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Annual Review of Entomology

Volume 61, 2016

The Molecular Evolution of Xenobiotic Metabolism and Resistance in Chelicerate Mites

Abstract

Chelicerate mites diverged from other arthropod lineages more than 400 million years ago and subsequently developed specific and remarkable xenobiotic adaptations. The study of the two-spotted spider mite, , for which a high-quality Sanger-sequenced genome was first available, revealed expansions and radiations in all major detoxification gene families, including P450 monooxygenases, carboxyl/cholinesterases, glutathione--transferases, and ATP-binding cassette transporters. Novel gene families that are not well studied in other arthropods, such as major facilitator family transporters and lipocalins, also reflect the evolution of xenobiotic adaptation. The acquisition of genes by horizontal gene transfer provided new routes to handle toxins, for example, the β-cyanoalanine synthase enzyme that metabolizes cyanide. The availability of genomic resources for other mite species has allowed researchers to study the lineage specificity of these gene family expansions and the distinct evolution of genes involved in xenobiotic metabolism in mites. Genome-based tools have been crucial in supporting the idiosyncrasies of mite detoxification and will further support the expanding field of mite-plant interactions.

Keyword(s): Acari, adaptation, bulked segregant analysis, chemoreceptor, gene family radiations, mapping, target site, xenosensor
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2016-03-11
2024-04-20
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Literature Cited

  1. Abbas RZ, Zaman MA, Colwell DD, Gilleard J, Iqbal Z. 1.  2014. Acaricide resistance in cattle ticks and approaches to its management: the state of play. Vet. Parasitol. 203:6–20 [Google Scholar]
  2. Agrawal AA. 2.  2000. Host-range evolution: adaptation and trade-offs in fitness of mites on alternative hosts. Ecology 81:500–8 [Google Scholar]
  3. Agut B, Gamir J, Jacas JA, Hurtado M, Flors V. 3.  2014. Different metabolic and genetic responses in citrus may explain relative susceptibility to Tetranychus urticae. Pest Manag. Sci. 70:1728–41 [Google Scholar]
  4. Ahn S-J, Dermauw W, Wybouw N, Heckel DG, Van Leeuwen T. 4.  2014. Bacterial origin of a diverse family of UDP-glycosyltransferase genes in the Tetranychus urticae genome. Insect Biochem. Mol. Biol. 50:43–57 [Google Scholar]
  5. Alba JM, Schimmel BCJ, Glas JJ, Ataide LMS, Pappas ML. 5.  et al. 2015. Spider mites suppress tomato defenses downstream of jasmonate and salicylate independently of hormonal crosstalk. New Phytol. 205:828–40 [Google Scholar]
  6. Asahi M, Kobayashi M, Matsui H, Nakahira K. 6.  2015. Differential mechanisms of action of the novel γ-aminobutyric acid receptor antagonist ectoparasiticides fluralaner (A1443) and fipronil. Pest Manag. Sci. 71:91–95 [Google Scholar]
  7. Auger P, Migeon A, Ueckermann EA, Tiedt L, Navajas Navarro M. 7.  2013. Evidence for synonymy between Tetranychus urticae and Tetranychus cinnabarinus (Acari, Prostigmata, Tetranychidae): review and new data. Acarologia 53:383–415 [Google Scholar]
  8. Bajda S, Dermauw W, Greenhalgh R, Nauen R, Tirry L. 8.  et al. 2015. Transcriptome profiling of a spirodiclofen susceptible and resistant strain of the European red mite Panonychus ulmi using strand-specific RNA-seq. BMC Genomics 16974
  9. Barati R, Hejazi M. 9.  2015. Reproductive parameters of Tetranychus urticae (Acari: Tetranychidae) affected by neonicotinoid insecticides. Exp. Appl. Acarol. 66:481–89 [Google Scholar]
  10. Bartley K, Wright HW, Bull RS, Huntley JF, Nisbet AJ. 10.  2015. Characterisation of Dermanyssus gallinae glutathione S-transferases and their potential as acaricide detoxification proteins. Parasites Vectors 8:1–12 [Google Scholar]
  11. Barrett RDH, Hoekstra HE. 11.  2011. Molecular spandrels: tests of adaptation at the genetic level. Nat. Rev. Genet. 12:767–80 [Google Scholar]
