Peculiarities of the e(y)2 Gene Evolution in Deuterostomes and Drosophilinae

Gene duplication, a major source of new genes in evolution, often occurs via reverse transcription of mRNA, leading to the integration of a retrocopy into a new genomic locus. Here, we performed an in-depth analysis of the evolutionary history of the <i>e(y)2</i> gene in Metazoa. The E(y)2 protein is a shared subunit of two highly conserved complexes involved in transcription regulation (the DUB module of the SAGA complex) and mRNA transport (TREX-2). In Deuterostomes, the <i>e(y)2</i> gene has undergone multiple independent retropositions, often giving rise to functional retrogenes. In contrast, among Protostomes, duplications of <i>e(y)2</i> were identified only in Drosophilinae and a member of the Lepidoptera family (<i>Manduca sexta</i>). In <i>Drosophila</i>, the retrocopy <i>e(y)2</i> acquired an almost ubiquitous expression pattern and compensates for the function of the parental gene in all tissues except the testes. The parental gene, <i>e(y)2b</i>, evolved a testis-specific expression pattern, lost the ability to incorporate into the DUB module, but retained nuclear envelope localization and the capacity to assemble into the TREX-2 complex. Knockout of the <i>D. melanogaster e(y)2b</i> gene resulted in reduced male fertility. Overall, our study highlights distinct evolutionary trajectories of the <i>e(y)2</i> gene in Deuterostomes and Protostomes.