An extended meiotic prophase is a hallmark of oogenesis. Hormonal signaling activates the CDK1/cyclin B kinase to promote meiotic maturation, which involves the nuclear maturation events of nuclear envelope breakdown, meiotic spindle assembly, and chromosome segregation. Cytoplasmic maturation involves major changes in oocyte protein translation and cytoplasmic organelles and is less well understood. In the nematode Caenorhabditis elegans, sperm release the major sperm protein (MSP) hormone to promote oocyte growth and meiotic maturation. A large translational regulatory ribonucleoprotein (RNP) complex containing the RNA-binding proteins OMA-1, OMA-2, and LIN-41 regulates meiotic maturation downstream of MSP signaling. To understand the control of protein translation during meiotic maturation, we purified LIN-41-containing RNPs and characterized their protein and RNA components. Protein constituents of LIN-41 RNPs include essential RNA-binding proteins, the GLD-2 cytoplasmic polyadenylase, the CCR4-NOT deadenylase complex, and translation initiation factors. RNA sequencing defined mRNAs associated with LIN-41 and OMA-1, as well as sets of mRNAs associated with either LIN-41 or OMA-1. As a class, transcripts that selectively associate with LIN-41 exhibit shortened poly(A) tails in
gld-2 mutants, suggesting that GLD-2 might stimulate their efficient translation. We analyzed the translational regulation of two transcripts specifically associated with LIN-41 that encode the RNA regulators, SPN-4 and MEG-1. We found that LIN-41 represses translation of
spn-4 and
meg-1; whereas, OMA-1 and OMA-2 promote their expression. Upon their synthesis, SPN-4 and MEG-1 assemble into LIN-41 RNPs in the oocyte prior to their functions in germline development in the embryo. Genetic results indicate that LIN-41 functions in oocytes to promote the activity of SPN-4 needed for the proper development of the germline of the next generation. This study defines a translational repression-to-activation switch as a key element of cytoplasmic maturation.