Relating molecular variation to phenotypic diversity is a central goal in evolutionary biology. In Arabidopsis thaliana, FLOWERING LOCUS C (FLC) is a major determinant of variation in vernalization—the acceleration of flowering by prolonged cold. Here, through analysis of 1307 A. thaliana accessions, we identify five predominant FLC haplotypes defined by noncoding sequence variation. Genetic and transgenic experiments show that they are functionally distinct, varying in FLC expression level and rate of epigenetic silencing. Allelic heterogeneity at this single locus accounts for a large proportion of natural variation in vernalization that contributes to adaptation of A. thaliana.

Is Winter Past?: Some plants are adapted to wait through the winter before their genetic programs for flowering are initiated. But the duration of winter varies with location, and thus, to avoid flowering too late into the summer or exposing blossoms to frost, the adaptation needs to hold the flowers off for just the right amount of time. Working with Arabidopsis thaliana , Coustham et al. (p. 584 , published online 12 July) identified a quantitative mechanism that “counts” off the duration of winter. FLC, a repressor of flowering, carries sequence polymorphisms that direct epigenetic events. Plants with fewer of these polymorphisms are adapted to short winters, and plants with all four polymorphisms are adapted to long winters.

The extent to which natural polymorphisms in noncoding sequences have functional consequences is still unknown. A large proportion of the natural variation in flowering inArabidopsis thalianaaccessions is due to noncodingcispolymorphisms that define distinct haplotypes ofFLOWERING LOCUS C(FLC). Here, we show that a single natural intronic polymorphism in one haplotype affectsFLCexpression and thus flowering by specifically changing splicing of theFLCantisense transcriptCOOLAIR. Altered antisense splicing increasesFLCexpression via a cotranscriptional mechanism involving capping of theFLCnascent transcript. Single noncoding polymorphisms can therefore be a major contributor to phenotypic evolution through modulation of noncoding transcripts.

We have explored the genetic basis of variation in vernalization requirement and response in Arabidopsis accessions, selected on the basis of their phenotypic distinctiveness. Phenotyping of F2 populations in different environments, plus fine mapping, indicated possible causative genes. Our data support the identification of FRI and FLC as candidates for the major-effect QTL underlying variation in vernalization response, and identify a weak FLC allele, caused by a Mutator-like transposon, contributing to flowering time variation in two N. American accessions. They also reveal a number of additional QTL that contribute to flowering time variation after saturating vernalization. One of these was the result of expression variation at the FT locus. Overall, our data suggest that distinct phenotypic variation in the vernalization and flowering response of Arabidopsis accessions is accounted for by variation that has arisen independently at relatively few major-effect loci.