Predicting the insecticide-driven mutations in a crop pest insect: Evidence for multiple polymorphisms of acetylcholinesterase gene with potential relevance for resistance to chemicals

Abstract

The silverleaf whitefly Bemisia tabaci (Gennadius, 1889) (Homoptera: Aleyrodidae) is a serious invasive herbivorous insect pest worldwide. The misuse and excessive use of pesticides hasve progressively selected B. tabaci specimens, progressively reducing the effectiveness of the treatments, and ultimately ending in the selection of pesticide-resistantce strains. The management of this crop pest has thus become challenging owing to the high levels of resistance to all major classes of recommended insecticides, including organophosphates (OPs). Here, we used in silico techniques for detecting molecular mutations in ace1 gene from naturally occurring B. tabaci variants, and monitor the presence and frequency of the detected mutations from 30 populations of the silver whitefly from Egypt and Pakistan. We found several point mutations in ace1-type acetylcholinesterase (ace1) in the studied B. tabaci B variants (MEAM1) naturally occurring in the field. By comparing ace1 sequence data and point mutations with those reportedfrom on an organophosphate-susceptible and an organophosphate-resistant strains of B. tabaci (SUD-S), and to ace1 sequence data retrieved from GenBank for that species and to nucleotide polymorphisms from other arthropods, we identified novel mutations that could potentially influence insecticide resistance. Seven Egyptian field strains had 100% homology with the fragment of the Israeli B. tabaci susceptible allele (SUD-SUD), revealing a high conservation of the sequence/nucleotide, and/or possible missense mutations. We also report novel amino acid substitutions (S369W, C316W, P317G, and P317F) as likely candidates conferring resistance to organophosphates. Indeed, the location of these mutations, which we visualized on the 3D crystal structure of acetylcholinesterase, occur lose to the access of the active site gorge of the enzyme. The phylogenetic analysis revealed that these novel gene sequences appeared at the top of the clade in the tree, suggesting that the reported novel point mutations have evolved recentlyHomology modeling and molecular docking analyses were performed to determine if the mutation-induced changes in form 1 acetylcholinesterase (AChE1) structure could confer resistance to carbamate and organophosphate insecticides. Mutations had small effects on binding energy (ΔGb) interactions between mutant AChE1 and insecticides; they altered the conformation of the peripheral anionic site of AChE1, and modified the enzyme surface, and these changes have potential effects on the target-site sensitivity. Altogether, the results from this study provides information on genic variants of B. tabaci ace1 for future monitoring insecticide resistance development and report a potential case of environmentally driven gene variations.

Insights into insecticide-resistance mechanisms in invasive species: Challenges and control strategies

“…There are four major types of target sites such as 1) The insensitivity of acetylcholine esterase (AChE) has been identified as an essential mechanism for pesticide resistance in numerous agricultural insect pests to carbamates and organophosphates ( Renault et al, 2022 ). Esterases are a diverse family of enzymes responsible for breaking down a wide range of ester bonds in both endogenous and exogenous substrates ( Memarizadeh et al, 2011 ) and play important roles in the insect’s ability to eliminate the toxic effects of insecticides.…”

Fitness costs of resistance to insecticides in insects

“…There have been reports of resistance to many organophosphate and carbamate chemicals ( Low et al, 2013 ) in Liriomyza sativae ( Askari-Saryazdi et al, 2015 ), Drosophila melanogaster ( Hubhachen et al, 2022 ), B. tabaci ( Renault et al, 2023 ) with a reduction or increase in acetylcholinesterase sensitivity as the major resistance mechanism. Metabolic enzymes as the driving force for altered susceptibility is also prevalent, for example, in M. domestica against chlorantraniliprole,- utilizing cytochrome P450 monooxygenase and esterase detoxifying enzymes ( Shah and Shad, 2020 ).…”

Limited genetic variability and spatial population structure in grasshoppers between natural and metal-contaminated areas in Egypt

“…Various forms of pollution can significantly alter the genetic composition of populations and influence genetic variation through 4 primary mechanisms: (i) increased mutation rates; (ii) directional selection favoring tolerant genotypes; (iii) genetic bottlenecks; and (iv) altered migration patterns ( Mussali-Galante et al 2014 ). Numerous studies have examined contaminant exposure effects on the genetics of both terrestrial ( Grzywacz et al 2012 , Giska et al 2015 , Renault et al 2023 ) and aquatic ( Gouin et al 2019 , 2023 , Švara et al 2022 ) populations. In addition to toxicants, natural phenomena like mutations, selection, stochastic processes, and migration can modify the genetic variability of populations ( Mussali-Galante et al 2014 ).…”