CRISPR/Cas9-mediated F1534S substitution in the voltage-gated sodium channel reveals its necessity and sufficiency for deltamethrin resistance in Aedes albopictus

Guo, Yijia; Zhou, Jingni; Zhao, Yijie; Deng, Jielin; Su, Xinghua; Tang, Jianxia; Zhu, Guoding; Zhou, Xiaojie; Gu, Jiande; Yan, Guiyun; James, Anthony A.; Chen, Xiaoguang

doi:10.1007/s10340-022-01557-6

Cited by 3 publications

(23 citation statements)

References 56 publications

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“…Most resistance association studies have been conducted since the 2017 statement of Moyes et al (2017) and reveal a consistent pattern of association between the F1534S mutation and resistance to type I and type II pyrethroids at a significant level. Functional studies have confirmed a causative function of this allele to pyrethroid resistance ( Yan et al 2020 , Guo et al 2022 ). The detection of F1534S (TCC) in China, the United States, and possibly Vietnam is of concern, suggesting that this resistant genotype ( Chen et al 2016 , Xu et al 2016 , Gao et al 2018 , Li et al 2018 , Wei et al 2021 , Wu et al 2021 , Guo et al 2022 , Yuan et al 2023 ) is already spreading.…”

Section: Discussionmentioning

confidence: 89%

“…Functional studies have confirmed a causative function of this allele to pyrethroid resistance ( Yan et al 2020 , Guo et al 2022 ). The detection of F1534S (TCC) in China, the United States, and possibly Vietnam is of concern, suggesting that this resistant genotype ( Chen et al 2016 , Xu et al 2016 , Gao et al 2018 , Li et al 2018 , Wei et al 2021 , Wu et al 2021 , Guo et al 2022 , Yuan et al 2023 ) is already spreading. A recent study by Chen et al (2021) included historical samples and revealed the presence of the F1534S mutation (TCC) in Ae .…”

Section: Discussionmentioning

confidence: 89%

“…A functional study using site-directed mutagenesis and electrophysiological assays in Xenopus oocytes ( Yan et al 2020 ) showed that mutations F1534S and F1534L conferred resistance to type I, but not type II pyrethroids. Most recently, the F1534S mutation has been verified as causing resistance to the type II pyrethroid, deltamethrin, in a study using CRISPR/Cas9 technology ( Guo et al 2022 ), contradicting findings of Yan et al (2020) .…”

Section: Resultsmentioning

confidence: 99%

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Diversity and distribution of sodium channel mutations in Aedes albopictus (Diptera: Culicidae)

Endersby-Harshman,

Schmidt,

Hoffmann

2024

Journal of Medical Entomology

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There is growing interest in insecticide resistance in the mosquito, Aedes albopictus (Skuse), as its potential for spreading diseases is increasing as urbanization and control efforts intensify. Here we review the presence and diversity of mutations in the voltage-sensitive sodium channel (Vssc) gene associated with pyrethroid resistance and report on additional surveys of these mutations in new populations with an analysis of their spread. The known diversity of these mutations has increased in recent years including the identification of 26 non-synonymous mutations, although phenotypic data associating mutations with resistance remain limited. We provide data on mutations in several new locations including those in Timor Leste, Indonesia, and Vanuatu. We use population genomic data from ddRAD analyses of target populations with the 1534C mutation to identify single nucleotide polymorphisms (SNPs) associated with the mutant to test for clustering of SNPs based on the presence of the 1534C mutation rather than population origin. Our findings suggest spread of resistance alleles via genetic invasion, which is further supported by patterns from a genome-wide principal components analysis. These data point to movement of resistance alleles across wide areas with likely impacts on local control options.

