Dual legacy of plant water-deficit-tolerance and watering history shapes rhizosphere microbial transplant outcomes in tomato post-drought recovery

Background Climate change is intensifying drought events, negatively affecting crop yields and quality. Enhancing plant recovery following drought is therefore critical for agricultural resilience. Within the holobiont framework, the plant microbiome plays a key role in modulating plant responses to environmental stress. Here, we evaluated the contribution of rhizosphere microbial transplants derived from Solanum lycopersicum cultivars differing in water-deficit-tolerance and prior exposure or not to water deficit to post-drought recovery in susceptible tomato plants. Results Physiological measurements, including net photosynthetic rate, relative water content, and water potential, showed that microbial community transplants from water-deficit-tolerant cultivars previously exposed to water deficit significantly enhanced post-drought recovery in susceptible plants, suggesting a dual legacy effect of host phenotype and irrigation history. High-throughput metabarcoding revealed marked temporal shifts in rhizosphere microbial communities between the initial (Ti) and post-recovery (Tf) stages. Bacterial alpha diversity increased significantly at Tf only for the tolerant inoculant under deficit irrigation, whereas fungal diversity showed more stable response across conditions. Beta-diversity analyses revealed clear separation between Ti and Tf communities for both bacteria and fungi. Community structure changes were highly pronounced in the inoculation treatments that produced the most contrasting post-drought recovery phenotypes (SFI: susceptible cultivar under full irrigation and TDI: tolerant cultivar under deficit irrigation), which formed distinct clusters in hierarchical analyses. Differential abundance analysis identified bacterial taxa enriched at Tf in TDI, while fungal communities displayed stage-specific markers. Functional annotation using FAPROTAX and FUNGuild revealed enrichment of nitrate reduction and anoxygenic photoautotrophy among bacterial functions, and saprotrophic guilds among fungal communities at Tf in TDI, suggesting increased nutrient cycling activity associated with post-drought recovery. Co-occurrence network analysis revealed contrasting interaction patterns, with higher connectivity in SFI and a greater contribution of fungal taxa and positive fungi-fungi interactions in TDI. Conclusions These results indicate that the legacy of rhizosphere microbiomes shaped by host water-deficit-tolerance and irrigation history is associated with enhanced post-drought recovery, involving the enrichment of specific microbial taxa and functional guilds. The concept of dual legacy provides a useful framework for understanding microbiome-mediated plant resilience.