A link between host plant adaptation and pesticide resistance in the polyphagous spider mite Tetranychus urticae

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 2, 2013, Pages

  Dermauw, Wannes ^a   Wybouw, Nicky ^a   Rombauts, Stephane ^a,b   Menten, Björn ^c   Vontas, John ^d   Grbić, Miodrag ^e,f   Clark, Richard M ^g   Feyereisen, René ^h   Van Leeuwen, Thomas ^a  

^a GHENT UNIVERSITY   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c GHENT UNIVERSITY HOSPITAL   (Belgium)

^d UNIVERSITY OF CRETE   (Greece)

^e UNIVERSITY OF WESTERN ONTARIO   (Canada)

^f UNIVERSITY OF LA RIOJA   (Spain)

^g UNIVERSITY OF UTAH   (United States)

^h CNRS   (France)

Author keywords

Genetic variation; Lipocalin; Major facilitator superfamily; Transcriptome; Xenosensors

Indexed keywords

CYTOCHROME P450; PESTICIDE;

AGRICULTURE; ARTICLE; CONTROLLED STUDY; DEFENSE MECHANISM; DETOXIFICATION; EVOLUTIONARY ADAPTATION; GENE EXPRESSION; GENE TRANSFER; GENETIC LINKAGE; GENETIC TRANSCRIPTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PESTICIDE RESISTANCE; PLAGUE; PLANT HERBIVORE INTERACTION; PRIORITY JOURNAL; TETRANYCHUS URTICAE; TOMATO;

ADAPTATION, BIOLOGICAL; ANIMALS; BASE SEQUENCE; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HERBIVORY; HOST-PATHOGEN INTERACTIONS; INSECT PROTEINS; INSECTICIDE RESISTANCE; LIKELIHOOD FUNCTIONS; LIPOCALINS; LYCOPERSICON ESCULENTUM; MICROARRAY ANALYSIS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PHASEOLUS; PHYLOGENY; TETRANYCHIDAE; TIME FACTORS; TOXICITY TESTS;

ACARI; ARTHROPODA; LYCOPERSICON ESCULENTUM; TETRANYCHIDAE; TETRANYCHUS URTICAE;

EID: 84872171542     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1213214110     Document Type: Article

References (116)

