New insight into foregut functions of xenobiotic detoxification in the cockroach Periplaneta americana

Abstract

The physiological functions of insect foregut, especially in xenobiotic detoxification, are scarcely reported because of unimportance in appearance and insufficient molecular information. The cockroach Periplaneta americana, an entomological model organism, provides perfect material to study physiological functions of foregut tissue due to its architectural feature. Through Illumina sequencing of foregut tissue from P. americana individuals (control) or insects treated with cycloxaprid, as a novel neonicotinoid insecticide, 54 193 166 clean reads were obtained and further assembled into 53 853 unigenes with an average length of 366 bp. Furthermore, the number of unigenes involved in xenobiotic detoxification was analyzed, mainly including 70 cytochrome P450s, 12 glutathione S-transferases (GSTs), seven carboxylesterases (CarEs) and seven adenosine triphosphate-binding cassette (ABC) transporters. Compared to control, the expression of 22 xenobiotic detoxification unigenes was up-regulated after cycloxaprid application, mainly containing 18 P450s, one GST, two CarEs and one ABC adenosine triphosphate transporter, indicating that the oxidation-reduction was the major reactive process to cycloxaprid application. Through quantitative real-time polymerase chain reaction analysis, the expression of selected unigenes (six P450s, one GST and one CarE) was up-regulated at least two-fold following cycloxaprid treatment, and was generally in agreement with transcriptome data. Compared to the previous midgut transcriptome of P. americana, it looks like the expressive abundance of the xenobiotic detoxification unigenes might be important factors to the detoxifying functional differences between foregut and midgut. In conclusion, insect foregut would also play important roles in the physiological processes related to xenobiotic detoxification.

An Antenna-Abundant Glutathione S-Transferase BdGSTd8 Participates in Detoxification of Two Organophosphorus Insecticides in Bactrocera dorsalis (Hendel)

“…In addition to insecticide induction assays, investigating tissue-specific expression patterns could also further contribute to the identification of resistance gene functions. Usually, detoxification genes are abundant in insect tissues such as Malpighian tubule, midgut, and fat body and play an important role in insecticide resistance. , In Plutella xylostella, PxGSTu is highly expressed in the Malpighian tubule and midgut and directly metabolizes chlorantraniliprole . Similarly, it has also been shown that resistance-related P450s genes are abundant in the Malpighian tubule and midgut with clothianidin resistance in Bradysia odoriphaga .…”

Rapid and Selective Absorption of Plant Defense Compounds From the Gut of a Sequestering Insect

“…In addition, lipophilic insecticides have been shown to be taken up into foregut tissue of the honeybee Apis mellifera ( Conner et al, 1978 ). The foregut may even play a role in insecticide detoxification, as treatment of the cockroach Periplaneta americana with the neonicotinoid insecticide cycloxaprid resulted in an upregulation of 22 putative xenobiotic detoxification genes in foregut tissue ( Zhang et al, 2018 ). Another study proposed that a sugar receptor that is strongly expressed in the foregut of larvae of the cotton bollworm Helicoverpa armigera (Noctuidae) is involved in regulating feeding behavior ( Xu et al, 2012 ).…”

Molecular Insights into the Insensitivity of Lepidopteran Pests to Cycloxaprid

“…furcifera and the cockroach P. Americana, respectively. However, in this study, only one CYP450 gene (CYP338) was upregulated in O.…”

“…For the white-backed planthopper Sogatella furcifera, 10 cytochrome P450 monooxygenase (CYP450) genes, 1 microsomal glutathione S-transferase (GST) gene, and 1 acetylcholinesterase gene were upregulated in response to a high-dose CYC treatment, whereas 5 CYP450 genes, 1 GST gene, and 2 carboxylesterase genes were upregulated in response to a low-dose CYC treatment . For the cockroach Periplaneta americana, 18 CYP450 genes, 1 GST gene, and 2 carboxylesterase genes were upregulated after a CYC treatment . In addition to target alteration and metabolic enhancement, penetration resistance is also a common mechanism of insecticide tolerance or resistance. − However, the genes involved in cuticle penetration have not been investigated in CYC-treated insects.…”

“…Transcriptomic technology is often used to study the interaction mechanisms between insects and pesticide molecules to identify the potential genes responsible for their tolerance or resistance. − The transcriptomic responses of several insect pests to CYC have been investigated, and different kinds of CYC-responsive genes have been identified. After continuous exposure to CYC, a 10-fold resistant strain of the small brown planthopper Laodelphax striatellus was selected, in which the transcripts of the nAChR α1 and β1 subunits were upregulated by 9.60-fold and 3.36-fold, respectively .…”