Tick acetylcholinesterases mediate the repellent effect of cinnamaldehyde, a primary compound found in cinnamon oil

Abstract

Background The control and prevention of ticks and tick-borne diseases relies on chemical insecticides and repellents. Plant-derived compounds potentially represent new and safer repellents. Cinnamaldehyde, a component of cinnamon oil, exhibits antibacterial, anti-inflammatory, acaricidal and repellent activity against ticks. Here we studied the molecular mechanism of the repellent effects of cinnamaldehyde on ticks. Methods Assessment of cinnamaldehyde as a tick repellent was conducted using a Y-tube olfactometer, transcriptomics and metabolomic analyses. Nymphs were exposed to cinnamaldehyde for 30 min, and the tick acetylcholinesterase (AchE) family was cloned and characterized. The role of AchE in cinnamaldehyde repellency was elucidated through the specific activity of the enzyme, electrophysiology, RNA interference and repellency tests. Results A 2% cinnamaldehyde treatment resulted in more than 90% nymph repellency within 6 h. Nymphs were exposed to cinnamaldehyde for 30 min, and subsequent transcriptome and metabolome analyses revealed the involvement of AchE in the response process. The HL-AchE family was cloned and functionally explored. AchE was transcribed in all tick developmental stages and tissues. Following cinnamaldehyde treatment, the transcript and protein levels of AchE were altered, and the specific activity of the enzyme significantly increased. RNAi was used to validate these findings. Following RNAi, electroantennography (EAG) tests demonstrated a significant decrease in response to various repellents as well as a significant decrease in repellency. Conclusions AchE mediates cinnamaldehyde-induced tick repellency, and the results provide insights into the mechanism of plant-derived tick repellents.