Distinct core promoter codes drive transcription initiation at key developmental transitions in a marine chordate
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Author(s)
Danks, GB
Navratilova, P
Lenhard, B
Thompson, EM
Type
Journal Article
Abstract
BACKGROUND: Development is largely driven by transitions between transcriptional programs. The initiation of transcription at appropriate sites in the genome is a key component of this and yet few rules governing selection are known. Here, we used cap analysis of gene expression (CAGE) to generate bp-resolution maps of transcription start sites (TSSs) across the genome of Oikopleura dioica, a member of the closest living relatives to vertebrates. RESULTS: Our TSS maps revealed promoter features in common with vertebrates, as well as striking differences, and uncovered key roles for core promoter elements in the regulation of development. During spermatogenesis there is a genome-wide shift in mode of transcription initiation characterized by a novel core promoter element. This element was associated with > 70% of male-specific transcription, including the use of cryptic internal promoters within operons. In many cases this led to the exclusion of trans-splice sites, revealing a novel mechanism for regulating which mRNAs receive the spliced leader. Binding of the cell cycle regulator, E2F1, is enriched at the TSS of maternal genes in endocycling nurse nuclei. In addition, maternal promoters lack the TATA-like element found in zebrafish and have broad, rather than sharp, architectures with ordered nucleosomes. Promoters of ribosomal protein genes lack the highly conserved TCT initiator. We also report an association between DNA methylation on transcribed gene bodies and the TATA-box. CONCLUSIONS: Our results reveal that distinct functional promoter classes and overlapping promoter codes are present in protochordates like in vertebrates, but show extraordinary lineage-specific innovations. Furthermore, we uncover a genome-wide, developmental stage-specific shift in the mode of TSS selection. Our results provide a rich resource for the study of promoter structure and evolution in Metazoa.
Date Issued
2018-02-26
Online Publication Date
2018-02-26
2018-03-20T09:48:16Z
Date Acceptance
2018-01-28
ISSN
1471-2164
Publisher
BioMed Central
Journal / Book Title
BMC Genomics
Volume
19
Issue
1
Copyright Statement
© The Author(s). 2018
Open Access
This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (
http://creativecommons.org/licenses/by/4.0/
), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the
Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver
(http://creativecommons.org/publicdomain/zero/1.0/
) applies to the data made available in this article, unless otherwise stated.
Open Access
This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (
http://creativecommons.org/licenses/by/4.0/
), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the
Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver
(http://creativecommons.org/publicdomain/zero/1.0/
) applies to the data made available in this article, unless otherwise stated.
Source Database
pubmed
Sponsor
Commission of the European Communities
Identifier
https://www.ncbi.nlm.nih.gov/pubmed/29482522
10.1186/s12864-018-4504-5
Grant Number
242048
Subjects
Core promoter
DNA methylation
Histone modification
MZT
Oogenesis
Operons
Spermatogenesis
TATA-box
Transcription initiation
06 Biological Sciences
11 Medical And Health Sciences
08 Information And Computing Sciences
Bioinformatics
Publication Status
Published
Country
England
Article Number
ARTN 164