  12. Bast J. 12.  2014. Transposable elements in sexual and asexual animals PhD Thesis, Georg-August-Universität, Göttingen, Germany
  13. Belliure B, Montserrat M, Magalhaes S. 13.  2010. Mites as models for experimental evolution studies. Acarologia (Paris) 50:513–29 [Google Scholar]
  14. Berenbaum M. 14.  1983. Coumarins and caterpillars: a case for coevolution. Evolution 37:163–79 [Google Scholar]
  15. Bogdanov S. 15.  2006. Contaminants of bee products. Apidologie 37:1–18 [Google Scholar]
  16. Bryon A, Wybouw N, Dermauw W, Tirry L, Van Leeuwen T. 16.  2013. Genome wide gene-expression analysis of facultative reproductive diapause in the two-spotted spider mite Tetranychus urticae. BMC Genomics 14:815 [Google Scholar]
  17. Burgess STG, Downing A, Watkins CA, Marr EJ, Nisbet AJ. 17.  et al. 2012. Development of a cDNA microarray for the measurement of gene expression in the sheep scab mite Psoroptes ovis. Parasites Vectors 5:30 [Google Scholar]
  18. Burgess STG, Nisbet A, Kenyon F, Huntley J. 18.  2011. Generation, analysis and functional annotation of expressed sequence tags from the ectoparasitic mite Psoroptes ovis. Parasites Vectors 4:145 [Google Scholar]
  19. Campbell E, Budge G, Bowman A. 19.  2010. Gene-knockdown in the honey bee mite Varroa destructor by a non-invasive approach: studies on a glutathione S-transferase. Parasites Vectors 3:73 [Google Scholar]
  20. Cao TNP. 20.  2014. Genome annotation and evolution of chemosensory receptors in spider mites PhD Thesis, Ghent Univ., Belgium
  21. Cassanelli S, Ahmad S, Duso C, Tirello P, Pozzebon A. 21.  2015. A single nucleotide polymorphism in the acetylcholinesterase gene of the predatory mite Kampimodromus aberrans (Acari: Phytoseiidae) is associated with chlorpyrifos resistance. Biol. Control 90:75–82 [Google Scholar]
  22. Chan T-F, Ji K-M, Yim AK-Y, Liu X-Y, Zhou J-W. 22.  et al. 2015. The draft genome, transcriptome, and microbiome of Dermatophagoides farinae reveal a broad spectrum of dust mite allergens. J. Allergy Clin. Immunol. 135:539–48 [Google Scholar]
  23. Croft BA. 23.  1990. Arthropod Biological Control Agents and Pesticides New York: Wiley
  24. Croft BA, Strickler K. 24.  1983. Natural enemy resistance to pesticides: documentation, characterization, theory and application. Pest Resistance to Pesticides GP Georghiou, T Saito 669–702 New York: Plenum [Google Scholar]
  25. Dabert M, Witalinski W, Kazmierski A, Olszanowski Z, Dabert J. 25.  2010. Molecular phylogeny of acariform mites (Acari, Arachnida): strong conflict between phylogenetic signal and long-branch attraction artifacts. Mol. Phylogenet. Evol. 56:222–41 [Google Scholar]
  26. Demaeght P, Dermauw W, Tsakireli D, Khajehali J, Nauen R. 26.  et al. 2013. Molecular analysis of resistance to acaricidal spirocyclic tetronic acids in Tetranychus urticae: CYP392E10 metabolizes spirodiclofen, but not its corresponding enol. Insect Biochem. Mol. Biol. 43:544–54 [Google Scholar]
  27. Demaeght P, Osborne EJ, Odman-Naresh J, Grbić M, Nauen R. 27.  et al. 2014. High resolution genetic mapping uncovers chitin synthase-1 as the target-site of the structurally diverse mite growth inhibitors clofentezine, hexythiazox and etoxazole in Tetranychus urticae. Insect Biochem. Mol. Biol. 51:52–61 [Google Scholar]
  28. Dermauw W, Ilias A, Riga M, Tsagkarakou A, Grbić M. 28.  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. 42:455–65 [Google Scholar]
  29. Dermauw W, Osborne E, Clark R, Grbić M, Tirry L, Van Leeuwen T. 29.  2013. A burst of ABC genes in the genome of the polyphagous spider mite Tetranychus urticae. BMC Genomics 14:317 [Google Scholar]
  30. Dermauw W, Van Leeuwen T. 30.  2014. The ABC gene family in arthropods: comparative genomics and role in insecticide transport and resistance. Insect Biochem. Mol. Biol. 45:89–110 [Google Scholar]
