Unraveling the effects of mushroom-tomato rotation and oxygenated subsurface drip irrigation on plant growth and development by phenotypic characterization and microbiome profiling in tomato

• Both MTR and OSDI enhance tomato plant growth, yield, quality, and soil health . • Combined application of MTR and OSDI exhibit synergistic benefits. • MTR and OSDI reshape fungal community assembly. • Plectosphaerella and Mortierella are key beneficial genera enriched by MTR and OSDI. Mushroom-vegetable crop rotation enables the sustainable reuse of spent mushroom substrate and improves soil health. Oxygenated subsurface drip irrigation (OSDI), an innovative water-saving irrigation technology, alleviates oxygen deficiency in crop root zones and improves crop yield and quality. However, the effects and underlying mechanisms of combined application of these two technologies on plant growth and development remains unclear. To address this, we established a mushroom ( Pleuroyus eryngii )-tomato ( Solanum lycopersicum L.) rotation system, and conducted phenotypic and microbiome analyses of tomato plants grown under four soil conditions: conventional soil, spent mushroom substrate-amended soil, oxygen-enriched conventional soil, and oxygen-enriched spent mushroom substrate-amended soil. We found that both mushroom-tomato rotation (MTR) and OSDI individually enhance tomato plant growth, root activity, fruit size, yield, quality, and soil properties, with their combination exhibiting synergistic benefits. Rhizosphere microbiome profiling reveals that both MTR and OSDI affect fungal community assembly, notably promoting beneficial fungi growth and suppressing pathogenic fungi proliferation. Furthermore, correlation analysis indicates that Plectosphaerella and Mortierella may function as positive regulators in the improvement of soil properties and tomato agronomic traits stimulated by MTR and OSDI, whereas Fusarium, Verticillium , Penicilium, and Humicola likely exhibit inhibitory roles. Taken together, our study suggests that MTR and OSDI promote tomato growth and development partly through reshaping the rhizosphere fungal community, with combined application yielding more substantial effects, thereby offering a sustainable agricultural strategy for vegetable farming.