A conserved odorant receptor detects the same 1-indanone analogs in a tortricid and a noctuid moth
Odorant receptors (ORs) interface animals with airborne chemical signals. They are under strong selection pressure and are therefore highly divergent in different taxa. Yet, some OR orthologs are highly conserved. These ORs may be tuned to odorants of broad importance, across species boundaries. Two...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2015-11-01
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| Series: | Frontiers in Ecology and Evolution |
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| Online Access: | http://journal.frontiersin.org/Journal/10.3389/fevo.2015.00131/full |
| _version_ | 1819096956341846016 |
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| author | Francisco eGonzalez Jonas M Bengtsson Jonas M Bengtsson William Benjamin Walker Maria Fátima Rodrigues Sousa Alberto Maria eCattaneo Nicolas eMontagné Arthur ede Fouchier Gianfranco eAnfora Emmanuelle eJacquin-Joly Peter eWitzgall Rickard eIgnell Marie eBengtsson |
| author_facet | Francisco eGonzalez Jonas M Bengtsson Jonas M Bengtsson William Benjamin Walker Maria Fátima Rodrigues Sousa Alberto Maria eCattaneo Nicolas eMontagné Arthur ede Fouchier Gianfranco eAnfora Emmanuelle eJacquin-Joly Peter eWitzgall Rickard eIgnell Marie eBengtsson |
| author_sort | Francisco eGonzalez |
| collection | DOAJ |
| description | Odorant receptors (ORs) interface animals with airborne chemical signals. They are under strong selection pressure and are therefore highly divergent in different taxa. Yet, some OR orthologs are highly conserved. These ORs may be tuned to odorants of broad importance, across species boundaries. Two widely distributed lepidopteran herbivores, codling moth Cydia pomonella (Tortricidae) feeding in apples and pears, and the African cotton leafworm Spodoptera littoralis (Noctuidae), a moth feeding on foliage of a wide range of herbaceous plants, both express a receptor ortholog, OR19, which shares 58% amino acid identity and 69% amino acid similarity. Following heterologous expression in the empty neuron system of Drosophila melanogaster, we show by single sensillum recordings that CpomOR19 and SlitOR19 show similar affinity to several substituted indanes. Tests with a series of compounds structurally related to 1-indanone show that 2-methyl-1-indanone, 2-ethyl-1-indanone, 3-methyl-1-indanone and 1-indanone elicit a strong response from both ORs. A keto group in position 1 is essential for biological activity and so are both rings of the indane skeleton. However, there is an important difference in steric complementary of the indane rings and the receptor. Methyl substituents on the benzene ring largely suppressed the response. On the other hand, alkyl substituents at position 2 and 3 of the five-membered ring increased the response indicating a higher complementarity with the receptor cavity, in both CpomOR19 and SlitOR19. Our results demonstrate a conserved function of an odorant receptor in two moths that are phylogenetically and ecologically distant. It is conceivable that a conserved OR is tuned to signals that are relevant for both species, although their ecological roles are yet unknown. Our finding demonstrates that functional characterization of ORs leads to the discovery of novel semiochemicals that have not yet been found through chemical analysis of odorants from insects and their associated host plants. |
| first_indexed | 2024-12-22T00:07:26Z |
| format | Article |
| id | doaj.art-08bbd9509cc54a49a8daa02aa98f6113 |
| institution | Directory Open Access Journal |
| issn | 2296-701X |
| language | English |
| last_indexed | 2024-12-22T00:07:26Z |
| publishDate | 2015-11-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Ecology and Evolution |
