The FKF1-ELF3-PRC2 module regulates flowering time in response to light in temperate grasses.

Abstract

The precise timing of flowering is critical to ensure reproductive success in plants. This process is coordinated by both endogenous and environmental cues. Light is a pivotal environmental cue fundamentally regulating plant growth and development. In temperate grasses, how light regulates flowering time remains largely unknown. Here, we characterize a blue-light photoreceptor, FLAVIN-BINDING, KELCH REPEAT, F-BOX 1 (FKF1), which functions as a flowering promoter in <i>Brachypodium distachyon</i>. Loss-of-function mutations in <i>FKF1</i> result in delayed flowering under long-day conditions, whereas overexpression of <i>FKF1</i> strongly accelerates flowering. We show that FKF1 controls the stability of floral repressor EARLY FLOWERING 3 (ELF3) in response to blue light. FKF1 directly interacts with and catalyzes the ubiquitination of ELF3, leading to protein degradation of ELF3 via the 26S proteasome pathway. Blue light can strengthen the interaction between FKF1 and ELF3, thereby accelerating degradation of ELF3. Moreover, ELF3 physically interacts with SWINGER and CURLY LEAF, two core subunits of Polycomb repressive complex 2 (PRC2), and mediates the subsequent deposition of histone H3 lysine 27 trimethylation (H3K27me3) for stable transcriptional silencing of the flowering activator <i>PHOTOPERIOD 1</i>. Remarkably, the FKF1-ELF3-PRC2 regulatory module-mediated flowering time control in response to light is likely conserved across temperate grasses. Our study elucidates the mechanism by which light modulates H3K27me3 deposition to regulate flowering time in temperate grasses. This mechanism also allows plants to adapt to dynamically changing environments.