Spatial expression of transcription factors in Drosophila embryonic organ development

Ann S Hammonds,Manolis Kellis,Susan E Celniker,Richard Weiszmann,Christopher A Bristow,Siqi Wu,Volker Hartenstein,William W Fisher,Bin Yu,Erwin Frise

doi:10.1186/gb-2013-14-12-r140

Abstract

BackgroundSite-specific transcription factors (TFs) bind DNA regulatory elements to control expression of target genes, forming the core of gene regulatory networks. Despite decades of research, most studies focus on only a small number of TFs and the roles of many remain unknown.ResultsWe present a systematic characterization of spatiotemporal gene expression patterns for all known or predicted Drosophila TFs throughout embryogenesis, the first such comprehensive study for any metazoan animal. We generated RNA expression patterns for all 708 TFs by in situ hybridization, annotated the patterns using an anatomical controlled vocabulary, and analyzed TF expression in the context of organ system development. Nearly all TFs are expressed during embryogenesis and more than half are specifically expressed in the central nervous system. Compared to other genes, TFs are enriched early in the development of most organ systems, and throughout the development of the nervous system. Of the 535 TFs with spatially restricted expression, 79% are dynamically expressed in multiple organ systems while 21% show single-organ specificity. Of those expressed in multiple organ systems, 77 TFs are restricted to a single organ system either early or late in development. Expression patterns for 354 TFs are characterized for the first time in this study.ConclusionsWe produced a reference TF dataset for the investigation of gene regulatory networks in embryogenesis, and gained insight into the expression dynamics of the full complement of TFs controlling the development of each organ system.

Highlights

Site-specific transcription factors (TFs) bind DNA regulatory elements to control expression of target genes, forming the core of gene regulatory networks
TF predictions, expression patterns, and annotations In order to identify a complete set of DNA-binding transcription factors, we used InterProScan [23] to search for patterns of amino acids that matched a set of 71 putative DNA binding domains (DBD) domain models collected from published TF annotation efforts [24,25] and from additional literature curation (Additional file 1: Table S1)
From this combination of computational predictions and literature curation, we identified 708 genes likely to encode sequence-specific DNA-binding TFs, representing a total of 73 DBD families (Figure 1 and Additional file 2: Table S2)

Summary

Introduction

Site-specific transcription factors (TFs) bind DNA regulatory elements to control expression of target genes, forming the core of gene regulatory networks. Large-scale embryonic mRNA expression pattern screens have been completed or are in progress for a number of model organisms including C. elegans, C. intestinalis, D. melanogaster, G. gallus, and X. laevis [7,8,9,10,11,12,13,14] and for specific tissue or developmental systems (for example, FlyTED, a Drosophila testis expression database, [15], and the Allen Brain Atlas of the adult mouse brain [16]). Many TFs remain poorly characterized, and half lack any description of their embryonic spatial expression patterns

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Discussion

Conclusion