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      RNA promotes phase separation of glycolysis enzymes into yeast G bodies in hypoxia

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          Abstract

          In hypoxic stress conditions, glycolysis enzymes assemble into singular cytoplasmic granules called glycolytic (G) bodies. G body formation in yeast correlates with increased glucose consumption and cell survival. However, the physical properties and organizing principles that define G body formation are unclear. We demonstrate that glycolysis enzymes are non-canonical RNA binding proteins, sharing many common mRNA substrates that are also integral constituents of G bodies. Targeting nonspecific endoribonucleases to G bodies reveals that RNA nucleates G body formation and maintains its structural integrity. Consistent with a phase separation mechanism of biogenesis, recruitment of glycolysis enzymes to G bodies relies on multivalent homotypic and heterotypic interactions. Furthermore, G bodies fuse in vivo and are largely insensitive to 1,6-hexanediol, consistent with a hydrogel-like composition. Taken together, our results elucidate the biophysical nature of G bodies and demonstrate that RNA nucleates phase separation of the glycolysis machinery in response to hypoxic stress.

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          Author and article information

          Contributors
          Role: Reviewing Editor
          Role: Senior Editor
          Journal
          eLife
          Elife
          eLife
          eLife
          eLife Sciences Publications, Ltd
          2050-084X
          16 April 2020
          2020
          : 9
          : e48480
          Affiliations
          [1 ]Department of Biology, Johns Hopkins University BaltimoreUnited States
          [2 ]National Institute of Biological Sciences BeijingChina
          [3 ]Department of Chemical Physiology, The Scripps Research Institute La JollaUnited States
          [4 ]Department of Biophysics, Johns Hopkins University BaltimoreUnited States
          University of Cambridge United Kingdom
          University of Cambridge United Kingdom
          University of Cambridge United Kingdom
          Author notes
          [†]

          EMBL-EBI, Wellcome Genome Campus, Hinxton, United Kingdom.

          [‡]

          Center for the Genetics of Host Defense, UT Southwestern Medical Center, Dallas, United States.

          Author information
          https://orcid.org/0000-0003-2960-0256
          https://orcid.org/0000-0001-5267-1672
          https://orcid.org/0000-0001-9838-3254
          Article
          48480
          10.7554/eLife.48480
          7162659
          32298230
          797df118-6966-413c-9677-77ded147f7ac
          © 2020, Fuller et al

          This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

          History
          : 15 May 2019
          : 31 March 2020
          Funding
          Funded by: FundRef http://dx.doi.org/10.13039/100000057, National Institute of General Medical Sciences;
          Award ID: RO1GM129301
          Award Recipient :
          Funded by: FundRef http://dx.doi.org/10.13039/100000057, National Institute of General Medical Sciences;
          Award ID: P41 GM103533
          Award Recipient :
          Funded by: FundRef http://dx.doi.org/10.13039/100000065, National Institute of Neurological Disorders and Stroke;
          Award ID: 1-RF1-NS113636-01
          Award Recipient :
          The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
          Categories
          Research Article
          Cell Biology
          Custom metadata
          Under hypoxic stress, when cellular demand for energy relies entirely on glycolysis, the machinery for glycolysis binds RNA and phase separates into G bodies, leading to enhanced glycolysis rates.

          Life sciences
          glycolysis,hypoxia,rna,phase separation,s. cerevisiae
          Life sciences
          glycolysis, hypoxia, rna, phase separation, s. cerevisiae

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