Floral regulators FLC and SOC1 directly regulate expression of the B3-type transcription factor TARGET OF FLC AND SVP 1 at the Arabidopsis shoot apex via antagonistic chromatin modifications

Integration of environmental and endogenous cues at plant shoot meristems determines the timing of flowering and reproductive development. The MADS box transcription factor FLOWERING LOCUS C (FLC) of Arabidopsis thaliana is an important repressor of floral transition, which blocks flowering until plants are exposed to winter cold. However, the target genes of FLC have not been thoroughly described, and our understanding of the mechanisms by which FLC represses transcription of these targets and how this repression is overcome during floral transition is still fragmentary. Here, we identify and characterize TARGET OF FLC AND SVP1 (TFS1), a novel target gene of FLC and its interacting protein SHORT VEGETATIVE PHASE (SVP). TFS1 encodes a B3-type transcription factor, and we show that tfs1 mutants are later flowering than wild-type, particularly under short days. FLC and SVP repress TFS1 transcription leading to deposition of trimethylation of Iysine 27 of histone 3 (H3K27me3) by the Polycomb Repressive Complex 2 at the TFS1 locus. During floral transition, after downregulation of FLC by cold, TFS1 transcription is promoted by SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1 (SOC1), a MADS box protein encoded by another target of FLC/SVP. SOC1 opposes PRC function at TFS1 through recruitment of the histone demethylase RELATIVE OF EARLY FLOWERING 6 (REF6) and the SWI/SNF chromatin remodeler ATPase BRAHMA (BRM). This recruitment of BRM is also strictly required for SQUAMOSA PROMOTER BINDING PROTEIN-LIKE 9 (SPL9) binding at TFS1 to coordinate RNAPII recruitment through the Mediator complex. Thus, we show that antagonistic chromatin modifications mediated by different MADS box transcription factor complexes play a crucial role in defining the temporal and spatial patterns of transcription of genes within a network of interactions downstream of FLC/SVP during floral transition. Author summary The initiation of flowering in plants is exquisitely sensitive to environmental signals, ensuring that reproduction occurs at the appropriate time of year. The sensitivity of these responses depends upon strong repression of flowering under inappropriate conditions. FLOWERING LOCUS C (FLC) and SHORT VEGETATIVE PHASE (SVP) are related transcription factors that act in concert to strongly inhibit flowering in crucifer plants through repressing transcription of their target genes. Many direct FLC/ SVP targets have been identified in genome-wide studies, however few of these genes have been characterized for their roles in regulating flowering time or other aspects of reproductive development. Here, we characterize TARGET OF FLC AND SVP1 (TFS1) as a novel target of FLC and SVP, and demonstrate that TFS1 contributes to proper flowering-time control. Moreover, we provide a detailed mechanistic view of how TFS1 transcription is controlled during reproductive development through the repressive activity of FLC/SVP being overcome by the transcriptional activator SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1. Thus we further elucidate the network of genes repressed by FLC/SVP to block flowering and determine mechanisms by which their repressive activity is overcome during the initiation of flowering.