Thermo-sensitive condensation of SUF4 tunes flowering time inArabidopsis thaliana

Abstract

ABSTRACTIntrinsically disordered proteins (IDP) lack stable tertiary structures, which allows them to change conformation and function under different physicochemical conditions. This may be highly advantageous for plants, which often use changes in their environment to trigger developmental events. For instance, some plants use exposure to winter temperatures as a cue to initiate flowering the following spring. Many of the genes involved in temperature-dependent flowering have been extensively studied inArabidopsis, yet how plants perceive temperature changes is poorly understood. Here, we explore the role of temperature-sensitive phase separation of the IDP and flowering-time regulator, SUPPRESSOR OF FRIGIDA 4 (SUF4), in modulating flowering time. SUF4 has a well-defined role in regulating temperature-dependent flowering time by activating the master floral suppressorFLOWERING LOCUS C (FLC). We show that in plant nuclei, SUF4 is a temperature-sensitive protein that assembles into biomolecular condensates in warm temperatures (20°C). When temperatures cool (4°C), SUF4 nuclear condensates disassemble, causing SUF4 to disperse within the nucleoplasm. Additionally, we demonstrate that the number of SUF4 condensates quantitatively correlates with flowering time. Progressive alterations to the amino acid composition of SUF4’s disordered region cause likewise progressive changes in temperature-dependent condensation bothin vitroandin vivo,FLCtranscription, and the onset of flowering. We also observe that SUF4 condensates coincide with the accumulation of other key flowering-time proteins (FRIGIDA and ELF7). These findings indicate that condensation of SUF4 likely plays a pivotal role in promoting flowering, possibly by concentrating and stabilizing the regulatory factors needed for the transcriptional activation ofFLCthrough temperature-dependent phase separation. This research suggests that in plants, IDPs can sense environmental cues and regulate critical developmental processes.