Insecticide-resistant Myzus persicae as an example of evolution by gene duplication

Devonshire, A. L.; Sawicki, R. M.

doi:10.1038/280140a0

Cited by 139 publications

(81 citation statements)

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“…A classic example of this is work on the duplicated esterases of the green peach (peach potato) aphid M. persicae. Following the original discovery that the numbers of copies of the E 4 gene could be correlated with the levels of resistance to several insecticides (Devonshire and Sawicki 1979), duplication of E 4 was put forward as the only resistance mechanism in Myzus and overexpression of the E 4 esterase was seen as being necessary and sufficient to catalyze and/or sequester a range of different insecticide classes, with the notable exception of pyrethroids. Variants such as Fast E 4 were described, but these were simply different duplication events that had led to the truncation of the enzyme and therefore resulted in a different (faster) electrophoretic mobility (Field and Devonshire 1998).…”

Section: Multiple Mechanisms Within a Single Genome: Aphids And Estermentioning

confidence: 99%

The Molecular Genetics of Insecticide Resistance

2013

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The past 60 years have seen a revolution in our understanding of the molecular genetics of insecticide resistance. While at first the field was split by arguments about the relative importance of mono-vs. polygenic resistance and field-vs. laboratory-based selection, the application of molecular cloning to insecticide targets and to the metabolic enzymes that degrade insecticides before they reach those targets has brought out an exponential growth in our understanding of the mutations involved. Molecular analysis has confirmed the relative importance of single major genes in target-site resistance and has also revealed some interesting surprises about the multi-gene families, such as cytochrome P450s, involved in metabolic resistance. Identification of the mutations involved in resistance has also led to parallel advances in our understanding of the enzymes and receptors involved, often with implications for the role of these receptors in humans. This Review seeks to provide an historical perspective on the impact of molecular biology on our understanding of resistance and to begin to look forward to the likely impact of rapid advances in both sequencing and genome-wide association analysis."Curiouser and curiouser!" cried Alice.Lewis Carroll L ewis Carroll sent Alice down a rabbit hole without the least idea of what was to happen next, but as Alice ventured deeper into Wonderland things became "Curiouser and curiouser!" So indeed have studies on the molecular basis of insecticide resistance. While starting with rather simplistic expectations about the role of single mutations in single genes, resistance has been shown to involve a panoply of multiple mutations in multiple genes, often with independent and complex origins. This review will attempt to place these current findings into context and to examine the extent to which the field has often been historically blindsided by dogma. My arguments will encompass key controversies debated in the field such as the relative importance of mono-vs. polygenic resistance and the implications of resistance-associated mutations for whole-organism fitness in the absence of pesticide. Importantly, we will also examine the role of dogma in shaping the way that resistance research has been pursued over the past 50 years. Key questions addressed are therefore: How many mutations per gene cause resistance? How many mechanisms are there per species (genome)? How many independent genetic origins (mutations) give rise to each mechanism? What new mechanisms are still undiscovered and how might they arise? Monogenic vs. Polygenic ResistanceCrow, DDT, and DrosophilaThe humble fruit fly Drosophila melanogaster has been a key tool in unlocking the molecular basis of insecticide resistance, and early studies by James Crow and others have helped to establish Drosophila as a genetic model for resistance studies. Studies of DDT resistance in Drosophila have also typified arguments surrounding mono-vs. polygenic inheritance of insecticide resistance. In his pioneering review of in...

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Section: Multiple Mechanisms Within a Single Genome: Aphids And Estermentioning

confidence: 99%

The Molecular Genetics of Insecticide Resistance

2013

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“…[30][31][32] This group also includes a subgroup with hemipteran CCEs, that is, five CCEs of A. pisum and Myzus persicae E4 and FE4, that are associated with resistance to OPs. [33][34][35] …”

