Volatile exposure mitigates tomato russet mite-induced biotic stress and is associated with preserved glandular trichomes and terpenoid defenses

The tomato russet mite, Aculops lycopersici , severely damages tomato plants by disrupting epidermal tissues, degrading type VI glandular trichomes, and suppressing defense-related responses. We tested whether the green leaf volatile (Z)-3-hexenyl propanoate [(Z)-3-HP] could enhance tomato resistance to mite-induced biotic stress. In a controlled laboratory assay, tomato cv. Moneymaker plants were exposed to (Z)-3-HP via polymeric dispensers for 48 h before A. lycopersici infestation, with exposure maintained thereafter. We also quantified JA- and SA-related defense gene expression by RT-qPCR and measured terpenoid and flavonoid contents. We further evaluated the approach in commercial greenhouse and open-field crops continuously exposed to (Z)-3-HP. Exposure reduced cumulative mite density by 55.8% in the laboratory, while cumulative mite pressure declined by 77.3% and 74.7% in greenhouse and open-field trials, respectively. Volatile exposure increased healthy type VI glandular trichomes and reduced amber-colored trichomes, indicating improved preservation of trichome condition during infestation. At the molecular level, (Z)-3-HP exposure was associated with selective defense-related responses rather than generalized JA- or SA-related activation. ICS showed the clearest volatile-associated response during infestation, while PIN2 showed evidence of late recovery in (Z)-3-HP-exposed plants. Terpenoid levels were maintained in exposed, infested plants, whereas flavonoids remained unchanged. Overall, (Z)-3-HP mitigated mite-induced biotic stress and was associated with preserved glandular trichome integrity, maintained terpenoid-associated defenses, and selective defense responses. Its consistent suppression of mite populations under commercial conditions supports its potential as a plant defense elicitor for sustainable tomato protection.