Thermo-sensitive condensation of SUF4 tunes flowering time in Arabidopsis thaliana

Abstract

Intrinsically 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 elicit a variety of responses, including developmental events. For instance, some plants delay flowering in the fall and require 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 in Arabidopsis, yet how plants coordinate their molecular states with seasonal temperature change 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 suppressor FLOWERING LOCUS C (FLC). We show that in plant nuclei, SUF4 is a temperature-sensitive protein that assembles into biomolecular condensates in warm temperatures (20{degrees}C). When temperatures cool (4{degrees}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 SUF4s disordered region cause likewise progressive changes in temperature-dependent condensation both in vitro and in vivo, FLC transcription, and the onset of flowering. Lastly, we 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 regulatory factors needed for the transcriptional activation of FLC through temperature-dependent phase separation. This research suggests that in plants, IDPs can sense environmental cues and regulate critical developmental processes. One-Sentence SummaryEvidence suggest that Arabidopsis uses temperature-sensitive condensation to regulate FLC transcription and flowering time.