Linkage and Association Mapping of Arabidopsis thaliana Flowering Time in Nature

Abstract

Flowering time is a key life-history trait in the plant life cycle. Most studies to unravel the genetics of flowering time in Arabidopsis thaliana have been performed under greenhouse conditions. Here, we describe a study about the genetics of flowering time that differs from previous studies in two important ways: first, we measure flowering time in a more complex and ecologically realistic environment; and, second, we combine the advantages of genome-wide association (GWA) and traditional linkage (QTL) mapping. Our experiments involved phenotyping nearly 20,000 plants over 2 winters under field conditions, including 184 worldwide natural accessions genotyped for 216,509 SNPs and 4,366 RILs derived from 13 independent crosses chosen to maximize genetic and phenotypic diversity. Based on a photothermal time model, the flowering time variation scored in our field experiment was poorly correlated with the flowering time variation previously obtained under greenhouse conditions, reinforcing previous demonstrations of the importance of genotype by environment interactions in A. thaliana and the need to study adaptive variation under natural conditions. The use of 4,366 RILs provides great power for dissecting the genetic architecture of flowering time in A. thaliana under our specific field conditions. We describe more than 60 additive QTLs, all with relatively small to medium effects and organized in 5 major clusters. We show that QTL mapping increases our power to distinguish true from false associations in GWA mapping. QTL mapping also permits the identification of false negatives, that is, causative SNPs that are lost when applying GWA methods that control for population structure. Major genes underpinning flowering time in the greenhouse were not associated with flowering time in this study. Instead, we found a prevalence of genes involved in the regulation of the plant circadian clock. Furthermore, we identified new genomic regions lacking obvious candidate genes.

QTL detection power of multi-parental RIL populations in Arabidopsis thaliana

“…This finding can be explained by the fact that association between haplomarkers, which differ only in state between subpopulations, and the phenotype cannot be as simply detected when population structure is corrected for during the QTL analysis (Yu et al, 2006;Sneller et al, 2009;Brachi et al, 2010). The analyses considering population structure calculated from haplomarker information were more effective in reducing the risk of false-positive QTL than the analyses considering population structure calculated from the pedigree information.…”

“…A problem of association-mapping populations, however, is that some individuals might be more related to each other than individuals are related on average, and this leads to false-positive associations between the pheno-and genotypes (Breseghello and Sorrells, 2006;Sneller et al, 2009). This problem cannot be completely prevented even by considering the population structure in the statistical analysis (Brachi et al, 2010). Furthermore, the loci that explain the difference between subpopulations cannot be detected with such approaches.…”

The relationship between parental genetic or phenotypic divergence and progeny variation in the maize nested association mapping population

“…Although GD estimates based on molecular marker estimates have been effective at grouping related germplasm (Melchinger et al, 1998), the relationship between GD in parents and genotypic variance components (GVCs) in their progenies has been reported as weak or non-significant across many studies (Helms et al, 1997;ManjarrezSandoval et al, 1997;Burkhamer et al, 1998;Melchinger et al, 1998;Bohn et al, 1999;Gumber et al, 1999;Brachi et al, 2010).…”

Local Selection Across a Latitudinal Gradient Shapes Nucleotide Diversity in Balsam Poplar, Populus balsamifera L

“…Surveys of natural allelic variation among A. thaliana accessions sampled from diverse latitudes have identified two flowering-time genes, FRIGIDA (FRI) and FLOWERING LOCUS C (FLC), that show evidence of local adaptation with latitude (Caicedo et al 2004;Stinchcombe et al 2004;Le Corre 2005). In other species, local selection has targeted members of the phytochrome gene family (PHYE) in Cardamine japonica (Ikeda et al 2009) and PHYB2 in Populus tremula (Ingvarsson et al 2006;Ingvarsson et al 2008) and components of the circadian clock (Böhlenius et al 2006;Slotte et al 2007;Brachi et al 2010;Ma et al 2010). These studies suggest that homologs of the A. thaliana flowering-time gene network underlie ecologically important adaptive variation in phenological responses in other species, making them promising candidates for studying the molecular basis of local adaptation, as well as testing the repeatability of evolution across taxa in genes that influence quantitative traits.…”