Canalization of Gene Expression and Domain Shifts in the Drosophila Blastoderm by Dynamical Attractors

Manu, Lucian; Surkova, Svetlana; Spirov, Alexander V.; Gursky, Vitaly V.; Janssens, Hilde; Kim, Ah-Ram; Radulescu, Ovidiu; Vanario-Alonso, Carlos E.; Sharp, David H.; Samsonova, Maria; Reinitz, John

doi:10.1371/journal.pcbi.1000303

Canalization of Gene Expression and Domain Shifts in the Drosophila Blastoderm by Dynamical Attractors

Journal Article · Fri Mar 13 00:00:00 EDT 2009 · PLoS Computational Biology (Online)

DOI:https://doi.org/10.1371/journal.pcbi.1000303· OSTI ID:1627190

Manu, Lucian ^[1]; Surkova, Svetlana ^[2]; Spirov, Alexander V. ^[3]; Gursky, Vitaly V. ^[4]; Janssens, Hilde ^[5]; Kim, Ah-Ram ^[3]; Radulescu, Ovidiu ^[6]; Vanario-Alonso, Carlos E. ^[3]; Sharp, David H. ^[7]; Samsonova, Maria ^[2]; Reinitz, John ^[3]

Stony Brook Univ., NY (United States). Center for Developmental Genetics. Dept. of Applied Matematics and Statistics; DOE/OSTI
St. Petersburg State Polytechnical Univ. (Russian Federation). Center for Advanced Studies. Dept. of Computational Biology
Stony Brook Univ., NY (United States). Center for Developmental Genetics. Dept. of Applied Matematics and Statistics
Russian Academy of Sciences (RAS), St. Petersburg (Russian Federation). The Ioffe Physico-Technical Inst. Theoretical Dept.
CRG – Centre de Regulacio Genomica, Barcelona (Spain). EMBL/CRG Research Unit in Systems Biology
Univ. of Rennes (France). Inst. of Mathematical Research of Rennes
Los Alamos National Lab. (LANL), Los Alamos, NM (United States). Theoretical Div.

The variation in the expression patterns of the gap genes in the blastoderm of the fruit fly Drosophila melanogaster reduces over time as a result of cross regulation between these genes, a fact that we have demonstrated in an accompanying article in PLoS Biology (see Manu et al., doi:10.1371/journal.pbio.1000049). This biologically essential process is an example of the phenomenon known as canalization. It has been suggested that the developmental trajectory of a wild-type organism is inherently stable, and that canalization is a manifestation of this property. Although the role of gap genes in the canalization process was established by correctly predicting the response of the system to particular perturbations, the stability of the developmental trajectory remains to be investigated. For many years, it has been speculated that stability against perturbations during development can be described by dynamical systems having attracting sets that drive reductions of volume in phase space. In this paper, we show that both the reduction in variability of gap gene expression as well as shifts in the position of posterior gap gene domains are the result of the actions of attractors in the gap gene dynamical system. Two biologically distinct dynamical regions exist in the early embryo, separated by a bifurcation at 53% egg length. In the anterior region, reduction in variation occurs because of stability induced by point attractors, while in the posterior, the stability of the developmental trajectory arises from a one-dimensional attracting manifold. This manifold also controls a previously characterized anterior shift of posterior region gap domains. Our analysis shows that the complex phenomena of canalization and pattern formation in the Drosophila blastoderm can be understood in terms of the qualitative features of the dynamical system. The result confirms the idea that attractors are important for developmental stability and shows a richer variety of dynamical attractors in developmental systems than has been previously recognized.

View Accepted Manuscript (DOE)

Research Organization:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; National Institutes of Health (NIH)

Grant/Contract Number:: AC52-06NA25396

OSTI ID:: 1627190

Journal Information:: PLoS Computational Biology (Online), Journal Name: PLoS Computational Biology (Online) Journal Issue: 3 Vol. 5; ISSN 1553-7358

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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Morphogen interpretation: concentration, time, competence, and signaling dynamics Sagner, Andreas; Briscoe, James The Francis Crick Institute https://doi.org/10.25418/crick.15188025	text	January 2021
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