A clustered set of three Sp-family genes is ancestral in the Metazoa: evidence from sequence analysis, protein domain structure, developmental expression patterns and chromosomal location

Nina D Schaeper,Ernst A Wimmer,Nikola-Michael Prpic

doi:10.1186/1471-2148-10-88

Abstract

BackgroundThe Sp-family of transcription factors are evolutionarily conserved zinc finger proteins present in many animal species. The orthology of the Sp genes in different animals is unclear and their evolutionary history is therefore controversially discussed. This is especially the case for the Sp gene buttonhead (btd) which plays a key role in head development in Drosophila melanogaster, and has been proposed to have originated by a recent gene duplication. The purpose of the presented study was to trace orthologs of btd in other insects and reconstruct the evolutionary history of the Sp genes within the metazoa.ResultsWe isolated Sp genes from representatives of a holometabolous insect (Tribolium castaneum), a hemimetabolous insect (Oncopeltus fasciatus), primitively wingless hexapods (Folsomia candida and Thermobia domestica), and an amphipod crustacean (Parhyale hawaienis). We supplemented this data set with data from fully sequenced animal genomes. We performed phylogenetic sequence analysis with the result that all Sp factors fall into three monophyletic clades. These clades are also supported by protein domain structure, gene expression, and chromosomal location. We show that clear orthologs of the D. melanogaster btd gene are present even in the basal insects, and that the Sp5-related genes in the genome sequence of several deuterostomes and the basal metazoans Trichoplax adhaerens and Nematostella vectensis are also orthologs of btd.ConclusionsAll available data provide strong evidence for an ancestral cluster of three Sp-family genes as well as synteny of this Sp cluster and the Hox cluster. The ancestral Sp gene cluster already contained a Sp5/btd ortholog, which strongly suggests that btd is not the result of a recent gene duplication, but directly traces back to an ancestral gene already present in the metazoan ancestor.

Highlights

The Strongylocentrotus purpuratus (Sp)-family of transcription factors are evolutionarily conserved zinc finger proteins present in many animal species
All available data suggest that a set of three Sp-family genes comprising one Sp1-4 gene, one Sp5/btd, and one Sp6-9 gene, is ancestral in the Metazoa (Fig. 10)
No data are yet available from the most basal metazoan group, the Porifera, but at least two Sp-family genes are linked in the basal metazoan T. adhaerens

Summary

Introduction

The Sp-family of transcription factors are evolutionarily conserved zinc finger proteins present in many animal species. [1,5]) The members of this Sp-family of transcription factors share three highly conserved Cys2His2-type zinc fingers, which bind to G-rich DNA elements, such as GC-boxes (GGGGCGGGG) and GT/CACC-boxes (GGTGTGGGG) [4]. These binding sites are present in many control regions of both tissuespecific and ubiquitously expressed genes [6,7] indicating that Sp-family transcription factors potentially regulate a large number of target genes. In the fly Drosophila melanogaster, the gene buttonhead (btd) codes for a member of the Sp-family, which represents an important factor for the formation of several head segments and is involved in the development of the central and peripheral nervous system [8,18,19,20]

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