A noncoding SNP in ELF3 alters ELF3β expression and confers adaptation of Arabidopsis to a continental climate

Plant circadian clocks govern the timing of physiological and developmental processes that determine growth, reproduction, and seasonal phenology. As a result, natural variation in clock genes can directly influence local adaptation, but the components of the clock that have already been targeted by selection are unclear. We found that naturally occurring variation in the core clock gene EARLY FLOWERING 3 (ELF3) determines circadian period length and has been selected for in hot, seasonal climates. We measured the circadian rhythms of 287 global Arabidopsis (Arabidopsis thaliana) accessions using a seedling transformation protocol with a circadian luciferase reporter. Genome-wide association studies identified multiple single nucleotide polymorphisms (SNPs) in ELF3, and their identities were used to define 3 haplogroups associated with seasonal variability in temperature. We found strong evidence of a selective sweep in haplogroups from continental climates, which is estimated to coincide with the most recent de-glaciation period in Europe. One of the SNPs is located within intron 2 of ELF3 in the region upstream of an alternative transcription start site affecting the expression of a shorter ELF3β transcript. Our results indicate the important role of subtle variation in a core circadian clock gene in adaptation to a changing climate.