The amphioxus rab GDP-dissociation inhibitor (GDI) gene is neural- specific: Implications for the evolution of chordate rab GDI genes

Abstract

The rab GDP-dissociation inhibitor (rab GDI) proteins are involved in the regulation of vesicle-mediated cellular transport. We isolated the amphioxus rab GDI gene, analyzed its expression during amphioxus development, and performed a phylogenetic analysis of the rab GDI family. In contrast to the two major rab GDI forms in mammals, the α and β forms, there is only one rab GDI isoform in amphioxus. Our analysis indicates that the occurrence of the α and β forms of rab GDI preceded the divergence of lineages leading to birds and mammals, and that the amphioxus rab GDI may have evolved directly from the common ancestor of both forms. While the mammalian rab GDI β genes are ubiquitously expressed, the rab GDI α genes are predominantly expressed in neural tissues. The expression analysis of the amphioxus rab GDI gene shows predominantly neural expression similar to that of the mammalian rab GDI α form, suggesting that the ancestral expression pattern of chordate rab GDI was neural. In addition, the chicken rab GDI β-like gene also shows neural-specific expression, which indicates that the neural expression was retained in both early postduplication α and β isoforms and that a novel function associated with ubiquitous expression may have evolved uniquely in mammals. These results reveal a likely scenario of functional divergence of the rab GDI genes after duplication of the ancestral gene. A similar pattern of evolution, in which one of the duplicated genes retained a role similar to that of the ancestral one while other genes were recruited into novel roles, was also observed in the analysis of chordate Otx and hedgehog genes. In the rab GDI, hedgehog, and Otx gene families, the gene retaining the ancestral role shows a lower rate of sequence evolution than its counterpart, which was recruited for a novel function.