Identification and analysis of odorant receptors expressed in the two main olfactory organs, antennae and palps, of Schistocerca americana

Abstract

Locusts depend upon their sense of smell and provide useful models for understanding olfaction. Extending this understanding requires knowledge of the molecular and structural organization of the olfactory system. Odor sensing begins with olfactory receptor neurons (ORNs), which express odorant receptors (ORs). In insects, ORNs are housed, in varying numbers, in olfactory sensilla. Because the organization of ORs within sensilla affects their function, it is essential to identify the ORs they contain. Here, using RNA sequencing, we identified 179 putative ORs in the transcriptomes of the two main olfactory organs, antenna and palp, of the locust Schistocerca americana. Quantitative expression analysis showed most putative ORs (140) are expressed in antennae while only 31 are in the palps. Further, our analysis identified one OR detected only in the palps and seven ORs that are expressed differentially by sex. An in situ analysis of OR expression suggested ORs are organized in non-random combinations within antennal sensilla. A phylogenetic comparison of OR predicted protein sequences revealed homologous relationships among two other Acrididae species. Our results provide a foundation for understanding the organization of the first stage of the olfactory system in S. americana, a well-studied model for olfactory processing.

From bristle to brain: embryonic development of topographic projections from basiconic sensilla in the antennal nervous system of the locust Schistocerca gregaria

“…In our developmental study here, we examine a sensory system in the locust Schistocerca gregaria involving basiconic-type sensilla (see Suppl. Figure 1 ; Slifer et al 1957 , 1959 ) implicated in olfaction, gustation, and mechanoreception (Hansson et al 1996 ; Ochieng et al 1998 ; Boronat-Garcia et al 2022 ; Cassau et al 2023 ). On hatching, these sensilla are found at fixed locations on only the six most distal segments (or annuli) of the antenna (Hansson et al 1996 ; Ochieng et al 1998 ; Chapman 2002 ) and project axons to the brain (see Hansson et al 1996 ).…”

“…Previous studies have shown that the distribution of sensilla on more proximal segments of acridid antennae changes during postembryonic development (Chapman and Greenwood 1986 ; Chapman 2002 ), is influenced by environmental effects (Chapman and Lee 1991 ), and varies according to diet (Chen et al 2003 ; Nakano et al 2022 ), and whether the locusts are in solitarious or gregarious phases (Greenwood and Chapman 1984 ; Ochieng and Hansson 1999 ). Expression of odorant receptors also varies by sex (Boronat-Garcia et al 2022 ), and this may account for sex-based differences in the physiological responses of olfactory neurons (Ochieng and Hansson 1999 ). Interestingly, although ecologically induced changes to functional ligands in the olfactory system of Drosophila may not affect all olfactory sensory neurons equally, the underlying neuronal wiring appears to be conserved despite ligand spectrum shifts (Keesey et al 2022 ).…”

“…These distal annuli bear a spectrum of sensilla that respond to various sensory stimuli (Hansson et al 1996 ; Ochieng et al 1998 ; Chapman 2002 ) and whose sensory neurons direct projections to the brain (see Hansson et al 1996 ). Among these sensilla are the basiconic-type bristles (see Slifer et al 1957 , 1959 ) that have been implicated in olfaction, gustation, and mechanoreception (Hansson et al 1996 ; Ochieng et al 1998 ; Boronat-Garcia et al 2022 ; Cassau et al 2023 ). Strikingly, on hatching, basiconic-type sensilla are not only found at fixed locations on an annulus, but also only on the most distal six annular segments of the antenna that form during embryogenesis (Chapman 2002 ).…”

From bristle to brain: embryonic development of labeled lines in the antennal nervous system of the locust Schistocerca gregaria

“…These apical annuli bear a spectrum of sensilla that encode environmental stimuli (Hansson et al 1996;Ochieng et al 1998; Chapman 2002) and whose sensory neurons project to the brain (see Hansson et al 1996). Among these sensilla are the basiconic-type bristles (see Slifer et al 1957Slifer et al , 1959) that have been implicated in olfaction, gustation and mechanoreception (Hansson et al 1996; Ochieng et al 1998;Boronat-Garcia et al 2022;Cassau et al 2023). The nding that on hatching, basiconic-type sensilla are found at conserved locations on each apical annular segment (Ochieng et al 1998; Chapman 2002) suggests these might serve as a model system for studying how information transfer from the antenna to the brain along labeled communication lines becomes established.…”

“…In our developmental study here we examine a labeled-line system in the locust Schistocerca gregaria involving basiconic-type sensilla (see Suppl. Figure1;Slifer et al 1957Slifer et al , 1959 implicated in olfaction, gustation and mechanoreception(Hansson et al 1996;Ochieng et al 1998;Boronat-Garcia et al 2022;Cassau et al 2023). On hatching, these sensilla are found at conserved locations on each apical segment (or annulus) of the antenna(Hansson et al 1996;Ochieng et al 1998;…”