The molecular basis of vernalization: The central role of FLOWERING LOCUS C (FLC)

Abstract

R ecently, we reported on a gene, FLOWERING LOCUS F (FLF), from Arabidopsis whose activity, as determined by steady-state mRNA levels, is correlated quantitatively with the period taken to initiate flowering (1). The FLF gene encodes a putative transcription factor of the MADS-box class, which, we concluded, acts as a repressor of floral induction. Genetic analyses of Arabidopsis ecotypes previously identified FLOW-ERING LOCUS C (FLC) as a semidominant repressor of floral induction (2-4). Because FLF has similar properties to FLC and maps to the same chromosomal region, the possibility arose that FLF and FLC are one and the same gene; this hypothesis has been confirmed by Michaels and Amasino (5). We suggest that the gene be referred to as FLC and the mutants flf-1 to flf-9 now be referred to as flc-11 to flc-19.In many plant species, flowering is promoted by a period of exposure to low temperature through a process known as vernalization. A number of the late-flowering mutants and ecotypes of Arabidopsis have a vernalization response. We found that the vernalization-responsive late-flowering mutants had a higher level of FLC transcript than was present in the wild types and, importantly, that the non-vernalization-responsive lateflowering mutants did not have increased FLC transcript levels. The vernalization-responsive ecotype C24, which is somewhat late-flowering, also has a high level of FLC transcript that is reduced by the low-temperature treatment (1). These observations suggested to us that FLC must be directly involved in the vernalization response.We have shown that reduction in the level of genomic methylation largely substitutes for the low-temperature treatment in promoting flowering (6-8), implicating a reduction in DNA methylation level as a component in the vernalization response. Early-flowering METHYLTRANSFERASE1 antisense plants, with a decreased level of genomic methylation, have a reduced level of FLC activity as compared with the nontransformed control (1). The correlation between FLC transcription and methylation levels implies that FLC is regulated by methylation status, but we are not able to say whether this is through an alteration of the methylation status of the FLC gene itself, or whether it involves other genes that regulate FLC expression.In this paper, we demonstrate that the FLC gene is involved directly in controlling the response to vernalization and more generally in the timing of the transition to the reproductive phase of development. We find that a reduction in FLC activity is a key component of the vernalization response in six late-flowering vernalization-responsive mutants and in the C24 and Pitztal ecotypes. The late-flowering mutants are mutated in genes that regulate the activity of the FLC gene. We further show that the quantitative responses in the promotion of flowering to various periods of exposure to low temperature are paralleled by the levels of FLC transcript, and that the changes observed at the transcriptional level are reflected in the level of the FLC pr...

Phylogenomic Synteny Network Analysis of MADS-Box Transcription Factor Genes Reveals Lineage-Specific Transpositions, Ancient Tandem Duplications, and Deep Positional Conservation

“…In Arabidopsis, the FLC gene and its closely related MAF genes are floral repressors and major regulators of flowering time (Michaels and Amasino, 1999;Sheldon et al, 2000). We found a cluster comprising 21 syntelogs of FLC and the MAF genes across the six examined Brassicaceae species and one Cleomaceae species (Tarenaya) (Figure 3, Cluster 23).…”

Reciprocal control of flowering time by OsSOC1 in transgenic Arabidopsis and by FLC in transgenic rice

“…In Brassica napus (Tadege et al ., 2001), the level of FLC activity correlates with the flowering times of different cultivars as it does in Arabidopsis ecotypes (Michaels and Amasino, 1999;Sheldon et al ., 1999Sheldon et al ., , 2000b, but there have been no references to FLC-like sequences in species outside the Brassicaceae. In monocots, including cereals, our understanding of the molecular basis of floral initiation is limited.…”

Analysis of the ArabidopsisMADS AFFECTING FLOWERINGGene Family:MAF2Prevents Vernalization by Short Periods of Cold [W]

“…During vernalization, FLC transcript and protein levels decrease, and the plants become competent to flower Amasino, 1999, 2001;Sheldon et al, 1999Sheldon et al, , 2000Johanson et al, 2000;Rouse et al, 2002). Additionally, overexpression of FLC from a 35S promoter of Cauliflower mosaic virus in the Landsberg accession (which lacks an active FRI allele) is sufficient to severely delay or prevent flowering and renders the plants insensitive to vernalization (Michaels and Amasino, 1999;Sheldon et al, 1999).…”

“…Therefore, vernalization can promote flowering by other mechanisms as well as via the repression of FLC. In addition, vernalization is a quantitative response to prolonged periods of cold (Sheldon et al, 2000); therefore, a mechanism must exist to ensure that vernalization does not occur in response to short periods of cold that last for only a few days.…”