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 (Z9‐14:Ac) and (Z)‐7‐dodecenyl acetate (Z7‐12:Ac) (100:3.9) 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 Z9‐14:Ac, but also comparably to (Z,E)‐9,12‐tetradecadienyl acetate (Z9,E12‐14:Ac) and weakly to (Z)‐9‐dodecenyl acetate (Z9‐12:Ac). Both SfruOR56 and SfruOR62 are specifically tuned to the minor sex pheromone component Z7‐12:Ac with varying intensities and sensitivities. In addition, SfruOR6 is activated only by Z9,E12‐14:Ac, and SfruOR16 by both (Z)‐9‐tetradecenol (Z9‐14:OH) and (Z)‐9‐tetradecenal (Z9‐14:Ald). 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 Z7‐12:Ac. Finally, using wind tunnel assay, we demonstrate that both Z9,E12‐14:Ac and Z9‐14:OH 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.

Identification and Characterization of Chemosensory Receptors in the Pheromone Gland-Ovipositor of Spodoptera frugiperda (J. E. Smith)

“…Two ORs in S . frugiperda , including SfruOR13 and SfruOR16, clustered in the lepidopteran PR clade [ 55 , 56 ] ( Figure 1 ).…”

“…Guo JM (2020) and Guo H (2022) had cloned the PR genes of S . frugiperda for functional studies [ 55 , 56 ]. Functional analyses by the Xenopus oocyte or Drosophila OR67d neuron recording system demonstrated that SfruOR13 robustly responds to the major sex pheromone component Z 9-14: Ac [ 55 , 56 ].…”

“…frugiperda for functional studies [ 55 , 56 ]. Functional analyses by the Xenopus oocyte or Drosophila OR67d neuron recording system demonstrated that SfruOR13 robustly responds to the major sex pheromone component Z 9-14: Ac [ 55 , 56 ]. SfruOR16 expressed in Drosophila OR67d neurons was strongly activated by Z 9-14: OH, which was demonstrated to be the antagonists of S .…”

“…SfruOR16 expressed in Drosophila OR67d neurons was strongly activated by Z 9-14: OH, which was demonstrated to be the antagonists of S . frugiperda sex pheromones [ 56 ]. The behavioral responses of H .…”

“…Studies of chemosensory receptors in S . frugiperda are currently confined to antennal transcriptome analysis and functional investigation of PRs [ 54 , 55 , 56 ]. The identity of the chemosensory genes in the S .…”