Rapid Transcription Fosters Coordinate snail Expression in the Drosophila Embryo

Michael Levine,Alistair Nicol Boettiger

doi:10.1016/j.celrep.2012.12.015

Michael Levine, Alistair Nicol Boettiger

Open Access

https://doi.org/10.1016/j.celrep.2012.12.015

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Abstract

Transcription is commonly held to be a highly stochastic process, resulting in considerable heterogeneity of gene expression among the different cells in a population. Here, we employ quantitative in situ hybridization methods coupled with high-resolution imaging assays to measure the expression of snail, a developmental patterning gene necessary for coordinating the invagination of the mesoderm during gastrulation of the Drosophila embryo. Our measurements of steady-state mRNAs suggest that there is very little variation in snail expression across the different cells that make up the mesoderm and that synthesis approaches the kinetic limits of Pol II processivity. We propose that rapid transcription kinetics and negative autoregulation are responsible for the remarkable homogeneity of snail expression and the coordination of mesoderm invagination.

Highlights

Recent studies suggest that inherent stochastic processes underlying transcription are a significant source of cell-cell variation in gene expression
We employ quantitative in situ hybridization methods coupled to high-resolution imaging assays to measure the expression of snail, a developmental patterning gene necessary for coordinating the invagination of the mesoderm during gastrulation of the Drosophila embryo
Our measurements of steady-state mRNAs suggest that there is very little variation in snail expression across the different cells comprising the mesoderm, and that synthesis approaches the kinetic limits of Pol II processivity

Summary

Introduction

Recent studies suggest that inherent stochastic processes underlying transcription are a significant source of cell-cell variation in gene expression. Such variation can be explained by theoretical considerations of diffusion-driven processes involving small numbers of molecules (Munsky et al, 2012). Many developmental processes, such as coordinated cell movements during gastrulation, are dependent upon uniform expression of key patterning genes. It remains to be understood what mechanisms exist to either compensate or correct the variation often observed during transcription to allow for the coordination of cell behavior within an embryonic tissue

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