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Genetic structure and insecticide resistance characteristics of fall armyworm populations invading China.

ABSTRACT: The rapid wide-scale spread of fall armyworm (Spodoptera frugiperda) has caused serious crop losses globally. However, differences in the genetic background of subpopulations and the mechanisms of rapid adaptation behind the invasion are still not well understood. Here we report the assembly of a 390.38-Mb chromosome-level genome of fall armyworm derived from south-central Africa using Pacific Bioscience (PacBio) and Hi-C sequencing technologies, with scaffold N50 of 12.9 Mb and containing 22,260 annotated protein-coding genes. Genome-wide resequencing of 103 samples and strain identification were conducted to reveal the genetic background of fall armyworm populations in China. Analysis of genes related to pesticide- and Bacillus thuringiensis (Bt) resistance showed that the risk of fall armyworm developing resistance to conventional pesticides is very high. Laboratory bioassay results showed that insects invading China carry resistance to organophosphate and pyrethroid pesticides, but are sensitive to genetically modified maize expressing the Bt toxin Cry1Ab in field experiments. Additionally, two mitochondrial fragments were found to be inserted into the nuclear genome, with the insertion event occurring after the differentiation of the two strains. This study represents a valuable advance toward improving management strategies for fall armyworm.

SUBMITTER: Zhang L

PROVIDER: S-EPMC7689805 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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Genetic structure and insecticide resistance characteristics of fall armyworm populations invading China.

Zhang Lei L Liu Bo B Zheng Weigang W Liu Conghui C Zhang Dandan D Zhao Shengyuan S Li Zaiyuan Z Xu Pengjun P Wilson Kenneth K Withers Amy A Jones Christopher M CM Smith Judith A JA Chipabika Gilson G Kachigamba Donald L DL Nam Kiwoong K d'Alençon Emmanuelle E Liu Bei B Liang Xinyue X Jin Minghui M Wu Chao C Chakrabarty Swapan S Yang Xianming X Jiang Yuying Y Liu Jie J Liu Xiaolin X Quan Weipeng W Wang Guirong G Fan Wei W Qian Wanqiang W Wu Kongming K Xiao Yutao Y

Molecular ecology resources 20200720 6

The rapid wide-scale spread of fall armyworm (Spodoptera frugiperda) has caused serious crop losses globally. However, differences in the genetic background of subpopulations and the mechanisms of rapid adaptation behind the invasion are still not well understood. Here we report the assembly of a 390.38-Mb chromosome-level genome of fall armyworm derived from south-central Africa using Pacific Bioscience (PacBio) and Hi-C sequencing technologies, with scaffold N50 of 12.9 Mb and containing 22,26 ...[more]

