Evolution of the pair rule gene network: Insights from a centipede

Jack Green,Michael Akam

doi:10.1016/j.ydbio.2013.06.017

Abstract

Comparative studies have examined the expression and function of homologues of the Drosophila melanogaster pair rule and segment polarity genes in a range of arthropods. The segment polarity gene homologues have a conserved role in the specification of the parasegment boundary, but the degree of conservation of the upstream patterning genes has proved more variable. Using genomic resources we identify a complete set of pair rule gene homologues from the centipede Strigamia maritima, and document a detailed time series of expression during trunk segmentation. We find supportive evidence for a conserved hierarchical organisation of the pair rule genes, with a division into early- and late-activated genes which parallels the functional division into primary and secondary pair rule genes described in insects. We confirm that the relative expression of sloppy-paired and paired with respect to wingless and engrailed at the parasegment boundary is conserved between myriapods and insects; suggesting that functional interactions between these genes might be an ancient feature of arthropod segment patterning. However, we find that the relative expression of a number of the primary pair rule genes is divergent between myriapods and insects. This corroborates suggestions that the evolution of upper tiers in the segmentation gene network is more flexible. Finally, we find that the expression of the Strigamia pair rule genes in periodic patterns is restricted to the ectoderm. This suggests that any direct role of these genes in segmentation is restricted to this germ layer, and that mesoderm segmentation is either dependent on the ectoderm, or occurs through an independent mechanism.

Highlights

The genetic dissection of the mechanism of segmentation in the fruit fly, Drosophila melanogaster, has laid the foundation for a growing body of comparative research on other arthropods (Nusslein-Volhard and Wieschaus, 1980; Peel et al, 2005)
Phylogenetic analysis confirms that there is no ambiguity about the many-to-many orthology of the genes examined, and suggests that, with the exception of hairy, where there are multiple gene family members in Strigamia, these are the result of lineage-specific duplications within the arthropods (Fig. S1)
With the exception of pax3/7-1 and opa2, all Strigamia homologues of the Drosophila pair rule genes are expressed in the ectodermal cell layer of the posterior disc and/or forming germ band before the formation of morphological segments

Summary

Introduction

The genetic dissection of the mechanism of segmentation in the fruit fly, Drosophila melanogaster, has laid the foundation for a growing body of comparative research on other arthropods (Nusslein-Volhard and Wieschaus, 1980; Peel et al, 2005). The Drosophila work identified a number of genes involved in segment pattern formation, and divided them into four functional categories based on their mutant phenotypes. These categories are maternal factors, gap genes, pair rule genes and segment polarity genes. The extent of conservation in the gene regulatory network that acts upstream of the segment polarity genes is not yet clear (Peel et al, 2005)

Methods

Results

Conclusion