Conserved noncoding transcription and core promoter regulatory code in early Drosophila development

  1. Philippe J Batut
  2. Thomas R Gingeras  Is a corresponding author
  1. Cold Spring Harbor Laboratory, United States

Abstract

Multicellular development is driven by regulatory programs that orchestrate the transcription of protein-coding and noncoding genes. To decipher this genomic regulatory code, and to investigate the developmental relevance of noncoding transcription, we compared genome-wide promoter activity throughout embryogenesis in 5 Drosophila species. Core promoters, generally not thought to play a significant regulatory role, in fact impart restrictions on the developmental timing of gene expression on a global scale. We propose a hierarchical regulatory model in which core promoters define broad windows of opportunity for expression, by defining a range of transcription factors from which they can receive regulatory inputs. This two-tiered mechanism globally orchestrates developmental gene expression, including extremely widespread noncoding transcription. The sequence and expression specificity of noncoding RNA promoters are evolutionarily conserved, implying biological relevance. Overall, this work introduces a hierarchical model for developmental gene regulation, and reveals a major role for noncoding transcription in animal development.

Data availability

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Philippe J Batut

    Watson School of Biological Sciences, Cold Spring Harbor Laboratory, Cold Spring Harbor, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4250-0663
  2. Thomas R Gingeras

    Watson School of Biological Sciences, Cold Spring Harbor Laboratory, Cold Spring Harbor, United States
    For correspondence
    gingeras@cshl.edu
    Competing interests
    Thomas R Gingeras, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9106-3573

Funding

Cold Spring Harbor Laboratory Watson School (Florence Gould Fellowship)

  • Philippe J Batut

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Alfonso Valencia, Barcelona Supercomputing Center - BSC, Spain

Ethics

Animal experimentation: see attached upload.

Version history

  1. Received: May 30, 2017
  2. Accepted: December 19, 2017
  3. Accepted Manuscript published: December 20, 2017 (version 1)
  4. Version of Record published: January 4, 2018 (version 2)

Copyright

© 2017, Batut & Gingeras

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Philippe J Batut
  2. Thomas R Gingeras
(2017)
Conserved noncoding transcription and core promoter regulatory code in early Drosophila development
eLife 6:e29005.
https://doi.org/10.7554/eLife.29005

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https://doi.org/10.7554/eLife.29005

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