Dissecting the genetic basis of climatic adaptation in wild relatives (Malus baccata) for climate-resilient apple breeding.

Climate change poses an increasing threat to global biodiversity and food security. As a wild relative of cultivated apples, Malus baccata exhibits broad environmental adaptability and robust stress tolerance. However, its effective utilization in breeding is constrained by the absence of a complete reference genome and insufficient population-level genomic characterization. In this study, we assembled a haplotype-resolved, telomere-to-telomere genome for M. baccata, providing unprecedented resolution for a wild apple reference genome. Population genomic analyses revealed four distinct genetic clusters. Among these, the Hebei Group 2 harbors the highest genetic diversity and heterozygosity, alongside the lowest runs of homozygosity, suggesting a complex history of genetic admixture in this population. By integrating population genomics with genotype-environment association analyses, we identified a series of climate-associated single-nucleotide polymorphisms and structural variants. A substantial proportion of these adaptive variants is localized within the coding and regulatory regions of candidate genes, providing a genomic basis for their roles in environmental adaptation. Notably, DREB1A/D and NAC6 are associated with temperature seasonality and annual precipitation, respectively. Furthermore, future climate projections indicate that the Northeastern (NE) clusters face the highest risk of maladaptation, especially under high-emission scenarios. Collectively, these findings provide critical insights into the genetic basis of climatic adaptation in wild apples, establishing a solid foundation for the conservation of crop wild relatives and the breeding of climate-resilient cultivars.