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Section: Discussionmentioning

confidence: 89%

Section: Discussionmentioning

confidence: 89%

Section: Resultsmentioning

confidence: 99%

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Diversity and distribution of sodium channel mutations in Aedes albopictus (Diptera: Culicidae)

Endersby-Harshman,

Schmidt,

Hoffmann

2024

Journal of Medical Entomology

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“…During the deltamethrin screening over 30 generations in previous work [ 14 ], an F1534S substitution was first observed at the early stages of resistance evolution, followed by an I1532T substitution and metabolic resistance (P450s, CCEs and GSTs) detected at later stages (Fig. 1 A).…”

Section: Resultsmentioning

confidence: 82%

“…However, the role of the two mechanisms in resistance evolution is poorly understood due to the complex history of insecticide use in the field and the different resistance phenotypes and genetic backgrounds of mosquito populations. In previous work [ 14 ], a laboratory-derived resistance strain (Lab-R) was established by selecting with deltamethrin, the most commonly-deployed pyrethroid [ 15 ], for 30 generations (Lab-R30) from the laboratory susceptible strain (Lab-S). An F1534S substitution in the VGSC was detected first after six generations of selection and was sufficient for the deltamethrin resistance phenotype.…”

Section: Introductionmentioning

confidence: 99%

The dynamics of deltamethrin resistance evolution in Aedes albopictus has an impact on fitness and dengue virus type-2 vectorial capacity

Guo,

Hu,

Zhou

et al. 2023

BMC Biol

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Background Worldwide invasion and expansion of Aedes albopictus, an important vector of dengue, chikungunya, and Zika viruses, has become a serious concern in global public health. Chemical insecticides are the primary means currently available to control the mosquito populations. However, long-term and large-scale use of insecticides has selected for resistance in the mosquito that is accompanied by a genetic load that impacts fitness. Results A number of laboratory strains representing different resistance mechanisms were isolated and identified from laboratory-derived, deltamethrin-resistant Ae. albopictus recovered in previous work. Resistance levels and fitness costs of the strains were evaluated and compared to characterize the evolution of the resistance genotypes and phenotypes. The heterozygous F1534S mutation (1534F/S) in the voltage gated sodium channel (vgsc) gene product (VGSC), first detected in early stages of resistance evolution, not only confers high-level resistance, but also produces no significant fitness costs, leading to the rapid spread of resistance in the population. This is followed by the increase in frequency of homozygous F1534S (1534S/S) mosquitoes that have significant fitness disadvantages, prompting the emergence of an unlinked I1532T mutation with fewer side effects and a mating advantage better adapted to the selection and reproductive pressures imposed in the experiments. Metabolic resistance with no significant fitness cost and mediating a high-tolerance resistance phenotype may play a dominant role in the subsequent evolution of resistance. The different resistant strains had similar vector competence for dengue virus type-2 (DENV-2). Furthermore, a comparative analysis of vectorial capacity revealed that increased survival due to deltamethrin resistance balanced the negative fitness cost effects and contributed to the risk of dengue virus (DENV) transmission by resistant populations. The progressive evolution of resistance results in mosquitoes with both target-site insensitivity and metabolic resistance with lower fitness costs, which further leads to resistant populations with both high resistance levels and vectorial capacity. Conclusions This study reveals a possible mechanism for the evolution of deltamethrin resistance in Aedes albopictus. These findings will help guide practical strategies for insecticide use, resistance management and the prevention and control of mosquito-borne disease.

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Genome editing in pests: basic science to applications

Chen,

Palli

2024

J Pest Sci

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CRISPR/Cas9-mediated F1534S substitution in the voltage-gated sodium channel reveals its necessity and sufficiency for deltamethrin resistance in Aedes albopictus

Cited by 3 publications

References 56 publications

Diversity and distribution of sodium channel mutations in Aedes albopictus (Diptera: Culicidae)

Diversity and distribution of sodium channel mutations in Aedes albopictus (Diptera: Culicidae)

The dynamics of deltamethrin resistance evolution in Aedes albopictus has an impact on fitness and dengue virus type-2 vectorial capacity

Genome editing in pests: basic science to applications

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