Nucleotide polymorphism affecting FLC expression underpins heading date variation in horticultural brassicas

Variation in flowering time and response to overwintering has been exploited to breed brassica vegetables that can be harvested year-round. Our knowledge of flowering time control now enables the investigation of the molecular basis of this important variation. Here, we show that a major determinant of heading date variation in Brassica oleracea is from variation in vernalization response through allelic variation at FLOWERING LOCUSC.C2 (BoFLC4). We characterize two alleles of BoFLC.C2 that are both functional and confer a requirement for vernalization, but they show distinct expression dynamics in response to cold. Complementation experiments in Arabidopsis thaliana revealed that the allelic variation results from cis polymorphism at BoFLC.C2, which quantitatively influences the degree of cold-induced epigenetic silencing. This results in one allelic variant conferring consistently later heading under both glasshouse and field conditions through reduced environmental sensitivity. Our results suggest that breeding of brassica varieties for commercially valuable variation in heading date has been achieved through the selection of cis polymorphism at FLC, similar to that underpinning natural variation in A.thaliana. This understanding will allow for the selection of alleles with distinct sensitivities to cold and robust heading dates under variable climatic conditions, and will facilitate the breeding of varieties more resistant to climate change. Significance Statement Being able to harvest different broccoli (Brassica oleracea) varieties throughout the year is a function of allelic differences at the floral repressor BoFLC.C2. Here, we show that epigenetic silencing and reactivation of expression after cold exposure of BoFLC.C2 are critical factors in this variation. Domestication in horticultural brassicas has therefore exploited similar cis polymorphism at FLC to that underpinning natural variation in Arabidopsis thaliana.