription body, in which the minor wave of genome activation is first detected in zebrafish. We identified the miR-430 cluster as having excessive copy number and the highest density of Pol-II-transcribed promoters in the genome, and this is required for forming the transcription body. However, this transcription body is not essential for, nor does it encompasse, minor wave transcription globally. Instead, distinct minor-wave-specific promoter architecture suggests that promoter-autonomous mechanisms regulate the minor wave of genome activation. The minor-wave-specific features also suggest distinct transcription initiation mechanisms between the minor and major waves of genome activation.",

keywords = "core promoter features, minor wave, miR-430, RNA Pol II, transcription body, zygotic genome activation",

author = "Yavor Hadzhiev and Lucy Wheatley and Ledean Cooper and Federico Ansaloni and Celina Whalley and Zhelin Chen and Sara Finaurini and Stefano Gustincich and Remo Sanges and Shawn Burgess and Andrew Beggs and Ferenc M{\"u}ller",

note = "Funding Information: This work was funded by a Wellcome Trust Investigator Award ( 106955/Z/15/Z ) and funding from the MDS Research Development Fund to F.M. and was supported in part (S.B.) by the Intramural Research Program of the NHGRI ( ZIAHG200386-06 ). We thank Genomics Birmingham for sequencing, the imaging facility of the Technology Hub core, and the BMSU facility at the University of Birmingham. We thank S. Branford and J.-B. Cazier for support from the University of Birmingham BlueBEAR/CaStLeS high performance computing cluster. We also thank A. Jimenez-Gonzalez for embryo injections and P. Balwierz for advice on gene copy-number calculations. We thank M. Lagha for their smiFISH protocol. We thank Darius Balciunas for providing the pDB783:Xla.crygc-attP-Gal4vp16-14UAS:eGFP plasmid. Publisher Copyright: {\textcopyright} 2022 The Authors",

year = "2023",

month = jan,

day = "23",

doi = "10.1016/j.devcel.2022.12.007",

language = "English",

volume = "58",

pages = "155--170.e8",

journal = "Developmental Cell",

issn = "1534-5807",

publisher = "Elsevier",

number = "2",

}

Hadzhiev, Y, Wheatley, L, Cooper, L, Ansaloni, F, Whalley, C, Chen, Z, Finaurini, S, Gustincich, S, Sanges, R, Burgess, S, Beggs, A & Müller, F 2023, 'The miR-430 locus with extreme promoter density forms a transcription body during the minor wave of zygotic genome activation', Developmental Cell, vol. 58, no. 2, pp. 155-170.e8. https://doi.org/10.1016/j.devcel.2022.12.007

TY - JOUR

T1 - The miR-430 locus with extreme promoter density forms a transcription body during the minor wave of zygotic genome activation

AU - Hadzhiev, Yavor

AU - Wheatley, Lucy

AU - Cooper, Ledean

AU - Ansaloni, Federico

AU - Whalley, Celina

AU - Chen, Zhelin

AU - Finaurini, Sara

AU - Gustincich, Stefano

AU - Sanges, Remo

AU - Burgess, Shawn

AU - Beggs, Andrew

AU - Müller, Ferenc

N1 - Funding Information: This work was funded by a Wellcome Trust Investigator Award ( 106955/Z/15/Z ) and funding from the MDS Research Development Fund to F.M. and was supported in part (S.B.) by the Intramural Research Program of the NHGRI ( ZIAHG200386-06 ). We thank Genomics Birmingham for sequencing, the imaging facility of the Technology Hub core, and the BMSU facility at the University of Birmingham. We thank S. Branford and J.-B. Cazier for support from the University of Birmingham BlueBEAR/CaStLeS high performance computing cluster. We also thank A. Jimenez-Gonzalez for embryo injections and P. Balwierz for advice on gene copy-number calculations. We thank M. Lagha for their smiFISH protocol. We thank Darius Balciunas for providing the pDB783:Xla.crygc-attP-Gal4vp16-14UAS:eGFP plasmid. Publisher Copyright: © 2022 The Authors

PY - 2023/1/23

Y1 - 2023/1/23

N2 - In anamniote embryos, the major wave of zygotic genome activation starts during the mid-blastula transition. However, some genes escape global genome repression, are activated substantially earlier, and contribute to the minor wave of genome activation. The mechanisms underlying the minor wave of genome activation are little understood. We explored the genomic organization and cis-regulatory mechanisms of a transcription body, in which the minor wave of genome activation is first detected in zebrafish. We identified the miR-430 cluster as having excessive copy number and the highest density of Pol-II-transcribed promoters in the genome, and this is required for forming the transcription body. However, this transcription body is not essential for, nor does it encompasse, minor wave transcription globally. Instead, distinct minor-wave-specific promoter architecture suggests that promoter-autonomous mechanisms regulate the minor wave of genome activation. The minor-wave-specific features also suggest distinct transcription initiation mechanisms between the minor and major waves of genome activation.

AB - In anamniote embryos, the major wave of zygotic genome activation starts during the mid-blastula transition. However, some genes escape global genome repression, are activated substantially earlier, and contribute to the minor wave of genome activation. The mechanisms underlying the minor wave of genome activation are little understood. We explored the genomic organization and cis-regulatory mechanisms of a transcription body, in which the minor wave of genome activation is first detected in zebrafish. We identified the miR-430 cluster as having excessive copy number and the highest density of Pol-II-transcribed promoters in the genome, and this is required for forming the transcription body. However, this transcription body is not essential for, nor does it encompasse, minor wave transcription globally. Instead, distinct minor-wave-specific promoter architecture suggests that promoter-autonomous mechanisms regulate the minor wave of genome activation. The minor-wave-specific features also suggest distinct transcription initiation mechanisms between the minor and major waves of genome activation.

KW - core promoter features

KW - minor wave

KW - miR-430

KW - RNA Pol II

KW - transcription body

KW - zygotic genome activation

UR - http://www.scopus.com/inward/record.url?scp=85146442686&partnerID=8YFLogxK

U2 - 10.1016/j.devcel.2022.12.007

DO - 10.1016/j.devcel.2022.12.007

M3 - Article

C2 - 36693321

AN - SCOPUS:85146442686

SN - 1534-5807

VL - 58

SP - 155-170.e8

JO - Developmental Cell

JF - Developmental Cell

IS - 2

ER -

The miR-430 locus with extreme promoter density forms a transcription body during the minor wave of zygotic genome activation

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

Access to Document

Fingerprint

Projects

The core promoter: an unexplored regulatory level of transcription during vertebrate development

Cite this