| spelling | doaj.art-08bbd9509cc54a49a8daa02aa98f61132022-12-21T18:45:32ZengFrontiers Media S.A.Frontiers in Ecology and Evolution2296-701X2015-11-01310.3389/fevo.2015.00131167166A conserved odorant receptor detects the same 1-indanone analogs in a tortricid and a noctuid mothFrancisco eGonzalez0Jonas M Bengtsson1Jonas M Bengtsson2William Benjamin Walker3Maria Fátima Rodrigues Sousa4Alberto Maria eCattaneo5Nicolas eMontagné6Arthur ede Fouchier7Gianfranco eAnfora8Emmanuelle eJacquin-Joly9Peter eWitzgall10Rickard eIgnell11Marie eBengtsson12Swedish University of Agricultural SciencesResearch and Innovation Centre, Fondazione Edmund MachStockholm UniversitySwedish University of Agricultural SciencesSwedish University of Agricultural SciencesResearch and Innovation Centre, Fondazione Edmund MachSorbonne Universités, UPMC Université Paris 6, Institute of Ecology and Environmental SciencesSorbonne Universités, UPMC Université Paris 6, Institute of Ecology and Environmental SciencesResearch and Innovation Centre, Fondazione Edmund MachINRA, Institute of Ecology and Environmental Sciences (iEES-Paris)Swedish University of Agricultural SciencesSwedish University of Agricultural SciencesSwedish University of Agricultural SciencesOdorant receptors (ORs) interface animals with airborne chemical signals. They are under strong selection pressure and are therefore highly divergent in different taxa. Yet, some OR orthologs are highly conserved. These ORs may be tuned to odorants of broad importance, across species boundaries. Two widely distributed lepidopteran herbivores, codling moth Cydia pomonella (Tortricidae) feeding in apples and pears, and the African cotton leafworm Spodoptera littoralis (Noctuidae), a moth feeding on foliage of a wide range of herbaceous plants, both express a receptor ortholog, OR19, which shares 58% amino acid identity and 69% amino acid similarity. Following heterologous expression in the empty neuron system of Drosophila melanogaster, we show by single sensillum recordings that CpomOR19 and SlitOR19 show similar affinity to several substituted indanes. Tests with a series of compounds structurally related to 1-indanone show that 2-methyl-1-indanone, 2-ethyl-1-indanone, 3-methyl-1-indanone and 1-indanone elicit a strong response from both ORs. A keto group in position 1 is essential for biological activity and so are both rings of the indane skeleton. However, there is an important difference in steric complementary of the indane rings and the receptor. Methyl substituents on the benzene ring largely suppressed the response. On the other hand, alkyl substituents at position 2 and 3 of the five-membered ring increased the response indicating a higher complementarity with the receptor cavity, in both CpomOR19 and SlitOR19. Our results demonstrate a conserved function of an odorant receptor in two moths that are phylogenetically and ecologically distant. It is conceivable that a conserved OR is tuned to signals that are relevant for both species, although their ecological roles are yet unknown. Our finding demonstrates that functional characterization of ORs leads to the discovery of novel semiochemicals that have not yet been found through chemical analysis of odorants from insects and their associated host plants.http://journal.frontiersin.org/Journal/10.3389/fevo.2015.00131/fullOlfactionfunctional characterizationolfactory receptorSpodoptera littoralisOrthologous genesCydia pomonella |
| spellingShingle | Francisco eGonzalez Jonas M Bengtsson Jonas M Bengtsson William Benjamin Walker Maria Fátima Rodrigues Sousa Alberto Maria eCattaneo Nicolas eMontagné Arthur ede Fouchier Gianfranco eAnfora Emmanuelle eJacquin-Joly Peter eWitzgall Rickard eIgnell Marie eBengtsson A conserved odorant receptor detects the same 1-indanone analogs in a tortricid and a noctuid moth Frontiers in Ecology and Evolution Olfaction functional characterization olfactory receptor Spodoptera littoralis Orthologous genes Cydia pomonella |
| title | A conserved odorant receptor detects the same 1-indanone analogs in a tortricid and a noctuid moth |
| title_full | A conserved odorant receptor detects the same 1-indanone analogs in a tortricid and a noctuid moth |
| title_fullStr | A conserved odorant receptor detects the same 1-indanone analogs in a tortricid and a noctuid moth |
| title_full_unstemmed | A conserved odorant receptor detects the same 1-indanone analogs in a tortricid and a noctuid moth |
| title_short | A conserved odorant receptor detects the same 1-indanone analogs in a tortricid and a noctuid moth |
| title_sort | conserved odorant receptor detects the same 1 indanone analogs in a tortricid and a noctuid moth |
| topic | Olfaction functional characterization olfactory receptor Spodoptera littoralis Orthologous genes Cydia pomonella |
| url | http://journal.frontiersin.org/Journal/10.3389/fevo.2015.00131/full |
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