An analysis of the tissue transcriptome of Spodoptera picta responding to lycorine

Food is a determining factor for successful growth and development. Insects have evolved tolerance and resistance to plant secondary compounds through long-term natural selection and coevolution, providing plasticity in feeding behavior; however, the potential underlying molecular mechanisms have seldom been investigated. The lily caterpillar, Spodoptera picta, shows a notable dietary preference for the lycorine-containing giant Crinum lily, Crinum asiaticum. Here we investigated the oligophagous larvae of S. picta and compared their host plants to those of the polyphagous tobacco cutworm, S. litura. These noctuid moths are closely related, having diverged only about 3 million years ago1. Comparative genomics, gene annotation, and phylogenetic analysis revealed a high genetic similarity (over 98%) encoding gustatory receptor and detoxification-related gene families between these two species, suggesting S. picta is also a possible polyphagous insect. This was supported by finding that S. picta can feed on a variety of unrelated plants. Subsequent LC-MS/MS analysis and transcriptomic and RNA interference studies in S. picta demonstrated that detoxification using genes SpicGST03, SpicGST33 and SpicABCC2 facilitate the excretion of 20-30% of lycorine obtained from feeding on C. asiaticum through their excrement whereas S. litura only excretes 2% of this toxin. Additionally, S. picta larvae accumulate lycorine on their cuticle, an effective defense against natural predators, revealing an unreported mechanism underlying a pivotal advantage for the preference of S. picta for its host plant C. asiaticum. Collectively, our findings highlight the roles of insect GSTs and ABC transporters in host plant adaptation, provide insights into the molecular basis for the evolutionary transition from polyphagy to oligophagy in these two species, and suggest potential molecular targets for studying plant-insect interactions.