Abstract

BackgroundAn increasing number of publications demonstrate conservation of function of cis-regulatory elements without sequence similarity. In invertebrates such functional conservation has only been shown for closely related species. Here we demonstrate the existence of an ancient arthropod regulatory element that functions during the selection of neural precursors. The activity of genes of the achaete-scute (ac-sc) family endows cells with neural potential. An essential, conserved characteristic of proneural genes is their ability to restrict their own activity to single or a small number of progenitor cells from their initially broad domains of expression. This is achieved through a process called lateral inhibition. A regulatory element, the sensory organ precursor enhancer (SOPE), is required for this process. First identified in Drosophila, the SOPE contains discrete binding sites for four regulatory factors. The SOPE of the Drosophila asense gene is situated in the 5' UTR.ResultsThrough a manual comparison of consensus binding site sequences we have been able to identify a SOPE in UTR sequences of asense-like genes in species belonging to all four arthropod groups (Crustacea, Myriapoda, Chelicerata and Insecta). The SOPEs of the spider Cupiennius salei and the insect Tribolium castaneum are shown to be functional in transgenic Drosophila. This would place the origin of this regulatory sequence as far back as the last common ancestor of the Arthropoda, that is, in the Cambrian, 550 million years ago.ConclusionsThe SOPE is not detectable by inter-specific sequence comparison, raising the possibility that other ancient regulatory modules in invertebrates might have escaped detection.

Highlights

  • An increasing number of publications demonstrate conservation of function of cis-regulatory elements without sequence similarity

  • We present evidence that gene duplications separating proneural from precursor-specific functions possibly occurred independently in different arthropod groups and that a sensory organ precursor enhancer (SOPE) in untranslated region (UTR) sequences in ase-like genes of all groups has been inherited from an ancestral achaete-scute homologue (ASH)/ase precursor gene in the last common ancestor of the Arthropoda

  • Conservation of coding sequences suggest duplication and subfunctionalization of an ancestral arthropod gene into proneural and ase-like functions A highly conserved basic helix-loop-helix (bHLH) domain characterizes proteins encoded by the ac-sc gene family, but outside this domain conservation is very low

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Summary

Introduction

An increasing number of publications demonstrate conservation of function of cis-regulatory elements without sequence similarity. The initiation of development of the nervous system in vertebrates and higher invertebrates involves the activity of proneural genes that encode transcription factors of the basic helix-loop-helix (bHLH) class [1] Their expression in the neuroectoderm endows cells with neural potential and contributes to the specification of neuronal identity. An essential, conserved characteristic of proneural genes is their ability to restrict their own activity to single or a Regulatory sequences involved in the restriction of proneural gene expression from proneural domains to selected neural precursors have mostly been studied in Drosophila melanogaster, in particular with respect to the ac-sc genes and their role in the development of sensory bristles of the adult peripheral nervous system.

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