Identification of multiple odorant receptors essential for pyrethrum repellency in Drosophila melanogaster.

Qiang Wang,Rufus Isaacs,Eugenio E Oliveira,Mengli Chen,Makoto Ihara,Yuzhe Du,Lan Jiang,Kazuhiko Matsuda,Yoshiko Nomura,Peng Xu,Ke Dong,Phil Duran,Yahui Liu,Genki Takamatsu,Felipe Andreazza,Subba Reddy Palli

doi:10.1371/journal.pgen.1009677

Abstract

Pyrethrum extract from dry flowers of Tanacetum cinerariifolium (formally Chrysanthemum cinerariifolium) has been used globally as a popular insect repellent against arthropod pests for thousands of years. However, the mechanistic basis of pyrethrum repellency remains unknown. In this study, we found that pyrethrum spatially repels and activates olfactory responses in Drosophila melanogaster, a genetically tractable model insect, and the closely-related D. suzukii which is a serious invasive fruit crop pest. The discovery of spatial pyrethrum repellency and olfactory response to pyrethrum in D. melanogaster facilitated our identification of four odorant receptors, Or7a, Or42b, Or59b and Or98a that are responsive to pyrethrum. Further analysis showed that the first three Ors are activated by pyrethrins, the major insecticidal components in pyrethrum, whereas Or98a is activated by (E)-β-farnesene (EBF), a sesquiterpene and a minor component in pyrethrum. Importantly, knockout of Or7a, Or59b or Or98a individually abolished fly avoidance to pyrethrum, while knockout of Or42b had no effect, demonstrating that simultaneous activation of Or7a, Or59b and Or98a is required for pyrethrum repellency in D. melanogaster. Our study provides insights into the molecular basis of repellency of one of the most ancient and globally used insect repellents. Identification of pyrethrum-responsive Ors opens the door to develop new synthetic insect repellent mixtures that are highly effective and broad-spectrum.

Highlights

Pyrethrum is a botanical insecticide extracted from dry flowers of Tanacetum cinerariifolium
We took advantage of Drosophila melanogaster as a model insect system for olfaction studies and conducted a series of electrophysiological, molecular genetic and behavioral experiments to understand the mechanism of pyrethrum repellency in D. melanogaster
We discovered that pyrethrum repels D. melanogaster by activating multiple odorant receptors (Ors)

Summary

Introduction

Pyrethrum is a botanical insecticide extracted from dry flowers of Tanacetum cinerariifolium ( known as Chrysanthemum cinerariifolium). This plant is grown commercially in many parts of the world, in East Africa and Australia, for extraction of pyrethrum, which accumulates in the flower achenes [1,2]. Pyrethrins and pyrethroids target voltage-gated sodium channels for their insecticidal effects [4,5,6], which is critical for the initiation and propagation of action potentials in the nervous system. Pyrethrins and pyrethroids promote activation of sodium channels and inhibit deactivation and inactivation, which lead to the disruption of the function of the nervous system

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Discussion

Conclusion