Integrated transcriptomic and lipidomic analyses reveal coordinated regulation of phosphatidic acid dynamics and membrane lipid remodeling in salt-tolerant tomato

• A rapid, selective, and sustained transcriptional reprogramming characterizes the tolerant response. • Tolerant tomatoes achieve rapid lipidomic homeostasis through targeted remodeling. • Integrated multi-omics uncovers stage-specific transcriptional regulators of lipid metabolism. • Phosphatidic acid (PA) acts as a critical signaling hub, integrated from multiple biosynthetic pathways. Soil salinization represents a significant abiotic stressor impairing crop productivity. During the initial phase of salt stress response, lipids act as pivotal functional molecules engaged in osmoregulation, energy storage, and signal transduction. They contribute to the maintenance of energy stability at the extracellular solution-plasma membrane interface and may depolarize cell surface potential, resulting in the opening of transmembrane calcium channels. Elucidating early plant responses, particularly lipid metabolic processes linked to membrane integrity and signal transduction, is crucial for enhancing salt tolerance in tomato. Here, we compared a salt-tolerant cultivar (LA0716, R) and a salt-sensitive cultivar (Jingfan 309, S) using integrated physiology, transcriptomics (RNA-seq), and untargeted lipidomics (LC-MS/MS). R exhibited a more rapid, coordinated, and efficient systemic response. Transcriptomics revealed early (1 h) and sustained activation of pathways such as glutathione metabolism and phenylpropanoid biosynthesis in R, alongside a more stable global gene expression profile. Lipidomics showed that R rapidly restored lipid homeostasis, with orderly membrane remodeling characterized by conversion of phosphatidylcholine (PC) to lysophosphatidylcholine (LPC) and coordinated responses in phosphatidic acid (PA) signaling. Integrated co-expression network analysis identified key gene clusters active during early and mid-late stress stages, significantly correlated with sphingolipid and glycerolipid levels and regulated temporally by MYB/Dof and ERF transcription factors. This study delineates dynamic gene expression and lipid metabolism changes in tomato roots under salt stress, demonstrating that tolerance is associated with rapid signal transduction and efficient membrane lipid remodeling. These findings provide key targets and a theoretical basis for molecular breeding of salt-tolerant crops.