Transcriptome Profiling of Neurosensory Perception Genes in Wing Tissue of Two Evolutionary Distant Insect Orders: Diptera (Drosophila melanogaster) and Hemiptera (Acyrthosiphon pisum)

Abstract

The neurogenesis and neuronal functions in insect wing have been understudied mainly due to technical hindrances that have prevented electrophysiology studies for decades. The reason is that the nano-architecture of the wing chemosensory bristles hampers the receptors accessibility of odorants/tastants to receptors in fixed setup, whereas in nature, the wing flapping mixes these molecules in bristle lymph. In this report, we analyzed the transcriptome of the wing tissue of two species phylogenetically strongly divergent: Drosophila melanogaster a generic model for diptera order (complete metamorphosis) and the aphid acyrthosiphon pisum, representative of hemiptera order (incomplete metamorphosis) for which a conditional winged/wingless polyphenism is under control of population density and resources. The transcriptome shows that extensive gene networks involved in chemosensory perception are active in adult wing for both species. Surprisingly, the specific transcripts of genes that are commonly found in eye were present in Drosophila wing but not in aphid. The analysis reveals that in the aphid conditional wing, expressed genes show strong similarities with those in the gut epithelia. This suggests that the epithelial cell layer between the cuticle sheets is persistent at least in young aphid adult, whereas it disappears after emergence in Drosophila. Despite marked differences between the two transcriptomes, the results highlight the probable universalism of wing chemosensory function in the holometabolous and hemimetabolous orders of winged insects.

The pleiotropic effects of Innexin genes expressed in Drosophila glia encompass wing chemosensory sensilla

“…A yet unexplored field is the role of the glial cell in mature sensilla in Drosophila and in diverse insect orders in general, along with the functional dialog between the trichogen, tormogen, thecogen, and sensory neurons. In support of the present study, we have published recently a RNAseq analysis on adult wing tissue that shows the expression of most of the eight Innexin genes (Agnel, Rocha, & Robichon, ). More surprisingly, the adult wing Innexin transcripts range from moderate to elevated levels.…”

“…This highly enriched material in sensilla with very little cellular contaminants allowed us to explore the presence and roles of innexin proteins at the interface glial cell/neuron. The RNAseq data set analysis on adult wing tissue was carried out and published elsewhere (Agnel et al, ), which allowed us to assess the presence of trancripts of most of Innexin family members from moderate to elevated level (see Figure a for the RPKMs). The transcripts of Inx2 and Ogre were additionally confirmed by PCR (Figure a).…”

“…This makes the process of absorption/emission of light in fluorescence microscopy highly constrained, the wing matrix acting as a barrier that annihilates and/or limits the imaging technologies. Many Gr (gustatory G protein coupled receptors), Ir (ionotropic receptor), and TRP (transient receptor potential channel) are known to be expressed in wing tissue (Agnel et al, ). The gene named repo that encodes a homeodomain transcription factor, specifically expressed in glial cells is considered as a reliable marker for this type of cells (Kremer, Jung, Batelli, Rubin, & Gaul, ).…”

“…Moreover, the calcium waves seem to be amplified and synchronized, which strongly suggests cell/cell communication. However, up to a recent study based on RNAseq analysis of wing tissue (Agnel et al, ) it was unknown whether the channel‐forming proteins of Innexin family (equivalent of Connexin in invertebrates) exist in adult Drosophila wing sensilla in contrast with their well documented expression in the wing imaginal disc, in the developing central nervous system of embryos and in lamina column beneath the retina (Bauer, Lehmann, Martini, Eckardt, & Hoch, ; Bauer et al, ; Curtin, Zhang, & Wyman, , ; Holcroft et al, ; Speder & Brand, ; Stebbings et al, ). We reasoned that silencing Inx 2 gene in Drosophila that turned out to be the most expressed isoform in wing imaginal disc might help to document their function and role in wing chemoreception.…”

Chemosensory sensilla of the Drosophila wing express a candidate ionotropic pheromone receptor

“…We note that many of the wing genes identified in our analysis, including both genes that are and are not enriched in chemosensory sensilla, were also recently identified in a different kind of RNA-seq comparison: between the entire wing of Drosophila and the wing and gut of a distantly related aphid, Acrytosiphon pisum [57]. In addition to a number of Obp , Che , and ppk genes, IR52a was among 12,188 genes found by that study to be expressed in the Drosophila wing, in agreement with our findings.…”