TDRD5 Is Required for Spermatogenesis and Oogenesis in Locusta migratoria

SIMPLE SUMMARY: Tudor domain-containing proteins (TDRDs) are a group of evolutionarily conserved and germline-enriched proteins, and most of them function in reproduction and the P-element-induced wimpy testis-interacting RNA (piRNA) pathway. We investigated LmTDRD5, a TDRD5 ortholog in Locusta migratoria. In males, LmTdrd5 knockdown delayed meiosis phase transition and reduced the number of elongated spermatids and sperm count. The expression levels of two haploid germ cell marker genes, LmCREM and LmACT, as well as the sperm tail marker gene LmQrich2 were downregulated. In females, LmTdrd5 knockdown decreased vitellogenin (Vg) and Vg receptor (VgR) transcript levels, thereby affecting ovarian development and oocyte maturation. Therefore, LmTdrd5 may play an important role in locust reproduction, indicative of a conserved primary function of TDRD5. ABSTRACT: Tudor family proteins exist in all eukaryotic organisms and play a role in many cellular processes by recognizing and binding to proteins with methylated arginine or lysine residues. TDRD5, a member of Tudor domain-containing proteins (TDRDs), has been implicated in the P-element-induced wimpy testis-interacting RNA (piRNA) pathway and germ cell development in some model species, but little is known about its function in other species. Therefore, we identified and characterized LmTDRD5, the TDRD5 ortholog in Locusta migratoria, a hemimetabolous pest. The LmTdrd5 gene has 19 exons that encode a protein possessing a single copy of the Tudor domain and three LOTUS domains at its N-terminus. qRT-PCR analysis revealed a high LmTdrd5 expression level in genital glands. Using RNA interference, LmTdrd5 knockdown in males led to a lag in meiosis phase transition, decreased spermatid elongation and sperm production, and downregulated the expression of the two germ cell-specific transcription factors, LmCREM and LmACT, as well as the sperm tail marker gene LmQrich2. LmTdrd5 knockdown in females reduced the expression levels of vitellogenin (Vg) and Vg receptor (VgR) and impaired ovarian development and oocyte maturation, thus decreasing the hatchability rate. These results demonstrate that LmTdrd5 is essential for germ cell development and fertility in locusts, indicating a conserved function for TDRD5.