The dynamic transmission of positional information in stau- mutants during Drosophila embryogenesis

Elife. 2020 Jun 8:9:e54276. doi: 10.7554/eLife.54276.

Abstract

It has been suggested that Staufen (Stau) is key in controlling the variability of the posterior boundary of the Hb anterior domain (xHb). However, the mechanism that underlies this control is elusive. Here, we quantified the dynamic 3D expression of segmentation genes in Drosophila embryos. With improved control of measurement errors, we show that the xHb of stau- mutants reproducibly moves posteriorly by 10% of the embryo length (EL) to the wild type (WT) position in the nuclear cycle (nc) 14, and that its variability over short time windows is comparable to that of the WT. Moreover, for stau- mutants, the upstream Bicoid (Bcd) gradients show equivalent relative intensity noise to that of the WT in nc12-nc14, and the downstream Even-skipped (Eve) and cephalic furrow (CF) show the same positional errors as these factors in WT. Our results indicate that threshold-dependent activation and self-organized filtering are not mutually exclusive and could both be implemented in early Drosophila embryogenesis.

Keywords: D. melanogaster; computational biology; developmental biology; developmental patterning; noise filtering; systems biology; threshold dependent model.

Plain language summary

Broadly speaking, all individuals of any animal species share a highly consistent shape and structure. Despite this, the activity of the genes that control these body patterns can vary significantly. There are currently two models that have been proposed for how noisy systems of genes, and the proteins they code, can produce consistent body patterns. The first, suggests the noise is essentially self-compensating so stably produces the same result, while the second invokes localized self-organizing systems that help to refine the structural details. In the early stages of development for the fruit fly, Drosophila melanogaster, one of the proteins that controls body patterns is called Hunchback (often just Hb for short). The Hb proteins are largely found at the front-end of the fly embryo, with a sharp drop near the middle. Normally the position of the drop in Hb varies between flies by around 1% of the total length of the fly embryo. Previous work has linked a gene called staufan (or stau for short) to the distribution of Hb in flies but the mechanism involved is unknown. Yang, Zhu, Kong et al. have now used a technique called light sheet microscopy to accurately measure the location of Hb proteins in fruit fly embryos. Without the stau gene, the average position of the drop in Hb proteins underwent a larger shift towards the rear at a key stage in development. Despite this altered behavior, the extent of variation between flies did not change. Similarly, the variation of other genes that control Hb location and that are controlled by Hb remained unchanged. As such, it seems stau affects Hb positioning but has no impact on variation between individuals. These findings suggest that both models for controlling variation in fly development could still be relevant and may operate together. This study also provides a new method for the more precise measurement of systems like these that may offer insights into the mechanisms involved in early embryonic development.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Body Patterning
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / embryology*
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / metabolism
  • Embryo, Nonmammalian
  • Embryonic Development / physiology*
  • Gene Expression Regulation, Developmental
  • Mutation
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism*

Substances

  • Drosophila Proteins
  • RNA-Binding Proteins
  • stau protein, Drosophila

Associated data

  • Dryad/10.5061/dryad.mcvdncjxw