Section: (L) Non-lepidopteran Jhesmentioning

confidence: 99%

Genomic and phylogenetic analysis of insect carboxyl/cholinesterase genes

Tsubota

Shiotsuki

2010

J. Pestic. Sci.

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The carboxyl/cholinesterase (CCE) superfamily is composed of functionally diverse proteins that hydrolyze carboxylic esters. CCEs are responsible not only for physiological regulation of particular endogenous compounds, such as hormones, pheromones, and acetylcholine, but also for the detoxification of exogenous compounds, such as those in the diet and in the environment. In some instances, CCEs are associated with insecticide resistance, 1) and the gene identification of CCEs is significant not only for elucidation of the mechanisms of insecticide resistance but also for the development of novel insecticidal compounds pesticides. Recent completion of genome projects and the availability of expressed sequence tag (EST) clones has enabled the identification of multiple CCEs in each insect species. 2-4) Here we describe the genomic and phylogenetic analyses of 425 insect CCEs found in eight insect species whose genomes have been completely sequenced, and discuss the implications of the constructed phylogenetic tree. Construction of the Phylogenetic TreeClustalW software was used to perform multiple sequence alignment prior to phylogenetic analysis. MEGA 4.0 5) was used to construct the phylogenetic tree using the neighborjoining method with the JTT matrix. To evaluate branch strength in the phylogenetic tree, bootstrap analysis of 500 replicates was performed. The amino acid sequences of genes used for phylogenetic analysis were retrieved from the National Center for Biotechnological Information site (http:// www.ncbi.nih.gov/). The accession number of each gene is listed in Supplemental Table S1. Potential signal peptides were predicted by the SignalP 3.0 program (http://www.cbs. dtu.dk/services/SignalP). Phylogenetic Analysis of Insect CCEsThe database search revealed 425 insect CCEs, including those from insects whose genomes have been completely sequenced, namely the dipterans Drosophila melanogaster, 1) Anopheles gambiae, 6) and Aedes aegypti; 7) the hymenopterans Apis mellifera 8) and Nasonia vitripennis; 9) lepidopteran Bombyx mori; 10,11) and the coleopteran Tribolium castaneum; 9) hemipteran Acyrthosiphon pisum. 12) The identified insect CCEs also included those of the lepidopterans Helicoverpa armigera and Spodoptera littoralis, in which EST clone analysis has been conducted, 13,14) and several other CCEs. Using these CCE amino acid sequences, a phylogenetic tree The complete genome sequence data of insects in five orders are now available. In this commentary we provide recent genomic and phylogenetic analyses of insect carboxyl/cholinesterases (CCEs). Multiple CCEs are found in each insect species, and at present the silkworm Bombyx mori has the largest number and diversity of CCEs. Phylogenetic analyses of the 425 CCE sequences identified species or order specific clustering, but for some CCEs 1:1 orthologous relationships were apparent. Phylogenetic analyses will be useful for further functional analysis of CCEs and the development of species-specific insecticides and/or synergists.

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“…The peach-potato aphid, Myzus persicae (Sulzer), combats organophosphorus and carbamate insecticides by overproducing insecticide-degrading carboxylesterases, encoded by amplified genes (Devonshire & Sawicki, 1979;Field et a!., 1993). Resistant aphids have one of two alternative amplified carboxylesterase genes, E4 or FE4, depending on their karyotype.…”

Section: Introductionmentioning

confidence: 99%

Chromosomal location of the amplified esterase genes conferring resistance to insecticides in Myzus persicae (Homoptera: Aphididae)

et al. 1995

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A genomic probe encompassing most of an esterase gene (E4) that is amplified in insecticideresistant Myzus persicae was hybridized in situ to mitotic and meiotic chromosome preparations of aphid clones of known esterase type and resistance level. Binding, which was detected using the biotin-avidin system located both known types of amplified esterase sequences (E4 and FE4). All except one of the E4-producing clones had a single amplified site, on autosome 3 near the breakpoint of an autosomal 1,3 translocation which previous work had shown to be genetically linked to insecticide resistance. The exceptional clone had two other E4-encoding sites. The most resistant FE4-producing clone (800F) had amplified sequences at five sites (three loci: two homozygous and one heterozygous). Altogether, amplified E4 and/or FE4 sequences were found on four of the five autosome pairs of M. persicae. Possible origins of these multiple loci are discussed.

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Insecticide-resistant Myzus persicae as an example of evolution by gene duplication

Cited by 139 publications

References 13 publications

The Molecular Genetics of Insecticide Resistance

The Molecular Genetics of Insecticide Resistance

Genomic and phylogenetic analysis of insect carboxyl/cholinesterase genes

Chromosomal location of the amplified esterase genes conferring resistance to insecticides in Myzus persicae (Homoptera: Aphididae)

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