MRG1/2 histone methylation readers and HD2C histone deacetylase associate in repression of the florigen gene FT to set a proper flowering time in response to day-length changes

• Published in: The New phytologist 2020-09, Vol.227 (5), p.1453-1466
• Main Authors: Guo, Zhihao, Li, Zepeng, Liu, Yuhao, An, Zengxuan, Peng, Maolin, Shen, Wen-Hui, Dong, Aiwu, Yu, Yu
• Format: Article
• Language: English
• Subjects: Arabidopsis; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Chromatin; Chromatography, Liquid; Circadian rhythm; Circadian rhythms; Connecting; Deacetylation; florigen; Florigen - metabolism; Flowering; FLOWERING LOCUS T gene; Flowers - genetics; Flowers - metabolism; Gene expression; Gene Expression Regulation, Plant; genes; Histone deacetylase; Histone Deacetylases - genetics; histone methylation reader; Histones; Histones - metabolism; Immunoprecipitation; Length; Loci; Methylation; Photoperiod; photoperiodic flowering; precipitin tests; solar radiation; Tandem Mass Spectrometry; Transcription; transcriptional repression
• ISSN: 0028-646X; 1469-8137
• DOI: 10.1111/nph.16616

Day-length changes represent an important cue for modulating flowering time. In Arabidopsis, the expression of the florigen gene FLOWERING LOCUS T (FT) exhibits a 24-h circadian rhythm under long-day (LD) conditions. Here we focus on the chromatin-based mechanism regarding the control of FT expression. We conducted co-immunoprecipitation assays along with LC-MS/MS analysis and identified HD2C histone deacetylase as the binding protein of the H3K4/H3K36 methylation reader MRG2. HD2C and MRG1/2 regulate flowering time under LD conditions, but not under short-day conditions. Moreover, HD2C functions as an effective deacetylase in planta, mainly targeting H3K9ac, H3K23ac and H3K27ac. At dusk, HD2C is recruited to FT to deacetylate histones and repress transcription in an MRG1/2-dependent manner. More importantly, HD2C competes with CO for the binding of MRG2, and the accumulation of HD2C at the FT locus occurs at the end of the day. Our findings not only reveal a histone deacetylation mechanism contributing to prevent FT overexpression and precocious flowering, but also support the model in which the histone methylation readers MRG1/2 provide a platform on chromatin for connecting regulatory factors involved in activating FT expression in response to daylight and decreasing FT expression around dusk under long days.