Amplification of a Cytochrome P450 Gene Is Associated with Resistance to Neonicotinoid Insecticides in the Aphid

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The aphid Myzus persicae is a globally significant crop pest that has evolved high levels of resistance to almost all classes of insecticide. To date, the neonicotinoids, an economically important class of insecticides that target nicotinic acetylcholine receptors (nAChRs), have remained an effective control measure; however, recent reports of resistance in M. persicae represent a threat to the long-term efficacy of this chemical class. In this study, the mechanisms underlying resistance to the neonicotinoid insecticides were investigated using biological, biochemical, and genomic approaches. Bioassays on a resistant M. persicae clone (5191A) suggested that P450-mediated detoxification plays a primary role in resistance, although additional mechanism(s) may also contribute. Microarray analysis, using an array populated with probes corresponding to all known detoxification genes in M. persicae, revealed constitutive over-expression (22-fold) of a single P450 gene (CYP6CY3); and quantitative PCR showed that the over-expression is due, at least in part, to gene amplification. This is the first report of a P450 gene amplification event associated with insecticide resistance in an agriculturally important insect pest. The microarray analysis also showed over-expression of several gene sequences that encode cuticular proteins (2–16-fold), and artificial feeding assays and in vivo penetration assays using radiolabeled insecticide provided direct evidence of a role for reduced cuticular penetration in neonicotinoid resistance. Conversely, receptor radioligand binding studies and nucleotide sequencing of nAChR subunit genes suggest that target-site changes are unlikely to contribute to resistance to neonicotinoid insecticides in M. persicae.

Vyšlo v časopise: Amplification of a Cytochrome P450 Gene Is Associated with Resistance to Neonicotinoid Insecticides in the Aphid. PLoS Genet 6(6): e32767. doi:10.1371/journal.pgen.1000999
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1000999

Souhrn

Zdroje

1. FeyereisenR

1995 Molecular biology of insecticide resistance. Toxicol Lett 82-3 83 90

2. BlackmanRL

EastopVF

2000 Aphids on the world's crops, an identification and information guide. Chichester, UK John Wiley & Sons Ltd.

3. FieldLM

DevonshireAL

FordeBG

1988 Molecular evidence that insecticide resistance in peach-potato aphids (Myzus persicae Sulz.) results from amplification of an esterase gene. Biochem J 251 309 312

4. DevonshireAL

FieldLM

FosterSP

MooresGD

WilliamsonMS

1998 The evolution of insecticide resistance in the peach-potato aphid, Myzus persicae. Philos Trans R Soc Lond B Biol Sci 353 1677 1684

5. NauenR

DenholmI

2005 Resistance of insect pests to neonicotinoid insecticides: Current status and future prospects. Arch Insect Biochem Physiol 58 200 215

6. MargaritopoulosJT

SkourasPJ

NikolaidouP

ManolikakiJ

MaritsaK

2007 Insecticide resistance status of Myzus persicae (Hemiptera: Aphididae) populations from peach and tobacco in mainland Greece. Pest Manag Sci 63 821 829

7. FosterSP

CoxD

OliphantL

MitchinsonS

DenholmI

2008 Correlated responses to neonicotinoid insecticides in clones of the peach-potato aphid, Myzus persicae (Hemiptera: Aphididae). Pest Manag Sci 64 1111 1114

8. LiuZW

WilliamsonMS

LansdellSJ

DenholmI

HanZJ

2005 A nicotinic acetylcholine receptor mutation conferring target-site resistance to imidacloprid in Nilaparvata lugens (brown planthopper). Proc Natl Acad Sci U S A 102 8420 8425

9. RauchN

NauenR

2003 Identification of biochemical markers linked to neonicotinoid cross resistance in Bemisia tabaci (Hemiptera: Aleyrodidae). Arch Insect Biochem Physiol 54 165 176

10. KarunkerI

BentingJ

LuekeB

PongeT

NauenR

2008 Over-expression of cytochrome P450 CYP6CM1 is associated with high resistance to imidacloprid in the B and Q biotypes of Bemisia tabaci (Hemiptera: Aleyrodidae). Insect Biochem Mol Biol 38 634 644

11. KarunkerI

MorouE

NikouD

NauenR

SertchookR

2009 Structural model and functional characterization of the Bemisia tabaci CYP6CM1vQ, a cytochrome P450 associated with high levels of imidacloprid resistance. Insect Biochem Mol Biol 39 697 706

12. DabornPJ

YenJL

BogwitzMR

Le GoffG

FeilE

2002 A single P450 allele associated with insecticide resistance in Drosophila. Science 297 2253 2256

13. PhilippouD

FieldLM

MooresGD

2009 Metabolic enzyme(s) confer imidacloprid resistance in a clone of Myzus persicae (Sulzer) (Hemiptera: Aphididae) from Greece. Pest Manag Sci 66 390 395

