Systematic determination of patterns of gene expression during Drosophila embryogenesis

By Pavel Tomancak, A. Beaton, R. Weiszmann, E. Kwan, S. Shu, Suzanna Lewis, S. Richards, Michael Ashburner, Volker Hartenstein, S. Celniker and 1 more. Genome Biology, 2002

753 citations recorded by the source corpus.

BackgroundCell-fate specification and tissue differentiation during development are largely achieved by the regulation of gene transcription.ResultsAs a first step to creating a comprehensive atlas of gene-expression patterns during Drosophila embryogenesis, we examined 2,179 genes by in situ hybridization to fixed Drosophila embryos. Of the genes assayed, 63.7% displayed dynamic expression patterns that were documented with 25,690 digital photomicrographs of individual embryos. The photomicrographs were annotated using controlled vocabularies for anatomical structures that are organized into a developmental hierarchy. We also generated a detailed time course of gene expression during embryogenesis using microarrays to provide an independent corroboration of the in situ hybridization results. All image, annotation and microarray data are stored in publicly available database. We found that the RNA transcripts of about 1% of genes show clear subcellular localization. Nearly all the annotated expression patterns are distinct. We present an approach for organizing the data by hierarchical clustering of annotation terms that allows us to group tissues that express similar sets of genes as well as genes displaying similar expression patterns.ConclusionsAnalyzing gene-expression patterns by in situ hybridization to whole-mount embryos provides an extremely rich dataset that can be used to identify genes involved in developmental processes that have been missed by traditional genetic analysis. Systematic analysis of rigorously annotated patterns of gene expression will complement and extend the types of analyses carried out using expression microarrays.

Subfields: Molecular Biology

View Paper: https://www.semanticscholar.org/paper/c477ac935be7a20891d85847b161319bf2a83e96

How researchers see this paper

The researchers whose trusted networks rank it highest, strongest advocate first. Every researcher gets a different order.

In Molecular Biology

Citations in the corpus

Transcription Factors Bind Thousands of Active and Inactive Regions in the Drosophila Blastoderm (2008, background): “, housekeeping genes) show weak A-P patterns at stage 5 [35,66,67].”
Dynamic reprogramming of chromatin accessibility during Drosophila embryo development (2011, background): “Initiated by a few maternally supplied regulatory proteins, by the blastoderm stage some 40 or so sequence-specific transcription factors control the spatial and temporal expression of around a thousand genes [9-14].”
The Loci of Evolution: How Predictable is Genetic Evolution? (2008, background): “Most genes are expressed in multiple tissues at multiple times in development (Tomancak et al. 2002).”
Systematic image-driven analysis of the spatial Drosophila embryonic expression landscape (2010, methodology): “Earlier, we used annotated gene-expression proﬁles to identify genes involved in developmental processes that were missed by traditional genetics (Tomancak et al , 2002, 2007).”
Trace Norm Regularization: Reformulations, Algorithms, and Multi-Task Learning (2010, methodology): “In Section 7 we report the results of experiments conducted on the automatic gene expression pattern image annotation task [26, 48].”
Gaussian Process Regression Networks (2011, methodology): “Tomancak et al. (2002) measured gene expression levels every hour for 12 hours during Drosophila embryogenesis; they then repeated this experiment for an independent replica (a second independent time series).”
Museum of spatial transcriptomics (2020, background): “(WM)ISH was the technology of choice in the late 1990s and the 2000s before the rise of highly multiplexed, high resolution, and more quantitative technologies, and has been used to create gene expression atlases in embryos of several species such as Drosophila melanogaster [25], Mus musculus, and G”
Uberon, an integrative multi-species anatomy ontology (2012, background): “4 [80] to encode GCIs and other advanced OWL features within OBO format.”
Visualization of image data from cells to organisms (2010, neutral): “Some large-scale experiments involving particularly complex read-outs have been annotated manually using controlled vocabularies 51 , in some cases—as for high-content analysis of gene expression during development—eased by the use of custom-built annotation tools 34,52,53 .”
Spatial expression of transcription factors in Drosophila embryonic organ development (2013, background): “Methods for in situ hybridization and image capture have been described previously [8,13,22].”
The Drosophila embryo at single-cell transcriptome resolution (2017, background): “approach to avoid heterogeneity is cell culture (5-11), but the amount of genomic and transcriptomic variation within most cell lines has been shown to be substantial and cultured cells are often poor in vivo proxies.”
A universal framework for regulatory element discovery across all genomes and data types. (2007, background): “The emergence of whole-genome microarrays (Fodor et al., 1993; Schena et al., 1995) and high-throughput in situ hybridization (Tomancak et al., 2002) has made it possible to probe the expression of all or most genes in an organism, as a function of space, time, genetic background, and environmental…”
The Carnegie Protein Trap Library: A Versatile Tool for Drosophila Developmental Studies (2007, methodology): “Visualizing patterns of gene expression within the intact tissues of transgenic organisms containing gene expression reporters may be the most general method (TOMANCAK et al. 2002).”