Identification of multiple odorant receptors essential for pyrethrum repellency in Drosophila melanogaster.
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 foun...
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2021
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oai:doaj.org-article:9ff3b702011842f9bf866d8b7d3404d12021-12-02T20:02:57ZIdentification of multiple odorant receptors essential for pyrethrum repellency in Drosophila melanogaster.1553-73901553-740410.1371/journal.pgen.1009677https://doaj.org/article/9ff3b702011842f9bf866d8b7d3404d12021-07-01T00:00:00Zhttps://doi.org/10.1371/journal.pgen.1009677https://doaj.org/toc/1553-7390https://doaj.org/toc/1553-7404Pyrethrum 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.Qiang WangPeng XuFelipe AndreazzaYahui LiuYoshiko NomuraPhil DuranLan JiangMengli ChenGenki TakamatsuMakoto IharaKazuhiko MatsudaRufus IsaacsEugenio E OliveiraYuzhe DuKe DongPublic Library of Science (PLoS)articleGeneticsQH426-470ENPLoS Genetics, Vol 17, Iss 7, p e1009677 (2021) |
| institution |
DOAJ |
| collection |
DOAJ |
| language |
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| topic |
Genetics QH426-470 |
| spellingShingle |
Genetics QH426-470 Qiang Wang Peng Xu Felipe Andreazza Yahui Liu Yoshiko Nomura Phil Duran Lan Jiang Mengli Chen Genki Takamatsu Makoto Ihara Kazuhiko Matsuda Rufus Isaacs Eugenio E Oliveira Yuzhe Du Ke Dong Identification of multiple odorant receptors essential for pyrethrum repellency in Drosophila melanogaster. |
| description |
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. |
| format |
article |
| author |
Qiang Wang Peng Xu Felipe Andreazza Yahui Liu Yoshiko Nomura Phil Duran Lan Jiang Mengli Chen Genki Takamatsu Makoto Ihara Kazuhiko Matsuda Rufus Isaacs Eugenio E Oliveira Yuzhe Du Ke Dong |
| author_facet |
Qiang Wang Peng Xu Felipe Andreazza Yahui Liu Yoshiko Nomura Phil Duran Lan Jiang Mengli Chen Genki Takamatsu Makoto Ihara Kazuhiko Matsuda Rufus Isaacs Eugenio E Oliveira Yuzhe Du Ke Dong |
| author_sort |
Qiang Wang |
| title |
Identification of multiple odorant receptors essential for pyrethrum repellency in Drosophila melanogaster. |
| title_short |
Identification of multiple odorant receptors essential for pyrethrum repellency in Drosophila melanogaster. |
| title_full |
Identification of multiple odorant receptors essential for pyrethrum repellency in Drosophila melanogaster. |
| title_fullStr |
Identification of multiple odorant receptors essential for pyrethrum repellency in Drosophila melanogaster. |
| title_full_unstemmed |
Identification of multiple odorant receptors essential for pyrethrum repellency in Drosophila melanogaster. |
| title_sort |
identification of multiple odorant receptors essential for pyrethrum repellency in drosophila melanogaster. |
| publisher |
Public Library of Science (PLoS) |
| publishDate |
2021 |
| url |
https://doaj.org/article/9ff3b702011842f9bf866d8b7d3404d1 |
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