  31. Dermauw W, Wybouw N, Rombauts S, Menten B, Vontas J. 31.  et al. 2013. A link between host plant adaptation and pesticide resistance in the polyphagous spider mite Tetranychus urticae. PNAS 110:E113–22Polyphagy leads to a preadaptation syndrome affecting acaricide toxicity and involves new detoxifying gene families. [Google Scholar]
  32. Despres L, David J, Gallet C. 32.  2007. The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol. Evol. 22:298–307 [Google Scholar]
  33. Dicke M, Van Beek TA, Posthumus MA, Ben Dom N, Van Bokhoven H, De Groot A. 33.  1990. Isolation and identification of volatile kairomone that affects acarine predator prey interactions. Involvement of host plant in its production. J. Chem. Ecol. 16:381–96 [Google Scholar]
  34. Dobler S, Dalla S, Wagschal V, Agrawal AA. 34.  2012. Community-wide convergent evolution in insect adaptation to toxic cardenolides by substitutions in the Na,K-ATPase. PNAS 109:13040–45 [Google Scholar]
  35. Dodds PN, Rathjen JP. 35.  2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11:539–48 [Google Scholar]
  36. Dulin F, Zatylny-Gaudin C, Ballandonne C, Guillet B, Bonafos R. 36.  et al. 2014. Protecting honey bees: identification of a new varroacide by in silico, in vitro, and in vivo studies. Parasitol. Res. 113:4601–10 [Google Scholar]
  37. Dunlop JA, Alberti G. 37.  2008. The affinities of mites and ticks: a review. J. Zool. Syst. Evol. Res. 46:1–18 [Google Scholar]
  38. Dunlop JA, Borners J, Burmester T. 38.  2014. Phylogeny of the chelicerates: morphological and molecular evidence. Deep Metazoan Phylogeny: The Backbone of the Tree of Life JW Wägele, T Bartolomaeus 399–412 Berlin/Boston: de Gruyter [Google Scholar]
  39. Dunlop JA, de Oliveira Bernardi LF. 39.  2014. An opilioacarid mite in Cretaceous Burmese amber. Naturwissenschaften 101:759–63 [Google Scholar]
  40. Dunlop JA, Selden PA. 40.  2009. Calibrating the chelicerate clock: a paleontological reply to Jeyaprakash and Hoy. Exp. Appl. Acarol. 48:183–97 [Google Scholar]
  41. Elbert A, Becker B, Hartwig J, Erdelen C. 41.  1991. Imidacloprid—a new systemic insecticide. Pflanzenschutz-Nachr. Bayer 44:113–36 [Google Scholar]
  42. Fahrbach SE, Smagghe G, Velarde RA. 42.  2012. Insect nuclear receptors. Annu. Rev. Entomol. 57:83–106 [Google Scholar]
  43. Fairbrother A, Purdy J, Anderson T, Fell R. 43.  2014. Risks of neonicotinoid insecticides to honeybees. Environ. Toxicol. Chem. 33:719–31 [Google Scholar]
  44. Fellous S, Angot G, Orsucci M, Migeon A, Auger P. 44.  et al. 2014. Combining experimental evolution and field population assays to study the evolution of host range breadth. J. Evol. Biol. 27:911–19 [Google Scholar]
  45. Feyereisen R. 45.  2014. Dealing with chemically adverse environments: transcriptomic and genomic insights from specialist and generalist herbivores Presented at Seventh International Symposium on Molecular Insect Science, 13–16 July 2014, Amsterdam, The Netherlands
  46. Feyereisen R, Dermauw W, Van Leeuwen T. 46.  2015. Genotype to phenotype, the molecular and physiological dimensions of resistance in arthropods. Pestic. Biochem. Physiol. 121:61–77 [Google Scholar]
  47. 47. ffrench-Constant RH 2013. The molecular genetics of insecticide resistance. Genetics 194:807–15 [Google Scholar]
  48. ffrench-Constant RH, Pittendrigh B, Vaughan A, Anthony N. 48.  1998. Why are there so few resistance-associated mutations in insecticide target genes?. Philos. Trans. R. Soc. B 353:1685–93 [Google Scholar]
  49. Fischer K, Walton S. 49.  2014. Parasitic mites of medical and veterinary importance—Is there a common research agenda?. Int. J. Parasitol. 44:955–67 [Google Scholar]
  50. Garbian Y, Maori E, Kalev H, Shafir S, Sela I. 50.  2012. Bidirectional transfer of RNAi between honey bee and Varroa destructor: Varroa gene silencing reduces. Varroa population. PLOS Pathog. 8:e1003035Transfer of dsRNA between honey bee and Varroa mites could be a conceptually novel approach to control Varroa parasitism. [Google Scholar]
