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Temporal Coordination of Gene Networks by Zelda in the Early Drosophila Embryo
Journal article   Open access   Peer reviewed

Temporal Coordination of Gene Networks by Zelda in the Early Drosophila Embryo

Chung-Yi Nien, Hsiao-Lan Liang, Stephen Butcher, Yujia Sun, Shengbo Fu, Tenzin Gocha, Nikolai Kirov, J. Robert Manak and Christine Rushlow
PLoS genetics, Vol.7(10), pp.e1002339-e1002339
10/2011
DOI: 10.1371/journal.pgen.1002339
PMCID: PMC3197689
PMID: 22028675
url
https://doi.org/10.1371/journal.pgen.1002339View
Published (Version of record) Open Access

Abstract

In past years, much attention has focused on the gene networks that regulate early developmental processes, but less attention has been paid to how multiple networks and processes are temporally coordinated. Recently the discovery of the transcriptional activator Zelda (Zld), which binds to CAGGTAG and related sequences present in the enhancers of many early-activated genes in Drosophila , hinted at a mechanism for how batteries of genes could be simultaneously activated. Here we use genome-wide binding and expression assays to identify Zld target genes in the early embryo with the goal of unraveling the gene circuitry regulated by Zld. We found that Zld binds to genes involved in early developmental processes such as cellularization, sex determination, neurogenesis, and pattern formation. In the absence of Zld, many target genes failed to be activated, while others, particularly the patterning genes, exhibited delayed transcriptional activation, some of which also showed weak and/or sporadic expression. These effects disrupted the normal sequence of patterning-gene interactions and resulted in highly altered spatial expression patterns, demonstrating the significance of a timing mechanism in early development. In addition, we observed prevalent overlap between Zld-bound regions and genomic “hotspot” regions, which are bound by many developmental transcription factors, especially the patterning factors. This, along with the finding that the most over-represented motif in hotspots, CAGGTA , is the Zld binding site, implicates Zld in promoting hotspot formation. We propose that Zld promotes timely and robust transcriptional activation of early-gene networks so that developmental events are coordinated and cell fates are established properly in the cellular blastoderm embryo. Development of a fertilized egg into a multicellular organism comprises a series of precisely timed events initially controlled by factors deposited into the egg. Some of these factors are localized to specific regions of the embryo and instruct cells to adopt certain fates. In this way, these “morphogen” factors lend pattern to the body plan so that different appendages are formed in the right places. In contrast, other factors are evenly distributed throughout the embryo and regulate processes concerning all cells. For example, in Drosophila , Zld is a ubiquitous factor that collectively activates batteries of genes essential for further development. Here we show that Zld also functions alongside the spatial morphogens to ensure timely and robust activation of their target genes. In the absence of Zld, activation of these genes is delayed, which derails the proper order of gene interactions and ultimately disrupts gene expression patterns. Our results demonstrate the significance of a timing mechanism in coordinating regulatory gene networks during early development, and they bring a new perspective to classical concepts of how spatial regulation can be achieved.
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