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Three-dimensional morphology and gene expression in the Drosophila blastoderm at cellular resolution II: dynamics

Soile VE Keränen1, Charless C Fowlkes2, Cris L Luengo Hendriks3, Damir Sudar3, David W Knowles3, Jitendra Malik2 and Mark D Biggin1*

Author Affiliations

1 Berkeley Drosophila Transcription Network Project, Genomics Division, Lawrence Berkeley National Laboratory, One Cyclotron Road, Berkeley, California 94720, USA

2 Berkeley Drosophila Transcription Network Project, Department of Electrical Engineering and Computer Science, University of California, Berkeley, California 94720, USA

3 Berkeley Drosophila Transcription Network Project, Life Sciences Division, Lawrence Berkeley National Laboratory, One Cyclotron Road, Berkeley, California 94720, USA

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Genome Biology 2006, 7:R124  doi:10.1186/gb-2006-7-12-r124

Published: 21 December 2006

Abstract

Background

To accurately describe gene expression and computationally model animal transcriptional networks, it is essential to determine the changing locations of cells in developing embryos.

Results

Using automated image analysis methods, we provide the first quantitative description of temporal changes in morphology and gene expression at cellular resolution in whole embryos, using the Drosophila blastoderm as a model. Analyses based on both fixed and live embryos reveal complex, previously undetected three-dimensional changes in nuclear density patterns caused by nuclear movements prior to gastrulation. Gene expression patterns move, in part, with these changes in morphology, but additional spatial shifts in expression patterns are also seen, supporting a previously proposed model of pattern dynamics based on the induction and inhibition of gene expression. We show that mutations that disrupt either the anterior/posterior (a/p) or the dorsal/ventral (d/v) transcriptional cascades alter morphology and gene expression along both the a/p and d/v axes in a way suggesting that these two patterning systems interact via both transcriptional and morphological mechanisms.

Conclusion

Our work establishes a new strategy for measuring temporal changes in the locations of cells and gene expression patterns that uses fixed cell material and computational modeling. It also provides a coordinate framework for the blastoderm embryo that will allow increasingly accurate spatio-temporal modeling of both the transcriptional control network and morphogenesis.