Diverse Functions of Insect Biogenic Amines as Neurotransmitters, Neuromodulators, and Neurohormones

Journal of Experimental Biology

Tiedemann

Zhang

et al. 2020

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.

Section: Introductionsupporting

confidence: 67%

Monoterpenes alter TAR1-driven physiology in Drosophila species

Journal of Experimental Biology

Tiedemann

Zhang

et al. 2020

“…This is then hydroxylated to OA by the tyramine β-hydroxylase (Tβh) [3]. The insect nervous tissues contain high levels of both OA and TA, supporting the view that they act as neurotransmitters [1]. Moreover, they act also as neuromodulators and neurohormones in a wide variety of physiological processes, also operating in a paracrine, endocrine, and autocrine fashion in peripheral organs [4,5].…”

Section: Introduction: the Tyraminergic And Octopaminergic Systems In Insectsmentioning

confidence: 92%

“…Together, they control and modulate a broad range of biological functions essential for the life of the insects. Whereas DA and 5-HT functions and pathways are highly conserved in both vertebrates and invertebrates, TA and OA can be considered the invertebrate counterparts of the catecholamines epinephrine and norepinephrine of vertebrates [ 1 ]. TA, OA, and the catecholamines epinephrine and norepinephrine have many features in common: They are synthesized from the same precursor amino acid (tyrosine), share both structural and functional characteristics such as interaction with G protein-coupled receptors (GPCRs), and regulate similar behavioral and physiological traits [ 2 ].…”

Section: Introduction: the Tyraminergic And Octopaminergic Systems In Insectsmentioning

confidence: 99%

The Insect Type 1 Tyramine Receptors: From Structure to Behavior

Roeder

Calò

et al. 2021

Insects

Tyramine is a neuroactive compound that acts as neurotransmitter, neuromodulator, and neurohormone in insects. Three G protein-coupled receptors, TAR1-3, are responsible for mediating the intracellular pathway in the complex tyraminergic network. TAR1, the prominent player in this system, was initially classified as an octopamine receptor which can also be activated by tyramine, while it later appeared to be a true tyramine receptor. Even though TAR1 is currently considered as a well-defined tyramine receptor and several insect TAR1s have been characterized, a defined nomenclature is still inconsistent. In the last years, our knowledge on the structural, biochemical, and functional properties of TAR1 has substantially increased. This review summarizes the available information on TAR1 from different insect species in terms of basic structure, its regulation and signal transduction mechanisms, and its distribution and functions in the brain and the periphery. A special focus is given to the TAR1-mediated intracellular signaling pathways as well as to their physiological role in regulating behavioral traits. Therefore, this work aims to correlate, for the first time, the physiological relevance of TAR1 functions with the tyraminergic system in insects. In addition, pharmacological studies have shed light on compounds with insecticidal properties having TAR1 as a target and on the emerging trend in the development of novel strategies for pest control.

“…xylostella (Ma et al, 2019a) suggesting that TAR1 could be involved in male specific functions such as development as well as reproduction. The high brain expression of HhTAR1 correlates well with the abundance of TAR1 in CNS of numerous insect species (El-Kholy et al, 2015;Hana & Lange, 2017a;Finetti et al, 2020) where it regulates several sensory processes (Roeder et al, 2003;Lange, 2009;Ohta & Ozoe, 2014;Neckameyer & Leal, 2017). Interestingly, HhTAR1…”

Section: Discussionmentioning

confidence: 89%

Tyramine receptor drives olfactory response to (E)-2-decenal in the stink bugHalyomorpha halys

Pezzi

Civolani

et al. 2020

Preprint

In insects, the tyramine receptor 1 (TAR1) has been shown to control several physiological functions, including olfaction. We investigated the molecular and functional profile of the Halyomorpha halys type 1 tyramine receptor gene (HhTAR1) and its role in olfactory functions of this pest. Molecular and pharmacological analyses confirmed that the HhTAR1 gene codes for a true TAR1. The RT-qPCR analysis revealed that HhTAR1 is expressed mostly in adult brain and antennae as well as in early development stages (eggs, 1st and 2nd instar nymphs). In particular, among the antennomeres that compose a typical H. halys antenna, HhTAR1 was more expressed in flagellomeres. Scanning electron microscopy (SEM) investigation revealed the type and distribution of sensilla on adult H. halys antennae: both flagellomeres appear rich in trichoid and grooved sensilla, known to be associated with olfactory functions. Through a RNAi approach, topically delivered HhTAR1 dsRNA induced a 50 % gene downregulation after 24 h in H. halys 2nd instar nymphs. An innovative behavioral assay revealed that HhTAR1 RNAi-silenced 2nd instar nymphs were less susceptible to the alarm pheromone component (E)-2 decenal as compared to control. These results provide critical information concerning the TAR1 role in olfaction regulation, especially alarm pheromone reception, in H. halys. Furthermore, considering the emerging role of TAR1 as target of biopesticides, this work paves the way for further investigation on innovative methods for controlling H. halys.