  51. Garwood RJ, Dunlop J. 51.  2014. Three-dimensional reconstruction and the phylogeny of extinct chelicerate orders. Peer J. 2:e641 [Google Scholar]
  52. Glas JJ, Alba JM, Simoni S, Villarroel CA, Stoops M. 52.  et al. 2014. Defense suppression benefits herbivores that have a monopoly on their feeding site but can backfire within natural communities. BMC Biol. 12:98The benefits of suppressing plant defenses may diminish in communities with natural competitors. [Google Scholar]
  53. Goldman-Huertas B, Mitchell RF, Lapoint RT, Faucher CP, Hildebrand JG, Whiteman NK. 53.  2015. Evolution of herbivory in Drosophilidae linked to loss of behaviors, antennal responses, odorant receptors, and ancestral diet. PNAS 112:3026–31 [Google Scholar]
  54. González-Cabrera J, Davies TGE, Field LM, Kennedy PJ, Williamson MS. 54.  2013. An amino acid substitution (L925V) associated with resistance to pyrethroids in Varroa destructor. PLOS ONE 8:e82941 [Google Scholar]
  55. Gordon HT. 55.  1961. Nutritional factors in insect resistance to chemicals. Annu. Rev. Entomol. 6:27–54 [Google Scholar]
  56. Grbić M, Khila A, Lee KZ, Bjelica A, Grbić V. 56.  et al. 2007. Mity model: Tetranychus urticae, a candidate for chelicerate model organism. BioEssays 29:489–96 [Google Scholar]
  57. Grbić M, Van Leeuwen T, Clark RM, Rombauts S, Rouze P. 57.  et al. 2011. The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature 479:487–92In-depth analysis of the first complete genome sequence of a chelicerate. [Google Scholar]
  58. Grinberg M, Perl-Treves R, Palevsky E, Shomer I, Soroker V. 58.  2005. Interaction between cucumber plants and the broad mite, Polyphagotarsonemus latus: from damage to defense gene expression. Entomol. Exp. Appl. 115:135–44 [Google Scholar]
  59. Guerrero FD, Pérez de Léon AA, Rodriguez-Vivas RI, Jonsson NN, Miller RJ, Andreotti R. 59.  2014. Acaricide research and development, resistance and resistance monitoring. Biology of Ticks DE Sonenshine, RR Roe 353–81 New York: Oxford Univ. Press [Google Scholar]
  60. Heckel DG. 60.  2014. Insect detoxification and sequestration strategies. Annual Plant Reviews 47 Insect-Pant Interactions DG Robinson, JC Rogers 77–114 Oxford: Wiley [Google Scholar]
  61. Heidel-Fischer HM, Vogel H. 61.  2015. Molecular mechanisms of insect adaptation to plant secondary compounds. Curr. Opin. Insect Sci. 8:8–14 [Google Scholar]
  62. Hogenhout SA, Bos JIB. 62.  2011. Effector proteins that modulate plant-insect interactions. Curr. Opin. Plant Biol. 14:422–28 [Google Scholar]
  63. Hubert J, Nesvorna M, Kamler M, Kopecky J, Tyl J. 63.  et al. 2014. Point mutations in the sodium channel gene conferring tau-fluvalinate resistance in Varroa destructor. Pest Manag. Sci. 70:889–94 [Google Scholar]
  64. Ilias A, Vontas J, Tsagkarakou A. 64.  2014. Global distribution and origin of target site insecticide resistance mutations in Tetranychus urticae. Insect Biochem. Mol. Biol. 48:17–28 [Google Scholar]
  65. James DG. 65.  1997. Imidacloprid increases egg production in Amblyseius victoriensis (Acari: Phytoseiidae). Exp. Appl. Acarol. 21:75–82 [Google Scholar]
  66. Jander G. 66.  2014. Revisiting plant-herbivore co-evolution in the molecular biology era. Annual Plant Reviews C Voelckel, G Jander 361–84 Chichester, UK: Wiley [Google Scholar]
  67. Jeschke P, Nauen R, Beck ME. 67.  2013. Nicotinic acetylcholine receptor agonists: a milestone for modern crop protection. Angew. Chem. Int. Ed. 52:9464–85 [Google Scholar]
  68. Jones JDG, Dangl JL. 68.  2006. The plant immune system. Nature 444:323–29 [Google Scholar]
  69. Kamau LM, Wright HM, Nisbet AJ, Bowman A. 69.  2013. Development of an RNA-interference procedure for gene knockdown in the poultry red mite, Dermanyssus gallinae: studies on histamine releasing factor and Cathepsin-D. Afr. J. Biotechnol. 12:1350–56 [Google Scholar]
  70. Kant MR, Jonckheere W, Knegt B, Lemos F, Liu J. 70.  et al. 2015. Mechanisms and ecological consequences of plant defence induction and suppression in herbivore communities. Ann. Bot. 115:1015–51 [Google Scholar]
