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The genus Spodoptera (Lepidoptera: Noctuidae) comprises some of the most polyphagous and destructive agricultural pests worldwide. The success of many species of this genus is due to their striking abilities to adapt to a broad range of host plants. Superfamilies of detoxification genes play a crucial role in the adaption to overcome plant defense mechanisms mediated by numerous secondary metabolites and toxins. Over the past decade, a substantial amount of expression data in Spodoptera larvae was produced for those genes in response to xenobiotics such as plant secondary metabolites, but also insecticide exposure. However, this information is scattered throughout the literature and in most cases does not allow to clearly identify candidate genes involved in host-plant adaptation and insecticide resistance. In the present review, we analyzed and compiled information on close to 600 pairs of inducers (xenobiotics) and induced genes from four main Spodoptera species: S. exigua, S. frugiperda, S. littoralis and S. litura. The cytochrome P450 monooxygenases (P450s; encoded by CYP genes) were the most upregulated detoxification genes across the literature for all four species. Most of the data was provided from studies on S. litura, followed by S. exigua, S. frugiperda and S. littoralis. We examined whether these detoxification genes were reported for larval survival under xenobiotic challenge in forward and reverse genetic studies. We further analyzed whether biochemical assays were carried out showing the ability of corresponding enzymes and transporters to breakdown and excrete xenobiotics, respectively. This revealed a clear disparity between species and the lack of genetic and biochemical information in S. frugiperda. Finally, we discussed the biological importance of detoxification genes for this genus and propose a workflow to study the involvement of these enzymes in an ecological and agricultural context.

International audience; Arthropods have well adapted to the vast array of chemicals they encounter in their environment. Whether these xenobiotics are plant allelochemicals or anthropogenic insecticides one of the strategies they have developed to defend themselves is the induction of detoxification enzymes. Although upregulation of detoxification enzymes and efflux transporters in response to specific inducers has been well described, in insects, yet, little is known on the transcriptional regulation of these genes. Over the past twenty years, an increasing number of studies with insects have used advanced genetic tools such as RNAi, CRISPR/Cas9 and reporter gene assays to dissect the genomic grounds of their xenobiotic response and hence contributed substantially in improving our knowledge on the players involved. Xenobiotics are partly recognized by various ?xenobiotic sensors? such as membranebound or nuclear receptors. This initiates a molecular reaction cascade ultimately leading to the translocation of a transcription factor to the nucleus that recognizes and binds to short sequences located upstream their target genes to activate transcription. To date, a number of signaling pathways were shown to mediate the upregulation of detoxification enzymes in arthropods and to play a role in either metabolic resistance to insecticides or hostplant adaptation. These include nuclear receptors AhR/ARNT and HR96, GPCRs, CncC and MAPK/CREB. Recent work reveals that upregulation and activation of some components of these pathways as well as polymorphism in the binding motifs of transcription factors are linked to insects? adaptive processes. The aim of this mini-review is to summarize and describe recent work that shed some light on the main regulatory routes of detoxification gene expression in insects.

The Colorado potato beetle (CPB),Leptinotarsa decemlineata(Say), is an agricultural pest of solanaceous crops which has developed insecticide resistance at an alarming rate. Up to this point, little consideration has been given to unintended, or inadvertent effects that non-insecticide xenobiotics may have on insecticide susceptibility inL. decemlineata. Fungicides, such as chlorothalonil and boscalid, are often used to control fungal pathogens in potato fields and are applied at regular intervals whenL. decemlineatapopulations are present in the crop. In order to determine whether fungicide use may be associated with elevated levels of insecticide resistance inL. decemlineata, we examined phenotypic responses inL. decemlineatato the fungicides chlorothalonil and boscalid. Using enzymatic and transcript abundance investigations we also examined modes of molecular detoxification in response to both insecticide (imidacloprid) and fungicide (boscalid and chlorothalonil) application to more specifically determine if fungicides and insecticides induce similar metabolic detoxification mechanisms. Both chlorothalonil and boscalid exposure induced a phenotypic, enzymatic and transcript response inL. decemlineatawhich correlates with known mechanisms of insecticide resistance.Key MessagesPrior-exposure to a fungicidal application changes the phenotypic response ofLeptinotarsa decemlineatato the insecticide imidaclopridBoth a fungicide and insecticide application activates similar molecular mechanisms of detoxification inLeptinotarsa decemlineataFungicidal xenobiotics may contribute to insecticide resistance inLeptinotarsa decemlineataAuthor Contribution StatementJC, SS, CB, AH, and RG conceived and designed research. JC, AC, DA, TD, and BS conducted experiments. JC and AC analyzed data. JC and RG wrote the manuscript. All authors read and approved the manuscript.