Rooting for sustainability: Pantoea ananatis D1-28 volatiles boost tomato growth and rhizosphere microbial diversity

Tomato (Solanum lycopersicum), a vital global crop rich in bioactive compounds, faces sustainability issues due to agrochemical overuse, necessitating eco-friendly biofertilizers like plant growth-promoting rhizobacteria (PGPR) for sustainable agriculture. This study aimed to identify superior PGPR strains with growth-enhancing volatile organic compounds (VOCs), characterize their VOC profiles, determine optimal VOC doses for growth promotion, and investigate their effects on root architecture, rhizosphere microbiome, and plant transcriptomics to elucidate mechanisms. Thirteen PGPR strains were screened for VOC-mediated tomato growth promotion. Key strains' VOCs were profiled using GC–MS. Dose-response assays tested core VOCs on growth and root architecture. Rhizosphere microbiome functional compartmentalization was analyzed, and transcriptomic profiling (KEGG pathway enrichment) of VOC-treated plants was performed. Three superior isolates (Pantoea ananatis D1-28, Burkholderia sp. D4-24, Burkholderia territorii D4-36) were identified, with D1-28 notably enhancing lateral roots and shoot biomass. GC–MS revealed strain-specific VOC profiles (31–37 compounds) sharing three core components: dimethyl disulfide (D), 2-nonanone (N), benzothiazole (B). Optimal doses profoundly remodeled root architecture and maximized growth: D (10⁻3 mmol/L), N (1 mmol/L), B (10⁻2 mmol/L). VOCs drove rhizosphere functional compartmentalization, enriching specific taxa. Transcriptomics identified 132 differentially enriched KEGG pathways (130 conserved), primarily linked to auxin biosynthesis, sulfur/nitrogen metabolism, energy metabolism, and carbohydrate metabolism, indicating analogous mechanisms. This study elucidates for the first time how P. ananatis VOCs coordinate plant hormone signaling, metabolic networks, and rhizosphere microecology to synergistically enhance tomato growth, providing a theoretical foundation for VOC-based green agricultural technologies.