The brown planthopper (BPH) Nilaparvata lugens (Stål) (Hemiptera: Delphacidae) is one of the most destructive rice pests in Asia. The application of insect-resistant rice cultivars is currently one of the principal means of controlling BPH. Understanding the physiological response mechanisms of BPH feeding on insect-resistant rice is the key for maintaining rice yield. Here, we measured the ecological fitness and analyzed the whole-body transcriptome and metabolome of BPH reared on susceptible cultivar Taichung Native 1 (TN1) and resistant cultivar Rathu Heenati (RH). Our results showed that RH significantly decreased the survival rate, female adult weight, honeydew secretion, the number of eggs laid per female and fat content of BPH. We identified 333 upregulated and 486 downregulated genes in BPH feeding on RH. These genes were mainly involved in energy metabolism, amino acid metabolism, hormone synthesis and vitamin metabolism pathways. We also detected 145 differentially accumulated metabolites in BPH reared on RH plants compared to BPH reared on TN1 plants, including multiple carbohydrates, amino acids, lipids, and some nucleosides. Combined analyses of transcriptome and metabolome showed that five pathways, including starch, sucrose, and galactose metabolism, were altered. The network for these pathways was subsequently visualized. Our results provide insights into the mechanisms of metabolite accumulation in BPH feeding on the RH rice variety. The results could help us better understand how insect-resistant rice cultivars combat BPH infestation, which is important for the comprehensive management of BPH.

Plants produce diverse secondary compounds as natural protection against microbial and insect attack. Most of these compounds, including bitters and acids, are sensed by insect gustatory receptors (Grs). Although some organic acids are attractive at low or moderate levels, most acidic compounds are potentially toxic to insects and repress food consumption at high concentrations. At present, the majority of the reported sour receptors function in appetitive behaviors rather than aversive taste responses. Here, using two different heterologous expression systems, the insect Sf9 cell line and the mammalian HEK293T cell line, we started from crude extracts of rice (Oryza sativa) and successfully identified oxalic acid (OA) as a ligand of NlGr23a, a Gr in the brown planthopper Nilaparvata lugens that feeds solely on rice. The antifeedant effect of OA on the brown planthopper was dose dependent, and NlGr23a mediated the repulsive responses to OA in both rice plants and artificial diets. To our knowledge, OA is the first identified ligand of Grs starting from plant crude extracts. These findings on rice–planthopper interactions will be of broad interest for pest control in agriculture and also for better understanding of how insects select host plants.

Terpenoids constitute a diverse group of primary and secondary metabolites that are extensively distributed in living organisms and play key roles in growth, development, and environmental adaptation. Terpenoids are derived from two isomeric precursors that are interconverted by isopentenyl-diphosphate delta-isomerase (IDI), in both the plastids and cytoplasm of plants. The plastidial pathway supplies precursors for diterpenoids and carotenoids, whereas the cytoplasmic pathway provides precursors for sesquiterpenoids and triterpenoids. A family of terpene synthases (TPSs) produce most terpenoids such as sesquiterpenes, hemiterpenes, monoterpenes, diterpenes and sesterterpenes, which in allotetraploid peanut (Arachis hypogaea L.) have been relatively underexplored. In this study, 77 AhTPS genes were identified in the peanut genome and phylogenetically classified into five subfamilies. These AhTPSs are organized in clusters across chromosomes and exhibit conserved gene structures and motifs within each subfamily. AhTPSs in the TPS-c and -e/f subfamilies, specifically copalyl diphosphate synthase (CPS) and kaurene synthase (KS), were localized to plastids through transient expression in Nicotiana benthamiana leaves. The expression of AhCPS3 was detected a significant increase in response to abscisic acid (ABA) and methyl jasmonate (MeJA), which was notably distinct from the expression patterns of other AhCPSs and AhKS. Furthermore, 12 terpenoids were identified during seed development. Module-trait correlation analysis disclosed that the expression levels of genes encoding AhCPSs (involved in diterpene biosynthesis) and phytoene synthases (AhPSYs, involved in carotenoid biosynthesis) were significantly correlated with the abundances of soyasaponins (triterpenoids) during seed development in peanut. Additionally, the gene encoding β-amyrin synthase (AhβAS), which produces the backbone of triterpenoids, was identified in a significant module and was also induced by ABA and MeJA. Protein-protein interaction networks indicated AhCPSs, AhPSYs, and AhβAS shared a common interacting protein, AhIDI. These findings provide valuable insights into the potential cross-talk in terpenoid biosynthesis across different cellular compartments.