<p>Volatile organic compounds (VOCs) from plant growth-promoting rhizobacteria (PGPR) regulate crop growth, but their dose-dependent effects in woody perennials are poorly understood. This study defined the dose–response relationships of VOCs from three PGPR strains (<i>Pantoea ananatis</i> D1-28, <i>Burkholderia</i> sp. D4-24, <i>Burkholderia territorii</i> D4-36) in apple. The optimal concentrations were 10⁴, 10⁶, and 10⁵&#xa0;CFU·mL⁻¹, with D1-28 exerting the strongest effect, increasing plant height, biomass, and root volume by up to 75%, 200%, and 276%, respectively. Investigating the underlying mechanisms, we found that the shared VOC monomers dimethyl disulfide (D) and benzothiazole (B) acted in a narrow concentration window (10^–1 and 10^–3&#xa0;mmol·L⁻¹), whereas 2-nonanone (N) was broadly effective (1–10^–3&#xa0;mmol·L⁻¹). Benzothiazole at 10^–3&#xa0;mmol·L⁻¹ was exceptionally effective, promoting increases of 85% in plant height and 296% in root volume. Further analysis showed that these VOCs upregulated auxin and nitrogen pathway genes and drove functional compartmentalization of the rhizosphere microbiome. Finally, whole-genome sequencing of D1-28 pinpointed the genetic network for VOC biosynthesis. Our findings pioneer a “Dose-Gene-Microbiome” model, which conceptualizes that PGPR-VOCs promote plant growth through three interconnected mechanisms: a strict dependence on optimal concentrations (Dose), direct regulation of plant gene expression (Gene), and beneficial remodeling of the root-associated microbial community (Microbiome). This model offers strategic targets for engineering advanced bioinoculants.</p> Graphical abstract <p></p>