Metabolic engineering of a 1,8‐cineole synthase enhances aphid repellence and increases trichome density in transgenic tobacco (Nicotiana tabacum L.)

Abstract BACKGROUND The green peach aphid ( Myzus persicae Sulzer) is a harmful agricultural pest that causes severe crop damage by directly feeding or indirectly vectoring viruses. 1,8‐cineole synthase (CINS) is a multiproduct enzyme that synthesizes monoterpenes, with 1,8‐cineole dominating the volatile organic compound profile. However, the relationship between aphid preference and CINS remains elusive. RESULTS Here, we present evidence that SoCINS, a protein from garden sage ( Salvia officinalis ), enhanced aphid repellence and increased trichome density in transgenic tobacco. Our results demonstrated that overexpression of SoCINS ( SoCINS ‐OE) led to the emission of 1,8‐cineole at a level of up to 181.5 ng per g fresh leaf. Subcellular localization assay showed that SoCINS localized to chloroplasts. A Y‐tube olfactometer assay and free‐choice assays revealed that SoCINS ‐OE plants had a repellent effect on aphids, without incurring developmental or fecundity‐related penalties. Intriguingly, the SoCINS ‐OE plants displayed an altered trichome morphology, showing increases in trichome density and in the relative proportion of glandular trichomes, as well as enlarged glandular cells. We also found that SoCINS ‐OE plants had significantly higher jasmonic acid (JA) levels than wild‐type plants. Furthermore, application of 1,8‐cineole elicited increased JA content and trichome density. CONCLUSION Our results demonstrate that SoCINS ‐OE plants have a repellent effect on aphids, and suggest an apparent link between 1,8‐cineole, JA and trichome density. This study presents a viable and sustainable approach for aphid management by engineering the expression of 1,8‐cineole synthase gene in plants, and underscores the potential usefulness of monoterpene synthase for pest control. © 2023 Society of Chemical Industry.