Kinetic sculpting of the seven stripes of the Drosophila even-skipped gene
Abstract
We used live imaging to visualize the transcriptional dynamics of the Drosophila melanogaster even-skipped gene at single-cell and high temporal resolution as its seven stripe expression pattern forms, and developed tools to characterize and visualize how transcriptional bursting varies over time and space. We find that despite being created by the independent activity of five enhancers, even-skipped stripes are sculpted by the same kinetic phenomena: a coupled increase of burst frequency and amplitude. By tracking the position and activity of individual nuclei, we show that stripe movement is driven by the exchange of bursting nuclei from the posterior to anterior stripe flanks. Our work provides a conceptual, theoretical and computational framework for dissecting pattern formation in space and time, and reveals how the coordinated transcriptional activity of individual nuclei shape complex developmental patterns.
Data availability
All of the raw and processed data described in this paper are available on Data Dryad at doi:10.6078/D1XX33 and computational notebooks with necessary data to regenerate analyses and figures is available in File S1 and at https://github.com/mbeisen/Berrocal_2020.
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Kinetic sculpting of the seven stripes of the Drosophila even-skipped geneDryad Digital Repository, https://doi.org/10.6078/D1XX33.
Article and author information
Author details
Funding
Howard Hughes Medical Institute (Investigator Award)
- Michael B Eisen
National Science Foundation (1652236)
- Hernan G Garcia
National Institutes of Health (DP2-OD024541-01)
- Hernan G Garcia
National Institutes of Health (5T32HG000047-18)
- Nicholas C Lammers
University of California Institute for Mexico and the United States (NA)
- Augusto Berrocal
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Robert H Singer, Albert Einstein College of Medicine, United States
Version history
- Received: July 31, 2020
- Accepted: October 9, 2020
- Accepted Manuscript published: December 10, 2020 (version 1)
- Version of Record published: February 5, 2021 (version 2)
Copyright
© 2020, Berrocal et al.
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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Histone H1 participates in chromatin condensation and regulates nuclear processes. Human somatic cells may contain up to seven histone H1 variants, although their functional heterogeneity is not fully understood. Here, we have profiled the differential nuclear distribution of the somatic H1 repertoire in human cells through imaging techniques including super-resolution microscopy. H1 variants exhibit characteristic distribution patterns in both interphase and mitosis. H1.2, H1.3, and H1.5 are universally enriched at the nuclear periphery in all cell lines analyzed and co-localize with compacted DNA. H1.0 shows a less pronounced peripheral localization, with apparent variability among different cell lines. On the other hand, H1.4 and H1X are distributed throughout the nucleus, being H1X universally enriched in high-GC regions and abundant in the nucleoli. Interestingly, H1.4 and H1.0 show a more peripheral distribution in cell lines lacking H1.3 and H1.5. The differential distribution patterns of H1 suggest specific functionalities in organizing lamina-associated domains or nucleolar activity, which is further supported by a distinct response of H1X or phosphorylated H1.4 to the inhibition of ribosomal DNA transcription. Moreover, H1 variants depletion affects chromatin structure in a variant-specific manner. Concretely, H1.2 knock-down, either alone or combined, triggers a global chromatin decompaction. Overall, imaging has allowed us to distinguish H1 variants distribution beyond the segregation in two groups denoted by previous ChIP-Seq determinations. Our results support H1 variants heterogeneity and suggest that variant-specific functionality can be shared between different cell types.