Molecular and chemical ecology of eggplant-insect herbivore interaction

Abstract

Lepidopteran pests cause severe crop losses. Synthetic pesticides are injudiciously used to control them, which causes environmental and health hazards. Therefore, the use of safe and eco-friendly botanicals as biopesticides is rapidly increasing. Spodoptera litura Fabricius (armyworm) is a polyphagous multi-insecticide-resistant lepidopteran pest that infests >100 plant species, including several crops. We explored secondary metabolite-rich Solanum melongena L. (eggplant) as a biopesticide source. By integrating metabolomics and reverse genetics approaches, we identified 5-O-caffeoylquinic acid (chlorogenic acid; CGA), an eggplant secondary metabolite, as a biopesticide against it. It caused high armyworm larval mortality. Nutritional indices revealed that CGA ingestion hampered larval digestion and metabolism, leading to slower larval growth and delayed pupation and eclosion. CGA biosynthesis gene-silenced eggplants were rendered more susceptible to armyworm infestation; resistance was restored upon CGA complementation. We also discovered the armyworm's counter-adaptation against CGA; first, it cleaved CGA using a carboxylesterase (CE) and then converted it to a non-toxic isomer 3-O-caffeoylquinic acid (neochlorogenic acid; neoCGA). By silencing this gene using plant-mediated RNAi (PMRi), we generated a loss-of-function phenotype, which showed high CGA-susceptibility. Our RNAi formulation developed for foliar application showed a similar effect. Lastly, the field application of CGA did not show the effect on the beneficial insects. Thus, CGA is a promising biopesticide candidate for the field trial phase against armyworm. In light of our findings, we propose a novel pest management strategy combining plant-based candidate insecticide(s) and PMRi-mediated silencing of counter-adaptation genes to combat armyworm and other lepidopteran pests in agronomically important plants.