1. Strong DR, Lawton JH, Southwood TRE (1984) Insects on Plants: Community Patterns and Mechanisms (Blackwell Scientific, Oxford).
2. Futuyma DJ, Agrawal AA (2009) Macroevolution and the biological diversity of plants and herbivores. Proc Natl Acad Sci USA 106(43):18054-18061.
3. Bernays EA, Chapman RF (1994) Host-Plant Selection by Phytophagous Insects (Chapman & Hall, New York).
4. Cornell HV, Hawkins BA (2003) Herbivore responses to plant secondary compounds: A test of phytochemical coevolution theory. Am Nat 161(4):507-522.
5. Berenbaum MR, Favret C, Schuler MA (1996) On defining key innovations in an adaptive radiation - cytochrome P450s and Papilionidae. Am Nat 148:S139-S155.
6. Thompson JN (1994) The Coevolutionary Process (Univ of Chicago Press, Chicago).
7. Ali JG, Agrawal AA (2012) Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci 17(5):293-302.
8. Krieger RI, Feeny PP, Wilkinson CF (1971) Detoxication enzymes in the guts of caterpillars: An evolutionary answer to plant defenses? Science 172(3983):579-581.
9. Berenbaum MR, Cohen MB, Schuler MA (1992) Cytochrome-P450 monooxygenase genes in oligophagous Lepidoptera. ACS Symp Ser 505:114-124.
10. Gordon HT (1961) Nutritional factors in insect resistance to chemicals. Annu Rev Entomol 6:27-54.
11. Croft BA, Strickler K (1983) Pest Resistance to Pesticides, eds Georghiou GP, Saito T (Plenum, New York), pp 669-702.
12. Rosenheim JA, Johnson MW, Mau RFL, Welter SC, Tabashnik BE (1996) Biochemical preadaptations, founder events, and the evolution of resistance in arthropods. J Econ Entomol 89:263-273.
13. Ahmad S (1986) Enzymatic adaptations of herbivorous insects and mites to phytochemicals. J Chem Ecol 12:533-560.
14. Berry RE, Yu SJ, Terriere LC (1980) Influence of host plants on insecticide metabolism and management of variegated cutworm (Lepidoptera, Noctuidae). J Econ Entomol 73:771-774.
15. Brattsten LB, Wilkinson CF, Eisner T (1977) Herbivore-plant interactions: Mixed-function oxidases and secondary plant substances. Science 196(4296):1349-1352.
16. Castle SJ, Prabhaker N, Henneberry TJ, Toscano NC (2009) Host plant influence on susceptibility of Bemisia tabaci (Hemiptera: Aleyrodidae) to insecticides. Bull Entomol Res 99(3):263-273.
17. Gould F, Carroll CR, Futuyma DJ (1982) Cross-resistance to pesticides and plant defenses: A study of the two-spotted spider-mite. Entomol Exp Appl 31:175-180.
18. Kennedy GG (1984) 2-tridecanone, tomatoes and Heliothis zea - potential incompatibility of plant antibiosis with insecticidal control. Entomol Exp Appl 35:305-311.
19. Li X, Baudry J, Berenbaum MR, Schuler MA (2004) Structural and functional divergence of insect CYP6B proteins: From specialist to generalist cytochrome P450. Proc Natl Acad Sci USA 101(9):2939-2944.
20. Li X, Zangerl AR, Schuler MA, Berenbaum MR (2000) Cross-resistance to alpha-cypermethrin after xanthotoxin ingestion in Helicoverpa zea (Lepidoptera: Noctuidae). J Econ Entomol 93(1):18-25.
21. Lindroth RL (1989) Chemical ecology of the luna moth effects of host plant on detoxification enzyme-activity. J Chem Ecol 15:2019-2029.
22. Sasabe M, Wen ZM, Berenbaum MR, Schuler MA (2004) Molecular analysis of CYP321A1, a novel cytochrome P450 involved in metabolism of plant allelochemicals (furanocoumarins) and insecticides (cypermethrin) in Helicoverpa zea. Gene 338(2):163-175.
23. Zeng RS, Wen Z, Niu G, Schuler MA, Berenbaum MR (2007) Allelochemical induction of cytochrome P450 monooxygenases and amelioration of xenobiotic toxicity in Helicoverpa zea. J Chem Ecol 33(3):449-461.
24. Yang XM, Margolies DC, Zhu KY, Buschman LL (2001) Host plant-induced changes in detoxification enzymes and susceptibility to pesticides in the twospotted spider mite (Acari: Tetranychidae). J Econ Entomol 94(2):381-387.
25. Yu SJ, Berry RE, Terriere LC (1979) Host plant stimulation of detoxifying enzymes in a phytophagous insect. Pestic Biochem Physiol 12:280-284.
26. Feyereisen R (2012) Insect Molecular Biology and Biochemistry, ed Gilbert LI (Academic Press, Elsevier, London), pp 236-316.
27. Li X, Schuler MA, Berenbaum MR (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol 52:231-253.
28. Després L, David JP, Gallet C (2007) The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol Evol 22(6):298-307.
29. Grbić M, et al. (2011) The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature 479(7374):487-492.
30. Agrawal AA (2000) Host-range evolution: Adaptation and trade-offs in fitness of mites on alternative hosts. Ecology 81:500-508.
