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

Cell. 2021 Aug 5;184(16):4284-4298.e27. doi: 10.1016/j.cell.2021.06.009. Epub 2021 Jul 6.

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.

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

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Arabidopsis / genetics
  • Arabidopsis / growth & development*
  • Arabidopsis / ultrastructure
  • Arabidopsis Proteins / chemistry
  • Arabidopsis Proteins / metabolism*
  • Arabidopsis Proteins / ultrastructure
  • Dehydration
  • Germination*
  • Imaging, Three-Dimensional
  • Intercellular Signaling Peptides and Proteins / chemistry
  • Intercellular Signaling Peptides and Proteins / metabolism*
  • Mutation / genetics
  • Plant Dormancy
  • Plants, Genetically Modified
  • Prions / metabolism*
  • Protein Domains
  • Protein Isoforms / metabolism
  • Seeds / growth & development*
  • Seeds / ultrastructure
  • Water / metabolism*

Substances

  • AT4G28300 protein, Arabidopsis
  • Arabidopsis Proteins
  • Intercellular Signaling Peptides and Proteins
  • Prions
  • Protein Isoforms
  • Water