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Multiple maternal proteins coordinate to restrict the translation of C. elegans nanos-2 to primordial germ cells

Although germ cell formation has been relatively well understood in worms and insects, how germ cell-specific developmental programs are initiated is not clear. In Caenorhabditis elegans, translational activation of maternal nos-2 mRNA is the earliest known molecular event specific to the germline founder cell P4. Cis-elements in nos-2 3′UTR have been shown to mediate translational control; however, the trans-acting proteins are not known. Here, we provide evidence that four maternal RNA-binding proteins, OMA-1, OMA-2, MEX-3 and SPN-4, bind nos-2 3′UTR to suppress its translation, and POS-1, another maternal RNA-binding protein, relieves this suppression in P4. The POS-1: SPN-4 ratio in P4 increases significantly over its precursor, P3; and POS-1 competes with SPN-4 for binding to nos-2 RNA in vitro. We propose temporal changes in the relative concentrations of POS-1 and SPN-4, through their effect on the translational status of maternal mRNAs such as nos-2, initiate germ cell-specific developmental programs in C. elegans.