Abstract
SummaryHow chemical signals are integrated at the peripheral sensory system of insects is still an enigma. Here we show that when coexpressed with Orco in Xenopus oocytes, an odorant receptor from the southern house mosquito, CquiOR32, generated inward (regular) currents when challenged with cyclohexanone and methyl salicylate, whereas eucalyptol and fenchone elicited inhibitory (upward) currents. Responses of CquiOR32-CquiOrco-expressing oocytes to odorants were reduced in a dose-dependent fashion by coapplication of inhibitors. This intrareceptor inhibition was also manifested in vivo in fruit flies expressing the mosquito receptor CquiOR32, as well in neurons on the antennae of the southern house mosquito. Likewise, an orthologue from the yellow fever mosquito, AaegOR71, showed intrareceptor inhibition in the Xenopus oocyte recording system and corresponding inhibition in antennal neurons. Inhibition was also manifested in mosquito behavior. Blood-seeking females were repelled by methyl salicylate, but repellence was significantly reduced when methyl salicylate was coapplied with eucalyptol.
Highlights
Integration of chemical signals at the peripheral sensory system remains one of the least understood mechanisms of insect olfaction, in mosquitoes
In the largest majority of reported cases (Hill et al, 2009; Syed and Leal, 2009; Liu et al, 2013; Ye et al, 2016), antennal neurons of Cx. quinquefasciatus displayed excitatory responses, but evidence for inhibitory responses, already known for Ae. aegypti (Ghaninia et al, 2007), is emerging for Cx. quinquefasciatus (Ye et al, 2016). It has been observed in moths (Kaissling, 1996), beetles (Nikonov and Leal, 2002), the fruit fly (Su et al, 2012), and mosquitoes (Tauxe et al, 2013) that activation of one neuron interferes with signaling of other olfactory receptor neurons (ORNs; referred to as olfactory sensory neurons)
Similar inhibition was observed when 2-heptanone was applied alone or coapplied with eucalyptol (Figure S5). These results further suggest that intrareceptor inhibition occurs in vivo as indicated by the inhibitory effect of eucalyptol on methyl salicylate responses
Summary
Integration of chemical signals at the peripheral sensory system (antennae, maxillary palps, and proboscis) remains one of the least understood mechanisms of insect olfaction, in mosquitoes. In the largest majority of reported cases (Hill et al, 2009; Syed and Leal, 2009; Liu et al, 2013; Ye et al, 2016), antennal neurons of Cx. quinquefasciatus displayed excitatory responses (increased spike frequency upon stimulus), but evidence for inhibitory responses (reduction in spontaneous activity upon stimulus), already known for Ae. aegypti (Ghaninia et al, 2007), is emerging for Cx. quinquefasciatus (Ye et al, 2016) It has been observed in moths (Kaissling, 1996), beetles (Nikonov and Leal, 2002), the fruit (vineger) fly (Su et al, 2012), and mosquitoes (Tauxe et al, 2013) that activation (firing) of one neuron interferes with signaling of other olfactory receptor neurons (ORNs; referred to as olfactory sensory neurons). Further studies unraveled a hitherto unknown mechanism of peripheral, intrareceptor inhibition in mosquito olfaction
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