14. FeyereisenR

2006 Evolution of insect P450. Biochem Soc Trans 34 1252 1255

15. NelsonDR

2009 The cytochrome P450 homepage. Hum Genomics 4 59 65

16. The International Aphid Genomics Consortium 2010 Genome sequence of the pea aphid Acyrthosiphon pisum PLoS Biol 8 e1000313 doi:10.1371/journal.pbio.1000313

17. RamseyJS

WilsonACC

de VosM

SunQ

TamborindeguyC

2007 Genomic resources for Myzus persicae: EST sequencing, SNP identification, and microarray design. BMC Genomics 8 423

18. RamseyJS

RiderDS

WalshTK

De VosM

GordonKHJ

2010 Comparative analysis of detoxification enzymes in Acyrthosiphon pisum and Myzus persicae. Insect Mol Biol 19 155 164

19. FieldLM

BlackmanRL

Tyler-SmithC

DevonshireAL

1999 Relationship between amount of esterase and gene copy number in insecticide-resistant Myzus persicae (Sulzer). Biochem J 339 737 742

20. MagkriotiCK

SpyropoulosIC

IconomidouVA

WillisJH

HamodrakasSJ

2004 cuticleDB: a relational database of Arthropod cuticular proteins. BMC Bioinformatics 5 138

21. MarcombeS

PoupardinR

DarrietF

ReynaudS

BonnetJ

2009 Exploring the molecular basis of insecticide resistance in the dengue vector Aedes aegypti: a case study in Martinique Island (French West Indies). BMC Genomics 10 494

22. FosterSP

DenholmI

ThompsonR

2003 Variation in response to neonicotinoid insecticides in peach-potato aphids, Myzus persicae (Hemiptera: Aphididae). Pest Manag Sci 59 166 173

23. LiXC

SchulerMA

BerenbaumMR

2007 Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol 52 231 253

24. WondjiCS

IrvingH

MorganJ

LoboNF

CollinsFH

2009 Two duplicated P450 genes are associated with pyrethroid resistance in Anopheles funestus, a major malaria vector. Genome Res 19 452 459

25. EmersonJJ

Cardoso-MoreiraM

BorevitzJO

LongM

2008 Natural selection shapes genome-wide patterns of copy-number polymorphism in Drosophila melanogaster. Science 320 1629 1631

26. GallotA

RispeC

LetermeN

GauthierJP

Jaubert-PossamaiS

2010 Cuticular proteins and seasonal photoperiodism in aphids. Insect Biochem Mol Biol doi:10.1016/j.ibmb.2009.12.001

27. VallesSM

DongK

BrennerRJ

2000 Mechanisms responsible for cypermethrin resistance in a strain of German cockroach, Blattella germanica. Pestic Biochem Physiol 66 195 205

28. AhmadM

DenholmI

BromilowRH

2006 Delayed cuticular penetration and enhanced metabolism of deltamethrin in pyrethroid-resistant strains of Helicoverpa armigera from China and Pakistan. Pest Manag Sci 62 805 810

29. WalterCM

PriceNR

1989 The uptake and penetration of pirimiphos-methyl into susceptible and resistant strains of the rust red flour beetle—Tribolium castaneum, herbst (coleoptera: tenebrionidae). Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 94 419 423

30. DjouakaRF

BakareAA

CoulibalyON

AkogbetoMC

RansonH

2008 Expression of the cytochrome P450s, CYP6P3 and CYP6M2 are significantly elevated in multiple pyrethroid resistant populations of Anopheles gambiae s.s. from Southern Benin and Nigeria. BMC Genomics 9 538

31. Guidelines for preventing and managing insecticide resistance in aphids on potatoes. Version April 2008 ed: Insecticide Resistance Action Group (IRAG-UK)

32. Two-Color Microarray-Based Gene Expression analysis (Quick Amp Labeling). Version 5.7 ed: Agilent Technologies

33. SaeedAI

SharovV

WhiteJ

LiJ

LiangW

2003 TM4: A free, open-source system for microarray data management and analysis. Biotechniques 34 374 378

34. ClevelandWS

DevlinSJ

1988 Locally Weighted Regression - An approach to regression-Analysis by local fitting. J Am Stat Assoc 83 596 610

35. TusherVG

TibshiraniR

ChuG

2001 Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98 10515 10515

36. PfafflMW

2001 A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29 e45

37. VandesompeleJ

PreterKD

PattynF

PoppeB

RoyNV

2002 Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3 research0034