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Comprehensive identification of Drosophila dorsal-ventral patterning genes using a whole-genome tiling array

ABSTRACT: Dorsal-ventral (DV) patterning of the Drosophila embryo is initiated by Dorsal, a sequence specific transcription factor distributed in a broad nuclear gradient in the precellular embryo.Previous studies have identified as many as 70 protein-coding genes and one microRNA gene that are directly or indirectly regulated by this gradient. A gene regulation network, or circuit diagram, including the functional interconnections among 40 Dorsal target genes and 20 associated tissue-specific enhancers, has been determined for the initial stages of gastrulation. Here, we attempt to extend this analysis by identifying additional DV patterning genes using a recently developed whole-genome tiling array. This analysis led to the identification of another 30 protein-coding genes, including the Drosophila homolog of Idax, an inhibitor of Wnt signaling. In addition, remote 5' exons were identified for at least 10 of the ~100 protein-coding genes that were missed in earlier annotations. As many as 9 intergenic, uncharacterized transcription units were identified, including two that contain known microRNAs, miR-1 and miR-9a. We discuss the potential functions of these newly identified genes, and suggest that intronic enhancers are a common feature of the DV gene network. Keywords: gene expression, dorsal-ventral pattern genes, tiling array

ORGANISM(S): Drosophila melanogaster

PROVIDER: GSE5434 | GEO | 2006/08/04

SECONDARY ACCESSION(S): PRJNA96097

REPOSITORIES: GEO

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Project description:The submitted data have been utilized in the following two papers: "Drosophila poised enhancers are generated during tissue patterning with the help of repression" (Koenecke et al 2016, Genome Research): Histone modifications are frequently used as markers for enhancer states, but how to interpret enhancer states in the context of embryonic development is not clear. The poised enhancer signature, involving H3K4me1 and low levels of H3K27ac, has been reported to mark inactive enhancers that are poised for future activation. However, future activation is not always observed and alternative reasons for the widespread occurrence of this enhancer signature have not been investigated. By analyzing enhancers during dorsal-ventral (DV) axis formation in the Drosophila embryo, we find that the poised enhancer signature is specifically generated during patterning in the tissue where the enhancers are not induced, including at enhancers that are known to be repressed by a transcriptional repressor. These results suggest that, rather than serving simply as an intermediate step before future activation, the poised enhancer state may mark enhancers for spatial activation during tissue patterning. We discuss the possibility that the poised enhancer state is more generally the result of repression by transcriptional repressors. "Genome-wide identification of Drosophila dorso-ventral enhancers by differential histone acetylation analysis" (Koenecke and Johnston et al 2016, Genome Biol): Background: Drosophila dorso-ventral (DV) patterning is one of the best-understood regulatory networks to date, and illustrates the fundamental role of enhancers in controlling patterning, cell fate specification and morphogenesis during development. Histone acetylation such as H3K27ac is an excellent marker for active enhancers, but it is challenging to obtain precise locations for enhancers as the highest levels of this modification flank the enhancer regions. How to best identify tissue-specific enhancers in a developmental system de novo with a minimal set of data is still unclear. Results: Using DV patterning as a test system, we develop a simple and effective method to identify tissue-specific enhancers de novo. We sample a broad set of candidate enhancer regions using data on CBP co-factor binding or ATAC-seq chromatin accessibility, and then identify those regions with significant differences in histone acetylation between tissues. This method identifies hundreds of novel DV enhancers and outperforms ChIP-seq data of relevant transcription factors when benchmarked with mRNA expression data and transgenic reporter assays. These DV enhancers allow the de novo discovery of the relevant transcription factor motifs involved in DV patterning and contain additional motifs that are evolutionarily conserved and for which the corresponding transcription factors are expressed in a DV-biased fashion. Finally, we identify novel target genes of the regulatory network, implicating morphogenesis genes as early targets of DV patterning. Conclusions: Taken together, our approach has expanded our knowledge of the DV patterning network even further and is a general method to identify enhancers in any developmental system, including mammalian development.

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Comprehensive identification of Drosophila dorsal-ventral patterning genes using a whole-genome tiling array

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