Over hundreds of millions of years of co-adaptation, co-evolution, and co-speciation, intricate and sophisticated interactions have developed between plants and herbivorous insects (Fürstenberg-Hägg et al., 2013, Scriber, 2013). In agricultural production, the interaction between plants and herbivorous insects is a prominent issue due to the annual crop output losses exceeding 15 % attributed to pest infestations (Mitchell et al., 2016, Nallu et al., 2018). In response to herbivorous insects, plants have evolved chemical defenses comprised of a wide array of secondary metabolites to deter herbivory (van der Linden et al., 2021). Consequently, herbivorous insects have evolved methods for detoxification or tolerance to potentially toxic plant secondary metabolites (Renwick and Chew, 1994, Näsvall et al., 2021). Herbivorous insects typically exhibit adaptations for feeding on a limited array of host plants that possess analogous secondary metabolites, and intricate defense mechanisms have evolved to counteract the diverse array of plant defense compounds (Renwick and Chew, 1994, Vogel et al., 2014). The quality of plants, influenced by specific nutrient components like carbon and nitrogen, is regarded as a significant factor in herbivorous insect fitness, impacting essential behaviors such as feeding, mating, and oviposition (Awmack and Leather, 2002, Simon et al., 2015, Carrasco et al., 2015). Therefore, the adaptation of herbivorous insects to plants is vital for their survival and colonization across diverse environments (Janz et al., 2006).

Lepidoptera constitutes one of the major groups of herbivorous insects globally, with nearly all Angiosperms and Gymnosperms susceptible to caterpillar infestation (Zhang et al., 2021). Diverse traits for adaptation to plant defenses in lepidopteran insects have been identified. Salivary proteins synthesized by lepidopteran insects may facilitate host plant adaptation by inhibiting plant defenses, including glucose oxidase (GOX) in Helicoverpa armigera and Manduca sexta, as well as apyrase in Helicoverpa zea (Eichenseer et al., 2010, Wu et al., 2012, Kallure et al., 2022). The prevalence of detoxifying and metabolic enzymes in the gut of lepidopteran insects may be another well-documented trait. Myrosinase and glucosinalate sulfatase have been identified as participants in the detoxification of glucosinolates and their metabolites in Plutella xylostella (Yang et al., 2012, Heidel-Fischer et al., 2019). Moreover, detoxification enzymes, including cytochrome P450 monooxygenases (P450s), carboxylesterases (CarEs), UDP-glycosyltransferases (UGTs), and glutathione S-transferases (GSTs) in lepidopteran insects, exhibited responsiveness to the detoxification of toxic chemicals present in host plants (Jin et al., 2019). Moreover, the gut microbiota constituted a significant trait for lepidopteran insects in their reaction to the plant’s defenses. Numerous studies have demonstrated that symbiotic bacteria significantly contribute to the detoxification of plant allelochemicals and enhance the fitness of host plants (Zhang et al., 2020, Sato et al., 2021).

The fall armyworm (FAW), Spodoptera frugiperda (J. E. Smith), is a predominantly herbivorous insect that has proliferated globally in recent years, presenting a significant danger to the security of global crop production (Nagoshi et al., 2020, Beuzelin et al., 2022). The larvae can feed on a diverse array of host plants, encompassing over 353 species, including maize, rice, wheat, and sorghum (Montezano et al., 2018). Due to the global epidemic, S. frugiperda garnered the attention of international plant protection professionals, and the interactions between FAW and host plants emerged as significant study focal points. The phenotype and fitness of S. frugiperda were examined when fed on various grain and oil crops, including maize, japonica and indica rice cultivars, sorghum, wheat, cotton, soybean, oilseed rape, sunflower, and solanaceous vegetables such as pepper (Capsicum annuum L.), tomato (Solanum lycopersicum Mill.), and aubergine (Solanum melongena L.) (He et al., 2021, Xie et al., 2021, Wu et al., 2021, Gopalakrishnan and Kalia, 2022, Wang et al., 2022). The mechanisms of FAW for maize and rice adaptation were elucidated. High flexibility in detoxifying gene families was deemed a crucial element in the speciation process of corn and rice strains (Silva-Brandão et al., 2017). The miRNAs in S. frugiperda in response to plant feeding were also examined (Moné et al., 2018). Recently, digesting protease enzymes, specifically trypsins (SfTry-3 and SfTry-7) and one chymotrypsin (Sfchym-9), have been identified as significant contributors to host plant adaptation (Hafeez et al., 2021a). Our prior research indicated that the growth rates of S. frugiperda larvae varied on two cruciferous vegetables, Brassica campestris and Brassica oleracea (Yuning et al., 2022). Nevertheless, the mechanisms underlying this pest’s adaptation to these two plants remain mostly unknown.

This study examined the performance of S. frugiperda when fed on two cruciferous vegetables: pakchoi (B. campestris L.) and purple cabbage (B. oleracea L.). Transcriptome and metabolome analyses were conducted in the midguts of larvae subjected to various foods for 7 days. The molecular variations in the midguts of larvae consuming diverse plants may offer novel insights into the plant adaptation strategies of S. frugiperda in relation to cruciferous vegetables and establish a basis for the management of S. frugiperda in agricultural settings.