Abstract
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.
Highlights
Perception of olfactory cues plays a fundamental role in insect life, and the olfactory system has evolved through adaptations to new environments, host, plant, and mate-finding signals (Bergstrom, 2008; Smadja and Butlin, 2009; Hansson and Stensmyr, 2011)
Comparison of protein sequences of putative orthologs from different lepidopteran species showed that the receptors OR21 and OR22 of B. mori, along with OR19 of S. littoralis, H. virescens, and C. pomonella cluster within one group (Figure 2)
sensillum recordings (SSRs) recordings from ab3A olfactory sensory neurons (OSNs) of D. melanogaster that expressed CpomOR19 showed that of 64 stimuli tested at the maximum dose of 100 μg loaded on filter paper, only 1-indanone elicited a strong electrophysiological response (>50 Hz; Table 1, Supplementary Figure 1)
Summary
Perception of olfactory cues plays a fundamental role in insect life, and the olfactory system has evolved through adaptations to new environments, host, plant, and mate-finding signals (Bergstrom, 2008; Smadja and Butlin, 2009; Hansson and Stensmyr, 2011). Several studies have shown that the family of odorant receptor (OR) genes, which encode for proteins that detect and discriminate odorants, is highly divergent among insect taxa and even among closely related species (JacquinJoly and Merlin, 2004; Su et al, 2009; Engsontia et al, 2014; Depetris-Chauvin et al, 2015). This suggests that olfactory systems have evolved rapidly to enable perception of relevant odor signals. Orthologous ORs are of particular interest since may be tuned to odorants that are behaviorally and ecologically relevant across species (Bohbot et al, 2011)
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