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

Circadian clocks are biological timekeepers that influence most aspects of plant biology and allow organisms to predict and adapt to daily and seasonal environmental cycles. In particular, the important role of circadian clocks in phenology has led to numerous examples of both functional variation in circadian clock genes within natural and domesticated plant populations. To assess variation of circadian rhythms in natural Arabidopsis populations, we have phenotyped 287 accessions using a seedling transformation protocol with a circadian luciferase reporter. A genome wide association study of circadian period identified multiple single nucleotide polymorphisms (SNPs) in the core clock gene EARLY FLOWERING 3 (ELF3). We identified three ELF3 haplogroups that are associated with seasonal variability in temperature found in continental climates and found strong evidence of a selective sweep coinciding 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 expression of a shorter ELF3β transcript. Our results indicate the important role of subtle variation in a core circadian clock gene in adaptation to changing climate.