Functional analysis of pheromone receptor repertoire in the fall armyworm, Spodoptera frugiperda.

ABSTRACT

BACKGROUND: The fall armyworm, Spodoptera frugiperda (J. E. Smith), is a polyphagous moth species that is spreading all around the globe. It uses (Z)-9-tetradecenyl acetate (Z9-14Ac) and (Z)-7-dodecenyl acetate (Z7-12Ac) (1003.9) as essential sex pheromone components. However, our understanding of the molecular basis of pheromone detection of S. frugiperda is still incomplete. RESULTS: Herein, we identified six PRs, i.e. SfruOR6, 11, 13, 16, 56, and 62, by transcriptome sequencing. Subsequently, we heterologously expressed them in Drosophila OR67d neurons and determined their response spectra with a large panel of sex pheromones and analogs. Among them, SfruOR13-expressing neurons strongly respond to the major sex pheromone component Z9-14Ac, but also comparably to (Z,E)-9,12-tetradecadienyl acetate (Z9,E12-14Ac) and weakly to (Z)-9-dodecenyl acetate (Z9-12Ac). Both SfruOR56 and SfruOR62 are specifically tuned to the minor sex pheromone component Z7-12Ac with varying intensities and sensitivities. In addition, SfruOR6 is activated only by Z9,E12-14Ac, and SfruOR16 by both (Z)-9-tetradecenol (Z9-14OH) and (Z)-9-tetradecenal (Z9-14Ald). However, the OR67d neurons expressing SfruOR11 remain silent to all compounds tested, a phenomenon commonly found in the OR11 clade of Noctuidae species. Next, using single sensillum recording, we characterized four sensilla types on the antennae of males, namely A, B, C and D types that are tuned to the ligands of PRs, thereby confirming that S. frugiperda uses both SfruOR56 and SfruOR62 to detect Z7-12Ac. Finally, using wind tunnel assay, we demonstrate that both Z9,E12-14Ac and Z9-14OH act as antagonists to the sex pheromone. CONCLUSION: We have deorphanized five PRs and characterized four types of sensilla responsible for the detection of pheromone compounds, providing insights into the peripheral encoding of sex pheromones in S. frugiperda.