  71. Kant MR, Sabelis MW, Haring MA, Schuurink RC. 71.  2008. Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defences. Proc. R. Soc. B 275:443–52 [Google Scholar]
  72. Karim S, Adamson SW. 72.  2012. RNA interference in ticks: a functional genomics tool for the study of physiology. Adv. Insect Physiol. 42:119–54 [Google Scholar]
  73. Kazimirova M, Stibraniova I. 73.  2013. Tick salivary compounds: their role in modulation of host defences and pathogen transmission. Front. Cell. Infect. Microbiol. 3:43 [Google Scholar]
  74. Kennedy C, Tierney K. 74.  2013. Xenobiotic protection/resistance mechanisms in organisms. Environmental Toxicology: Selected Entries from the Encyclopedia of Sustainability Science and Technology EA Laws 689–721 New York: Springer [Google Scholar]
  75. Khila A, Grbić M. 75.  2007. Gene silencing in the spider mite Tetranychus urticae: dsRNA and siRNA parental silencing of the Distal-less gene. Dev. Genes Evol. 217:241–51 [Google Scholar]
  76. Krantz GW, Walter DE. 76.  2009. A Manual of Acarology Lubbock: Texas Tech Univ. Press
  77. Kwon DH, Choi JY, Je YH, Lee SH. 77.  2012. The overexpression of acetylcholinesterase compensates for the reduced catalytic activity caused by resistance-conferring mutations in Tetranychus urticae. Insect Biochem. Mol. Biol. 42:212–19Gene amplification of a mutated AChE results in overexpression that compensates for reduced AChE activity. [Google Scholar]
  78. Kwon DH, Clark JM, Lee SH. 78.  2010. Extensive gene duplication of acetylcholinesterase associated with organophosphate resistance in the two-spotted spider mite. Insect Mol. Biol. 19:195–204 [Google Scholar]
  79. Kwon DH, Clark JM, Lee SH. 79.  2015. Toxicodynamic mechanisms and monitoring of acaricide resistance in the two-spotted spider mite. Pestic. Biochem. Physiol. 121:97–101 [Google Scholar]
  80. Kwon DH, Lee SW, Ahn JJ, Lee SH. 80.  2014. Determination of acaricide resistance allele frequencies in field populations of Tetranychus urticae using quantitative sequencing. J. Asia Pac. Entomol. 17:99–103 [Google Scholar]
  81. Kwon DH, Park JH, Lee SH. 81.  2013. Screening of lethal genes for feeding RNAi by leaf disc-mediated systematic delivery of dsRNA in Tetranychus urticae. Pestic. Biochem. Physiol. 105:69–75 [Google Scholar]
  82. Kwon DH, Yoon KS, Clark JM, Lee SH. 82.  2010. A point mutation in a glutamate-gated chloride channel confers abamectin resistance in the two-spotted spider mite, Tetranychus urticae Koch. Insect Mol. Biol. 19:583–91 [Google Scholar]
  83. Lee SH, Kim YH, Kwon DH, Cha DJ, Kim JH. 83.  2015. Mutation and duplication of arthropod acetylcholinesterase: implications for pesticide resistance and tolerance. Pestic. Biochem. Physiol. 120:118–24 [Google Scholar]
  84. Li X, Schuler M, Berenbaum M. 84.  2007. Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu. Rev. Entomol. 52:231–53 [Google Scholar]
  85. Liu J, Jonckheere W, Wybouw N, Schuurinck R, Van Leeuwen T, Kant M. 85.  2014. A family of small secreted salivary proteins of spider mites which may interfere with plant defenses Presented at XIV International Congress of Acarology, 13–18 July, Kyoto, Japan
  86. Liu Y, Ma S, Wang X, Chang J, Gao J. 86.  et al. 2014. Highly efficient multiplex targeted mutagenesis and genomic structure variation in Bombyx mori cells using CRISPR/Cas9. Insect Biochem. Mol. Biol. 49:35–42 [Google Scholar]
  87. Liu Z, Tan J, Huang ZY, Dong K. 87.  2006. Effect of a fluvalinate-resistance-associated sodium channel mutation from varroa mites on cockroach sodium channel sensitivity to fluvalinate, a pyrethroid insecticide. Insect Biochem. Mol. Biol. 36:885–89 [Google Scholar]
  88. Magalhães S, Blanchet E, Egas M, Olivieri I. 88.  2009. Are adaptation costs necessary to build up a local adaptation pattern?. BMC Evol. Biol. 9:182 [Google Scholar]
  89. Marr EJ, Sargison ND, Nisbet AJ, Burgess STG. 89.  2014. RNA interference for the identification of ectoparasite vaccine candidates. Parasite Immunol. 36:616–26 [Google Scholar]
