The Sensilla-Specific Expression and Subcellular Localization of SNMP1 and SNMP2 Reveal Novel Insights into Their Roles in the Antenna of the Desert Locust Schistocerca gregaria

Abstract

Insect olfactory sensilla house olfactory sensory neurons (OSNs) and supports cells (SCs). The olfactory sensory processes require, besides the odorant receptors (ORs), insect-specific members of the CD36 family, named sensory neuron membrane proteins (SNMPs). While SNMP1 is considered to act as a coreceptor in the OR-mediated detection of pheromones, SNMP2 was found to be expressed in SCs; however, its function is unknown. For the desert locust, Schistocerca gregaria, we previously visualized mRNA for SNMP1 in OSNs and SNMP2 mRNA in cells associated with OSN clusters. Towards an understanding of their functional implication, it is imperative to explore the cellular and the subcellular localization the SNMP proteins. Therefore, we have generated polyclonal antibodies against SNMP1 and SNMP2 and used fluorescence immunohistochemistry (FIHC) to visualize the SNMP proteins. We found SNMP1 in the somata and respective dendrites of all OSNs in trichoid sensilla and in subsets of OSNs in basiconic sensilla. Notably, SNMP1 was also detected in SCs of these sensilla types. In contrast, SNMP2 protein was only visualized in SCs of basiconic and coeloconic sensilla, but not of trichoid sensilla. Exploring the subcellular localization by electron microscopy using anti-SNMP1-ab and anti-SNMP2-ab revealed an immunogold labelling of SC microvilli bordering the sensillum lymph. Together our findings suggest a dual role of SNMP1 in the antenna of S. gregaria, in some OSN subpopulations in odor detection as well as in functions of some SCs, whereas the role of SNMP2 is limited to the functions of support cells.

The specific expression patterns of sensory neuron membrane proteins are retained throughout the development of the desert locust Schistocerca gregaria

“…Furthermore, a rapid activation and deactivation of pheromone-induced activity of OSNs was found to depend on SNMP1 ( Li et al., 2014 ). While functional studies on the SNMP2-type are missing, the current data demonstrate broad expression in antennal SCs ( Gu et al., 2013 ; Blankenburg et al., 2019 ; Jiang et al., 2016 ) and a localization in their microvilli membrane bordering the sensillum lymph ( Cassau et al., 2022 ). Based on these finding and its homology to the CD36 protein family of lipid receptors and transporters, a role of SNMP2 in clearing the sensillum lymph from lipophilic odorants or their degradation products has been suggested ( Cassau and Krieger, 2021 ; Forstner et al., 2008 ; Blankenburg et al., 2019 ).…”

“…Together our data suggest a role of SNMP2 limited to the functions of SCs, whereas SNMP1 seems to fulfill a dual function in the antenna of adult S. gregaria , i.e. in odor detection in OSN subpopulations as well as a function in certain SCs ( Cassau et al., 2022 ).

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“…Desert locusts, Schistocerca gregaria , were reared under crowded (gregarious) conditions as previously described ( Seidelmann et al., 2000 ; Cassau et al., 2022 ) . Briefly, 100 to 150 individuals were kept in metal cages (50 × 50 × 50 cm) with metal grids at the bottom and at two sides.…”

“…Thus, both the OSNs and the SCs of a sensillum express the proteins acting in the primary process of odor detection. In addition to OBPs and olfactory receptors, studies mainly in moths, flies and locusts ( Rogers et al., 1997 ; Benton et al., 2007 ; Jiang et al., 2016 ; Cassau et al., 2022 ; Blankenburg et al., 2019 ) have demonstrated that certain OSNs and SCs also express subtypes of so-called sensory neuron membrane proteins (SNMPs) representing another group of proteins critical in the primary process of odor detection ( Cassau and Krieger, 2021 ).…”

“…Recently, we elucidated the expression topography of the SNMP1 and SNMP2 protein in the antenna of adult S. gregaria in the gregarious phase ( Cassau et al., 2022 ). Using fluorescence immunohistochemistry (FIHC) and immunogold labelling experiments we revealed a detailed picture of their expression and localization across the OSNs and SCs of the three morphologically distinct olfactory sensilla types ( Fig.…”