Evolutionary history of the iroquois/Irx genes in metazoans

BACKGROUND: The iroquois (iro/Irx) genes encode transcriptional regulators that belong to the TALE superclass of homeodomain proteins and have key functions during development in both vertebrates and insects. The Irx genes occur in one or two genomic clusters containing three genes each within the Drosophila and several vertebrate genomes, respectively. The similar genomic organization in Drosophila and vertebrates is widely considered as a result of convergent evolution, due to independent tandem gene duplications. In this study, we investigate the evolutionary history of the Irx genes at the scale of the whole metazoan kingdom. RESULTS: We identified in silico the putative full complement of Irx genes in the sequenced genomes of 36 different species representative of the main metazoan lineages, including non bilaterian species, several arthropods, non vertebrate chordates, and a basal vertebrate, the sea lamprey. We performed extensive phylogenetic analyses of the identified Irx genes and defined their genomic organizations. We found that, in most species, there are several Irx genes, these genes form two to four gene clusters, and the Irx genes are physically linked to a structurally and functionally unrelated gene known as CG10632 in Drosophila. CONCLUSION: Three main conclusions can be drawn from our study. First, an Irx cluster composed of two genes, araucan/caupolican and mirror, is ancestral to the crustaceans+insects clade and has been strongly conserved in this clade. Second, three Irx genes were probably present in the last common ancestor of vertebrates and the duplication that has given rise to the six genes organized into two clusters found in most vertebrates, likely occurred in the gnathostome lineage after its separation from sea lampreys. Third, the clustered organization of the Irx genes in various evolutionary lineages may represent an exceptional case of convergent evolution or may point to the existence of an Irx gene cluster ancestral to bilaterians.