Spatial information dynamics during early zebrafish development

Abstract

During development inherited information directs growth and specifies the complex spatial organization of cells and molecules. Here we show that a new information metric, the k-space information (kSI), captures the growth and emergence of spatial organization in a developing embryo. Using zebrafish as a model, we quantify the rate of development over the first 24h and demonstrate that important developmental landmarks are associated with well-defined transitions in information dynamics. The rate of development during this time is highest immediately before and after gastrulation, as well early in the segmentation period. We also find that the majority of the information arises from spatial correlations on the length scale of 20-80 μm, but there are contributions from many length scales that change over time. A comparison of the information dynamics in the maternal-zygotic one-eyed pinhead mutant, which is defective in mesoderm induction, with the wild-type embryo shows that the information dynamics diverge near the onset of gastrulation. Subsequently the mutant lacks a peak in the information dynamics that appears to be associated with the formation of trunk somites in the wild-type embryo. These findings provide a common and objective basis by which to quantify spatial organization, compare mutants and quantify developmental dynamics. The kSI can also be applied to any form of developmental data of arbitrary dimensions, and it offers a broad conceptual framework with which to organize the large amounts of data emerging from various sources.