PMID: 32619331

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Project description:BackgroundSpodoptera frugiperda, fall armyworm (FAW) is the major pest of maize in Brazil and has readily acquired field resistance to a broad range of synthetic insecticides and to Bacillus thuringiensis (Bt) insecticidal proteins expressed in important crops. This study aims to understand patterns of cross-resistance in FAW by investigating the toxicological profile of a Bt-resistant Brazilian strain (Sf_Des) in comparison to a Bt-susceptible strain (Sf_Bra).ResultsLaboratory bioassays with 15 active substances of nine mode of action classes revealed that Sf_Des has a medium level of resistance to deltamethrin and chlorpyrifos. Very high cross-resistance was observed among Cry1 toxins, but high susceptibility against Vip3A. Strain Sf_Des exhibited - depending on the substrate - up to 19-fold increased cytochrome P450 activity in comparison to Sf_Bra. RNA-Seq data support a major role of P450 enzymes in the detoxification of insecticides because we detected 85 P450 transcripts upregulated in Sf_Des. Quantitative reverse transcription polymerase chain reaction (RT-qPCR) analysis confirmed that CYP9A-like and CYP6B39 are significantly upregulated (>200-fold) in Sf_Des in comparison to Sf_Bra strain. No target-site mutation linked to pyrethroid resistance was detected, but mutations in the AChE linked to organophosphate resistance were observed in Sf_Des. A Gene Ontology (GO) analysis of differentially expressed genes (DEG) categorized most of them into the biological process category, involved in oxidation-reduction and metabolic processes.ConclusionOur results indicate that multiple/cross-resistance mechanisms may have developed in the Sf_Des strain to conventional insecticides and Bt insecticidal proteins. The systematic toxicological analysis presented will help to guide recommendations for an efficient resistance management. © 2020 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Project description:In an emergency response to the introduction, subsequent detection and rapid spread of the invasive insect pest fall armyworm (FAW), Spodoptera frugiperda (J.E. Smith) in the country, Government of India offered ad-hoc approval for few pesticide molecules namely, emamectin benzoate, spinetoram, chlorantraniliprole, novaluron, thiodicarb, and λ-cyhalothrin for FAW management in corn crop across the country. Five major maize (corn) growing geographical areas (i.e., Bihar, Delhi, Karnataka, Punjab and Tamil Nadu) were selected during the main crop season of 2020 (Oct-Nov), and sampled for the target-insect populations. The insect populations were lab-reared on maize leaves (15-20 days old); the F1 generation insects (third instar, 25-30 mg/larva) were subjected to bioassay to determine susceptibility levels of FAW against ad-hoc recommended insecticides. The previously reported target-site molecular variations in the genes ace, encoding acetylcholinesterase (AChE), and vgsc, encoding voltage-gated sodium channel were analyzed. Among the five test-populations, Bihar test-population recorded least susceptibility to all the test-pesticides, whereas the South Indian populations (Karnataka, Tamil Nadu) were found most susceptible. North Indian and South Indian test-insect populations formed two distinct groups in terms of susceptibility levels, speculatively on account of prevailing climatic factors. Being the population with least ace mutation frequency, but with the higher resistance ratio for all the test-pesticides, Bihar insect population implies a bigger role of broad range detoxification machinery than the narrow scope of target site insensitivity. Though, resistance has not developed to the recommended insecticides by FAW, except the case of low-medium resistance development; which is better explained due to behavioural avoidance of synthetic pyrethroid (λ-cyhalothrin). However, there is no room for complacency. Resistance-monitoring tools such as location/region-specific determination of discriminating diagnostic concentrations/doses for FAW in recommended insecticides are to be devised at the earliest.Supplementary informationThe online version contains supplementary material available at 10.1007/s13205-022-03303-2.

Project description:Vector control largely relies on neurotoxic chemicals, and insecticide resistance (IR) directly threatens their effectiveness. In some cases, specific alleles cause IR, and knowledge of the genetic diversity and gene flow among mosquito populations is crucial to track their arrival, rise, and spread. Here we evaluated Aedes aegypti populations' susceptibility status, collected in 2016 from six different municipalities of Rio de Janeiro state (RJ), to temephos, pyriproxyfen, malathion, and deltamethrin. We collected eggs of Ae. aegypti in Campos dos Goytacazes (Cgy), Itaperuna (Ipn), Iguaba Grande (Igg), Itaboraí (Ibr), Mangaratiba (Mgr), and Vassouras (Vsr). We followed the World Health Organization (WHO) guidelines and investigated the degree of susceptibility/resistance of mosquitoes to these insecticides. We used the Rockefeller strain as a susceptible positive control. We genotyped the V1016I and F1534C knockdown resistance (kdr) alleles using qPCR TaqMan SNP genotyping assay. Besides, with the use of Ae. aegypti SNP-chip, we performed genomic population analyses by genotyping more than 15,000 biallelic SNPs in mosquitoes from each population. We added previous data from populations from other countries to evaluate the ancestry of RJ populations. All RJ Ae. aegypti populations were susceptible to pyriproxyfen and malathion and highly resistant to deltamethrin. The resistance ratios for temephos was below 3,0 in Cgy, Ibr, and Igg populations, representing the lowest rates since IR monitoring started in this Brazilian region. We found the kdr alleles in high frequencies in all populations, partially justifying the observed resistance to pyrethroid. Population genetics analysis showed that Ae. aegypti revealed potential higher migration among some RJ localities and low genetic structure for most of them. Future population genetic studies, together with IR data in Ae aegypti on a broader scale, can help us predict the gene flow within and among the Brazilian States, allowing us to track the dynamics of arrival and changes in the frequency of IR alleles, and providing critical information to improving vector control program.

Dataset Information

Genetic structure and insecticide resistance characteristics of fall armyworm populations invading China.

Publications

Genetic structure and insecticide resistance characteristics of fall armyworm populations invading China.

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