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

Journal Article · · GenomeBiology.com
 [1];  [2];  [3];  [3];  [3];  [2];  [3]
  1. Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); DOE/OSTI
  2. University of California, Berkeley, CA (United States)
  3. Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

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

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); Academy of Finland; National Institute of General Medical Sciences (NIGMS); National Human Genome Research Institute (NHGRI)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1626709
Journal Information:
GenomeBiology.com, Journal Name: GenomeBiology.com Journal Issue: 12 Vol. 7; ISSN 1465-6906
Publisher:
BioMed CentralCopyright Statement
Country of Publication:
United States
Language:
English

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A quantitative atlas of Even-skipped and Hunchback expression in Clogmia albipunctata (Diptera: Psychodidae) blastoderm embryos journal January 2014
Developmental roles of 21 Drosophila transcription factors are determined by quantitative differences in binding to an overlapping set of thousands of genomic regions journal January 2009
A gene expression atlas of a bicoid-depleted Drosophila embryo reveals early canalization of cell fate journal February 2015
Predicting Ancestral Segmentation Phenotypes from Drosophila to Anopheles Using In Silico Evolution journal May 2016
Cellular resolution models for even skipped regulation in the entire Drosophila embryo journal August 2013
The gap gene network journal October 2010
Accurate measurements of dynamics and reproducibility in small genetic networks journal January 2013
Design principles for generating robust gene expression patterns in dynamic engineered tissues journal February 2013
The Intersection of Theory and Application in Elucidating Pattern Formation in Developmental Biology journal January 2009
Automated cellular annotation for high-resolution images of adult Caenorhabditis elegans journal June 2013
Kinetic sculpting of the seven stripes of the Drosophila even-skipped gene posted_content January 2018
Arthropod segmentation journal September 2019
A damped oscillator imposes temporal order on posterior gap gene expression in Drosophila journal February 2018
Hunchback is counter-repressed to regulate even-skipped stripe 2 expression in Drosophila embryos journal September 2018
A damped oscillator imposes temporal order on posterior gap gene expression in Drosophila. text January 2018
Arthropod segmentation. journalarticle January 2019
Odd-paired controls frequency doubling in Drosophila segmentation by altering the pair-rule gene regulatory network text January 2016
Mathematical modeling of gene expression: a guide for the perplexed biologist journal January 2011
Odd-paired controls frequency doubling in Drosophila segmentation by altering the pair-rule gene regulatory network journal August 2016

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