Abstract
In developing embryos, gene regulatory networks drive cells towards discrete terminal fates, a process called canalization. We studied the behavior of the anterior-posterior segmentation network in Drosophila melanogaster embryos by depleting a key maternal input, bicoid (bcd), and measuring gene expression patterns of the network at cellular resolution. This method results in a gene expression atlas containing the levels of mRNA or protein expression of 13 core patterning genes over six time points for every cell of the blastoderm embryo. This is the first cellular resolution dataset of a genetically perturbed Drosophila embryo that captures all cells in 3D. We describe the technical developments required to build this atlas and how the method can be employed and extended by others. We also analyze this novel dataset to characterize the degree and timing of cell fate canalization in the segmentation network. We find that in two layers of this gene regulatory network, following depletion of bcd, individual cells rapidly canalize towards normal cell fates. This result supports the hypothesis that the segmentation network directly canalizes cell fate, rather than an alternative hypothesis whereby cells are initially mis-specified and later eliminated by apoptosis. Our gene expression atlas provides a high resolution picture of a classic perturbation and will enable further computational modeling of canalization and gene regulation in this transcriptional network.
Highlights
Specialization of cell fate underlies the diversity of metazoan form and function
We found that all gap gene cell fates present in the bcddepleted embryo were present in wild type
The techniques we describe can be readily applied to other genetic perturbations, and the gene expression atlas of a bcd depleted embryo we present will be a useful resource for computational analysis and modeling of gene regulation in Drosophila blastoderm embryos
Summary
Specialization of cell fate underlies the diversity of metazoan form and function. Cell fates are specified robustly and precisely by gene regulatory networks that pattern embryos (Davidson, 2006). Anterior-posterior patterning of the embryo is controlled by the well-characterized segmentation network Received 11 September 2014; Accepted 1 December 2014 et al, 2012) Computational models of this network have tested the sufficiency of known connections, proposed new connections and tested network-level properties (reviewed by Wunderlich and DePace, 2011; Jaeger et al, 2012)
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