Transcriptional Memory in the Drosophila Embryo

Abstract

Transmission of active transcriptional states from mother to daughter cells has the potential to foster precision in the gene expression programs underlying development. Such transcriptional memory has been specifically proposed to promote rapid reactivation of complex gene expression profiles following successive mitoses in Drosophila development [1]. By monitoring transcription in living Drosophila embryos, we provide the first evidence for transcriptional memory in animal development. We specifically monitored the activities of stochastically expressed transgenes in order to distinguish active and inactive mother cells and the behaviors of their daughter nuclei following mitosis. Quantitative analyses reveal that there is a 4-fold higher probability for rapid reactivation following mitosis when the mother experienced transcription. Moreover, memory nuclei activate transcription twice as fast as neighboring inactive mothers, thus leading to augmented levels of gene expression. We propose that transcriptional memory is a mechanism of precision, which helps coordinate gene activity during embryogenesis. § Correspondance : msl2@princeton.edu, mounia.lagha@igmm.cnrs.fr. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. Experimental ProceduresAll MS2 containing transgenic embryos were generated by the targeted integration (VK33) of snaEnhancer<minimal promoter<24X-MS2 repeats-yellow plasmids [10]. Histone-RFP and MCP-GFP are maternally provided by a stock described in [6]. All movies have been acquired using a 780lsm Zeiss confocal microscope with the following settings: 40× oil objective, a 2.1 zoomed 512×512 16bit/ pixel image, with bidirectional scanning, 21 z-stacks, 0.5μm apart. Under these conditions, the time resolution is in the range of 15-20 seconds per frame. Image processing of the MS2-MCP-GFP signal is performed in a semi-automatic way using custom Matlab algorithms, based on our previously published work [5]. See supplementary information for details on transgenic fly stocks, molecular biology, imaging and quantification.

Distinct heterochromatin‐like domains promote transcriptional memory and silence parasitic genetic elements in bacteria

“…Given the sophisticated regulatory logic implemented at the idn promoter by a combination of local (GlaR, GntR, IdnR) and global (CRP) regulators, it is unclear what additional function is played by the apparently repressive EPOD covering this region. Drawing inspiration from the behavior of chromatin modifications in eukaryotes (e.g., Francis & Kingston, 2001;Kundu et al, 2007;Lagha et al, 2017;Palozola et al, 2019), we hypothesized that one function of EPODs could be to facilitate transcriptional memory. We thus performed head-to-head competition experiments in KDGcontaining and glucose-containing media comparing the growth of cells that have been exposed to KDG (Fig 4A).…”