Locally adapted Arabidopsis thaliana accessions show transcriptomic plasticity in a multi-timescale analysis of whole-genome gene expression in a natural environment.

Discerning the genes, regulatory networks and environmental cues involved in plant development represents a major goal in the plant sciences. However, genes and regulatory networks have not evolved in controlled environmental conditions but in natural environments. Hence, conducting experiments in natural settings is of paramount importance to dissect the underlying mechanisms of plant development realistically. We undertook common garden experiments in a natural environment in two contrasting years to quantify whole-genome gene expression patterns over diurnal, seasonal and annual timescales across the life-cycle phenology of Arabidopsis thaliana. Natural accessions were locally adapted to their environments by adjusting key life-history traits across an altitudinal gradient in southern Spain. We found that accession, seasonal (across developmental stages) and diurnal (morning and afternoon) comparisons chiefly structured whole-genome gene expression. We detected most of the differentially expressed genes from various biological functions and flowering-related regulatory pathways as shared among all natural accessions. Nevertheless, accessions more similar in early flowering time also exhibited more similar gene expression patterns. We also detected several flowering time genes from all known regulatory pathways across timescales, particularly from the photoperiod and circadian clock pathways. Overall, our results stressed the remarkable plasticity in both life-cycle phenology and whole-genome gene expression patterns in natural A. thaliana accessions, showed that local adaptation in fitness-related life-history traits can also be detected at the whole-genome gene expression level and highlighted the value of natural accessions with respect to laboratory strains for in natura gene expression experiments.