Integration of Spatiotemporal Multi-Omics in Peach Fruit Unravels a Metabolic Niche and the Genetic Basis of Trichome-Mediated Stress Adaptation.

Fruit development involves precise spatiotemporal coordination of gene expression and metabolism across diverse tissues. However, a systems-level understanding of this coordination, particularly during early organogenesis, remains limited. Here, we integrate spatial transcriptomics (ST) and Mass Spectrometry Imaging (MSI) to construct a multidimensional atlas of early fruit development in peach (Prunus persica) and its glabrous variant, nectarine. Our analysis revealed extensive metabolic heterogeneity, with distinct metabolites compartmentalized in specific tissues. Comparative analysis indicated that nectarines undergo metabolic adjustments, characterized by enhanced α-linolenic acid metabolism and altered regulation of the pyruvate/TCA cycle. Spatially resolved transcriptomics identified nine tissue-specific clusters, including a trichome-specific cluster exclusive to peach. We identified key marker genes underpinning functional specialization, such as Prupe.2G005300 (LOX2) in mesocarp jasmonate biosynthesis and Prupe.8G047900 (LAC15) in xylem integrity. Regulatory network analysis implicated nine stress-responsive transcription factors in species divergence. Furthermore, we identified and functionally characterized Prupe.7G196500 as a novel candidate regulator that integrates jasmonate signaling to concurrently promote trichome development and is associated with drought tolerance in a heterologous system. This study provides the first spatially resolved multi-omics resource for a Rosaceae fruit, offering fundamental insights into spatial metabolic compartmentalization, species-specific adaptation, and the genetic integration of developmental and environmental responses.