Transcriptome profiling of chemosensory appendages in the malaria vector Anopheles gambiae reveals tissue- and sex-specific signatures of odor coding

Abstract

BackgroundChemosensory signal transduction guides the behavior of many insects, including Anopheles gambiae, the major vector for human malaria in sub-Saharan Africa. To better understand the molecular basis of mosquito chemosensation we have used whole transcriptome RNA sequencing (RNA-seq) to compare transcript expression profiles between the two major chemosensory tissues, the antennae and maxillary palps, of adult female and male An. gambiae.ResultsWe compared chemosensory tissue transcriptomes to whole body transcriptomes of each sex to identify chemosensory enhanced genes. In the six data sets analyzed, we detected expression of nearly all known chemosensory genes and found them to be highly enriched in both olfactory tissues of males and females. While the maxillary palps of both sexes demonstrated strict chemosensory gene expression overlap, we observed acute differences in sensory specialization between male and female antennae. The relatively high expression levels of chemosensory genes in the female antennae reveal its role as an organ predominately assigned to chemosensation. Remarkably, the expression of these genes was highly conserved in the male antennae, but at much lower relative levels. Alternatively, consistent with a role in mating, the male antennae displayed significant enhancement of genes involved in audition, while the female enhancement of these genes was observed, but to a lesser degree.ConclusionsThese findings suggest that the chemoreceptive spectrum, as defined by gene expression profiles, is largely similar in female and male An. gambiae. However, assuming sensory receptor expression levels are correlated with sensitivity in each case, we posit that male and female antennae are perceptive to the same stimuli, but possess inverse receptive prioritizations and sensitivities. Here we have demonstrated the use of RNA-seq to characterize the sensory specializations of an important disease vector and grounded future studies investigating chemosensory processes.

Odorant receptor-mediated sperm activation in disease vector mosquitoes

“…A previous RNA sequencing (RNAseq) study in A. gambiae adults revealed that a subset of AgOrs is enhanced in whole male bodies (5). One interpretation of those data is that AgOrs are functional in nonhead tissues in males where they are used in noncanonical chemosensory roles.…”

“…RPKM values for bodies and antennae are from ref. 5. Asterisks indicate transcripts that were present in at least one of four testes samples as determined by an independent microarray analysis (30); double asterisks indicate transcripts that displayed enhanced expression in testes relative to at least one other tissue; nd, not determined; probe for these transcripts not included on microarray (30).…”

“…In total, we found 14 AgGrs, 17 AgIrs, and six AgObps with RPKMs greater than 1, among which two AgGrs, four AgIrs, and five AgObps had transcript abundances above the median of the entire testis transcriptome (Dataset S1). These highly expressed chemosensory genes include AgGr22, which encodes a carbon dioxide receptor, and several conserved AgIrs with significant antennal expression (5).…”

“…transcriptomics | cell signaling | gamete | chemical ecology | Culicidae T o date, studies of odorant receptor (OR) expression and function in mosquitoes and other insects have been limited to adult and larval appendages where the fundamental properties of insect chemosensation continue to be elucidated (1)(2)(3)(4)(5)(6). Unlike their mammalian counterparts, which function strictly as G protein-coupled receptors (GPCRs), insect ORs generally act as heteromeric ion channels of at least two subunits: a highly conserved coreceptor (Orco) and a ligand-recognizing receptor (ORx) (7)(8)(9)(10)(11), although evidence for second messenger signaling has also been observed (12,13), especially in sex pheromone signaling (14).…”

Global Transcriptome Changes Underlying Colony Growth in the Opportunistic Human Pathogen Aspergillus fumigatus

“…To limit the number of false positives, we employed a conservative approach to identify differentially expressed genes by implementing both biological and statistical cutoffs for significance (56). For our biological cutoff, we compared the fold difference of RPKM values between BF and PL conditions by calculating the relative RPKM (rRPKM ϭ RPKM BF /RPKM PL ) of each gene.…”