Adaptable P body physical states differentially regulate bicoid mRNA storage during early Drosophila development

Summary

Ribonucleoprotein condensates can exhibit diverse physical states in vitro and in vivo. Despite considerable progress, the relevance of condensate physical states for in vivo biological function remains limited. Here, we investigated the physical properties of processing bodies (P bodies) and their impact on mRNA storage in mature Drosophila oocytes. We show that the conserved DEAD-box RNA helicase Me31B forms viscous P body condensates, which adopt an arrested physical state. We demonstrate that structurally distinct proteins and protein-protein interactions, together with RNA, regulate the physical properties of P bodies. Using live imaging and in situ hybridization, we show that the arrested state and integrity of P bodies support the storage of bicoid (bcd) mRNA and that egg activation modulates P body properties, leading to the release of bcd for translation in the early embryo. Together, this work provides an example of how physical states of condensates regulate cellular function in development.

Graphical abstract

Highlights

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  P bodies adopt an arrested physical state in the mature oocyte

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  Multivalent interactions and structurally distinct proteins regulate P body properties

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  The arrested state and integrity of P bodies support the storage of bicoid mRNA

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  Egg activation modulates P body properties and leads to release of bicoid mRNA

Abstract

Sankaranarayanan et al. show that P bodies, conserved ribonucleoprotein condensates found in Drosophila oocytes, are regulated by specific structural features and weak multivalent interactions. In vivo, P bodies adopt an arrested physical state that is critical for the storage of the bicoid patterning mRNA until egg activation.