Liquid-to-solid phase transition of oskar ribonucleoprotein granules is essential for their function in Drosophila embryonic development

Summary

Asymmetric localization of oskar ribonucleoprotein (RNP) granules to the oocyte posterior is crucial for abdominal patterning and germline formation in the Drosophila embryo. We show that oskar RNP granules in the oocyte are condensates with solid-like physical properties. Using purified oskar RNA and scaffold proteins Bruno and Hrp48, we confirm in vitro that oskar granules undergo a liquid-to-solid phase transition. Whereas the liquid phase allows RNA incorporation, the solid phase precludes incorporation of additional RNA while allowing RNA-dependent partitioning of client proteins. Genetic modification of scaffold granule proteins or tethering the intrinsically disordered region of human fused in sarcoma (FUS) to oskar mRNA allowed modulation of granule material properties in vivo. The resulting liquid-like properties impaired oskar localization and translation with severe consequences on embryonic development. Our study reflects how physiological phase transitions shape RNA-protein condensates to regulate the localization and expression of a maternal RNA that instructs germline formation.

Graphical abstract

Highlights

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  oskar RNP granules in the developing oocyte are solid-like condensates

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  oskar RNP granules undergo liquid-to-solid phase transition in vitro

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  The liquid phase incorporates mRNA, while the solid phase enriches specific proteins

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  Perturbing the solid state impairs oskar localization, translation, and development

Abstract

Liquid-to-solid phase transition of oskar RNP granules ensures Drosophila embryonic development by regulating oskar mRNA localization and translation.