31. Magalhães S, Blanchet E, Egas M, Olivieri I (2009) Are adaptation costs necessary to build up a local adaptation pattern? BMC Evol Biol 9:182.
32. Fry JD (1989) Evolutionary adaptation to host plants in a laboratory population of the phytophagous mite Tetranychus urticae Koch. Oecologia 81:559-565.
33. Magalhães S, Fayard J, Janssen A, Carbonell D, Olivieri I (2007) Adaptation in a spider mite population after long-term evolution on a single host plant. J Evol Biol 20(5):2016-2027.
34. Van Leeuwen T, Vontas J, Tsagkarakou A, Dermauw W, Tirry L (2010) Acaricide resistance mechanisms in the two-spotted spider mite Tetranychus urticae and other important Acari: A review. Insect Biochem Mol Biol 40(8):563-572.
35. Carrière Y (2003) Haplodiploidy, sex, and the evolution of pesticide resistance. J Econ Entomol 96(6):1626-1640.
36. Denholm I, Cahill M, Dennehy TJ, Horowitz AR (1998) Challenges with managing insecticide resistance in agricultural pests, exemplified by the whitefly Bemisia tabaci. Philos Trans R Soc B Biol Sci 353(1376):1757-1767.
37. Khajehali J, Van Nieuwenhuyse P, Demaeght P, Tirry L, Van Leeuwen T (2011) Acaricide resistance and resistance mechanisms in Tetranychus urticae populations from rose greenhouses in the Netherlands. Pest Manag Sci 67(11):1424-1433.
38. Van Leeuwen T, Dermauw W, Grbic M, Tirry L, Feyereisen R (2012) Spider mite control and resistance management: Does a genome help? Pest Manag Sci, 10.1002/ps.3335.
39. Bitume EV, et al. (2011) Heritability and artificial selection on ambulatory dispersal distance in Tetranychus urticae: Effects of density and maternal effects. PLoS ONE 6(10):e26927.
40. Kennedy GG, Smitley DR (1985) Spider Mites. Their Biology, Natural Enemies and Control, eds Helle W, Sabelis MW (Elsevier, Amsterdam), Vol 1A, pp 233-242.
41. Van Leeuwen T, et al. (2012) Population bulk segregant mapping uncovers resistance mutations and the mode of action of a chitin synthesis inhibitor in arthropods. Proc Natl Acad Sci USA 109(12):4407-4412.
42. Hughes TR, et al. (2001) Expression profiling using microarrays fabricated by an inkjet oligonucleotide synthesizer. Nat Biotechnol 19(4):342-347.
43. Van Leeuwen T, Van Pottelberge S, Tirry L (2005) Comparative acaricide susceptibility and detoxifying enzyme activities in field-collected resistant and susceptible strains of Tetranychus urticae. Pest Manag Sci 61(5):499-507.
44. Marchler-Bauer A, et al. (2011) CDD: A Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39(Database issue):D225-D229.
45. Vaillancourt FH, Bolin JT, Eltis LD (2006) The ins and outs of ring-cleaving dioxygenases. Crit Rev Biochem Mol Biol 41(4):241-267.
46. Ferraroni M, et al. (2005) Crystal structure of the hydroxyquinol 1,2-dioxygenase from Nocardioides simplex 3E, a key enzyme involved in polychlorinated aromatics biodegradation. J Biol Chem 280(22):21144-21154.
47. Matera I, et al. (2010) Catechol 1,2-dioxygenase from the Gram-positive Rhodococcus opacus 1CP: Quantitative structure/activity relationship and the crystal structures of native enzyme and catechols adducts. J Struct Biol 170(3):548-564.
48. Vetting MW, Ohlendorf DH (2000) The 1.8 A crystal structure of catechol 1,2-dioxygenase reveals a novel hydrophobic helical zipper as a subunit linker. Structure 8(4):429-440.
49. Goodrich-Blair H, Clarke DJ (2007) Mutualism and pathogenesis in Xenorhabdus and Photorhabdus: Two roads to the same destination. Mol Microbiol 64(2):260-268.
50. Paper JM, Scott-Craig JS, Adhikari ND, Cuomo CA, Walton JD (2007) Comparative proteomics of extracellular proteins in vitro and in planta from the pathogenic fungus Fusarium graminearum. Proteomics 7(17):3171-3183.
51. Yang F, et al. (2012) Secretomics identifies Fusarium graminearum proteins involved in the interaction with barley and wheat. Mol Plant Pathol 13(5):445-453.
52. Ganfornina MD, Kayser H, Sanchez D (2006) Lipocalins, eds Åkerström B, Borregaard N, Flower DR, Salier JP (Landes Bioscience, Austin, TX), pp 49-74.
53. Breustedt DA, Schönfeld DL, Skerra A (2006) Comparative ligand-binding analysis of ten human lipocalins. Biochim Biophys Acta 1764(2):161-173.
54. Ribeiro JMC, et al. (2006) An annotated catalog of salivary gland transcripts from Ixodes scapularis ticks. Insect Biochem Mol Biol 36(2):111-129.
55. Flower DR, North ACT, Sansom CE (2000) The lipocalin protein family: Structural and sequence overview. Biochim Biophys Acta 1482(1-2):9-24.
56. Sanchez D, et al. (2006) Lipocalins, eds Åkerström B, Borregaard N, Flower DR, Salier JP (Landes Bioscience, Austin, TX), pp 5-16.
