Tudor domain containing protein 5-like (Tdrd5l) identifies a novel germline body and regulates maternal RNAs during oogenesis

Abstract

Tudor domain-containing proteins are conserved across the animal kingdom for their function in germline development and fertility. Previously, we demonstrated that Tudor domain-containing protein 5-like (Tdrd5l) plays an important role in the germline where it promotes male identity. However, Tdrd5l is also expressed in both the ovary and testis during later stages of germline development, suggesting that it plays a role in germline differentiation in both sexes. We found that Tdrd5l localizes to a potentially novel germline body and plays a role in post-transcriptional gene regulation. RNA sequencing of Tdrd5l-mutant ovaries compared to wild-type showed that differentially expressed genes were enriched for maternally deposited RNAs. Additionally, embryos laid by Tdrd5l-mutant females exhibited reduced viability and displayed dorsal appendage defects suggesting a failure of proper dorsal-ventral (D/V) patterning. As D/V patterning is dependent on gurken (grk), we examined Grk expression during oogenesis. We observed premature accumulation of Grk protein in nurse cells indicating that translation is no longer properly repressed during mRNA transport to the oocyte. We also observed increased nurse cell accumulation of the cytoplasmic polyadenylation element binding protein Oo18 RNA-Binding Protein (Orb or CPEB), a translational activator of Grk. Decreasing orb function was able to partially rescue the Tdrd5l-mutant phenotype, and so defects in Orb are likely a primary cause of the defects in Tdrd5l mutants. Our data indicate that Tdrd5l is important for translational repression of maternal mRNAs such as orb, and possibly others, following their synthesis in the nurse cells and during their transport to the oocyte.