Monoterpenes alter TAR1-driven physiology in Drosophila species

Abstract

Monoterpenes are molecules with insecticide properties whose mechanism of action is however not completely elucidated. Furthermore, they seem to be able to modulate the monoaminergic system and several behavioural aspects in insects. In particular, tyramine (TA) and octopamine (OA) and their associated receptors orchestrate physiological processes such as feeding, locomotion and metabolism. Here we show that monoterpenes not only act as biopesticides in Drosophila species but can cause complex behavioural alterations that require a functional type 1 tyramine receptors (TAR1s). Variations in metabolic traits as well as locomotory activity were evaluated in both Drosophila suzukii and Drosophila melanogaster after treatment with three monoterpenes. A TAR1 defective D. melanogaster strain (TAR1PL00408) was used to better understand the relationships between the receptor and monoterpenes-related behavioural changes. Immunohistochemistry analysis revealed that, in the D. melanogaster brain, TAR1 appeared to be mainly expressed in the pars intercerebralis, lateral horn, olfactory and optic lobes and suboesophageal ganglion lobes.In comparison to the D. melanogaster wild type, the TAR1PL00408 flies showed a phenotype characterized by higher triglyceride levels and food intake as well as lower locomotory activity. The monoterpenes, tested at sublethal concentrations, were able to induce a downregulation of the TAR1 coding gene in both Drosophila species. Furthermore, monoterpenes also altered the behaviour in D. suzukii and D. melanogaster wild types 24 h after a continuous monoterpene exposure. Interestingly, they were ineffective in modifying the physiological performances of TAR1 defective flies. In conclusion, it appears that monoterpenes not only act as biopesticides for Drosophila but they can also interfere with its behaviour and metabolism in a TAR1-dependent fashion.

The Insect Type 1 Tyramine Receptors: From Structure to Behavior

“…RNAi-mediated D. melanogaster TAR1 silencing, targeted to the fat body, indeed triggered a ILP2 reduction in insulin-producing cells, located in the pars intercerebralis, and an increased TG accumulation [77], confirming a significant role for TAR1 in lipid metabolism. Furthermore, the increased TG levels in TAR1 PL00408 flies correlates well with other traits observed, such as enhanced food intake, lower movement propensity, and lower metabolic rate [66]. It has recently been proposed that TAR1 could be involved in processes related to sugar sensibility and food intake regulation.…”

“…Moreover, this mechanism controlling locomotor behavior requires a functional TAR1 in D. melanogaster [76]. However, these observations do not rule out the possibility that TAR1-mediated movement alterations could be controlled by other nervous areas rich in TAR1 transcripts such as the central complex [66]. TAR1 has also been shown to influence the gustatory responses.…”

“…In D. melanogaster, the receptor is mainly expressed in the central nervous system (CNS) [32]. Through Gal4/UAS technology, D. melanogaster TAR1 transcripts were found to be abundant in the pars intercerebralis, in the mushroom bodies, and in the antennal and olfactory lobes [66]. A higher expression of TAR1 in nervous tissues compared to the periphery was also observed in D. suzukii, Chilo suppressalis, R. prolixus, P. xylostella, H. halys, Mamestra brassicae, and Agrotis ipsilon, suggesting a crucial role of the receptor in controlling a broad range of physiological functions and behaviors [36,[44][45][46][47][48]50].…”

“…TAR1 has also been shown to influence the gustatory responses. The D. melanogaster TAR1 PL00408 defective line exhibited higher body fat accumulation, starvation resistance, and food intake in comparison to wildtype flies [66,77], thus suggesting that nutritional constraints work through a functional TA-dependent pathway, even if the precise mechanism by which TAR1 modulates these essential metabolic traits is still unknown. Some indications came from D. melanogaster, where, like many other insects, lipids are mainly stored in the fat body.…”

“…An intriguing hypothesis suggests that also the ratio between TA and OA receptors might influence behavioral decisions and physiological states. This aspect is evident in social insects, including honeybees, in which both the levels of TA and OA and the expression patterns of the TA and OA receptors seem to influence the caste identities, characterized by well-defined physiological and behavioral profiles [65,66,96]. Moreover, the capacity of insects to adapt to particular environmental events or to food deprivation could also be influenced by this complex tyraminergic system and deserves to be further investigated.…”