Match!

Multiple P450s and Variation in Neuronal Genes Underpins the Response to the Insecticide Imidacloprid in a Population of Drosophila melanogaster

Published on Dec 1, 2017in Scientific Reports4.011
· DOI :10.1038/s41598-017-11092-5
Shane Denecke4
Estimated H-index: 4
(University of Melbourne),
Roberto Fusetto3
Estimated H-index: 3
(University of Melbourne)
+ 5 AuthorsPhilip Batterham33
Estimated H-index: 33
(University of Melbourne)
Abstract
Insecticide resistance is an economically important example of evolution in response to intense selection pressure. Here, the genetics of resistance to the neonicotinoid insecticide imidacloprid is explored using the Drosophila Genetic Reference Panel, a collection of inbred Drosophila melanogaster genotypes derived from a single population in North Carolina. Imidacloprid resistance varied substantially among genotypes, and more resistant genotypes tended to show increased capacity to metabolize and excrete imidacloprid. Variation in resistance level was then associated with genomic and transcriptomic variation, implicating several candidate genes involved in central nervous system function and the cytochrome P450s Cyp6g1 and Cyp6g2. CRISPR-Cas9 mediated removal of Cyp6g1 suggested that it contributed to imidacloprid resistance only in backgrounds where it was already highly expressed. Cyp6g2, previously implicated in juvenile hormone synthesis via expression in the ring gland, was shown to be expressed in metabolically relevant tissues of resistant genotypes. Cyp6g2 overexpression was shown to both metabolize imidacloprid and confer resistance. These data collectively suggest that imidacloprid resistance is influenced by a variety of previously known and unknown genetic factors.
  • References (48)
  • Citations (16)
📖 Papers frequently viewed together
1 Citations
26 Citations
20173.56Genetics
21 Citations
78% of Scinapse members use related papers. After signing in, all features are FREE.
References48
Newest
#1Roberto Fusetto (University of Melbourne)H-Index: 3
#2Shane Denecke (University of Melbourne)H-Index: 4
Last. Philip Batterham (University of Melbourne)H-Index: 33
view all 5 authors...
Resistance to insecticides through enhanced metabolism is a worldwide problem. The Cyp6g1 gene of the vinegar fly, Drosophila melanogaster, is a paradigm for the study of metabolic resistance. Constitutive overexpression of this gene confers resistance to several classes of insecticides, including the neonicotinoid imidacloprid (IMI). The metabolism of IMI in this species has been previously shown to yield oxidative and nitro-reduced metabolites. While levels of the oxidative metabolites are cor...
10 CitationsSource
#1Gaëlle Le Goff (CNRS: Centre national de la recherche scientifique)H-Index: 12
#2Frédérique Hilliou (CNRS: Centre national de la recherche scientifique)H-Index: 15
The massive use of DDT as insecticide between 1940 and 1970 has resulted in the emergence of resistant population of insects. One of the main metabolic mechanisms developed by resistant insects involves detoxification enzymes such as cytochrome P450s. These enzymes can metabolize the insecticide to render it less toxic and facilitate its elimination from the organism. The P450 Cyp6g1 was identified as the major factor responsible for DDT resistance in Drosophila melanogaster field populations. I...
22 CitationsSource
#1Danielle Christesen (University of Melbourne)H-Index: 1
#2Ying Ting Yang (University of Melbourne)H-Index: 4
Last. Trent Perry (University of Melbourne)H-Index: 12
view all 7 authors...
In Drosophila melanogaster larvae, the ring gland (RG) is a control center that orchestrates major developmental transitions. It is a composite organ, consisting of the prothoracic gland, the corpus allatum, and the corpora cardiaca, each of which synthesizes and secretes a different hormone. Until now, the RG’s broader developmental roles beyond endocrine secretion have not been explored. RNA sequencing and analysis of a new transcriptome resource from D. melanogaster wandering third instar lar...
12 CitationsSource
#1Jason Somers (University of Melbourne)H-Index: 4
#2Hang Ngoc Bao Luong (University of Melbourne)H-Index: 2
Last. Trent Perry (University of Melbourne)H-Index: 12
view all 5 authors...
Nicotinic acetylcholine receptors (nAChRs) are a highly conserved gene family that form pentameric receptors involved in fast excitatory synaptic neurotransmission. The specific roles individual nAChR subunits perform in Drosophila melanogaster and other insects are relatively uncharacterized. Of the 10 D. melanogaster nAChR subunits, only three have described roles in behavioral pathways; D α 3 and D α 4 in sleep, and D α 7 in the escape response. Other subunits have been associated with resist...
