Cell type-specific transcriptional plasticity in a multi-organ atlas reveals organ-independent companion cell regulatory programs in grapevine

Plants comprise both cell types shared across organs and those restricted to specific tissues. How the transcriptional programs defining cell identity are maintained or remodeled across organ contexts remains poorly understood, particularly in long-lived perennials, for which cell type-resolved transcriptomic data remain scarce. We generated a multi-organ single-nucleus transcriptomic atlas of the dwarf grapevine cultivar Pixie, comprising over 220,000 nuclei from nine organs, including roots, green stems, pre-anthesis flowers, dormant buds, young and old leaves, and berries at three developmental stages, each sampled in duplicates. We annotated 46 distinct cell types, reconstructed developmental trajectories within selected cell types, and inferred gene regulatory networks at cell type resolution. Broadly distributed cell types, including epidermis, xylem parenchyma, and phloem parenchyma, exhibited pronounced organ-dependent transcriptional divergence, with organ identity accounting for 65% of regulon activity variance across the atlas. In contrast, companion cells maintained organ-independent regulatory programs, representing the stable end of a continuum of transcriptional plasticity that spans shared cell types. We identified cell-type–specific transcription factor expression and inferred gene regulatory networks using motif-based regulon analysis, revealing candidate regulators of cell identity and tissue specialization. Together, this atlas provides a reference framework for cell type-resolved functional genomics in a perennial woody crop.