Dynamic patterning by the Drosophila pair-rule network reconciles long-germ and short-germ segmentation.

Erik Clark,Claude Desplan

doi:10.1371/journal.pbio.2002439

Abstract

Drosophila segmentation is a well-established paradigm for developmental pattern formation. However, the later stages of segment patterning, regulated by the “pair-rule” genes, are still not well understood at the system level. Building on established genetic interactions, I construct a logical model of the Drosophila pair-rule system that takes into account the demonstrated stage-specific architecture of the pair-rule gene network. Simulation of this model can accurately recapitulate the observed spatiotemporal expression of the pair-rule genes, but only when the system is provided with dynamic “gap” inputs. This result suggests that dynamic shifts of pair-rule stripes are essential for segment patterning in the trunk and provides a functional role for observed posterior-to-anterior gap domain shifts that occur during cellularisation. The model also suggests revised patterning mechanisms for the parasegment boundaries and explains the aetiology of the even-skipped null mutant phenotype. Strikingly, a slightly modified version of the model is able to pattern segments in either simultaneous or sequential modes, depending only on initial conditions. This suggests that fundamentally similar mechanisms may underlie segmentation in short-germ and long-germ arthropods.

Highlights

IntroductionThe fruit fly Drosophila melanogaster has a segmented body plan
Like other arthropods, the fruit fly Drosophila melanogaster has a segmented body plan
I propose that Eve conveys positional information largely via its expression dynamics, which are decoded downstream by the rest of the pair-rule gene network. (Interestingly, while “French flag” type morphogen gradient mechanisms have been proposed to underpin many developmental patterning systems, several modern studies have found that the reality often involves complex dynamics [58,110,111,112,113].)

Summary

Introduction

The fruit fly Drosophila melanogaster has a segmented body plan. This segmental pattern is laid down in the embryo during the first 3 hours of development During this time, the anteroposterior (AP) axis of the blastoderm is progressively patterned down to cellular-level resolution by an elaborate, multi-tiered network of genes and their encoded transcription factors [1,2]. The anteroposterior (AP) axis of the blastoderm is progressively patterned down to cellular-level resolution by an elaborate, multi-tiered network of genes and their encoded transcription factors [1,2] These genes were first identified in a landmark genetic screen [3,4], and their regulatory interactions have subsequently been dissected by 3 decades of genetic experiments. This involves transducing a double segment pattern of early pair-rule gene expression, in which each set of stripes is offset slightly from the others, into a single-segment pattern of segment-polarity gene expression, in which most genes are expressed in discrete, non-overlapping domains [6,7,8]

Methods

Results

Discussion

Conclusion