Establishment and maintenance of heritable chromatin structure during early Drosophila embryogenesis
Abstract
During embryogenesis, the initial chromatin state is established during a period of rapid proliferative activity. We have measured with three-minute time resolution how heritable patterns of chromatin structure are initially established and maintained during the midblastula transition (MBT). We find that regions of accessibility are established sequentially, where enhancers are opened in advance of promoters and insulators. These open states are stably maintained in highly condensed mitotic chromatin to ensure faithful inheritance of prior accessibility status across cell divisions. The temporal progression of establishment is controlled by the biological timers that control the onset of the MBT. In general, acquisition of promoter accessibility is controlled by the biological timer that measures the nucleo-cytoplasmic (N:C) ratio whereas timing of enhancer accessibility is regulated independently of the N:C ratio. These different timing classes each associate with binding sites for two transcription factors, GAGA-factor and Zelda, previously implicated in controlling chromatin accessibility at ZGA.
Data availability
-
ATAC-seq analysis of chromatin accessibility and nucleosome positioning in Drosophila melanogaster precellular blastoderm embryosPublicly available at the NCBI Gene Expression Omnibus (accession no: GSE83851).
-
Zelda binding in the early Drosophila melanogaster embryo marks regions subsequently activated at the maternal-to-zygotic transitionPublicly available at the NCBI Gene Expression Omnibus (accession no: GSE30757) .
-
Genomewide analysis of Insulator protein binding sites in Drosophila embryos at E0-12Publicly available at the NCBI Gene Expression Omnibus (accession no: GSE16245) .
-
Drosophila at different time points of development: ChIP-chip, ChIP-seq, RNA-seqPublicly available at the NCBI Gene Expression Omnibus (accession no: GSE15292) .
Article and author information
Author details
Funding
National Institutes of Health (F32HD072653)
- Shelby A Blythe
Howard Hughes Medical Institute
- Shelby A Blythe
- Eric F Wieschaus
National Institutes of Health (R37HD15587)
- Eric F Wieschaus
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Allan C Spradling, Howard Hughes Medical Institute, Carnegie Institution for Science, United States
Version history
- Received: July 28, 2016
- Accepted: November 21, 2016
- Accepted Manuscript published: November 23, 2016 (version 1)
- Version of Record published: December 14, 2016 (version 2)
Copyright
© 2016, Blythe & Wieschaus
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.
Metrics
-
- 6,232
- Page views
-
- 1,348
- Downloads
-
- 89
- Citations
Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Developmental Biology
- Neuroscience
Development of the nervous system depends on signaling centers – specialized cellular populations that produce secreted molecules to regulate neurogenesis in the neighboring neuroepithelium. In some cases, signaling center cells also differentiate to produce key types of neurons. The formation of a signaling center involves its induction, the maintenance of expression of its secreted molecules, and cell differentiation and migration events. How these distinct processes are coordinated during signaling center development remains unknown. By performing studies in mice, we show that Lmx1a acts as a master regulator to orchestrate the formation and function of the cortical hem (CH), a critical signaling center that controls hippocampus development. Lmx1a co-regulates CH induction, its Wnt signaling, and the differentiation and migration of CH-derived Cajal–Retzius neurons. Combining RNAseq, genetic, and rescue experiments, we identified major downstream genes that mediate distinct Lmx1a-dependent processes. Our work revealed that signaling centers in the mammalian brain employ master regulatory genes and established a framework for analyzing signaling center development.
-
- Developmental Biology
- Evolutionary Biology
Cephalochordates and tunicates represent the only two groups of invertebrate chordates, and extant cephalochordates – commonly known as amphioxus or lancelets – are considered the best proxy for the chordate ancestor, from which they split around 520 million years ago. Amphioxus has been an important organism in the fields of zoology and embryology since the 18th century, and the morphological and genomic simplicity of cephalochordates (compared to vertebrates) makes amphioxus an attractive model for studying chordate biology at the cellular and molecular levels. Here we describe the life cycle of amphioxus, and discuss the natural histories and habitats of the different species of amphioxus. We also describe their use as laboratory animal models, and discuss the techniques that have been developed to study different aspects of amphioxus.