Diversity of insecticide resistance mechanisms and spectrum in European populations of the codling moth,Cydia pomonella

The codling moth, Cydia pomonella L. (Lepidoptera, Tortricidae), is a serious invasive pest of pome fruits. Currently, C. pomonella management mainly relies on the application of insecticides, which have driven the development of resistance in the insect. Understanding the genetic mechanisms of insecticide resistance is of great significance for developing new pest resistance management techniques and formulating effective resistance management strategies. Using existing genome resequencing data, we performed selective sweep analysis by comparing two resistant strains and one susceptible strain of the insect pest and identified seven genes, among which, two (glycine receptor and glutamate receptor) were under strong insecticide selection, suggesting their functional importance in insecticide resistance. We also found that eight genes including CYP6B2, CYP307a1, 5-hydroxytryptamine receptor, cuticle protein, and acetylcholinesterase, are potentially involved in cross-resistance to azinphos-methyl and deltamethrin. Moreover, among several P450s identified as positively selected genes, CYP6B2, CYP4C1, and CYP4d2 showed the highest expression level in larva compared to other stages tested, and CYP6B2 also showed the highest expression level in midgut, supporting the roles they may play in insecticide metabolism. Our results provide several potential genes that can be studied further to advance understanding of complexity of insecticide resistance mechanisms in C. pomonella.

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Cross-Resistance of the Codling Moth against Different Isolates of Cydia pomonella Granulovirus Is Caused by Two Different but Genetically Linked Resistance Mechanisms

Viruses ◽

10.3390/v13101952 ◽

2021 ◽

Vol 13 (10) ◽

pp. 1952

Author(s):

Annette J. Sauer ◽

Eva Fritsch ◽

Karin Undorf-Spahn ◽

Kento Iwata ◽

Regina G. Kleespies ◽

...

Keyword(s):

Biological Control Agent ◽

Cydia Pomonella ◽

Codling Moth ◽

Resistance Mechanisms ◽

Cross Resistance ◽

Viral Gene ◽

Type I ◽

Type Ii ◽

Cydia Pomonella Granulovirus ◽

Type Ii Resistance

Cydia pomonella granulovirus (CpGV) is a widely used biological control agent of the codling moth. Recently, however, the codling moth has developed different types of field resistance against CpGV isolates. Whereas type I resistance is Z chromosomal inherited and targeted at the viral gene pe38 of isolate CpGV-M, type II resistance is autosomal inherited and targeted against isolates CpGV-M and CpGV-S. Here, we report that mixtures of CpGV-M and CpGV-S fail to break type II resistance and is expressed at all larval stages. Budded virus (BV) injection experiments circumventing initial midgut infection provided evidence that resistance against CpGV-S is midgut-related, though fluorescence dequenching assay using rhodamine-18 labeled occlusion derived viruses (ODV) could not fully elucidate whether the receptor binding or an intracellular midgut factor is involved. From our peroral and intra-hemocoel infection experiments, we conclude that two different (but genetically linked) resistance mechanisms are responsible for type II resistance in the codling moth: resistance against CpGV-M is systemic whereas a second and/or additional resistance mechanism against CpGV-S is located in the midgut of CpR5M larvae.

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Investigation of insecticide-resistance status of Cydia pomonella in Chinese populations

Bulletin of Entomological Research ◽

10.1017/s0007485315000115 ◽

2015 ◽

Vol 105 (3) ◽

pp. 316-325 ◽

Cited By ~ 10

Author(s):

X.-Q. Yang ◽

Y.-L. Zhang

Keyword(s):

Insecticide Resistance ◽

Cydia Pomonella ◽

Resistance Mutation ◽

Codling Moth ◽

Northwestern China ◽

Invasive Pest ◽

Native Page ◽

Chinese Populations ◽

Care Activity ◽

Chlorpyrifos Ethyl

AbstractThe codling moth Cydia pomonella (L.) is an economically important fruit pest and it has been directly targeted by insecticides worldwide. Serious resistance to insecticides has been reported in many countries. As one of the most serious invasive pest, the codling moth has populated several areas in China. However, resistance to insecticides has not been reported in China. We investigated the insecticide-resistance status of four field populations from Northwestern China by applying bioassays, enzyme activities, and mutation detections. Diagnostic concentrations of lambda-cyhalothrin, chlorpyrifos-ethyl, carbaryl, and imidacloprid were determined and used in bioassays. Field populations were less susceptible to chlorpyrifos-ethyl and carbaryl than laboratory strain. Insensitive populations displayed an elevated glutathione S-transferases (GSTs) activity. Reduced carboxylesterase (CarE) activity was observed in some insecticide insensitive populations and reduced acetylcholinesterase activity was observed only in the Wuw population. The cytochrome P450 polysubstrate monooxygenases activities in four field populations were not found to be different from susceptible strains. Neither the known-resistance mutation F399V in the acetylcholinesterase (AChE) gene, ace1, nor mutations in CarE gene CpCE-1 were found in adult individuals from our field populations. Native-PAGE revealed that various CarE isozymes and AChE insensitivity were occurring among Chinese populations. Our results indicate that codling moth populations from Northwestern China were insensitivity to chlorpyrifos-ethyl and carbaryl. Increased GST activity was responsible for insecticides insensitivity. Decreased CarE activity, as well as the presence of CarE and AChE polymorphisms might also be involved in insecticides insensitivity. New management strategies for managing this pest are discussed.

