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Spatial expression of transcription factors in Drosophila embryonic organ development

Ann S Hammonds1, Christopher A Bristow234, William W Fisher1, Richard Weiszmann1, Siqi Wu15, Volker Hartenstein6, Manolis Kellis23, Bin Yu5, Erwin Frise1 and Susan E Celniker1*

Author Affiliations

1 Department of Genome Dynamics, Division of Life Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA

2 Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, Cambridge, MA 02139, USA

3 The Broad Institute of Massachusetts Institute of Technology and Harvard, Cambridge, MA 02142, USA

4 Current Address: Institute for Applied Cancer Science, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA

5 Department of Statistics, University of California Berkeley, Berkeley, CA 94720, USA

6 Department of Molecular Cell and Developmental Biology, University of California Los Angeles, Los Angeles, CA 90095, USA

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Genome Biology 2013, 14:R140  doi:10.1186/gb-2013-14-12-r140

Published: 20 December 2013

Abstract

Background

Site-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.

Results

We 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.

Conclusions

We 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.