57. Ganfornina MD, Gutiérrez G, Bastiani M, Sánchez D (2000) A phylogenetic analysis of the lipocalin protein family. Mol Biol Evol 17(1):114-126.
58. Wade NM, Tollenaere A, Hall MR, Degnan BM (2009) Evolution of a novel carotenoid-binding protein responsible for crustacean shell color. Mol Biol Evol 26(8):1851-1864.
59. Shayeghi M, et al. (2005) Identification of an intestinal heme transporter. Cell 122(5):789-801.
60. Misra JR, Horner MA, Lam G, Thummel CS (2011) Transcriptional regulation of xenobiotic detoxification in Drosophila. Genes Dev 25(17):1796-1806.
61. Pascussi J-M, et al. (2008) The tangle of nuclear receptors that controls xenobiotic metabolism and transport: Crosstalk and consequences. Annu Rev Pharmacol Toxicol 48:1-32.
62. Yano S, Takabayashi J, Takafuji A (2001) Trade-offs in performance on different plants may not restrict the host plant range of the phytophagous mite, Tetranychus urticae. Exp Appl Acarol 25(5):371-381.
63. Gotoh T, Bruin J, Sabelis MW, Menken SBJ (1993) Host race formation in Tetranychus urticae - Genetic differentiation, host-plant preference, and mate choice in a tomato and a cucumber strain. Entomol Exp Appl 68:171-178.
64. Kant MR, Sabelis MW, Haring MA, Schuurink RC (2008) Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defences. Proc R Soc B Biol Sci 275(1633):443-452.
65. Berenbaum MR (2002) Postgenomic chemical ecology: From genetic code to ecological interactions. J Chem Ecol 28(5):873-896.
66. King-Jones K, Horner MA, Lam G, Thummel CS (2006) The DHR96 nuclear receptor regulates xenobiotic responses in Drosophila. Cell Metab 4(1):37-48.
67. Dunlop JA (2010) Geological history and phylogeny of Chelicerata. Arthropod Struct Dev 39(2- 3):124-142.
68. Roopesh K, et al. (2010) Biotransformation of procyanidins by a purified fungal dioxygenase: Identification and characterization of the products using mass spectrometry. Process Biochem 45:904-913.
69. Roopesh K, et al. (2012) Dioxygenase from Aspergillus fumigatus MC8: Molecular modelling and in silico studies on enzyme-substrate interactions. Mol Simul 38:144-151.
70. Richards TA, Dacks JB, Jenkinson JM, Thornton CR, Talbot NJ (2006) Evolution of filamentous plant pathogens: Gene exchange across eukaryotic kingdoms. Curr Biol 16(18):1857-1864.
71. Richards TA, et al. (2011) Horizontal gene transfer facilitated the evolution of plant parasitic mechanisms in the oomycetes. Proc Natl Acad Sci USA 108(37):15258-15263.
72. Chudzinski-Tavassi AM, et al. (2010) A lipocalin sequence signature modulates cell survival. FEBS Lett 584(13):2896-2900.
73. Mullin C, Croft B (1983) Host-related alterations of detoxification enzymes in Tetranychus urticae (Acari: Tetranychidae). Environ Entomol 12:1278-1282.
74. Walker DW, Muffat J, Rundel C, Benzer S (2006) Overexpression of a Drosophila homolog of apolipoprotein D leads to increased stress resistance and extended lifespan. Curr Biol 16(7):674-679.
75. Charron J-BF, Ouellet F, Houde M, Sarhan F (2008) The plant Apolipoprotein D ortholog protects Arabidopsis against oxidative stress. BMC Plant Biol 8:86.
76. Ganfornina MD, et al. (2008) Apolipoprotein D is involved in the mechanisms regulating protection from oxidative stress. Aging Cell 7(4):506-515.
77. Bi JL, Felton GW (1995) Foliar oxidative stress and insect herbivory - Primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance. J Chem Ecol 21:1511-1530.
78. Hildebrand DF, Rodriguez JG, Brown GC, Luu KT, Volden CS (1986) Peroxidative responses of leaves in 2 soybean genotypes injured by 2-spotted spider-mites (Acari, Tetranychidae). J Econ Entomol 79:1459-1465.
79. Pao SS, Paulsen IT, Saier MH, Jr. (1998) Major facilitator superfamily. Microbiol Mol Biol Rev 62(1):1-34.
80. Reddy VS, Shlykov MA, Castillo R, Sun EI, Saier MH, Jr. (2012) The major facilitator superfamily (MFS) revisited. FEBS J 279(11):2022-2035.
81. Hillen W, Berens C (1994) Mechanisms underlying expression of Tn10 encoded tetracycline resistance. Annu Rev Microbiol 48:345-369.
82. Kretschmer M, et al. (2009) Fungicide-driven evolution and molecular basis of multidrug resistance in field populations of the grey mould fungus Botrytis cinerea. PLoS Pathog 5(12):e1000696.
83. Saidijam M, et al. (2006) Microbial drug efflux proteins of the major facilitator superfamily. Curr Drug Targets 7(7):793-811.
84. Krieger M, et al. (1979) Reconstituted low density lipoprotein: A vehicle for the delivery of hydrophobic fluorescent probes to cells. J Supramol Struct 10(4):467-478.
