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

Dev Cell. 2021 Oct 25;56(20):2886-2901.e6. doi: 10.1016/j.devcel.2021.09.021. Epub 2021 Oct 15.

Abstract

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.

Keywords: Drosophila; axis patterning; biomolecular condensates; intrinsically disordered regions; in vivo imaging; mRNA regulation; phase separation; processing bodies; ribonucleoprotein.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Body Patterning / genetics
  • Body Patterning / physiology*
  • DEAD-box RNA Helicases / metabolism
  • Drosophila / growth & development
  • Drosophila / metabolism
  • Drosophila Proteins / metabolism
  • Embryo, Nonmammalian / metabolism*
  • Homeodomain Proteins / metabolism*
  • Processing Bodies / metabolism
  • RNA, Messenger, Stored / metabolism*
  • Trans-Activators / metabolism

Substances

  • Drosophila Proteins
  • Homeodomain Proteins
  • RNA, Messenger, Stored
  • Trans-Activators
  • DEAD-box RNA Helicases