SUMMARY Maternal mRNAs synthesized during oogenesis initiate the development of future generations. Some maternal mRNAs are either somatic or germline determinants and must be translationally repressed until embryogenesis. However, the translational repressors themselves are temporally regulated. We used polar granule component (pgc), a Drosophila maternal mRNA, to ask how maternal transcripts are repressed while the regulatory landscape is shifting. pgc, a germline determinant, is translationally regulated throughout oogenesis. We find that different conserved RNA-binding proteins bind a 10-nt sequence in the 3′ UTR of pgc mRNA to continuously repress translation at different stages of oogenesis. Pumilio binds to this sequence in undifferentiated and early-differentiating oocytes to block Pgc translation. After differentiation, Bruno levels increase, allowing Bruno to bind the same sequence and take over translational repression of pgc mRNA. We have identified a class of maternal mRNAs that are regulated similarly, including zelda, the activator of the zygotic genome.

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Highlightsd Ski complex mediated RNA degradation is required in the germline for fertility.d A subset of early oogenic RNAs are degraded concurrent with oocyte specification.d Early oogenic RNAs are degraded utilizing components of the No Go Decay pathway.d Degradation of early oogenic RNAs is required for maintenance of oocyte fate.

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32Maternal mRNAs are synthesized during oogenesis to initiate the development of future 33 generations. Some maternal mRNAs are determinants of somatic or germline fate and 34 must be translationally repressed until embryogenesis. However, the translational 35 repressors themselves are also temporally regulated. We use polar granule component 36 (pgc), a Drosophila maternal mRNA, as a model system to ask how maternal mRNAs 37 are repressed while the regulatory landscape is continually shifting. pgc, a potent 38 transcriptional silencer and germline determinant, is translationally regulated throughout 39 oogenesis. We find that the 3'UTR of pgc mRNA contains a conserved ten-nucleotide 40 sequence that is bound by different conserved RNA binding proteins (RBPs) at different 41 stages of oogenesis to continuously repress translation except for a brief expression in 42 the stem cell daughter. Pumilio (Pum) binds to this sequence in undifferentiated and 43 early differentiating oocytes and recruits other temporally restricted translational 44 regulators to block pgc translation. After differentiation, Pum levels diminish and Bruno 45 (Bru) levels increase, allowing Bru to bind the same 3'UTR sequence and take over 46 translational repression of pgc mRNA. We have identified a class of maternal mRNAs 47 regulated during oogenesis by both Pum and Bru, including Zelda, activator of the 48 zygotic genome, which contain this core 10-nt regulatory sequence. Our data suggests 49 that this hand off mechanism is more generally utilized to inhibit translation of maternal 50 mRNAs during oogenesis.