Molecular evidence for the role of the ovipositor of the fall armyworm: Where to lay or not to lay?

Abstract

Oviposition behavior in insects has received considerable attention, but studies have mainly focused on the antennae, neglecting the role of the ovipositor. In this study, we investigated the functional characteristics of the ovipositor in oviposition site selection by the fall armyworm (FAW) Spodoptera frugiperda, a destructive invasive pest of maize and other cereals. In oviposition choice assays females exhibited significant repellency to isothiocyanate (ITC), volatiles specific to non-preferred cruciferous plants. Females retained repellency to ITC or attraction to maize volatiles even after antennae removal. Scanning electron microscopy indicated the presence of olfactory-associated sensilla on the ovipositor. Comparative transcriptome analysis and in vitro functional studies showed that S. frugiperda odorant binding protein 30 (SfruOBP30), exclusively expressed in the ovipositor, displayed a broad sensitivity toward 18 maize volatiles and 10 ITC compounds. Site-directed mutant assay revealed that Ser71 and Ser85 were the key binding sites for SfruOBP30 interacting with ITCs and key maize volatiles, respectively. Silencing the expression of SfruOBP30 resulted in the loss of bias in oviposition of FAW, significantly inhibiting their ability to avoid ITCs and locate the maize substrate. Overall, we propose that the ovipositor does not just seek out advantageous conditions for immature stages but more importantly, avoids potential risks during the oviposition process. Apparently, the involvement of SfruOBP30 plays a critical role in detecting both beneficial and harmful substances during this intricate process.