Abstract

BackgroundGene gain and subsequent retention or loss during evolution may be one of the underlying mechanisms involved in generating the diversity of metazoan nervous systems. However, the causal relationships acting therein have not been studied extensively.ResultsWe identified the gene PsGEF (protostome-specific GEF), which is present in all the sequenced genomes of insects and limpet but absent in those of sea anemones, deuterostomes, and nematodes. In Drosophila melanogaster, PsGEF encodes a short version of a protein with the C2 and PDZ domains, as well as a long version with the C2, PDZ, and RhoGEF domains through alternative splicing. Intriguingly, the exons encoding the RhoGEF domain are specifically deleted in the Daphnia pulex genome, suggesting that Daphnia PsGEF contains only the C2 and PDZ domains. Thus, the distribution of PsGEF containing the C2, PDZ, and RhoGEF domains among metazoans appears to coincide with the presence of mushroom bodies. Mushroom bodies are prominent neuropils involved in the processing of multiple sensory inputs as well as associative learning in the insect, platyhelminth, and annelid brains. In the adult Drosophila brain, PsGEF is expressed in mushroom bodies, antennal lobe, and optic lobe, where it is necessary for the correct axon branch formation of alpha/beta neurons in mushroom bodies. PsGEF genetically interacts with Rac1 but not other Rho family members, and the RhoGEF domain of PsGEF induces actin polymerization in the membrane, thus resulting in the membrane ruffling that is observed in cultured cells with activated forms of Rac.ConclusionThe specific acquisition of PsGEF by the last common ancestor of protostomes followed by its retention or loss in specific animal species during evolution demonstrates that there are some structural and/or functional features common between insect and lophotrochozoan nervous systems (for example, mushroom bodies), which are absent in all deuterostomes and cnidarians. PsGEF is therefore one of genes associated with the diversity of metazoan nervous systems.

Highlights

  • Gene gain and subsequent retention or loss during evolution may be one of the underlying mechanisms involved in generating the diversity of metazoan nervous systems

  • Identification of PsGEF gene uniquely shared between insects and limpets A large-scale comparison of the genomes of five insects (D. melanogaster, Anopheles gambiae, Aedes aegypti, Apis mellifera, and Tribolium castaneum) and five vertebrates (Homo sapiens, Mus musculus, Monodelphis domestica, Gallus gallus, and Tetraodon nigroviridis) revealed that there were approximately 1,000 insect-specific orthologous genes [1]

  • (page number not for citation purposes) http://www.biomedcentral.com/1741-7007/7/21 highly expressed in the Drosophila central nervous system (CNS) by screening transgenic lines in which GAL4 was inserted in the promoter regions of candidate genes, in order to understand the genetic basis for the development and functions specific for the insect nervous system

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Summary

Introduction

Gene gain and subsequent retention or loss during evolution may be one of the underlying mechanisms involved in generating the diversity of metazoan nervous systems. The number of vertebrate-specific genes is five times larger than that of insect-specific genes, indicating that vertebrates have more complex gene pools than insects. If some of these vertebrate genes are shared with lophotrochozoans (the third large superphylum of Bilateria), this would imply that they were present in the last common ancestor of Bilateria (Urbilateria) and have been lost from insects during evolution [2,3]. If some of these insect genes are shared with lophotrochozoans, this would suggest that they were acquired by the last common ancestor of protostomes but not deuterostomes. Such genes have not been reported to date

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