85. Herz J, Strickland DK (2001) LRP: A multifunctional scavenger and signaling receptor. J Clin Invest 108(6):779-784.
86. May P, Woldt E, Matz RL, Boucher P (2007) The LDL receptor-related protein (LRP) family: An old family of proteins with new physiological functions. Ann Med 39(3):219-228.
87. Daborn PJ, et al. (2002) A single p450 allele associated with insecticide resistance in Drosophila. Science 297(5590):2253-2256.
88. David JP, et al. (2005) The Anopheles gambiae detoxification chip: A highly specific microarray to study metabolic-based insecticide resistance in malaria vectors. Proc Natl Acad Sci USA 102(11):4080-4084.
89. Govind G, et al. (2010) Unbiased transcriptional comparisons of generalist and specialist herbivores feeding on progressively defenseless Nicotiana attenuata plants. PLoS ONE 5(1):e8735.
90. Ibrahim MMS (2009) Effect of the host plant on susceptibility of the two-spotted spider mite, Tetranychus urticae Koch, (Acari: Tetranychidae) to some acaricides. J Agric Sci Mansoura Univ 34:10735-10744.
91. Neiswander CR, Rodriguez JG, Neiswander RB (1950) Natural and induced variations in two-spotted spider mite populations. J Econ Entomol 43:633-636.
92. Agrawal AA, Vala F, Sabelis MW (2002) Induction of preference and performance after acclimation to novel hosts in a phytophagous spider mite: Adaptive plasticity? Am Nat 159(5):553-565.
93. Snyder MJ, Glendinning JI (1996) Causal connection between detoxification enzyme activity and consumption of a toxic plant compound. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 179(2):255-261.
94. Feyereisen R (2011) Arthropod CYPomes illustrate the tempo and mode in P450 evolution. Biochim Biophys Acta 1814(1):19-28.
95. Roush RT, McKenzie JA (1987) Ecological genetics of insecticide and acaricide resistance. Annu Rev Entomol 32:361-380.
96. McKenzie JA, Batterham P (1994) The genetic, molecular and phenotypic consequences of selection for insecticide resistance. Trends Ecol Evol 9(5):166-169.
97. ffrench-Constant RH, Daborn PJ, Le Goff G (2004) The genetics and genomics of insecticide resistance. Trends Genet 20(3):163-170.
98. Dermauw W, et al. (2012) The cys-loop ligand-gated ion channel gene family of Tetranychus urticae: Implications for acaricide toxicology and a novel mutation associated with abamectin resistance. Insect Biochem Mol Biol 42(7):455-465.
99. Futuyma DJ, Peterson SC (1985) Genetic variation in the use of resources by insects. Annu Rev Entomol 30:217-238.
100. Via S (1990) Ecological genetics and host adaptation in herbivorous insects: The experimental study of evolution in natural and agricultural systems. Annu Rev Entomol 35:421-446.
101. Gould F (1979) Rapid host range evolution in a population of the phytophagous mite Tetranychus urticae Koch. Evolution 33:791-802.
102. Ayroles JF, et al. (2009) Systems genetics of complex traits in Drosophila melanogaster. Nat Genet 41(3):299-307.
103. Celorio-Mancera Mdl P, Heckel DG, Vogel H (2012) Transcriptional analysis of physiological pathways in a generalist herbivore: Responses to different host plants and plant structures by the cotton bollworm, Helicoverpa armigera. Entomol Exp Appl 144:123-133.
104. Van Pottelberge S, Van Leeuwen T, Nauen R, Tirry L (2009) Resistance mechanisms to mitochondrial electron transport inhibitors in a field-collected strain of Tetranychus urticae Koch (Acari: Tetranychidae). Bull Entomol Res 99(1):23-31.
105. Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265-267.
106. Van Dongen S (2000) Graph clustering by flow simulation. PhD thesis (Univ of Utrecht, Utrecht, The Netherlands).
107. Huang W, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4(1):44-57.
108. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403-410.
109. Punta M, et al. (2012) The Pfam protein families database. Nucleic Acids Res 40(Database issue):D290-D301.
110. Larkin MA, et al. (2007) Clustal W and clustal X version 2.0. Bioinformatics 23(21):2947-2948.
111. Edgar RC (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792-1797.
112. Abascal F, Zardoya R, Posada D (2005) ProtTest: Selection of best-fit models of protein evolution. Bioinformatics 21(9):2104-2105.
113. Jobb G, von Haeseler A, Strimmer K (2004) TREEFINDER: A powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol 4:18.
114. Tamura K, et al. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731-2739.
115. Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340(4):783-795.
116. Cole C, Barber JD, Barton GJ (2008) The Jpred 3 secondary structure prediction server. Nucleic Acids Res 36(Web Server issue):W197-W201.