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PLoS One
2013 Oct 08;810:e77345. doi: 10.1371/journal.pone.0077345.
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Functional evolution of a multigene family: orthologous and paralogous pheromone receptor genes in the turnip moth, Agrotis segetum.
Zhang DD
,
Löfstedt C
.
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Lepidopteran pheromone receptors (PRs), for which orthologies are evident among closely related species, provide an intriguing example of gene family evolution in terms of how new functions may arise. However, only a limited number of PRs have been functionally characterized so far and thus evolutionary scenarios suffer from elements of speculation. In this study we investigated the turnip moth Agrotis segetum, in which female moths produce a mixture of chemically related pheromone components that elicit specific responses from receptor cells on male antennae. We cloned nine A. segetum PR genes and the Orco gene by degenerate primer based RT-PCR. The nine PR genes, named as AsegOR1 and AsegOR3-10, fall into four distinct orthologous clusters of known lepidopteran PRs, of which one contains six paralogues. The paralogues are under relaxed selective pressure, contrasting with the purifying selection on other clusters. We identified the receptors AsegOR9, AsegOR4 and AsegOR5, specific for the respective homologous pheromone components (Z)-5-decenyl, (Z)-7-dodecenyl and (Z)-9-tetradecenyl acetates, by two-electrode voltage clamp recording from Xenopus laevis oocytes co-expressing Orco and each PR candidate. These receptors occur in three different orthologous clusters. We also found that the six paralogues with high sequence similarity vary dramatically in ligand selectivity and sensitivity. Different from AsegOR9, AsegOR6 showed a relatively large response to the behavioural antagonist (Z)-5-decenol, and a small response to (Z)-5-decenyl acetate. AsegOR1 was broadly tuned, but most responsive to (Z)-5-decenyl acetate, (Z)-7-dodecenyl acetate and the behavioural antagonist (Z)-8-dodecenyl acetate. AsegOR8 and AsegOR7, which differ from AsegOR6 and AsegOR1 by 7 and 10 aa respectively, showed much lower sensitivities. AsegOR10 showed only small responses to all the tested compounds. These results suggest that new receptors arise through gene duplication, and relaxed evolutionary constraints or positive selection among paralogues allow functional divergence to occur in spite of purifying selection being the norm.
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24130875
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Figure 2. Distinct response profiles of the six AsegOR paralogues from Cluster I.Response profiles of (A) AsegOR9, (B) AsegOR1 and AsegOR7, (C) AsegOR6 and AsegOR8, (D) AsegOR10. The upper part of each panel indicates current trace of injected oocyte upon successive exposures to 100 μM stimuli. Each chemical was applied at the time point indicated by arrowheads for 20 s. The lower part of each panel indicates mean values ± SE of the stimulated currents in nA. Number of replicates for each receptor is indicated in the legend. Letters above bars represent significant level at p <0.05 (one-way-ANOVA followed a LSD test); single or two asterisks in (B) and (C) represent different sensitivities of two receptors to same ligand (p <0.05 or p<0.01 respectively, t-test).
Figure 3. Response profiles and dose responses of (A) AsegOR4 and (B) AsegOR5.The upper part of each panel indicates current trace of injected oocyte upon successive exposures to 100 μM stimuli. Each chemical was applied at the time point indicated by arrowheads for 20 s. The middle part of each panel indicates mean values ± SE of the stimulated currents in nA, one-way-ANOVA followed a LSD test, p <0.05. The lower part of each panel indicates the responses of the receptors at different doses of ligand. Number of replicates for each receptor is indicated in the legend.
Figure 4. Response profiles and dose responses of AsegOR3.The upper part indicates current trace of injected oocyte upon successive exposures to 100 μM stimuli. Each chemical was applied at the time point indicated by arrowheads for 20 s. The lower indicates mean values ± SE of the stimulated currents in nA, one-way-ANOVA followed a LSD test, p <0.05. Number of replicates for each receptor is indicated in the legend.
Figure 5. The six AsegOR paralogues from Cluster I vary in ligand sensitivity.(A) The dose responses of the six paralogues to the pheromone component Z5-10:OAc. (B) The dose responses of AsegOR6 and AsegOR8 to the behavioural antagonist Z5-10:OH. Number of replicates for each receptor is indicated in the legend.
Figure 6. Summary of the response profiles of AsegOR1, AsegOR3-10 and the putative locations of PRs in the ORNs.(A) Representation of ORNs in trichoid sensilla of A. segetum, depicting suggested associations between PRs and ORNs. The different types of ORNs were identified in previous single-sensillum recordings [11-13]. (B) The response profiles of AsegOR1 and AsegOR3-10 in the presence of seven test compounds at a dose of 100 μM. Circles of different sizes represent the response magnitudes. Black circles indicate the responses of the most active ligand(s) of each receptor, whereas grey circles indicate responses evoked by other stimuli.
Figure 1. Neighbor-joining phylogenetic tree of AsegORs with functionally identified PR sequences in Lepidoptera.The tree was rooted with Orco lineage in Lepidoptera. Percentage bootstrap support (1000 replicates) values over 50 are shown at corresponding nodes. AsegORs and AsegOR\Orco are indicated with arrowheads. The nonsynonymous (dN) to synonymous (dS) substitution rate (ω) was labelled in the tree. Cluster II, III and IV have a uniform ω rate for all branches, as labelled at the right side, whereas Cluster I has various ω rate for all branches within the lineage, as labelled on the left on each branch. Genbank accession numbers of the protein sequences used in this phylogenetic tree were concluded in Table S2.
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