Viscoelasticity and advective flow of RNA underlies nucleolar form and function

Joshua A. Riback, Jorine M. Eeftens, Daniel S.W. Lee, Sofia A. Quinodoz, Anita Donlic, Natalia Orlovsky, Lennard Wiesner, Lien Beckers, Lindsay A. Becker, Amy R. Strom, Ushnish Rana, Michele Tolbert, Byron W. Purse, Ralph Kleiner, Richard Kriwacki, Clifford P. Brangwynne

Research output: Contribution to journalArticlepeer-review

7 Scopus citations

Abstract

The nucleolus is the largest biomolecular condensate and facilitates transcription, processing, and assembly of ribosomal RNA (rRNA). Although nucleolar function is thought to require multiphase liquid-like properties, nucleolar fluidity and its connection to the highly coordinated transport and biogenesis of ribosomal subunits are poorly understood. Here, we use quantitative imaging, mathematical modeling, and pulse-chase nucleotide labeling to examine nucleolar material properties and rRNA dynamics. The mobility of rRNA is several orders of magnitude slower than that of nucleolar proteins, with rRNA steadily moving away from the transcriptional sites in a slow (∼1 Å/s), radially directed fashion. This constrained but directional mobility, together with polymer physics-based calculations, suggests that nascent rRNA forms an entangled gel, whose constant production drives outward flow. We propose a model in which progressive maturation of nascent rRNA reduces its initial entanglement, fluidizing the nucleolar periphery to facilitate the release of assembled pre-ribosomal particles.

Original languageEnglish (US)
Pages (from-to)3095-3107.e9
JournalMolecular Cell
Volume83
Issue number17
DOIs
StatePublished - Sep 7 2023

All Science Journal Classification (ASJC) codes

  • Molecular Biology
  • Cell Biology

Keywords

  • biomolecular condensate
  • liquid-liquid phase separation
  • membraneless organelle
  • nucleolus
  • ribonucleoprotein assembly
  • ribosome biogenesis
  • transcription
  • viscoelasticity

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