Loss of FLOWERING LOCUS C Activity Eliminates the Late-Flowering Phenotype of FRIGIDA and Autonomous Pathway Mutations but Not Responsiveness to Vernalization

Abstract

The MADS domain-containing transcription factor FLOWERING LOCUS C ( FLC ) acts as an inhibitor of flowering and is a convergence point for several pathways that regulate flowering time in Arabidopsis. In naturally occurring late-flowering ecotypes, the FRIGIDA ( FRI ) gene acts to increase FLC levels, whereas the autonomous floral promotion pathway and vernalization act to reduce FLC expression. Previous work has shown that the Landsberg erecta allele of FLC , which is not a null allele, is able to partially suppress the late-flowering phenotype of FRIGIDA and mutations in the autonomous pathway. In this study, using a null allele of FLC , we show that the late-flowering phenotype of FRIGIDA and autonomous pathway mutants are eliminated in the absence of FLC activity. In addition, we have found that the downregulation of SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1 by FRI and autonomous pathway mutants also is mediated by FLC . Complete loss of FLC function, however, does not eliminate the effect of vernalization. Thus, FRI and the autonomous pathway may act solely to regulate FLC expression, whereas vernalization is able to promote flowering via FLC -dependent and FLC -independent mechanisms. INTRODUCTIONThe promotion of flowering in response to prolonged exposure to cold temperatures is an adaptation to prevent plants from flowering in the fall, prior to winter, and to enable them to flower in spring. This promotion, known as vernalization, does not initiate flowering directly but renders the meristem competent to respond to other environmental and developmental flowering signals (reviewed in Chouard, 1960;Michaels and Amasino, 2000). Although the physiology of vernalization has been studied extensively in many species, the molecular mechanism of vernalization remains largely unknown. In Arabidopsis, many naturally occurring ecotypes are relatively late flowering unless they are vernalized (Napp-Zinn, 1979;Karlsson et al., 1993), and thus they behave as winter annuals. Summer annual strains, in contrast, do not require vernalization for early flowering. Crosses between winter and summer annual strains have shown that the winter annual habit is caused by the interaction of two dominant genes: FLOWERING LOCUS C ( FLC ) (Koornneef et al., 1994;Lee et al., 1994) and FRIGIDA ( FRI ) (Burn et al., 1993;Lee et al., 1993;Clarke and Dean, 1994). FLC encodes a MADS domain-containing transcription factor that acts as an inhibitor of flowering, and FRI is required for FLC expression (Michaels and Amasino, 1999; Sheldon et al., 1999). Most summer annual ecotypes of Arabidopsis contain nonfunctional alleles of FRI (Johanson et al., 2000) and thus have low levels of FLC expression (Michaels and Amasino, 1999; Sheldon et al., 1999). Vernalization is able to eliminate the late-flowering phenotype caused by FLC and FRI (Lee and Amasino, 1995) and results in a downregulation of FLC levels (Michaels and Amasino, 1999; Sheldon et al., 1999). This suppression of FLC expression by vernalization is stable for the remainder of the plant...

Genetic Architecture of Flowering Time in Maize As Inferred From Quantitative Trait Loci Meta-analysis and Synteny Conservation With the Rice Genome

“…Thanks to the Maize Genome Sequencing Project loci in maize are not associated with QTL for flowering time, suggesting that phytochromes have no contribu- (Chandler and Brendel 2002), an increasing amount of genomic sequences will be available for regions intion in the photoperiodic control of flowering. This is supported by results of Takano et al (2001), which volved in the variation of traits of interest. This will facilitate to a large extent the identification of candidate showed no significant difference for plant height and heading date between wild-type and phyA mutant rice genes for QTL.…”

“…Then these signals are transducted and integrated by the CONSTANS (CO) gene (Suarez-Lopez et al 2001). The autonomous and 1 reduction of the expression of FLOWERING LOCUS C cereals using restriction fragment length polymorphism (RFLP) has shown considerable marker-order conserva-(FLC), which encodes a floral repressor (Michaels and Amasino 2001). Mutations affecting GA synthesis delay tion.…”

Functional Redundancy and New Roles for Genes of the Autonomous Floral-Promotion Pathway

“…We also evaluated the flowering time of the triple mutants. As reported previously, the late-flowering phenotype of fpa, fld, fve, and ld is eliminated in an flc-null background (Michaels and Amasino, 2001;He et al, 2003; Fig. 4F).…”

“…The late-flowering phenotype of AP single mutants is due to elevated levels of FLC expression and is eliminated by loss-of-function mutations in flc (Michaels and Amasino, 2001). To determine whether FLC also plays a role in the pleiotropic phenotypes of AP double mutants, fpa fld flc, fpa ld flc, and fpa fve flc triple mutants were created.…”

Regulation of flowering time by FVE, a retinoblastoma-associated protein

“…Mutations in these genes increase levels of FLC mRNA, resulting in a photoperiod-independent flowering delay. The increased FLC expression and late flowering of plants with mutations of the autonomous pathway can be reverted by vernalization 3,4 , and flc null mutations completely correct the late flowering of plants with mutations of this pathway 8 . These effects indicate that the primary function of the autonomous pathway is the negative regulation of FLC.…”