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Research Article
Monoterpenes alter TAR1-driven physiology in Drosophila species
Luca Finetti, Lasse Tiedemann, Xiaoying Zhang, Stefano Civolani, Giovanni Bernacchia, Thomas Roeder
Journal of Experimental Biology 2021 224: jeb232116 doi: 10.1242/jeb.232116 Published 7 January 2021
Luca Finetti
1Department of Life Sciences and Biotechnology, University of Ferrara, 44121 Ferrara, Italy
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Lasse Tiedemann
2Laboratory of Molecular Physiology, Department of Zoology, Kiel University, 24098 Kiel, Germany
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Xiaoying Zhang
2Laboratory of Molecular Physiology, Department of Zoology, Kiel University, 24098 Kiel, Germany
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Stefano Civolani
1Department of Life Sciences and Biotechnology, University of Ferrara, 44121 Ferrara, Italy
3InnovaRicerca s.r.l. Monestirolo, 44124 Ferrara, Italy
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Giovanni Bernacchia
1Department of Life Sciences and Biotechnology, University of Ferrara, 44121 Ferrara, Italy
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  • ORCID record for Giovanni Bernacchia
  • For correspondence: bhg@unife.it troeder@zoologie.uni-kiel.de
Thomas Roeder
2Laboratory of Molecular Physiology, Department of Zoology, Kiel University, 24098 Kiel, Germany
4German Center for Lung Research (DZL), Airway Research Center North (ARCN), 24098 Kiel, Germany
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  • For correspondence: bhg@unife.it troeder@zoologie.uni-kiel.de
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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 also can cause complex behavioural alterations that require 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 monoterpene-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 wild-type D. melanogaster, 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 wild-type D. suzukii and D. melanogaster 24 h after continuous monoterpene exposure. Interestingly, they were ineffective in modifying the physiological performance of TAR1-defective flies. In conclusion, it appears that monoterpenes not only act as biopesticides for Drosophila but also can interfere with Drosophila behaviour and metabolism in a TAR1-dependent fashion.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    Conceptualization: G.B., T.R.; Methodology: L.F., L.T., X.Z., S.C.; Data curation: L.T., L.F.; Writing - original draft: L.F.; Writing - review & editing: G.B., T.R.; Supervision: G.B., T.R.; Project administration: G.B., T.R.

  • Funding

    This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.

  • Supplementary information

    Supplementary information available online at https://jeb.biologists.org/lookup/doi/10.1242/jeb.232116.supplemental

  • Received June 26, 2020.
  • Accepted November 13, 2020.
  • © 2021. Published by The Company of Biologists Ltd
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Keywords

  • Drosophila
  • Monoterpenes
  • Tyramine receptor
  • Metabolism
  • Behaviour

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Research Article
Monoterpenes alter TAR1-driven physiology in Drosophila species
Luca Finetti, Lasse Tiedemann, Xiaoying Zhang, Stefano Civolani, Giovanni Bernacchia, Thomas Roeder
Journal of Experimental Biology 2021 224: jeb232116 doi: 10.1242/jeb.232116 Published 7 January 2021
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Research Article
Monoterpenes alter TAR1-driven physiology in Drosophila species
Luca Finetti, Lasse Tiedemann, Xiaoying Zhang, Stefano Civolani, Giovanni Bernacchia, Thomas Roeder
Journal of Experimental Biology 2021 224: jeb232116 doi: 10.1242/jeb.232116 Published 7 January 2021

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