Sex pheromone receptors of the lightbrown apple moth, Epiphyas postvittana, support a second major pheromone receptor clade within the Lepidoptera

Authors: YUVARAJ, JOTHI - Lund University; JORDAN, MELISSA - New Zealand Institute Of Plant & Food Research; ZHANG, DAN-DAN - Lund University; ANDERSSON, MARTIN - Lund University; LÖFSTEDT, CHRISTER - Lund University; NEWCOMB, RICHARD - New Zealand Institute Of Plant & Food Research; Corcoran, Jacob

Submitted to: Journal of Insect Biochemistry and Molecular Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/27/2021
Publication Date: 12/29/2021
Citation: Yuvaraj, J., Jordan, M.D., Zhang, D., Andersson, M., Löfstedt, C., Newcomb, R.D., Corcoran, J. 2021. Sex pheromone receptors of the lightbrown apple moth, Epiphyas postvittana, support a second major pheromone receptor clade within the Lepidoptera. Journal of Insect Biochemistry and Molecular Biology. 141. Article 103708. https://doi.org/10.1016/j.ibmb.2021.103708.
DOI: https://doi.org/10.1016/j.ibmb.2021.103708

Interpretive Summary: The lightbrown apple moth, Epiphyas postvittana, is a highly invasive agricultural pest native to Australia which has been introduced to several regions of the world including Oceania, North America and Europe. The larvae of this pest cause reduced production in various horticultural crops, including apples and pears, by damaging leaves which leads to reduced plant growth and fruit production. Historically, the pest has been controlled through the use of insecticides and natural predators, however more recently control tactics have shifted towards the use of the moth’s own sex pheromone compounds to trap the pest and to interfere with its ability to reproduce. While these mating disruption strategies have proven somewhat effective in controlling the lightbrown apple moth, they could potentially be improved or enhanced through a better understanding of how the moth detects sex pheromones in the environment. Previously, using a genetic approach, we identified 70 odorant receptors of which ten were identified as being potential sex pheromone receptors based on phylogenetics and gene expression analyses. In this study we expressed the ten receptors in two different in vitro assay systems and tested their ability to respond to the sex pheromone compounds used by this moth. We found that six of these receptors responded to biologically relevant sex pheromone compounds. These results will serve as a foundation for future studies in which these receptors are targeted using molecular or pharmacological approaches in an effort to develop additional tools to control this agricultural pest.

Technical Abstract: Sex pheromones facilitate species-specific sex communication within the Lepidoptera. They are detected by specialized pheromone receptors (PRs), most of which found to date fall into a single monophyletic receptor lineage (frequently referred to as “the PR clade”) within the odorant receptor (OR) family. Here we investigated the PRs of the invasive horticultural pest, Epiphyas postvittana, commonly known as the lightbrown apple moth. Ten candidate PRs were selected based on their male-biased expression in antennae or their relationship to the PR clade for assessment of function in both HEK293 cells and Xenopus oocytes. Of these, six ORs responded to E. postvittana (‘Epos’) sex pheromone components, including both behavioral agonists (male attractants) and antagonists which inhibit sex pheromone attraction in males. In phylogenies, four of the characterized receptors (EposOR1, 6, 7 and 45) fall within the PR clade and two other male-biased receptors (EposOR30 and 34) group together well outside the PR clade. This new clade of pheromone receptors includes the receptor for (E)-11-tetradecenyl acetate (EposOR30), which is the main component of the sex pheromone blend for this species. Interestingly, receptors of the two clades do not segregate by preference for compounds associated with behavioral response (agonist or antagonist), isomer type (E or Z) or functional group (alcohol or acetate), with examples of each scattered across both clades. Phylogenetic comparison with PRs from other species reveals a second major clade of lepidopteran ORs including, EposOR30 and 34, that has been co-opted into sex pheromone detection across the Lepidoptera. This second clade of sex pheromone receptors has an origin that likely predates the split between the major lepidopteran families.