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A chromosome-level genome assembly of Cydia pomonella provides insights into chemical ecology and insecticide resistance

Nature Communications ◽

10.1038/s41467-019-12175-9 ◽

2019 ◽

Vol 10 (1) ◽

Cited By ~ 18

Author(s):

Fanghao Wan ◽

Chuanlin Yin ◽

Rui Tang ◽

Maohua Chen ◽

Qiang Wu ◽

...

Keyword(s):

Insecticide Resistance ◽

Genome Assembly ◽

Association Studies ◽

Receptor Gene ◽

Cydia Pomonella ◽

Codling Moth ◽

Invasive Pest ◽

Z Chromosome ◽

Genome Wide Association Studies ◽

Chromosome Level

Abstract The codling moth Cydia pomonella, a major invasive pest of pome fruit, has spread around the globe in the last half century. We generated a chromosome-level scaffold assembly including the Z chromosome and a portion of the W chromosome. This assembly reveals the duplication of an olfactory receptor gene (OR3), which we demonstrate enhances the ability of C. pomonella to exploit kairomones and pheromones in locating both host plants and mates. Genome-wide association studies contrasting insecticide-resistant and susceptible strains identify hundreds of single nucleotide polymorphisms (SNPs) potentially associated with insecticide resistance, including three SNPs found in the promoter of CYP6B2. RNAi knockdown of CYP6B2 increases C. pomonella sensitivity to two insecticides, deltamethrin and azinphos methyl. The high-quality genome assembly of C. pomonella informs the genetic basis of its invasiveness, suggesting the codling moth has distinctive capabilities and adaptive potential that may explain its worldwide expansion.

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Pest Management Challenges and Control Practices in Codling Moth: A Review

Insects ◽

10.3390/insects11010038 ◽

2020 ◽

Vol 11 (1) ◽

pp. 38 ◽

Cited By ~ 1

Author(s):

Martina Kadoić Balaško ◽

Renata Bažok ◽

Katarina M. Mikac ◽

Darija Lemic ◽

Ivana Pajač Živković

Keyword(s):

Insecticide Resistance ◽

Insect Pest ◽

Cydia Pomonella ◽

Genetic Research ◽

Codling Moth ◽

Fruit Production ◽

Control Measures ◽

Effective Control ◽

Pome Fruit ◽

Proactive Management

The codling moth, Cydia pomonella L., is a serious insect pest in pome fruit production worldwide with a preference for apple. The pest is known for having developed resistance to several chemical groups of insecticides, making its control difficult. The control and management of the codling moth is often hindered by a lack of understanding about its biology and ecology, including aspects of its population genetics. This review summarizes the information about the origin and biology of the codling moth, describes the mechanisms of resistance in this pest, and provides an overview of current research of resistant pest populations and genetic research both in Europe and globally. The main focus of this review is on non-pesticide control measures and anti-resistance strategies which help to reduce the number of chemical pesticides used and their residues on food and the local environment. Regular monitoring for insecticide resistance is essential for proactive management to mitigate potential insecticide resistance. Here we describe techniques for the detection of resistant variants and possibilities for monitoring resistance populations. Also, we present our present work on developing new methods to maintain effective control using appropriate integrated resistance management (IRM) strategies for this economically important perennial pest.

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Worldwide variability of insecticide resistance mechanisms in the codling moth, Cydia pomonella L. (Lepidoptera: Tortricidae)

Bulletin of Entomological Research ◽

10.1017/s0007485308006366 ◽

2008 ◽

Vol 99 (4) ◽

pp. 359-369 ◽

Cited By ~ 41

Author(s):

M. Reyes ◽

P. Franck ◽

J. Olivares ◽

J. Margaritopoulos ◽

A. Knight ◽

...