7 CitationsSource
#1Paul Battlay (University of Melbourne)H-Index: 5
#2Joshua M. Schmidt (University of Melbourne)H-Index: 7
Last. Charles Robin (University of Melbourne)H-Index: 20
view all 4 authors...
26 CitationsSource
#1Shane Denecke (University of Melbourne)H-Index: 4
#2Cameron J. Nowell (Monash University)H-Index: 17
Last. Philip Batterham (University of Melbourne)H-Index: 33
view all 5 authors...
Toxicological assays measuring mortality are routinely used to describe insecticide response, but sub-lethal exposures to insecticides can select for resistance and yield additional biological information describing the ways in which an insecticide impacts the insect. Here we present the Wiggle Index (WI), a high-throughput method to quantify insecticide response by measuring the reduction in motility during sub-lethal exposures in larvae of the vinegar fly Drosophila melanogaster. A susceptible...
9 CitationsSource
#1Aris IliasH-Index: 8
#2Jacques LagnelH-Index: 16
Last. Anastasia TsagkarakouH-Index: 19
view all 7 authors...
Background Bemisia tabaci is one of the most damaging agricultural pests world-wide. Although its control is based on insecticides, B. tabaci has developed resistance against almost all classes of insecticides, including neonicotinoids.
16 CitationsSource
#1Wen Huang (NCSU: North Carolina State University)H-Index: 24
#2Mary Anna Carbone (NCSU: North Carolina State University)H-Index: 21
Last. Trudy F. C. Mackay (NCSU: North Carolina State University)H-Index: 65
view all 8 authors...
Understanding how DNA sequence variation is translated into variation for complex phenotypes has remained elusive but is essential for predicting adaptive evolution, for selecting agriculturally important animals and crops, and for personalized medicine. Gene expression may provide a link between variation in DNA sequence and organismal phenotypes, and its abundance can be measured efficiently and accurately. Here we quantified genome-wide variation in gene expression in the sequenced inbred lin...
59 CitationsSource
#1Chris Bass (Rothamsted Research)H-Index: 38
#2Ian Denholm (University of Hertfordshire)H-Index: 56
Last. Ralf Nauen (Bayer)H-Index: 56
view all 4 authors...
Abstract The first neonicotinoid insecticide, imidacloprid, was launched in 1991. Today this class of insecticides comprises at least seven major compounds with a market share of more than 25% of total global insecticide sales. Neonicotinoid insecticides are highly selective agonists of insect nicotinic acetylcholine receptors and provide farmers with invaluable, highly effective tools against some of the world's most destructive crop pests. These include sucking pests such as aphids, whiteflies...
154 CitationsSource
#1Takashi AbeH-Index: 3
#2Daisuke YamazakiH-Index: 3
Last. Tetsuya TabataH-Index: 17
view all 7 authors...
3 CitationsSource
Cited By16
Newest
#1Vassilis Douris (FORTH: Foundation for Research & Technology – Hellas)H-Index: 1
#2Shane Denecke (FORTH: Foundation for Research & Technology – Hellas)H-Index: 4
Last. John Vontas (FORTH: Foundation for Research & Technology – Hellas)H-Index: 42
view all 6 authors...
Abstract Chemical insecticides are a major tool for the control of many of the world's most damaging arthropod pests. However, their intensive application is often associated with the emergence of resistance, sometimes with serious implications for sustainable pest control. To mitigate failure of insecticide-based control tools, the mechanisms by which insects have evolved resistance must be elucidated. This includes both identification and functional characterization of putative resistance gene...
1 CitationsSource
#1Qianqian Xiao (NAU: Nanjing Agricultural University)
#2Lei Deng (NAU: Nanjing Agricultural University)
Last. Min Wu (NAU: Nanjing Agricultural University)H-Index: 8
view all 9 authors...
Laodelphax striatellus (Fallen) is an important rice pest species which has developed high resistance to imidacloprid. Previous studies have demonstrated that CYP6AY3v2 and CYP353D1v2 were constitutively overexpressed in a imidacloprid resistant strain and can metabolize imidacloprid to mediated metabolic resistance. Further studies still needed to explore whether there are other L. striatellus P450 enzymes that can also metabolize imidacloprid. In this study, the expression level of L. striatel...
Source
#1Shane DeneckeH-Index: 4
#1Shane DeneckeH-Index: 1
Last. John VontasH-Index: 42
view all 9 authors...
BACKGROUND: Stink bugs are an emerging threat to crop security in many parts of the globe, but there are few genetic resources available to study their physiology at a molecular level. This is especially true for tissues such as the midgut, which forms the barrier between ingested material and the inside of the body. RESULTS: Here, we focus on the midgut of the southern green stink bug Nezara viridula and use both transcriptomic and proteomic approaches to create an atlas of expression along the...
