Evolution of the metazoan-specific importin alpha gene family

Importin alphas are import receptors for nuclear localization signal-containing proteins. Most animal importin alphas assort into alpha1, alpha2, and alpha3 groups. Studies in Drosophila melanogaster, Caenorhabditis elegans, and mouse suggest that the animal importin alpha gene family evolved from ancestral plant-like genes to serve paralog-specific roles in gametogenesis. To explore this hypothesis we extended the phylogenetic analysis of the importin alpha gene family to nonbilateral animals and investigated whether animal-like genes occur in premetazoan taxa. Maximum likelihood analysis suggests that animal-like importin alpha genes occur in the Choanoflaggelate Monosiga brevicollis and the amoebozoan Dictyostelium; however, both of these results are caused by long-branch attraction effects. The absence of animal-like alpha genes in premetazoan taxa is consistent with the hypothesis that they duplicated and then specialized to function in animal gametogenesis. The gene structures of the importin alphas provide insight into how the animal importin alpha gene family may have evolved from the most likely ancestral gene. Interestingly, animal alpha1s are more similar to plant and fungal alpha1-like sequences than they are to animal alpha2s or alpha3s. We show that animal alpha1 genes share most of their introns with plant alpha1-like genes, and alpha2s and alpha3s share many more intron positions with each other than with the alpha1s. Together, phylogenetics and gene structure analysis suggests a parsimonious path for the evolution of the mammalian importin alpha gene family from an ancestral alpha1-like progenitor. Finally, these results establish a rational basis for a unified nomenclature of the importin alpha gene family.