Diel modulation of perireceptor activity influences olfactory sensitivity in diurnal and nocturnal mosquitoes

Abstract

Olfaction and diel-circadian rhythm regulate different behaviors, including host-seeking, feeding, and locomotion, in mosquitoes that are important for their capacity to transmit disease. Diel-rhythmic changes of the odorant-binding proteins (OBPs) in olfactory organs are primarily accountable for olfactory rhythmicity. To better understand the molecular rhythm regulating nocturnal and diurnal behaviors in mosquitoes, we performed a comparative RNA-sequencing study of the peripheral olfactory and brain tissues of female Anopheles culicifacies and Aedes aegypti. Data analysis revealed a significant upregulation of genes encoding: OBPs and xenobiotic-metabolizing enzymes including Cytochrome P450 (CYP450) during photophase in Aedes aegypti and the dusk-transition phase in Anopheles culicifacies, hypothesizing their possible function in the regulation of perireceptor events and olfactory sensitivity. RNA interference studies and application of CYP450 inhibitors, coupled with electroantennographic recordings with Anopheles gambiae and Aedes aegypti, established that CYP450 plays a role in odorant detection and antennal sensitivity. Furthermore, brain tissue transcriptome and RNAi-mediated knockdown revealed that daily temporal modulation of neuronal serine proteases may have a crucial function in olfactory signal transmission, thereby affecting olfactory sensitivity. These findings provide a rationale to further explore the species-specific rhythmic expression pattern of the neuro-olfactory encoded molecular factors, which could pave the way to develop and implement successful mosquito control methods.

Keywords

central clock; cytochrome P450; electroantennography; olfaction; serine protease; transcriptome; xenobiotic-metabolizing enzyme

Published in

The Febs Journal
2025
Publisher: WILEY

SLU Authors

• Pelletier, Julien

  • Department of Plant Protection Biology, Swedish University of Agricultural Sciences
    

• Gupta, Satyajeet

  • Department of Plant Protection Biology, Swedish University of Agricultural Sciences
    

• Ignell, Rickard

  • Department of Plant Protection Biology, Swedish University of Agricultural Sciences
    

UKÄ Subject classification

Molecular Biology
Behavioral Sciences Biology

Publication identifier

• DOI: https://doi.org/10.1111/febs.17418

Permanent link to this page (URI)

https://res.slu.se/id/publ/140651