Source
#1Helen Young (University of Melbourne)H-Index: 8
#2Shane DeneckeH-Index: 4
Last. Alexandre Fournier-Level (University of Melbourne)H-Index: 15
view all 4 authors...
Pesticides are now chronically found in numerous ecosystems incurring widespread toxic effects on multiple organisms. For insects, the larvae are very exposed to pesticide pollution and the acute effect of insecticides on larvae has been characterized in a range of species. However, the carry-on effects in adults of sublethal exposure occurring in larvae are not well characterized. Here, we use a collection of strains of Drosophila melanogaster differing in their larval resistance to a commonly ...
Source
#1Jeffrey G. Scott (Cornell University)H-Index: 49
#2Nicolas Buchon (Cornell University)H-Index: 22
Abstract Insecticides are valuable and widely used tools for the control of pest insects. Despite the use of synthetic insecticides for >50 years, we continue to have a limited understanding of the genes that influence the key steps of the poisoning process. Major barriers for improving our understanding of insecticide toxicity have included a narrow range of tools and/or a large number of candidate genes that could be involved in the poisoning process. Herein, we discuss the numerous tools and ...
1 CitationsSource
#1Pavlína Kellerová (Charles University in Prague)H-Index: 2
#2Petra Matoušková (Charles University in Prague)H-Index: 10
Last. Lenka Skálová (Charles University in Prague)H-Index: 21
view all 8 authors...
Abstract Haemonchus contortus, one of the most pathogenic of all small ruminant parasites, have developed resistance to all used anthelmintics. Detoxification enzymes, e.g. cytochromes P450 (CYPs) and efflux transporters P-glycoproteins (P-gps), which represent the main defense system against harmful xenobiotics, have been suggested to contribute to drug resistance development. The present study was designed to compare the constitutive expression of individual CYPs and P-gps in females and males...
Source
#1Lili Sun (NEFU: Northeast Forestry University)H-Index: 15
#2Peng Liu (NEFU: Northeast Forestry University)H-Index: 2
Last. Chuanwang Cao (NEFU: Northeast Forestry University)H-Index: 5
view all 8 authors...
The ocular albinism type 1 (OA1), a pigment cell-specific integral membrane glycoprotein, is a member of the G-protein-coupled receptor (GPCR) superfamily that binds to heterotrimeric G proteins in mammalian cells. We aimed to characterize the physiological functions of an insect OA1 in regulation of insecticide stress tolerance. In present study, we investigated the roles of LdOA1 in response to deltamethrin stresses in both Lymantria dispar and Drosophila melanogaster. LdOA1 was expressed at t...
Source
#1Dimitra Tsakireli (FORTH: Foundation for Research & Technology – Hellas)H-Index: 6
#2Maria Riga (FORTH: Foundation for Research & Technology – Hellas)H-Index: 1
Last. John Vontas (FORTH: Foundation for Research & Technology – Hellas)H-Index: 42
view all 5 authors...
Abstract Overexpression of the cytochrome P450 monooxygenase CYP6A51 has been previously associated with pyrethroid resistance in the Mediterranean fruit fly (medfly) Ceratitis capitata, an important pest species worldwide; however, this association has not been functionally validated. We expressed CYP6A51 gene in Escherichia coli and produced a functional enzyme with preference for the chemiluminescent substrate Luciferin-ME EGE. In vitro metabolism assays revealed that CYP6A51 is capable of me...
3 CitationsSource
#1Llewellyn Green (University of Melbourne)H-Index: 3
#2Paul Battlay (University of Melbourne)H-Index: 5
Last. Charles Robin (University of Melbourne)H-Index: 20
view all 5 authors...
Insecticide resistance is a paradigm of microevolution, and insecticides are responsible for the strongest cases of recent selection in the genome of Drosophila melanogaster . Here we use a naive population and a novel insecticide class to examine the ab initio genetic architecture of a potential selective response. Genome-wide association studies (GWAS) of chlorantraniliprole susceptibility reveal variation in a gene of major effect, Stretchin Myosin light chain kinase ( Strn-Mlck ), which we v...
3 CitationsSource
#1Alexandre Fournier-Level (University of Melbourne)H-Index: 15
#2Robert T. Good (University of Melbourne)H-Index: 21
Last. Charles Robin (University of Melbourne)H-Index: 20
view all 11 authors...
Imidacloprid, the world’s most used insecticide, has caused considerable controversy due to harmful effects on non-pest species and increasing evidence showing that insecticides have become the primary selective force in many insect species. The genetic response to insecticides is heterogeneous across populations and environments, leading to more complex patterns of genetic variation than previously thought. This motivated the investigation of imidacloprid resistance at different temperatures in...
3 CitationsSource