Keyword(s):

Enzyme Activities ◽

Cydia Pomonella ◽

Significant Proportion ◽

Codling Moth ◽

Resistance Mechanisms ◽

The Czech Republic ◽

Mixed Function Oxidases ◽

Enzymatic Systems ◽

Glutathione S Transferases

AbstractThe activity of detoxifying enzymes (glutathione-S-transferases (GST), mixed-function oxidases (MFO), and esterases (EST)) and the presence of insensitive variants of target proteins (sodium channel and acetylcholinesterase) were examined in individual male and female codling moths. Twenty-nine populations from 11 countries and two laboratory strains were examined. Populations were classified as either unsprayed or sprayed. The ranges of enzyme activities across field populations varied 15-fold, 485-fold and fourfold for GST, MFO and EST, respectively. MFO was the only enzyme whose activity differed in a binomial classification of orchards based on their spray history. Few differences in enzyme activities were found due to sex among populations; and, in these cases, males had higher GST and lower MFO and EST activities than females. Activities of the three enzymatic systems across all populations were positively correlated. Populations from Greece, Argentina and Uruguay had significant percentages of moths with elevated GST and MFO activities. The co-occurrence of moths expressing both elevated MFO and low EST activities was found in conventional orchards from the Czech Republic and France. Chile was the only country where populations from treated orchards did not include a significant proportion of individuals with enhanced enzyme activity. The kdr mutation was found at significant levels in ten populations from five countries, including all French and Argentinean populations. The mutation in AChE was only detected in the Spanish population.

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Pleiotropy of insecticide resistance in the codling moth, Cydia pomonella

Entomologia Experimentalis et Applicata ◽

10.1046/j.1570-7458.2001.00838.x ◽

2001 ◽

Vol 99 (3) ◽

pp. 381-386 ◽

Cited By ~ 53

Author(s):

Thomas Boivin ◽

Cécile Chabert D'Hières ◽

Jean C. Bouvier ◽

Dominique Beslay ◽

Benoît Sauphanor

Keyword(s):

Insecticide Resistance ◽

Cydia Pomonella ◽

Codling Moth

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Insecticide resistance may enhance the response to a host-plant volatile kairomone for the codling moth, Cydia pomonella (L.)

The Science of Nature ◽

10.1007/s00114-007-0222-6 ◽

2007 ◽

Vol 94 (6) ◽

pp. 449-458 ◽

Cited By ~ 8

Author(s):

Benoît Sauphanor ◽

Pierre Franck ◽

Thérèse Lasnier ◽

Jean-François Toubon ◽

Dominique Beslay ◽

...

Keyword(s):

Insecticide Resistance ◽

Host Plant ◽

Cydia Pomonella ◽

Codling Moth ◽

Host Plant Volatile ◽

Plant Volatile

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Phenological segregation of insecticide resistance alleles in the codling moth Cydia pomonella (Lepidoptera: Tortricidae): a case study of ecological divergences associated with adaptive changes in populations

Genetics Research ◽

10.1017/s0016672303006244 ◽

2003 ◽

Vol 81 (3) ◽

pp. 169-177 ◽

Cited By ~ 19

Author(s):

THOMAS BOIVIN ◽

JEAN-CHARLES BOUVIER ◽

DOMINIQUE BESLAY ◽

BENOIT SAUPHANOR

Keyword(s):

Insecticide Resistance ◽

Cydia Pomonella ◽

Codling Moth ◽

Reproductive Season ◽

Pleiotropic Effects ◽

Adaptive Changes ◽

South Eastern ◽

Trade Offs ◽

Seasonal Regulation ◽

Selection For

Intrapopulation variability in the seasonal regulation of insect lifecycles has been shown to be due partly to genetic changes. Selection for insecticide resistance in the codling moth Cydia pomonella results from allelic substitution at two to three loci in south-eastern French populations of this species. However, such an adaptive process has been associated with an increased heterogeneity in the developmental responses to climatic factors such as temperature. In this paper, we investigate whether such pleiotropic effects of resistance on development induce a significant discrepancy in seasonal regulation in this species. The seasonal changes in a susceptible and two insecticide-resistant homozygous genotypes of C. pomonella, as well as their reciprocal F1 progeny, were followed under natural conditions during the reproductive season through the emergence events of adults, within-generation developmental rates and the number of generations. A significant delay in the occurrences of homozygous resistant genotypes resulted from significantly lower pre-imaginal developmental times relative to homozygous susceptible ones. Subsequent assessment of the number of generations indicated significantly higher diapause propensities in carriers of the resistance alleles (37·0–76·2%) than in susceptible homozygotes (6·7%), which mostly pupated towards a third generation of adults. In the light of these findings, pleiotropic effects of adaptive changes might be a crucial source of divergence in seasonal regulation at the population level, involving significant life-history trade-offs. In addition to man-made selective factors during the reproductive season, such an effect on the lifecycle could be a key component in the process of selection for resistance genes in south-eastern France C. pomonella populations.

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