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Vernalization, the requirement of a long exposure to low temperatures to accelerate flowering, is an essential adaptation of plants to cold winters. The vernalization gene VRN-1 plays an important role in this process in diploid (Triticum monococcum) and polyploid wheat (Triticum aestivum). We have recently shown that the diploid wheat VRN-A(m)1 gene was similar to the Arabidopsis (Arabidopsis thaliana L. Heynh.) APETALA1 meristem identity gene. We also showed that dominant Vrn-A(m)1 alleles were the result of loss-of-function mutations in regulatory regions recognized by a VRN-1 repressor, likely VRN-2. This model predicts that only the dominant Vrn-1 allele will be transcribed in lines carrying both recessive and dominant alleles. Here, we confirm this prediction in young isogenic lines of hexaploid wheat carrying different dominant Vrn-A1, Vrn-B1, and Vrn-D1 alleles, and also in heterozygous VRN-1 diploid wheat plants. However, a few weeks later, transcripts from the recessive alleles were also detected in both the polyploid and heterozygous diploid spring plants. Transcription of the recessive alleles was preceded by a reduction of the transcript levels of VRN-2. These results suggest that the dominant Vrn-1 allele or a gene regulated by VRN-1 down-regulates the VRN-2 repressor facilitating the transcription of the recessive alleles in unvernalized plants. We also show here that the level of VRN-1 transcripts in early developmental stages is critical for flowering initiation. A reduction of VRN-1 transcript levels by RNA interference delayed apex transition to the reproductive stage, increased the number of leaves, and delayed heading time by 2 to 3 weeks. We hypothesize that the coordinated transcription of dominant and recessive alleles may contribute to an earlier attainment of the VRN-1 transcript level threshold required to trigger flowering initiation in polyploid wheat.