Natural Variation in Arabidopsis lyrata Vernalization Requirement Conferred by a FRIGIDA Indel Polymorphism

Abstract

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.

Population structure and historical biogeography of European Arabidopsis lyrata

“…However, the divergence time between the central-northern European populations based on nuclear loci appears to substantially predate the LGM (Ross-Ibarra et al, 2008), suggesting the population subdivision is not very recent. A similar asymmetric allelic distribution pattern was also observed from a survey of diversity at the FRIGDA locus (Kuittinen et al, 2007), which showed the central European populations lack the common northern allele. We speculate the northern populations are derived from a source population independent of the central Europe stock (for example northern Europe or Siberia), or represent a fraction of diversity that is no longer extant in the central European range.…”

“…So far a large proportion of adaptation and diversity studies have used 'standard' sampling locations (for example Esja Mountain, Karhumaki, Mjällom, Plech, Reykjavik). A growing number of studies have used collections from both central and northern European territories (Kuittinen et al, 2007;Leinonen et al, 2009), which we show here to be genetically structured. Future adaptation studies should ideally continue this wider sampling approach when testing for local adaptation.…”

“…Consequently genomic studies should consider population history when testing hypothesis, for example, selective sweeps and genome scans. While recombination appears effective in restoring linkage equilibrium in A. lyrata, as indicated by the rapid linkage disequilibrium decay around gene sequences (Wright et al, 2006;Kuittinen et al, 2007;Ross-Ibarra et al, 2008), polymorphisms may still remain locally structured over nearby nucleotide sites.…”

“…Arabidopsis lyrata is an outcrossing perennial that shows extensive phenotypic variation and grows in natural habitats that span a large ecological range (Jonsell et al, 1995;Kivimäki et al, 2007;Leinonen et al, 2009;Sandring and Å gren, 2009). Already several local adaptation/ selection studies have been published (Kivimäki et al, 2007;Kuittinen et al, 2007;Leinonen et al, 2009), with special emphasis on studying self-incompatibility evolution Schierup et al, 2006;Mable and Adam, 2007). More of such studies are likely to emerge with the recent availability of the genomic sequence, which makes a comprehensive study of A. lyrata's phylogeographic structure timely.…”

miR824-Regulated AGAMOUS-LIKE16 Contributes to Flowering Time Repression in Arabidopsis

“…The Col-FRI background is not a native genotype but a combination of natural Arabidopsis alleles. The close relatives of Arabidopsis harbor a functional FRI copy (Kuittinen et al, 2008), and worldwide, some 60% of Arabidopsis genotypes feature a functional FRI allele (Johanson et al, 2000;Stinchcombe et al, 2004;Shindo et al, 2005;Korves et al, 2007;Brachi et al, 2010). Since the linkage disequilibrium between loci is rare in Arabidopsis (Kim et al, 2007), many natural genotypes may exhibit a combination of alleles similar to Col-FRI.…”