  90. Marr EJ, Sargison ND, Nisbet AJ, Burgess STG. 90.  2015. Gene silencing by RNA interference in the house dust mite, Dermatophagoides pteronyssinus. Mol. Cell Probes 29522–26
  91. Martel C, Zhurov V, Navarro M, Martinez M, Cazaux M. 91.  et al. 2015. Tomato whole genome transcriptional response to Tetranychus urticae identifies divergence of spider mite-induced responses between tomato and Arabidopsis. Mol. Plant Microbe Interact. 28:343–61 [Google Scholar]
  92. McBride CS, Arguello JR. 92.  2007. Five Drosophila genomes reveal nonneutral evolution and the signature of host specialization in the chemoreceptor superfamily. Genetics 177:1395–416 [Google Scholar]
  93. Meikle W, Sammataro D, Neumann P, Pflugfelder J. 93.  2012. Challenges for developing pathogen-based biopesticides against Varroa destructor (Mesostigmata: Varroidae). Apidologie 43:501–14 [Google Scholar]
  94. Michelmore RW, Paran I, Kesseli RV. 94.  1991. Identification of markers linked to disease-resistance genes by bulked segregant analysis - a rapid method to detect markers in specific genomic regions by using segregating populations. PNAS 88:9828–32 [Google Scholar]
  95. Misra JR, Horner MA, Lam G, Thummel CS. 95.  2011. Transcriptional regulation of xenobiotic detoxification in Drosophila. Genes Dev. 25:1796–806 [Google Scholar]
  96. Misra JR, Lam G, Thummel CS. 96.  2013. Constitutive activation of the Nrf2/Keap1 pathway in insecticide-resistant strains of Drosophila. Insect Biochem. Mol. Biol. 43:1116–24 [Google Scholar]
  97. Missbach C, Dweck HK, Vogel H, Vilcinskas A, Stensmyr MC. 97.  et al. 2014. Evolution of insect olfactory receptors. eLife 3:e02115 [Google Scholar]
  98. Mithöfer A, Boland W. 98.  2012. Plant defense against herbivores: chemical aspects. Annu. Rev. Plant. Biol. 63:431–50 [Google Scholar]
  99. Miyazaki J, Stiller WN, Truong TT, Xu Q, Hocart CH. 99.  et al. 2014. Jasmonic acid is associated with resistance to twospotted spider mites in diploid cotton (Gossypium arboreum). Funct. Plant Biol. 41:748–57 [Google Scholar]
  100. Mounsey KE, McCarthy JS, Walton SF. 100.  2013. Scratching the itch: new tools to advance understanding of scabies. Trends Parasitol. 29:35–42 [Google Scholar]
  101. Mullin C, Croft B. 101.  1983. Host-related alterations of detoxification enzymes in Tetranychus urticae (Acari: Tetranychidae). Environ. Entomol. 12:1278–82 [Google Scholar]
  102. Mullin CA, Croft BA, Strickler K, Matsumura F, Miller JR. 102.  1982. Detoxification enzyme differences between a herbivorous and predatory mite. Science 217:1270–72 [Google Scholar]
  103. Nakanishi T, Kato Y, Matsuura T, Watanabe H. 103.  2014. CRISPR/Cas-mediated targeted mutagenesis in Daphnia magna. PLOS ONE 9:e98363 [Google Scholar]
  104. Nyoni BN, Gorman K, Mzilahowa T, Williamson MS, Navajas M. 104.  et al. 2011. Pyrethroid resistance in the tomato red spider mite, Tetranychus evansi, is associated with mutation of the para-type sodium channel. Pest Manag. Sci. 67:891–97 [Google Scholar]
  105. Oakeshott JG, Claudianos C, Campbell PM, Newcomb RD, Russell RJ. 105.  2005. Biochemical genetics and genomics of insect esterases. Comprehensive Molecular Insect Science LI Gilbert 309–81 Amsterdam: Elsevier [Google Scholar]
  106. Oldroyd BP. 106.  2007. What's killing American honey bees?. PLOS Biol. 5:e168 [Google Scholar]
  107. O'Reilly AO, Williamson MS, González-Cabrera J, Turberg A, Field LM. 107.  et al. 2014. Predictive 3D modelling of the interactions of pyrethroids with the voltage-gated sodium channels of ticks and mites. Pest Manag. Sci. 70:369–77 [Google Scholar]
  108. Ozoe Y. 108.  2013. γ-aminobutyrate- and glutamate-gated chloride channels as targets of insecticides. Adv. Insect Physiol. 44:211–86 [Google Scholar]
  109. Pal C, Papp B, Lercher MJ. 109.  2005. Adaptive evolution of bacterial metabolic networks by horizontal gene transfer. Nat. Genet. 37:1372–75 [Google Scholar]
