Climate drives plasticity and genetic adaptation in apple trees

Perennial crops can respond to climate change through phenotypic plasticity and genetic adaptation, yet how these processes interact and are shaped by domestication and population history remains poorly understood in long-lived species. We combined controlled reciprocal climate experiments with phenotypic, transcriptomic, and genomic analyses in cultivated apple (Malus domestica) and its wild relatives. We grew 1,248 seedlings from four wild apple populations under four simulated European climates alongside M. domestica. Early survival and twelve phenotypic traits were quantified, and gene expression was analyzed in 96 individuals using RNA sequencing, together with DNA sequencing from a previous study. Early seedling survival revealed strong population-specific responses to climate. Phenotypic and transcriptional responses to climate were widespread and largely conserved, with a core set of climate-responsive genes enriched for stress- and nutrient-related functions and evolving under strong purifying selection. Population-specific regulatory responses were limited and largely reflected genetic divergence. Domestication was associated with altered expression patterns and reduced deleterious mutation load. These results show that climate responses in apple seedlings reflect a balance between conserved plastic responses and population-specific genetic constraints shaped by evolutionary history and domestication, with implications for predicting climate resilience in perennial crops.