The evolution of Dscam genes across the arthropods.

Sophie Ao Armitage,Rebecca Y Freiburg,Joachim Kurtz,Ignacio G Bravo

doi:10.1186/1471-2148-12-53

Sophie Ao Armitage, Rebecca Y Freiburg + Show 2 more

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https://doi.org/10.1186/1471-2148-12-53

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Abstract

BackgroundOne way of creating phenotypic diversity is through alternative splicing of precursor mRNAs. A gene that has evolved a hypervariable form is Down syndrome cell adhesion molecule (Dscam-hv), which in Drosophila melanogaster can produce thousands of isoforms via mutually exclusive alternative splicing. The extracellular region of this protein is encoded by three variable exon clusters, each containing multiple exon variants. The protein is vital for neuronal wiring where the extreme variability at the somatic level is required for axonal guidance, and it plays a role in immunity where the variability has been hypothesised to relate to recognition of different antigens. Dscam-hv has been found across the Pancrustacea. Additionally, three paralogous non-hypervariable Dscam-like genes have also been described for D. melanogaster. Here we took a bioinformatics approach, building profile Hidden Markov Models to search across species for putative orthologs to the Dscam genes and for hypervariable alternatively spliced exons, and inferring the phylogenetic relationships among them. Our aims were to examine whether Dscam orthologs exist outside the Bilateria, whether the origin of Dscam-hv could lie outside the Pancrustacea, when the Dscam-like orthologs arose, how many alternatively spliced exons of each exon cluster were present in the most common recent ancestor, and how these clusters evolved.ResultsOur results suggest that the origin of Dscam genes may lie after the split between the Cnidaria and the Bilateria and supports the hypothesis that Dscam-hv originated in the common ancestor of the Pancrustacea. Our phylogeny of Dscam gene family members shows six well-supported clades: five containing Dscam-like genes and one containing all the Dscam-hv genes, a seventh clade contains arachnid putative Dscam genes. Furthermore, the exon clusters appear to have experienced different evolutionary histories.ConclusionsDscam genes have undergone independent duplication events in the insects and in an arachnid genome, which adds to the more well-known tandem duplications that have taken place within Dscam-hv genes. Therefore, two forms of gene expansion seem to be active within this gene family. The evolutionary history of this dynamic gene family will be further unfolded as genomes of species from more disparate groups become available.

Highlights

One way of creating phenotypic diversity is through alternative splicing of precursor mRNAs
We examine i) whether Down syndrome cell adhesion molecule (Dscam) orthologs exist outside the Bilateria, if this is the case, it would suggest the origin of the Dscam gene family lies further back than previously believed, ii) whether the origin of Dscam-hv could lie outside the Pancrustacea, iii) when the Dscam-like orthologs arose, iv) how many alternatively spliced exons of each exon cluster were present at the base of the Arthropoda, Pancrustacea and the Insecta and v) whether the three exon clusters evolved
These findings suggest that the Dscam genes duplicated independently in the insects and an arachnid genome, which adds to the two independent DSCAM gene copies found in vertebrate genomes

Summary

Introduction

One way of creating phenotypic diversity is through alternative splicing of precursor mRNAs. A gene that has evolved a hypervariable form is Down syndrome cell adhesion molecule (Dscam-hv), which in Drosophila melanogaster can produce thousands of isoforms via mutually exclusive alternative splicing. The protein is vital for neuronal wiring where the extreme variability at the somatic level is required for axonal guidance, and it plays a role in immunity where the variability has been hypothesised to relate to recognition of different antigens. The biological complexity of an organism does not appear to correlate with the number of protein-coding genes in that organism. Dscam-hv is interesting because of its versatility due to the extreme diversity that it encodes, and because the nervous and immune systems may exert different selection pressures on this gene [24]

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