Abstract
Day-length is important for regulating the transition to reproductive development (flowering) in plants. In the model plant Arabidopsis thaliana, the transcription factor CONSTANS (CO) promotes expression of the florigen FLOWERING LOCUS T (FT), constituting a key flowering pathway under long-day photoperiods. Recent studies have revealed that FT expression is regulated by changes of histone modification marks of the FT chromatin, but the epigenetic regulators that directly interact with the CO protein have not been identified. Here, we show that the Arabidopsis Morf Related Gene (MRG) group proteins MRG1 and MRG2 act as H3K4me3/H3K36me3 readers and physically interact with CO to activate FT expression. In vitro binding analyses indicated that the chromodomains of MRG1 and MRG2 preferentially bind H3K4me3/H3K36me3 peptides. The mrg1 mrg2 double mutant exhibits reduced mRNA levels of FT, but not of CO, and shows a late-flowering phenotype under the long-day but not short-day photoperiod growth conditions. MRG2 associates with the chromatin of FT promoter in a way dependent of both CO and H3K4me3/H3K36me3. Vice versa, loss of MRG1 and MRG2 also impairs CO binding at the FT promoter. Crystal structure analyses of MRG2 bound with H3K4me3/H3K36me3 peptides together with mutagenesis analysis in planta further demonstrated that MRG2 function relies on its H3K4me3/H3K36me3-binding activity. Collectively, our results unravel a novel chromatin regulatory mechanism, linking functions of MRG1 and MRG2 proteins, H3K4/H3K36 methylations, and CO in FT activation in the photoperiodic regulation of flowering time in plants.
Highlights
The timing of floral transition from vegetative to reproductive development is a critical event in the plant life cycle and is coordinated by internal and environmental cues [1,2,3]
We present Arabidopsis MRG1/2 as novel chromatin effectors directly involved in the CO-FLOWERING LOCUS T (FT) photoperiodic flowering
MRG2 can directly target in vivo the FT promoter chromatin in a H3K4me3/H3K36me3level dependent manner
Summary
The timing of floral transition from vegetative to reproductive development is a critical event in the plant life cycle and is coordinated by internal and environmental cues [1,2,3]. In Arabidopsis, the photoperiodic flowering pathway is regulated by the transcription factor CONSTANS (CO) and the florigen FLOWERING LOCUS T (FT) [4]. Circadian-clock regulated CO mRNA and light-dependent stabilization of CO protein are crucial for activation of FT expression in leaves under long days (LDs) but not short days (SDs); the FT protein is translocated to the shoot apical meristem, where it promotes flowering [4]. Histone lysine methylation is an important epigenetic mechanism for the regulation of gene expression. Recent studies have revealed that chromatin mechanisms play important roles in flowering time by regulating the expression of key flowering-regulatory genes [7]. FT expression is affected by several factors, including
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