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Dorone Y, Boeynaems S, Flores E, et al. A prion-like protein regulator of seed germination undergoes hydration-dependent phase separation. Cell. 2021;184(16):4284-4298.e27doi: 10.1016/j.cell.2021.06.009.
Dorone, Y., Boeynaems, S., Flores, E., Jin, B., Hateley, S., Bossi, F., Lazarus, E., Pennington, J. G., Michiels, E., De Decker, M., Vints, K., Baatsen, P., Bassel, G. W., Otegui, M. S., Holehouse, A. S., Exposito-Alonso, M., Sukenik, S., Gitler, A. D., & Rhee, S. Y. (2021). A prion-like protein regulator of seed germination undergoes hydration-dependent phase separation. Cell, 184(16), 4284-4298.e27. https://doi.org/10.1016/j.cell.2021.06.009
Dorone, Yanniv, et al. "A prion-like protein regulator of seed germination undergoes hydration-dependent phase separation." Cell vol. 184,16 (2021): 4284-4298.e27. doi: https://doi.org/10.1016/j.cell.2021.06.009
Dorone Y, Boeynaems S, Flores E, Jin B, Hateley S, Bossi F, Lazarus E, Pennington JG, Michiels E, De Decker M, Vints K, Baatsen P, Bassel GW, Otegui MS, Holehouse AS, Exposito-Alonso M, Sukenik S, Gitler AD, Rhee SY. A prion-like protein regulator of seed germination undergoes hydration-dependent phase separation. Cell. 2021 Aug 05;184(16):4284-4298.e27. doi: 10.1016/j.cell.2021.06.009. Epub 2021 Jul 06. PMID: 34233164; PMCID: PMC8513799.
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Cell. 2021 Aug 05;184(16):4284-4298.e27. doi: 10.1016/j.cell.2021.06.009. Epub 2021 Jul 06.

A prion-like protein regulator of seed germination undergoes hydration-dependent phase separation.

Cell

Yanniv Dorone, Steven Boeynaems, Eduardo Flores, Benjamin Jin, Shannon Hateley, Flavia Bossi, Elena Lazarus, Janice G Pennington, Emiel Michiels, Mathias De Decker, Katlijn Vints, Pieter Baatsen, George W Bassel, Marisa S Otegui, Alex S Holehouse, Moises Exposito-Alonso, Shahar Sukenik, Aaron D Gitler, Seung Y Rhee

Affiliations

  1. Department of Plant Biology, Carnegie Institution for Science, Stanford, CA 94305, USA; Department of Biology, Stanford University, Stanford, CA 94305, USA.
  2. Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305, USA.
  3. Department of Chemistry and Chemical Biology, UC Merced, Merced, CA 95340, USA.
  4. Department of Plant Biology, Carnegie Institution for Science, Stanford, CA 94305, USA.
  5. Center for Quantitative Cell Imaging, University of Wisconsin, Madison, WI 53706, USA.
  6. EM-platform@VIB Bio Imaging Core and VIB Center for Brain and Disease Research, KU Leuven, 3000 Leuven, Belgium; Switch Laboratory, Department of Cellular and Molecular Medicine, KU Leuven, 3000 Leuven, Belgium.
  7. EM-platform@VIB Bio Imaging Core and VIB Center for Brain and Disease Research, KU Leuven, 3000 Leuven, Belgium; KU Leuven - University of Leuven, Department of Neurosciences, Experimental Neurology, and Leuven Brain Institute (LBI), 3000 Leuven, Belgium.
  8. EM-platform@VIB Bio Imaging Core and VIB Center for Brain and Disease Research, KU Leuven, 3000 Leuven, Belgium.
  9. School of Life Sciences, University of Warwick, Coventry CV4 7AL, UK.
  10. Center for Quantitative Cell Imaging, University of Wisconsin, Madison, WI 53706, USA; Department of Botany, University of Wisconsin, Madison, WI 53706, USA.
  11. Department of Biochemistry and Molecular Biophysics, Washington University School of Medicine, St. Louis, MO 63110, USA; Center for Science and Engineering of Living Systems (CSELS), Washington University in St. Louis, St. Louis, MO 63130, USA.
  12. Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305, USA. Electronic address: [email protected].
  13. Department of Plant Biology, Carnegie Institution for Science, Stanford, CA 94305, USA. Electronic address: [email protected].

PMID: 34233164 PMCID: PMC8513799 DOI: 10.1016/j.cell.2021.06.009

Abstract

Many organisms evolved strategies to survive desiccation. Plant seeds protect dehydrated embryos from various stressors and can lay dormant for millennia. Hydration is the key trigger to initiate germination, but the mechanism by which seeds sense water remains unresolved. We identified an uncharacterized Arabidopsis thaliana prion-like protein we named FLOE1, which phase separates upon hydration and allows the embryo to sense water stress. We demonstrate that biophysical states of FLOE1 condensates modulate its biological function in vivo in suppressing seed germination under unfavorable environments. We find intragenic, intraspecific, and interspecific natural variation in FLOE1 expression and phase separation and show that intragenic variation is associated with adaptive germination strategies in natural populations. This combination of molecular, organismal, and ecological studies uncovers FLOE1 as a tunable environmental sensor with direct implications for the design of drought-resistant crops, in the face of climate change.

Copyright © 2021 Elsevier Inc. All rights reserved.

Keywords: adaptation; bet hedging; biomolecular condensate; intrinsically disordered proteins; phase separation; prion-like; salt stress; seed germination; water sensing; water stress

Conflict of interest statement

Declaration of interests Y.D., S.B., A.D.G., and S.Y.R. are inventors on a provisional patent application filed with the U.S. Patent and Trademark Office on August 7(th) 2020 by Leland Stanford Univer

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