Independent neofunctionalization of Dxo1 in Saccharomyces and Candida led to 25S rRNA processing function

Abstract

Eukaryotic genomes typically encode one member of the DXO/Dxo1/Rai1 family of enzymes, which can hydrolyze the 5′ ends of RNAs with a variety of structures that deviate from the canonical ^7mGpppN. In contrast, the Saccharomyces genome encodes two family members and the second copy, Dxo1, is a distributive 5′ exoribonuclease that is required for the final maturation of the 5′ end of 25S rRNA from a 25S′ precursor. Here we show that this 25S rRNA maturation function is not conserved across kingdoms, but arose in the budding yeasts. Interestingly, the origin of 25S processing capacity coincides with the duplication of this gene, and this capacity is absent in the nonduplicated genes. Strikingly, two different clades of budding yeasts have undergone parallel evolution: Both duplicated their DXO/Dxo1/Rai1 gene, and in both cases, one copy gained the 25S processing function. This was accompanied by many parallel sequence changes, a remarkable case of reproducible neofunctionalization.