Drosophila doublefault protein coordinates multiple events during male meiosis by controlling mRNA translation

Abstract

During the extended prophase of Drosophila gametogenesis, spermatocytes undergo robust gene transcription and store many transcripts in the cytoplasm in a repressed state, until translational activation of select mRNAs in later steps of spermatogenesis. Here we characterize the Drosophila Doublefault (Dbf) protein as a C2H2-zinc finger protein, primarily expressed in testes, that is required for normal meiotic division and spermiogenesis. Loss of Dbf causes premature centriole disengagement and affects spindle structure, chromosome segregation and cytokinesis. We show that Dbf interacts with the RNA binding protein Syncrip/hnRNPQ, a key regulator of localized translation in Drosophila. We propose that the pleiotropic effects of dbf loss-of-function mutants are associated with the requirement for dbf function for translation of specific transcripts in spermatocytes. In agreement with this hypothesis, Dbf protein binds cyclin B mRNA and is essential for translation of cyclin B in mature spermatocytes.