Time-dependent stabilization of the +1 nucleosome is an early step in the transition to stable cold-induced repression of FLC

Abstract

In vernalized Arabidopsis, the extent of FLC repression and promotion of flowering are correlated with the length of winter (low temperature exposure), but how plants measure the duration of winter is unknown. Repression of FLC occurs in two phases: establishment and maintenance. This study investigates the early events in the transition between establishment and maintenance of repression. Initial repression was rapid but transient; within 24 h of being placed at low temperatures FLC transcription was reduced by 40% and repression was complete after 5 days in the cold. The extent to which repression was maintained depended on the length of the cold treatment. Occupancy of the +1 nucleosome in FLC chromatin increased in a time-dependent manner over a 4-week low temperature treatment concomitant with decreased histone acetylation and increased trimethylation of histone H3 lysine 27 (H3K27me3). Mutant analyses showed that increased nucleosome occupancy occurred independent of histone deacetylation and increased H3K27me3, suggesting that it is an early step in the switch between transient and stable repression. Both altered histone composition and deacetylation contributed to increased nucleosome occupancy. The time-dependency of the steps required for the switch between transient and stable repression suggests that the duration of winter is measured by the chromatin state at FLC. A chromatin-based switch is consistent with finding that each FLC allele in a cell undergoes this transition independently. Significance Statement In vernalized Arabidopsis, the extent of FLC repression and promotion of flowering are correlated with the length of winter, but how plants measure the duration of winter is unknown. This study shows that there is a time-dependent increase in the stability of the first nucleosome in the FLC gene that correlates with both the length of cold and stable FLC repression, suggesting that plants measure the duration of winter at the level of FLC chromatin.