Explorations of the polygenic genetic architecture of flowering time in the worldwide Arabidopsis thaliana population

As a locally adapted complex trait, flowering time in Arabidopsis thaliana has attracted much attention in genetics. Most studies have, however, focused on contributions by individual loci rather than the joint contributions by the large number of loci in the genetic architecture of flowering time to local and global adaptation. In an earlier study, we reported 46 loci associated with flowering time variation during growth at 10°C, 16°C or both in the 1,001-genomes collection of Arabidopsis thaliana accessions. Here, we explore how these loci together contribute to differences among genetically defined, and geographically divided, subpopulations across the native range of this species. Our approach was to define flowering time as a trait, and the measurements at 10 and 16 °C as two independent measurements of it. This facilitated explorations of the dynamics in the genetic architecture –which loci contribute and their effects– of flowering time across growth temperatures and their potential roles in local and global adaptation. The overall flowering time differences between populations could be explained by subtle changes in allele-frequencies and gradual changes in phenotype due to globally present alleles. More extreme local adaptations were on several occasions due to contributions by regional alleles with relatively large effects. About 2/3 of the 48 evaluated flowering time loci had similar effects on flowering time at 10°C and 16°C, while the remaining 1/3 had different effects in the two temperatures, suggesting an important contribution of gene by temperature interactions to this trait. There are also indications that co-evolution of functionally connected alleles in local populations has been important for local adaptation. Overall, this study provides deeper insights to the polygenic genetic basis of flowering time variation in Arabidopsis thaliana across a wide range of ecological habitats.Author SummaryMany genes can affect flowering time in Arabidopsis thaliana, but their contribution to natural flowering time variation in the worldwide population is largely unknown. We explored how 48 loci associated with flowering time, measured at 10°C and 16°C, or their difference, for the same wild collected 1,001-genomes Arabidopsis thaliana accessions together contribute to differences among the genetically defined and geographically divided subpopulations from the native species range. The overall flowering time differences among these subpopulations could be explained by the joint small effects of globally present alleles, suggesting an important contribution by polygenic adaptation for this trait. Most alleles with large effects on flowering were present only in some populations, facilitating more extreme local adaptations. Long-range LD was observed between genes in several biological pathways, indicating possible local adaptation via co-evolution of functionally connected polymorphisms. The genetic architecture of flowering time was also found to depend on the growth temperature. Most flowering time loci had similar effects on flowering time measured at 10°C and 16°C, but the effects of about 1/3 of them had effects that varied with temperature. Overall, new insights are provided to how the polygenic architecture of flowering time has facilitated its colonisation of a wide range of ecological habitats.