Pheromone sensing in Drosophila requires support cell-expressed Osiris 8

Abstract

Background The nose of most animals comprises multiple sensory subsystems, which are defined by the expression of different olfactory receptor families. Drosophila melanogaster antennae contain two morphologically and functionally distinct subsystems that express odorant receptors (Ors) or ionotropic receptors (Irs). Although these receptors have been thoroughly characterized in this species, the subsystem-specific expression and roles of other genes are much less well-understood. Results Here we generate subsystem-specific transcriptomic datasets to identify hundreds of genes, encoding diverse protein classes, that are selectively enriched in either Or or Ir subsystems. Using single-cell antennal transcriptomic data and RNA in situ hybridization, we find that most neuronal genes—other than sensory receptor genes—are broadly expressed within the subsystems. By contrast, we identify many non-neuronal genes that exhibit highly selective expression, revealing substantial molecular heterogeneity in the non-neuronal cellular components of the olfactory subsystems. We characterize one Or subsystem-specific non-neuronal molecule, Osiris 8 (Osi8), a conserved member of a large, insect-specific family of transmembrane proteins. Osi8 is expressed in the membranes of tormogen support cells of pheromone-sensing trichoid sensilla. Loss of Osi8 does not have obvious impact on trichoid sensillar development or basal neuronal activity, but abolishes high sensitivity responses to pheromone ligands. Conclusions This work identifies a new protein required for insect pheromone detection, emphasizes the importance of support cells in neuronal sensory functions, and provides a resource for future characterization of other olfactory subsystem-specific genes.

Activity-dependent survival of odorant receptor neurons in ants

“…The latter are likely support cells located near the antennal cuticle which surround the dendrites of ORNs, and these cells do not die in the orco mutant. There are 3 types of support cells as identified in Drosophila : thecogen (sheath) cells, trichogen (shaft) cells, and tormogen (socket) cells ( 42, 43 ). It remains unclear which cell type expresses HsOr370 .…”

“…Interestingly, when we reanalyzed the published data from Drosophila snRNA-seq ( 32 ), we found that a few Ir but no Or genes are expressed in glial and support cells. As these cells are derived from the same developmental lineage as ORNs ( 32, 42 ), it is tempting to speculate that certain Drosophila Ir and Harpegnathos Or genes are turned on in non-neuronal cells under the same regulatory process as in ORNs. Leaky Or expression has been observed in mammals, where Or genes are co-expressed with neighboring non- Or genes in non-neuronal cells ( 27 ).…”

“…Then, each individual neuron was classified in the following way, where + stand for expression (neighborhood p-value < 0.05) and -stands for the lack of expression: LOC105188823 / Rh50 and LOC105188598 / nompC were chosen as markers of ammoniaand mechanosensory neurons, respectively, following (52,76). Finally, cells that belong to clusters expressing LOC105181500 / repo were classified as glia (77), LOC105191850 / Mhc was used as the marker of muscle cells (32), LOC105181616 / grh-positive cells were classified as epithelium (32), and the expression of LOC105187024 / sv was used to identify neuronal support cells (32,42).…”

Osirisgene family defines the cuticle nano-patterns ofDrosophila

“…Mutations of a subset of Osiris genes have been reported (Ando et al 2019a;Scalzotto et al 2022;Scholl et al 2023), but no comprehensive mutagenesis of the Osiris gene has been performed before. Preliminary experiments to knock down Osi genes with transgenic UAS-RNAi strains (Dietzl et al 2007;Ni et al 2008) gave mixed results: some RNAi constructs caused lethality while others did not (Supplementary Table S2).…”

Conserved orthology in termite chemosensory gene families

“…Odorant Receptors (ORs) and Ionotropic Receptors (IRs) are the two arguably most important protein families involved in the detection of volatile cues in insects (Clyne et al, 1999;Gao and Chess, 1999;Vosshall et al, 1999;Benton et al, 2009;Gomez-Diaz et al, 2018). The ORs and IRs have different structures and are expressed in OSNs associated with distinct olfactory sensillum types (Benton et al, 2009;Scalzotto et al, 2022). Insect ORs are derived from insect Gustatory Receptors (GRs); ORs and GRs form a superfamily with a common phylogenetic origin (Robertson et al, 2003;Thoma et al, 2019).…”