Peptidergic control of a fruit crop pest: the spotted-wing drosophila, Drosophila suzukii

Authors: GOUGH, CAROLINE - University Of Leeds; FAIRLAMB, GRACE - University Of Leeds; PRIBYLOVA, PETRA - University Of Leeds; Nachman, Ronald; AUDSLEY, NEIL - Fera Science Ltd; ISAAC, R. ELWYN - University Of Leeds

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/2/2017
Publication Date: 11/10/2017
Citation: Gough, C.S., Fairlamb, G.M., Bell, P., Nachman, R.J., Audsley, N., Isaac, R.E. 2017. Peptidergic control in a fruit crop pest: The spotted-wing drosophila, Drosophila suzukii. PLoS ONE 12(11):e0188021. https://doi.org/10.1371/journal.pone.0188021.
DOI: https://doi.org/10.1371/journal.pone.0188021

Interpretive Summary: Because of problems with the development of resistance to conventional pesticides, there is a critical need for new concepts and alternative approaches in controlling insect pests. The basic premise of this research is that neuropeptides (short chains of amino acids) serve as potent messengers in insects to regulate vital functions. Nevertheless, neuropeptides in and of themselves hold little promise as pest control agents because of susceptibility to being degraded in the target pest and inability to penetrate the outside surface of insects. New, selective control measures may be developed by designing metabolically stable mimics of these neuropeptides that interact with the active site within the agricultural or medical pest in such a way as to either inhibit or over-stimulate critical neuropeptide-regulated life functions. We report that a biostable, non-peptide mimic of neuropeptides of the ‘myosuppressin’ class that regulate digestive tract movement and digestion can mimic myosuppressin inhibition of contractions of the gut in a major pest of soft fruit, the spotted wing drosophila fly. Oral administration of the non-peptide mimic resulted in a 60% reduction in the passage of food through the gut and early mortality, specifically a 5-fold reduction in their lifespan. The work identifies a pest control agent lead and brings us steps closer to the development of practical neuropeptide-like substances that will be effective in controlling fruit pests in an environmentally friendly fashion.

Technical Abstract: Neuropeptides play an important role in the regulation of feeding in insects and offer potential targets for the development of new chemicals to control insect pests. A pest that has attracted much recent attention is the highly invasive Drosophila suzukii, a polyphagous pest that can cause serious economic damage to soft fruits. Previously we showed by mass spectrometry the presence of the neuropeptide myosuppressin (TDVDHVFLRFamide) in the nerve bundle suggesting that this peptide is involved in regulating the function of the crop, which in adult dipteran insects has important roles in the processing of food, the storage of carbohydrates and the movement of food into the midgut for digestion. In the present study antibodies that recognise the C-terminal RFamide epitope of myosuppressin stain axons in the crop nerve bundle and reveal peptidergic fibres covering the surface of the crop. We also show using an in vitro bioassay that the neuropeptide is a potent inhibitor (EC50 of 3.0 nM) of crop contractions and that this inhibition is mimicked by the non-peptide myosuppressin agonist, benzethonium chloride (Bztc). Myosuppressin also inhibited the peristaltic contractions of the adult midgut, but was a much weaker agonist (EC50 = 7.2 uM). The oral administration of Bztc (5 mM) in a sucrose diet to adult female D. suzukii over 4 hours resulted in a 60% reduction in the passage of food through the gut and longer exposure to dietary Bztc led to early mortality. We therefore suggest that myosuppressin and its cognate receptors are potential targets for disrupting feeding behaviour of adult D. suzukii.