TORC1-dependent translation drives chromatin remodeling during the germ-cell-to-maternal transition in Drosophila

Proper oogenesis requires a programmed transition from an undifferentiated germ-cell gene expression program to a maternal gene-expression state. While this process depends on the heterochromatin-mediated silencing of germ-cell genes, the upstream mechanisms that enforce this transcriptional shift remain unclear. Here, we uncover a translation-driven chromatin remodeling program that promotes oocyte fate in Drosophila. Through a loss of function screen, we identify TORC1 activity (Mio, Raptor), ribosome biogenesis (Zfrp8, Bystin, Aramis), and a translation factor (eEF1α1) as essential for silencing the germ-cell program. We show that TORC1 activity increases during oocyte specification, and that disruption of TORC1 activity, translation, or ribosome biogenesis during this window impairs heterochromatin maintenance at germ-cell gene loci. Polysome profiling reveals that Zfrp8 promotes translation of the nuclear pore component Nucleoporin 44A (Nup44A), whose function is independently required for chromatin organization and repression of a cohort of germ-cell genes. Taken together, our findings reveal that a transient increase in translation orchestrates chromatin remodeling to ensure commitment to oocyte fate.