Odorant receptor-mediated sperm activation in disease vector mosquitoes

Abstract

Insects, such as the malaria vector mosquito, Anopheles gambiae, depend upon chemoreceptors to respond to volatiles emitted from a range of environmental sources, most notably blood meal hosts and oviposition sites. A subset of peripheral signaling pathways involved in these insect chemosensory-dependent behaviors requires the activity of heteromeric odorant receptor (OR) ion channel complexes and ligands for numerous A. gambiae ORs (AgOrs) have been identified. Although AgOrs are expressed in nonhead appendages, studies characterizing potential AgOr function in nonolfactory tissues have not been conducted. In the present study, we explore the possibility that AgOrs mediate responses of spermatozoa to endogenous signaling molecules in A. gambiae. In addition to finding AgOr transcript expression in testes, we show that the OR coreceptor, AgOrco, is localized to the flagella of A. gambiae spermatozoa where Orco-specific agonists, antagonists, and other odorant ligands robustly activate flagella beating in an Orco-dependent process. We also demonstrate Orco expression and Orco-mediated activation of spermatozoa in the yellow fever mosquito, Aedes aegypti. Moreover, we find Orco localization in testes across distinct insect taxa and posit that OR-mediated responses in spermatozoa may represent a general characteristic of insect reproduction and an example of convergent evolution.transcriptomics | cell signaling | gamete | chemical ecology | Culicidae

A conditional Orco requirement in the somatic cyst cells for maintaining spermatids in a tight bundle in Drosophila testis

“…Previous studies have indicated orco expression in the testes of these organisms (Pitts et al 2014). AgOrco is localized along the spermatid tails, and treatment with the Orco agonist resulted in the activation and movement of the spermatozoa (Pitts et al 2014).…”

“…Thus, it is essential for the functioning of all ORs. Also, Orco plays a critical role in sperm activation in A. Gambea (Pitts et al 2014). The AgOrco is reported to localize along the sperm tail (Pitts et al 2014).…”

Molecular characterization of sugar taste receptors in the cotton bollworm Helicoverpa armigera

“…Ocro-specific agnoists, antagonists, as well as other odorant compounds could robustly activate flagella beating. Therefore, chemosensory receptors may mediate sperm activation in insects (Pitts et al 2014). Another study reported that sugar detection is related to ovarian maturation in female Phormia regina (Solari et al 2015).…”

“…Five sugar GRs were first identified from the model insect of Lepidoptera, Bombyx mori (Wanner and Robertson 2008). Since then, a number of lepidopteran sugar GRs were identified and studied (Pitts et al 2014;Zhang et al 2011). Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), one of the most destructive agricultural pests, feed on a large number of cultivated crops including cotton, tomato, soybeans, and corn.…”

Pest Control Compounds Targeting Insect Chemoreceptors: Another Silent Spring?

“…However, whether Orco is activated or inhibited, the negative impact on the insect sense of smell, and thus behavior, may well be similar. Additionally, Orco has been shown to be present in the testes and spermatozoa of insects, with Orco agonists and antagonists affecting flagella beating and thus the movement of mosquito spermatozoa (Pitts et al, 2014). These compounds might therefore also directly and broadly interfere with insect reproduction, and by disrupting multiple aspects of the insect life cycle could potentially be very efficient in insect control.…”