  110. Pasay C, Arlian L, Morgan M, Vyszenski-Moher D, Rose A. 110.  et al. 2008. High-resolution melt analysis for the detection of a mutation associated with permethrin resistance in a population of scabies mites. Med. Vet. Entomol. 22:82–88 [Google Scholar]
  111. Pascussi J-M, Gerbal-Chaloin S, Duret C, Daujat-Chavanieu M, Vilarem M-J, Maurel P. 111.  2008. The tangle of nuclear receptors that controls xenobiotic metabolism and transport: crosstalk and consequences. Annu. Rev. Pharmacol. Toxicol. 48:1–32 [Google Scholar]
  112. Pavlidi N, Tseliou V, Riga M, Nauen R, Van Leeuwen T. 112.  et al. 2015. Functional characterization of glutathione S-transferases associated with insecticide resistance in Tetranychus urticae. Pestic. Biochem. Physiol. 121:53–60 [Google Scholar]
  113. Pepato A, Klimov P. 113.  2015. Origin and higher-level diversification of acariform mites - evidence from nuclear ribosomal genes, extensive taxon sampling, and secondary structure alignment. BMC Evol. Biol. 15:178 [Google Scholar]
  114. Pomerantz A, Hoy M. 114.  2015. RNAi-mediated knockdown of transformer-2 in the predatory mite Metaseiulus occidentalis via oral delivery of double-stranded RNA. Exp. Appl. Acarol. 65:17–27 [Google Scholar]
  115. Price KL, Lummis SCR. 115.  2014. An atypical residue in the pore of Varroa destructor GABA-activated RDL receptors affects picrotoxin block and thymol modulation. Insect Biochem. Mol. Biol. 55:19–25 [Google Scholar]
  116. Pritchard J, Kuster T, Sparagano O, Tomley F. 116.  2015. Understanding the biology and control of the poultry red mite Dermanyssus gallinae: a review. Avian Pathol. 44:143–53 [Google Scholar]
  117. Ribeiro JMC, Alarcon-Chaidez F, Francischetti IMB, Mans BJ, Mather TN. 117.  et al. 2006. An annotated catalog of salivary gland transcripts from Ixodes scapularis ticks. Insect Biochem. Mol. Biol. 36:111–29 [Google Scholar]
  118. Rice RE, Strong FE. 118.  1962. Bionomics of the tomato russet mite, Vasates lycopersici (Massee). Ann. Entomol. Soc. Am. 55:431–35 [Google Scholar]
  119. Riddick EW, Simmons AM. 119.  2014. Do plant trichomes cause more harm than good to predatory insects?. Pest Manag. Sci. 70:1655–65 [Google Scholar]
  120. Riga M, Myridakis A, Tsakireli D, Morou E, Stephanou EG. 120.  et al. 2015. Functional characterization of the Tetranychus urticae CYP392A11, an up-regulated cytochrome P450 conferring resistance to the METI acaricides cyenopyrafen and fenpyroximate. Insect Biochem. Mol. Biol. 65:91–99 [Google Scholar]
  121. Riga M, Tsakireli D, Ilias A, Morou E, Myridakis A. 121.  et al. 2014. Abamectin is metabolized by CYP392A16, a cytochrome P450 associated with high levels of acaricide resistance in Tetranychus urticae. Insect Biochem. Mol. Biol. 46:43–53 [Google Scholar]
  122. Roopesh K, Guyot S, Sabu A, Haridas M, Isabelle PG. 122.  et al. 2010. Biotransformation of procyanidins by a purified fungal dioxygenase: identification and characterization of the products using mass spectrometry. Process. Biochem. 45:904–13 [Google Scholar]
  123. Rosenheim JA, Johnson MW, Mau RFL, Welter SC, Tabashnik BE. 123.  1996. Biochemical preadaptations, founder events, and the evolution of resistance in arthropods. J. Econ. Entomol. 89:263–73 [Google Scholar]
  124. Rosenkranz P, Aumeier P, Ziegelmann B. 124.  2010. Biology and control of Varroa destructor. J. Invertebr. Pathol. 103:S96–119 [Google Scholar]
  125. Roy L, Chauve C, Delaporte J, Inizan G, Buronfosse T. 125.  2009. Exploration of the susceptibility of AChE from the poultry red mite Dermanyssus gallinae (Acari: Mesostigmata) to organophosphates in field isolates from France. Exp. Appl. Acarol. 48:19–30 [Google Scholar]
  126. Roy M. 126.  1993. État actuel de la lutte biologique contre les acariens phytophages par des acariens prédateurs. Phytoprotection 74:41–49 [Google Scholar]
  127. Santamaria M, Hernandez-Crespo P, Ortego F, Grbić V, Grbić M. 127.  et al. 2012. Cysteine peptidases and their inhibitors in Tetranychus urticae: a comparative genomic approach. BMC Genomics 13:307 [Google Scholar]
