Heat-induced secondary dormancy contributes to local adaptation in Arabidopsis thaliana

Seeds should not germinate under conditions in which seedling development cannot be sustained. Dormancy, which allows seeds to remain inactive in an environment that would otherwise enable germination, helps optimize the timing of germination. The induction of a secondary type of dormancy after seed dispersal allows seeds to fine-tune germination to prevailing environmental conditions. In this study, we explore the relevance of secondary dormancy in response to heat for adaptation to local environments by characterizing natural variation in heat-induced secondary dormancy within a collection of 361 Arabidopsis thaliana accessions originating from across the European geographical range. We found that the acquisition of secondary dormancy varies with levels of primary dormancy and after-ripening. We found that both primary dormancy and heat-induced secondary dormancy formed an adaptive cline along temperature and precipitation gradients. The slope of this cline was steeper for secondary dormancy than for primary dormancy, indicating that secondary dormancy contributes most to local adaptation. Using species distribution models, we find that genotypes with high secondary dormancy are predicted to be more resilient to future climate change. We further identified several regions in the genome that specifically controlled the levels of secondary dormancy, one of which contained a novel candidate gene for secondary dormancy variation. Our findings show that secondary dormancy is a complex adaptive mechanism and a predominant contributor to the dormancy trait syndrome that favors plant survival in habitats exposed to harsh summers.