Glandular prickles in Rosa hybrida accumulate specific sesquiterpenes implicated in defense against aphid pests

Rose, a plant of immense ornamental value and economic importance, is often infested by herbivory and insectivory. To overcome this, rose plants have evolved epidermal appendages, namely prickles, which accumulate distinct secondary metabolites that protect the rose plants against pests. The hard, edgy, and sharp appendages found mainly on stems and leaves are called non-glandular prickles (NGPs). Interestingly, rose plants bear distinct soft and glandular appendages, which are present beneath the flower bud and petioles, referred to as glandular prickle (GPs). The NGPs, being sharp structures and accumulating secondary metabolites, are implicated in protecting against herbivores; the relevance of GPs, however, is unclear. Given their presence beneath flower bud, we speculated that GPs might be involved in defense against insect pests. Investigation of morphology, diversity, and development of GPs in Rosa hybrida cv. ‘Superstar Supreme (SS)’ in open field conditions revealed that GPs are epidermal/cortical outgrowths with a multicellular stalk and a glandular head with a cavity that seems to release exudates. The targeted biochemical assessment revealed an accumulation (and release in exudates) of secondary metabolites, including lignin, flavonoids, and terpenes, that were likely involved in defense against insect pests. In agreement, red-colored aphids were found trapped in the GPs beneath the floral bud, reinforcing the notion that GPs or exudates likely contain insect attractants and insecticidal metabolites. Acetylcholine esterase inhibition assay indicated the insecticidal potential of GPs. Untargeted metabolite analysis revealed accumulation and release of volatile sesquiterpene hydrocarbons, such as β-cis-caryophyllene, γ-muurolene and β-Copaene, that likely deter aphids by either direct insecticidal effect or attracting their predators to feed on them. These findings provided significant insights that GPs in rose accumulate specific secondary metabolites and are involved in defense against aphid pests, protecting the newly grown floral bud.