Natural variation in Arabidopsis lyrata vernalization requirement conferred by a FRIGIDA indel polymorphism

Species share homologous genes to a large extent, but it is not yet known to what degree the same loci have been targets for natural selection in different species. Natural variation in flowering time is determined to a large degree by 2 genes, FLOWERING LOCUS C and FRIGIDA, in Arabidopsis thaliana. Here, we examine whether FRIGIDA has a role in differences in flowering time between and within natural populations of Arabidopsis lyrata, a close outcrossing perennial relative of A. thaliana. We found 2 FRIGIDA sequence variants producing potentially functional proteins but with a length difference of 14 amino acids. These variants conferred a 15-day difference in flowering time in an association experiment in 2 Scandinavian populations. The difference in flowering time between alleles was confirmed with transformation to A. thaliana. Because the north European late-flowering populations harbor both late- and early sequence variants at intermediate frequencies and the late-flowering variant is most frequent in the southern early flowering European population, other genetic factors must be responsible for the flowering time differences between the populations. The length polymorphism occurs at high frequencies also in several North American populations. The occurrence of functional variants at intermediate frequencies in several populations suggests that the variation may be maintained by balancing selection. This is in contrast to A. thaliana, where independent loss-of-function mutations at the FRIGIDA gene are responsible for differences between populations and local adaptation.