On the dynamic nature of positional information

Abstract

Morphogenetic fields are among the most fundamental concepts of embryology. However, they are also among the most ill-defined, since they consist of dynamic regulatory processes whose exact nature remains elusive. In order to achieve a more rigorous definition of a developmental field, Lewis Wolpert introduced the concept of positional information illustrated by his French Flag model. Here we argue that Wolpert's positional information—a static coordinate system defining a field—lacks essential properties of the original field concept. We show how data-driven mathematical modeling approaches now enable us to study regulatory processes in a way that is qualitatively different from our previous level of understanding. As an example, we review our recent analysis of segmentation gene expression in the blastoderm embryo of the fruit fly Drosophila melanogaster. Based on this analysis, we propose a revised French Flag, which incorporates the dynamic, feedback-driven nature of pattern formation in the Drosophila blastoderm. BioEssays 28: 1102–1111, 2006.