Abstract

The Drosophila embryo transiently exhibits a double-segment periodicity, defined by the expression of seven 'pair-rule' genes, each in a pattern of seven stripes. At gastrulation, interactions between the pair-rule genes lead to frequency doubling and the patterning of 14 parasegment boundaries. In contrast to earlier stages of Drosophila anteroposterior patterning, this transition is not well understood. By carefully analysing the spatiotemporal dynamics of pair-rule gene expression, we demonstrate that frequency-doubling is precipitated by multiple coordinated changes to the network of regulatory interactions between the pair-rule genes. We identify the broadly expressed but temporally patterned transcription factor, Odd-paired (Opa/Zic), as the cause of these changes, and show that the patterning of the even-numbered parasegment boundaries relies on Opa-dependent regulatory interactions. Our findings indicate that the pair-rule gene regulatory network has a temporally modulated topology, permitting the pair-rule genes to play stage-specific patterning roles.

Highlights

  • Segmentation is a developmental process that subdivides an animal body axis into similar, repeating units (Hannibal and Patel, 2013)

  • We have found that many regulatory interactions between the pair-rule genes are not constant over the course of Drosophila segmentation, but instead undergo coordinated changes at the end of cellularisation

  • We are not the first to notice that certain regulatory interactions do not apply to all stages of pair-rule gene expression (Baumgartner and Noll, 1990; Manoukian and Krause, 1992; Manoukian and Krause, 1993; Fujioka et al, 1995; Saulier-Le Drean et al, 1998)

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Summary

Introduction

Segmentation is a developmental process that subdivides an animal body axis into similar, repeating units (Hannibal and Patel, 2013). In all arthropods yet studied, the segmental stripes of segment-polarity genes are initially patterned by a group of transcription factors known as the ’pair-rule’ genes (Green and Akam, 2013; Peel et al, 2005; Damen et al, 2005). The pair-rule genes were originally identified in a screen for mutations affecting the segmental pattern of the Drosophila melanogaster larval cuticle (NussleinVolhard and Wieschaus, 1980). They appeared to be required for the patterning of alternate segment boundaries ( ’pair-rule’) and were subsequently found to be expressed in stripes of double-segment periodicity (Hafen et al, 1984; Akam, 1987)

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