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Hydration-dependent phase separation of a prion-like protein regulates seed germination during water stress

View ORCID ProfileYanniv Dorone, View ORCID ProfileSteven Boeynaems, View ORCID ProfileBenjamin Jin, Flavia Bossi, Eduardo Flores, View ORCID ProfileElena Lazarus, View ORCID ProfileEmiel Michiels, Mathias De Decker, View ORCID ProfilePieter Baatsen, View ORCID ProfileAlex S. Holehouse, View ORCID ProfileShahar Sukenik, View ORCID ProfileAaron D. Gitler, View ORCID ProfileSeung Y. Rhee
doi: https://doi.org/10.1101/2020.08.07.242172
Yanniv Dorone
1Department of Plant Biology, Carnegie Institution for Science, Stanford, California 94305, USA
2Department of Biology, Stanford University, Stanford, CA 94305, USA
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Steven Boeynaems
3Department of Genetics, Stanford University School of Medicine, Stanford, California 94305, USA
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Benjamin Jin
1Department of Plant Biology, Carnegie Institution for Science, Stanford, California 94305, USA
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Flavia Bossi
1Department of Plant Biology, Carnegie Institution for Science, Stanford, California 94305, USA
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Eduardo Flores
4Department of Chemistry and Chemical Biology, UC Merced, Merced, CA 95340, USA
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Elena Lazarus
1Department of Plant Biology, Carnegie Institution for Science, Stanford, California 94305, USA
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Emiel Michiels
5VIB Center for Brain and Disease Research, 3000 Leuven, Belgium
6Switch Laboratory, Department of Cellular and Molecular Medicine, KU Leuven, 3000 Leuven, Belgium
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Mathias De Decker
5VIB Center for Brain and Disease Research, 3000 Leuven, Belgium
7KU Leuven – University of Leuven, Department of Neurosciences, Experimental Neurology, and Leuven Brain Institute (LBI), 3000 Leuven, Belgium
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Pieter Baatsen
5VIB Center for Brain and Disease Research, 3000 Leuven, Belgium
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Alex S. Holehouse
8Department of Biochemistry and Molecular Biophysics, Washington University School of Medicine, St. Louis, Missouri 63110, USA
9Center for Science and Engineering of Living Systems (CSELS), Washington University in St. Louis, St. Louis, MO 63130, USA
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Shahar Sukenik
4Department of Chemistry and Chemical Biology, UC Merced, Merced, CA 95340, USA
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Aaron D. Gitler
3Department of Genetics, Stanford University School of Medicine, Stanford, California 94305, USA
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  • For correspondence: srhee@carnegiescience.edu agitler@stanford.edu
Seung Y. Rhee
1Department of Plant Biology, Carnegie Institution for Science, Stanford, California 94305, USA
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  • For correspondence: srhee@carnegiescience.edu agitler@stanford.edu
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ABSTRACT

Many organisms evolved strategies to survive and thrive under extreme desiccation. Plant seeds protect dehydrated embryos from a variety of stressors and can even lay dormant for millennia. While hydration is the key trigger that reactivates metabolism and kick-starts germination, the exact mechanism by which the embryo senses 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 the biophysical states of FLOE1 condensates modulate its biological function in vivo in suppressing seed germination under unfavorable environments. We also find intragenic, intraspecific, and interspecific natural variations in phase separation propensity of FLOE1 homologs. These findings demonstrate a physiological role of phase separation in a multicellular organism and have direct implications for plant ecology and agriculture, especially the design of drought resistant crops, in the face of climate change.

Competing Interest Statement

The authors have declared no competing interest.

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Posted August 07, 2020.
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Hydration-dependent phase separation of a prion-like protein regulates seed germination during water stress
Yanniv Dorone, Steven Boeynaems, Benjamin Jin, Flavia Bossi, Eduardo Flores, Elena Lazarus, Emiel Michiels, Mathias De Decker, Pieter Baatsen, Alex S. Holehouse, Shahar Sukenik, Aaron D. Gitler, Seung Y. Rhee
bioRxiv 2020.08.07.242172; doi: https://doi.org/10.1101/2020.08.07.242172
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Hydration-dependent phase separation of a prion-like protein regulates seed germination during water stress
Yanniv Dorone, Steven Boeynaems, Benjamin Jin, Flavia Bossi, Eduardo Flores, Elena Lazarus, Emiel Michiels, Mathias De Decker, Pieter Baatsen, Alex S. Holehouse, Shahar Sukenik, Aaron D. Gitler, Seung Y. Rhee
bioRxiv 2020.08.07.242172; doi: https://doi.org/10.1101/2020.08.07.242172

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