Contributions of γ-Aminobutyric Acid (GABA) Receptors for the Activities of Pectis brevipedunculata Essential Oil against Drosophila suzukii and Pollinator Bees

Abstract

The γ-aminobutyric acid (GABA) receptors play pivotal roles in the transmission of neuronal information in the nervous system of insects, which has led these proteins to be targeted by synthetic and natural products. Here, we assessed the insecticidal potential of the essential oil of Pectis brevipedunculata (Gardner) Sch. Bip., a neotropical Asteraceae plant used in traditional medicine, for controlling Drosophila suzukii (Matsumura) adults by feeding exposure. By using in silico approaches, we disentangle the contribution of GABA receptors and other potential neuronal targets (e.g., acetylcholinesterase, glutathione-S-transferases) in insects that may explain the essential oil differential activities against D. suzukii and two essential pollinator bees (Apis mellifera Linnaeus and Partamona helleri Friese). Neral (26.7%) and geranial (33.9%) were the main essential oil components which killed D. suzukii with an estimated median lethal concentration (LC₅₀) of 2.25 µL/mL. Both pollinator forager bee species, which would likely contact this compound in the field, were more tolerant to the essential oil and did not have their diet consumptions affected by the essential oil. Based on the molecular predictions for the three potential targets and the essential oil main components, a higher affinity of interaction with the GABA receptors of D. suzukii (geranial -6.2 kcal/mol; neral -5.8 kcal/mol) in relation to A. mellifera (geranial -5.2 kcal/mol; neral -4.9 kcal/mol) would contribute to explaining the difference in toxicities observed in the bioassays. Collectively, our findings indicated the involvement of GABA receptors in the potential of P. brevipedunculata essential oil as an alternative tool for controlling D. suzukii.

Keywords: biorational pesticides; molecular docking predictions; non-target organisms; plant-based insecticides.

Figure 1

Pectis brevipedunculata essential oil affecting the survival of Drosophila suzukii. Mortality was assessed after 24 h of exposure by feeding. The LC₅₀ represents the lethal concentration average followed by their upper and lower limits. The bars indicate the standard errors. χ² = Chi-square test; p = Probability value.

Figure 2

Effects of exposure to Pectis brevipedunculata essential oil on the bees of species Apis mellifera and Partamona helleri. The bees were exposed to the essential oil by feeding for 5 h. After this period, the insects received a diet containing only sugar syrup (50% [m/v]). After 24 h, mortality was evaluated for A. mellifera (a) and P. helleri (c). During the entire period, the consumption of diets for A. mellifera (b) and P. helleri (d) was determined by weighing the diets. The control represents the insects that received diets containing dimethylsulfoxide (1.2 µL/mL), polysorbate 20 (0.6 µL/mL), and sugar syrup. LC₅₀ represents the lethal concentration obtained from the concentration-mortality curve for Drosophila suzukii. The vertical bars indicate the standard errors. The horizontal bars indicate the significant difference according to the t-test (p < 0.05).

Figure 3

Citral isomers interacting with GABA receptors from Drosophila suzukii and Apis mellifera. (a) The protein 3D structure of the D. suzukii GABA receptor with the citral isomers. (b) The protein 3D structure of the A. mellifera GABA receptor with the citral isomers. (c) The 2D interaction maps showing the molecular interactions between amino acids from the binding site environments of D. suzukii GABA receptor with the citral isomers. (d) The 2D interaction maps showing the molecular interactions between amino acids from the binding site environments of A. mellifera GABA receptor with the citral isomers.