Plant-Derived Tick Repellents Activate the Honey Bee Ectoparasitic Mite TRPA1

Abstract

We have identified and characterized the TRPA1 channel of Varroa destructor (VdTRPA1), a major ectoparasitic mite of honey bee. One of the two VdTRPA1 isoforms, VdTRPA1L, was activated by a variety of plant-derived compounds, including electrophilic compounds, suggesting that chemical activation profiles are mostly shared between arthropod TRPA1 channels. Nevertheless, carvacrol and α-terpineol activated VdTRPA1L but not a honey bee noxious-stimuli-sensitive TRPA, AmHsTRPA, and Drosophila melanogaster TRPA1. Activation of VdTRPA1L in D. melanogaster taste neurons by the above compounds was sufficient to modify the gustatory behaviors. Carvacrol and α-terpineol repelled V. destructor in a laboratory assay, and α-terpineol repressed V. destructor entry for reproduction into the brood cells in hives. Understanding the functions of parasite TRP channels not only gives clues about the evolving molecular and cellular mechanisms of parasitism but also helps in the development of control methods.

Insect TRP channels as targets for insecticides and repellents

“…41,42) In fact, plant-derived repellents carvacrol and alpha-terpineol that activate the varroa mite TRPA1L channel but not the honey bee HsTRPA channel repressed mite entry into brood cells in hives, showing some potential for the use of TRPA1-activating compounds in apiculture. 43) TRPA1 operating downstream of -Gq/phopshoplipase C signaling cascade is also required in Drosophila for the avoidance of the repellent citronellal, whereas the Anopheles gambiae TRPA1 is directly activated by citronellal. 44) The roles of Pain and Pyx in detecting noxious heat have already been mentioned above.…”

Varroa chemosensory proteins: some are conserved across Arthropoda but others are arachnid specific

“…Two transcripts were assigned to the TRP group; both possess a 'TRP' annotation in the BLAST hit and the two functionally important domains: the transient receptor ion channel domain (TRP_2, IPR013555) as well as the protein-binding site of the ankyrin repeat (IPR002110) (Peng, Kashio, et al, 2015). A local BLASTn search, using the reported Varroa VdTRPA1-L as query (accession ID: AB930121), found high similarity to one of the two TRPs in the current study (TRINITY_DN30598_c0_g1_i2, e-value = 8.81E-10).…”

“…Interestingly, all upregulated transcripts are clustered together in the phylogenetic analysis, along with other arachnid sequences, whereas transcripts not exhibiting differential expression clustered closer to D. melanogaster ENaCs. In particular, the L isoform of the receptor is activated by electrophilic compounds as well as various plant-derived tick repellents, specifically α-terpineol, which also repelled Varroa in laboratory and hive experiments (Peng, Kashio, et al, 2015). However, their expression profiles in chemosensory organs and their functions have not been evaluated.…”

“…One member, Varroa TRPA1, is particularly interesting considering its in vitro response to tick repellents (Peng, Kashio, et al, 2015), some of which are hive relevant compounds, such as nerol [one of the seven Nasanov gland components of worker honeybees (Pickett et al, 1982)]. In particular, the L isoform of the receptor is activated by electrophilic compounds as well as various plant-derived tick repellents, specifically α-terpineol, which also repelled Varroa in laboratory and hive experiments (Peng, Kashio, et al, 2015). Our observation showing upregulation of VdTRPA1-L in the Varroa forelegs compared to the rear legs further emphasizes the possible role of this transcript as a receptor for host cues.…”

α-Terpineol Induces Gastric Retention of Liquids by Inhibiting Vagal Parasympathetic Pathways in Rats

“…Some reports indicate that α-terpineol possesses inhibitory effects on nerves. In a recent study, Peng et al [18] revealed that α-terpineol activates the TRPA1 channels of Varroa destructor, a major ectoparasitic mite of the honeybee. Such findings raise the possibility that α-terpineol is a candidate to induce inhibition of nerve conduction by acting on TRP proteins.…”