Multi-Omics Reveals Domestication-Associated Shifts in Phosphorus Adaptation Strategies in Tomato

Phosphorus (P) limitation is a major selective pressure in plant evolution and a persistent constraint on modern crop production. However, how domestication has reshaped P adaptation strategies remains poorly understood. Here, we compared wild (Solanum pimpinellifolium) and cultivated (Solanum lycopersicum) tomatoes under contrasting P conditions using integrated physiological, ionomic, and transcriptomic analyses. Our findings reveal distinct P strategies between the examined genotypes. Cultivated tomatoes achieved higher biomass under sufficient P supply but were highly sensitive to P deficiency, responding through acquisition-driven phenotypic plasticity characterized by extensive root remodeling and enhanced external P mobilization. In contrast, wild accessions maintained growth and higher P use efficiency under low P by relying on an optimized internal P management strategy, including efficient P uptake, preferential allocation to photosynthetically active tissues, and effective remobilization from older leaves. Consistently, ionomic profiling revealed that wild tomatoes preserved coordinated macro- and micronutrient homeostasis under P stress. Tissue-specific transcriptomic analyses further uncovered pronounced divergence in P-responsive regulation, with cultivated tomatoes showing predominantly root-centered responses, whereas wild accessions exhibited strong activation in old source leaves. This tissue-specific specialization was accompanied by a putative regulatory divergence, with HD-ZIP transcription factors enriched in cultivated tomatoes and G2-like and bHLH factors central in wild accessions. Together, our results indicate that modern cultivars exhibit a stronger reliance on external P acquisition and greater growth sensitivity under sustained P limitation compared to wild accessions, which showed relatively more stable internal P allocation patterns, highlighting wild germplasm as a resource for improving crop P efficiency.