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.

Vertebrate Embryonic Cleavage Pattern Determination

“…An effect of changing cell dimensions on cleavage plane orientation has also been implicated in the regulation of the thickness of epithelial layers at later stages of development (Da Silva-Buttkus et al 2008; Luxenburg et al 2011; Lázaro-Diéguez et al 2015). The stereotypic pattern of division orientation in zebrafish embryos ceases to be apparent at the seventh cycle and beyond (Kimmel et al 1995; Hoh et al 2013). …”

Light-sheet microscopy: a tutorial

“…This is an essential characteristic required for all sorts of developmental biology studies [15][16][17][18], such as organogenesis [19], cell migration [20,21], cardiac development [22][23][24][25], vascular development [26,27], neuro-development [28,29], and generally any kind of in vivo studies. Drosophila melanogaster [2,[30][31][32] and zebrafish [19,26,30,[33][34][35][36] have traditionally been the most widely used samples in this field, but it fits well many others, such as worm embryos [28,37] and other small organisms or plants [38][39][40].…”

A practical guide to bioimaging research data management in core facilities

“…It has been showcased that new research can be based on existing image data from other studies. [145][146][147] The reuse potential of quality-controlled, annotated data that are findable and accessible in open, interoperable formats was demonstrated by Williams et al 118 and FAIR open data are expected to advance bioimage informatics. 148 Especially in the era of AI-based analysis, segmentation and hypothesis building, well-annotated and quality-controlled research data are essential for training models and obtaining reliable results, 15,149 and data have been reused for novel algorithm development.…”

“…It has been showcased that new research can be based on existing image data from other studies 145–147 . The reuse potential of quality‐controlled, annotated data that are findable and accessible in open, interoperable formats was demonstrated by Williams et al 118 .…”