Molecular basis of peripheral olfactory plasticity in Rhodnius prolixus, a Chagas disease vector

Abstract

Olfaction is fundamental for most animals and critical for different aspects of triatomine biology, including host-seeking, reproduction, avoidance of predators, and aggregation in shelters. Ethological and physiological aspects of these olfactory-mediated behaviors are well-understood, but their molecular bases are still largely unknown. Here we investigated changes in the molecular mechanisms at the peripheral olfactory level in response to different physiological and developmental conditions. For this, the antennal expression levels of the odorant (Orco) and ionotropic (IR8a, IR25a, and IR76b) coreceptor genes were determined in Rhodnius prolixus by means of quantitative real-time PCR (qRT-PCR) analysis. Gene expression changes were analyzed to test the effect of feeding and imaginal molt for both sexes. Moreover, we analyzed whether expression of these genes changed during the early life of adult bugs. Under these conditions bugs display distinct behavioral responses to diverse chemical stimuli. A significantly decreased expression was induced by blood feeding on all coreceptor genes. The expression of all genes was significantly increased following the imaginal molt. These results show that olfactory coreceptor genes have their expression altered as a response to physiological or developmental changes. Our study suggests that olfactory coreceptor genes confer adaptability to the peripheral olfactory function, probably underlying the known plasticity of triatomine olfactory-mediated behavior.

The molecular sensory machinery of a Chagas disease vector: expression changes through imaginal moult and sexually dimorphic features

“…As observed in other insects2728, Orco was the odorant receptor showing highest expression in bug antennae (Fig. 2) and the imaginal increase in Orco expression seen in our transcriptome was previously reported for R. prolixus antennae based on qRT-PCR31. Interestingly, only one OR presented differential expression between sexes (Supplementary Table S7), while the bulk of the chemosensory repertoire seemed to remain mostly similar.…”

Transcriptomics supports local sensory regulation in the antenna of the kissing bugRhodnius prolixus

“…Fifteen takeout genes were identified in the R. prolixus genome, while Ribeiro, et al 50 identified 18 potential takeout transcripts in a midgut transcriptome of this species and Marchant, et al 51 identified 25 takeout transcripts in the transcriptome of the kissing-bug Triatoma brasiliensis. Consistently, these numbers match the scale of those found in Anopheles gambiae (10); Acyrthosiphon pisum (17); and Bombyx mori (14) genomes 52 . R. prolixus to genes present a cluster organization ( Supplementary Fig.4S), probably due to gene duplication events, as it was previously observed in other insects 52 .…”

“…Relevant aspects of its neuroethology, such as host odour-mediated behaviour 3,4 , circadian modulation 5 , the action of biogenic amines and neuropeptides 6 or the expression of behavioural plasticity 7,8 have been thoroughly studied. Recently, molecular processes related to sensory function have been characterized for R. prolixus, such as the tissue-specific expression profiles of odorant receptor genes 9 and related changes associated to development and nutrition 10 . Additionally, neuropeptide precursor genes were described for R. prolixus 11 and the dynamics of neuropeptide expression or release at diverse physiological conditions were characterized for processes such as feeding or ecdysis 12,13 .…”

“…Similar changes have been documented at the molecular level, with altered gene expression associated to feeding 20 or age 21 . In fact, variations in gene expression depending on nutritional status or development have been described for olfactory correceptors in the antennae of R. prolixus 10 . Nevertheless, information about elements regulating sensory gene transcription and the abundance of the corresponding proteins in insect peripheral organs is very limited [22][23][24][25] .…”

Under-Expression of Chemosensory Genes in Domiciliary Bugs of the Chagas Disease Vector Triatoma brasiliensis

“…In the fly Glossina morsitans , transcription of CSP genes was related to host searching behavior [76]. A recent study of bloodsucking bugs [77] revealed that, in R . prolixus , some odorant and ionotropic coreceptor genes are less expressed after a blood feeding.…”