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Open Access Research article

Mechanisms of gap gene expression canalization in the Drosophila blastoderm

Vitaly V Gursky1*, Lena Panok23, Ekaterina M Myasnikova4, Manu3, Maria G Samsonova4, John Reinitz235 and Alexander M Samsonov1

Author Affiliations

1 Theoretical Department, Ioffe Physical-Technical Institute of the Russian Academy of Sciences, St. Petersburg, 194021 Russia

2 Department of Applied Mathematics and Statistics, and Center for Developmental Genetics, Stony Brook University, Stony Brook, NY 11794-3600, USA

3 Chicago Center for Systems Biology, and Department of Ecology and Evolution, The University of Chicago, Chicago, IL 60637, USA

4 Department of Computational Biology, Center for Advanced Studies, St. Petersburg State Polytechnical University, St. Petersburg, 195259 Russia

5 Department of Statistics, and Department of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, IL 60637, USA

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BMC Systems Biology 2011, 5:118  doi:10.1186/1752-0509-5-118

Published: 28 July 2011

Abstract

Background

Extensive variation in early gap gene expression in the Drosophila blastoderm is reduced over time because of gap gene cross regulation. This phenomenon is a manifestation of canalization, the ability of an organism to produce a consistent phenotype despite variations in genotype or environment. The canalization of gap gene expression can be understood as arising from the actions of attractors in the gap gene dynamical system.

Results

In order to better understand the processes of developmental robustness and canalization in the early Drosophila embryo, we investigated the dynamical effects of varying spatial profiles of Bicoid protein concentration on the formation of the expression border of the gap gene hunchback. At several positions on the anterior-posterior axis of the embryo, we analyzed attractors and their basins of attraction in a dynamical model describing expression of four gap genes with the Bicoid concentration profile accounted as a given input in the model equations. This model was tested against a family of Bicoid gradients obtained from individual embryos. These gradients were normalized by two independent methods, which are based on distinct biological hypotheses and provide different magnitudes for Bicoid spatial variability. We showed how the border formation is dictated by the biological initial conditions (the concentration gradient of maternal Hunchback protein) being attracted to specific attracting sets in a local vicinity of the border. Different types of these attracting sets (point attractors or one dimensional attracting manifolds) define several possible mechanisms of border formation. The hunchback border formation is associated with intersection of the spatial gradient of the maternal Hunchback protein and a boundary between the attraction basins of two different point attractors. We demonstrated how the positional variability for hunchback is related to the corresponding variability of the basin boundaries. The observed reduction in variability of the hunchback gene expression can be accounted for by specific geometrical properties of the basin boundaries.

Conclusion

We clarified the mechanisms of gap gene expression canalization in early Drosophila embryos. These mechanisms were specified in the case of hunchback in well defined terms of the dynamical system theory.