A pair of readers of histone H3K4 methylation recruit Polycomb repressive complex 2 to regulate photoperiodic flowering

Abstract

In flowering plants, the transition from vegetative growth to reproduction or flowering, is often timed by seasonal changes in day length (photoperiod). In the model flowering plant Arabidopsis thaliana, the photoperiodic cue increasing day length or long day, through the photoperiod pathway, induces a daily rhythmic activation of the florigen gene FLOWERING LOCUS T (FT) to promote flowering. Under inductive long days (LDs), FT expression is activated around dusk, but to be repressed overnight and into the early afternoon the next day. The mechanism underlying the daily oscillation of FT repression to ensure long-day induction of flowering remains unclear. Here, we report that AtING1 and AtING2, Arabidopsis homologs of the mammalian Inhibitor of Growth (ING) proteins, read di- and tri-methylated histone 3 lysine 4 (H3K4me2/me3) on FT chromatin and further recruit Polycomb-repressive complex 2 (PRC2) to repress FT expression at night and into the early afternoon the next day, following FT activation at dusk in LDs. This prevents precocious flowering under inductive LDs. Our study reveals that a previously-undescribed chromatin-regulatory module: H3K4me2/me3-ING1/2-PRC2, which timely represses FT expression following the daily rhythmic FT activation at dusk by the long-day pathway, to prevent excessive FT expression and thus precisely control the timing of the transition to flowering in response to inductive photoperiodic signals.