Plant-insect interaction beyond folivory: chemical ecology of a non-folivore herbivore Leucinodes orbonalis’s interaction with its host Solanum melongena

Abstract

Plant-insect herbivore interactions have been researched mainly using folivore models. Leaf's responses to insect folivory and insect’s counter-responses have been rigorously studied. Interactions of frugivores, the fruit-feeding insects, with their host plant have not been studied. As a frugivore model, we used Leucinodes orbonalis (Lepidoptera), the eggplant shoot, and fruit borer (ESFB). It is a specialist pest of eggplant (Solanum melongena, Solanaceae). Eggplant cultivation faces severe and widespread infestation (45- 90 % yield loss) by this multi-insecticide-resistant pest. For effective integrated pest management, it is necessary to understand the chemistry of this interacting plant-pest system, where chemical ecology gives us a platform. I tried to understand eggplant-ESFB interaction during two of ESFB’s growth stages- moth and larva. We analyzed ESFB females’ eggplant variety preferences for oviposition. We observed that their preferences for different varieties varied, and they did not oviposit on the Himalayan eggplant variety RC-RL-22 (RL22). We hypothesized that eggplant volatiles influence ovipositing females’ host choices. Gas chromatography-mass spectrometry analysis showed that geraniol was released only by RL22. Its exogenous application on susceptible varieties reduced oviposition by >90%. To further validate geraniol’s role in RL22’s ESFB-deterrence, we identified eggplant’s geraniol synthase gene and confirmed its role by heterologous expression of its protein with in-vitro characterization. Then we silenced RL22’s geraniol synthase gene using virus-induced gene silencing. Geraniol biosynthesis suppression rendered RL22 ESFB-susceptible; foliar geraniol application on the geraniol synthase-silenced plants restored oviposition deterrence. We inferred that ESFB females use olfactory cues for host choice and prefer low-geraniol hosts. The use of natural compounds like geraniol, which influence the chemical ecology of oviposition can reduce the load of hazardous larvicidal pesticides. We also studied plant’s response to ESFB frugivory. We observed that ESFB infestation of fruits was associated with increased flowering at the apical buds of the infested-fruit bearing branches. Whether flowering was induced by ESFB infestation was investigated. Liquid chromatography-mass spectrometry-based phytohormone profiling revealed that after two days of ESFB frugivory, abscisic acid (ABA) was induced (~5-fold) in the fruit. It also showed that ABA was induced in the sink leaf (>3-fold) after five days of frugivory. To find whether the fruit-induced ABA moved to the leaf, we infiltrated the deuterium-labeled ABA (d6-ABA) into fruit; we observed that it was transported to leaf, indicating a frugivory-induced fruit to leaf ABA signaling. Both ABA infiltration in fruit and its application on leaf induced flowering at the apical bud similar to frugivory. We inferred that ESFB frugivory induces ABA in fruit. It acts as a long-distance signal to the leaf, where it plays role in flowering induction. From the ecological perspective, such flowering induction may help compensating for plant’s fruit loss or may ensure fruits for ESFB’s next generation. Together, our findings unfold the chemistry of fruit-frugivore interaction. Moreover, this work has agricultural applications- geraniol’s oviposition deterrence can be used in ESFB management and the knowledge of the flowering induction mechanism can be used for productivity enhancement.