Abstract
The silverleaf whitefly Bemisia tabaci (Gennadius, 1889) (Homoptera: Aleyrodidae) is a serious invasive herbivorous insect pest worldwide. The excessive use of pesticides has progressively selected B. tabaci specimens, reducing the effectiveness of the treatments, and ultimately ending in the selection of pesticide-resistant strains. The management of this crop pest has thus become challenging owing to the level of resistance to all major classes of recommended insecticides. Here, we used in silico techniques for detecting sequence polymorphisms in ace1 gene from naturally occurring B. tabaci variants, and monitor the presence and frequency of the detected putative mutations from 30 populations of the silverleaf whitefly from Egypt and Pakistan. We found several point mutations in ace1-type acetylcholinesterase (ace1) in the studied B. tabaci variants naturally occurring in the field. By comparing ace1 sequence data from an organophosphate-susceptible and an organophosphate-resistant strains of B. tabaci 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. Homology 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 provide information on genic variants of B. tabaci ace1 for future monitoring insecticide resistance development and report a potential case of environmentally driven gene variations.
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Acknowledgements
The authors thank Professor James Nation and Professor Ioannis Eleftherianos for helpful discussions and edits on former versions of the article. Dr Alaa Elgohary is acknowledged for her technical help in 3D structural modeling and for molecular docking.
Funding
DR is supported by funded by the International Research Project (IRP) “Phenomic responses of invertebrates to changing environments and multiple stress (PRICES, InEE-CNRS) and by IUF ENVIE.” The funding bodies had no effect on the design of the study and collection, analysis and interpretation of data, and on the writing of the manuscript.
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AM and DR conceived and designed the study. AM, AE, and DR analyzed the data. AM, AE, and DR interpreted the results and prepared the figures and the tables. AM and DR wrote the first version of the manuscript. AM, and DR reviewed the drafts of the manuscript.
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Supplementary information
Supplementary Information S1.
GenBank accession numbers of the silverleaf whitefly Bemisia tabaci ace-1 genes. Field strain designation, the predicted sensitivity* (R: resistant; S: susceptible) of the analyzed B. tabaci populations from Egypt are provided (DOCX 20 kb)
Supplementary Information S2.
Alignment of the AChEs’ prototype model (Torpedo californica AChE, TcAChE) and B. tabaci AChE1 (BtAChE1). In the substrate binding domain, black triangles indicate amino acid residues that have the same position in both sequences. Red and blue triangles indicate amino acid residues from B. tabaci and T. californica sequences, respectively. The amino acid residues forming the catalytic triad (active site) of BtAChE1 are S262, E388, and H501. The dagger (†) and double dagger (‡) symbols indicate numbering in TcAChE and BtAChE1 sequences, respectively. Sequence gaps were excluded from numbering. (DOCX 43 kb)
Supplementary Information S3.
Molecular phylogeny of AChE1 from B. tabaci alongside with some other insect species, constructed with the neighbor-joining method. Cluster reliability was assessed with the nonparametric bootstrapping (10000 iterations). Branch labels refer to species, common name, GenBank accession number; the status (R; resistant, S; susceptible) of the B. tabaci tested strains is indicated. The evolutionary distance among species is shown at the bottom of the figure. The tree was rooted with AChE1 of the tick Rhipicephalus microplus as an outgroup. (DOCX 540 kb)
Supplementary Information S4.
Occurrence of mutations in specific segments of AChE1-type acetylcholinesterases from a range of insects, ticks, and mites according to ESTHER database. Variations in certain amino acid residues (particularly the hollow and black boxed ones) are represented. Question marks (?) indicate the position where the mutation has occurred in the aligned sequence and was correlated to the insecticide resistance. Exclamation points (!) highlight the other mutations points that were not related to insecticide resistance. The analysis encompasses some selected insect AChE1s resistant to organophosphates and/or to carbamates. Numbering the amino acid residues in the selected B. tabaci sequence segments from the present study follows the grey-shaded B. tabaci resistant allele sequence (ABV45412.1) (Alon et al. 2008). (DOCX 268 kb)
Supplementary Information S5.
The average binding energies of the different organophosphate (A-K) and carbamate (L-V) pesticides in the wild type (WT) and in the eleven studied mutants (F392W, S369W, L370V, C316W, P317G, P317F, G251D, N252R, P253S, C329S, and L330T). (DOCX 2565 kb)
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Renault, D., Elfiky, A. & Mohamed, A. Predicting the insecticide-driven mutations in a crop pest insect: Evidence for multiple polymorphisms of acetylcholinesterase gene with potential relevance for resistance to chemicals. Environ Sci Pollut Res 30, 18937–18955 (2023). https://doi.org/10.1007/s11356-022-23309-w
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DOI: https://doi.org/10.1007/s11356-022-23309-w