  128. Sarmento RA, Lemos F, Bleeker PM, Schuurink RC, Pallini A. 128.  et al. 2011. A herbivore that manipulates plant defence. Ecol. Lett. 14:229–36 [Google Scholar]
  129. Schmidt AR, Jancke S, Lindquist EE, Ragazzi E, Roghi G. 129.  et al. 2012. Arthropods in amber from the Triassic Period. PNAS 109:14796–801 [Google Scholar]
  130. Schneeberger K. 130.  2014. Using next-generation sequencing to isolate mutant genes from forward genetic screens. Nat. Rev. Genet. 15:662–76 [Google Scholar]
  131. Smissaert HR. 131.  1964. Cholinesterase inhibition in spider mites susceptible and resistant to organophosphate. Science 143:129–31 [Google Scholar]
  132. Solomon MG, Easterbrook MA, Fitzgerald JD. 132.  1993. Mite-management programmes based on organophosphate-resistant Typhlodromus pyri in UK apple orchards. Crop Prot. 12:249–54 [Google Scholar]
  133. Song F, You Z, Yao X, Cheng J, Liu Z, Lin K. 133.  2009. Specific loops D, E and F of nicotinic acetylcholine receptor β1 subunit may confer imidacloprid selectivity between Myzus persicae and its predatory enemy Pardosa pseudoannulata. Insect Biochem. Mol. Biol. 39:833–41 [Google Scholar]
  134. Sparagano OAE, George DR, Harrington DWJ, Giangaspero A. 134.  2014. Significance and control of the poultry red mite, Dermanyssus gallinae. Annu. Rev. Entomol. 59:447–66 [Google Scholar]
  135. Sun W, Valero MC, Seong KM, Steele LD, Huang IT. 135.  et al. 2015. A glycine insertion in the estrogen-related receptor ERR is associated with enhanced expression of three cytochrome P450 genes in transgenic Drosophila melanogaster. PLOS ONE 10:e0118779 [Google Scholar]
  136. Tsagkarakou A, Van Leeuwen T, Khajehali J, Ilias A, Grispou M. 136.  et al. 2009. Identification of pyrethroid resistance associated mutations in the para sodium channel of the two-spotted spider mite Tetranychus urticae (Acari: Tetranychidae). Insect Mol. Biol. 18:583–93 [Google Scholar]
  137. van Engelsdorp D, Evans JD, Saegerman C, Mullin C, Haubruge E. 137.  et al. 2009. Colony collapse disorder: a descriptive study. PLOS ONE 4:e6481 [Google Scholar]
  138. Van Leeuwen T, Demaeght P, Osborne EJ, Dermauw W, Gohlke S. 138.  et al. 2012. Population bulk segregant mapping uncovers resistance mutations and the mode of action of a chitin synthesis inhibitor in arthropods. PNAS 109:4407–12A high-resolution mapping method reveals chitin synthase 1 as the target site of etoxazole. [Google Scholar]
  139. Van Leeuwen T, Dermauw W, Grbić M, Tirry L, Feyereisen R. 139.  2013. Spider mite control and resistance management: Does a genome help?. Pest Manag. Sci. 69:156–59 [Google Scholar]
  140. Van Leeuwen T, Tirry L, Yamamoto A, Nauen R, Dermauw W. 140.  2015. The economic importance of acaricides in the control of phytophagous mites and an update on recent acaricide mode of action research. Pestic. Biochem. Physiol. 121:12–21 [Google Scholar]
  141. Van Leeuwen T, Vanholme B, Van Pottelberge S, Van Nieuwenhuyse P, Nauen R. 141.  et al. 2008. Mitochondrial heteroplasmy and the evolution of insecticide resistance: non-Mendelian inheritance in action. PNAS 105:5980–85Mitochondrially encoded bifenazate resistance, heteroplasmy, and genetic bottlenecking as a new paradigm for resistance. [Google Scholar]
  142. Van Leeuwen T, Vontas J, Tsagkarakou A, Dermauw W, Tirry L. 142.  2010. Acaricide resistance mechanisms in the two-spotted spider mite Tetranychus urticae and other important Acari: a review. Insect Biochem. Mol. Biol. 40:563–72 [Google Scholar]
  143. Van Leeuwen T, Vontas J, Tsagkarakou A, Tirry L. 143.  2009. Mechanisms of acaricide resistance in the two-spotted spider mite Tetranychus urticae. Biorational Control of Arthropod Pests I Ishaaya, AR Horowitz 347–93 Dordrecht, Neth: Springer [Google Scholar]
  144. Van Nieuwenhuyse P, Demaeght P, Dermauw W, Khalighi M, Stevens CV. 144.  et al. 2012. On the mode of action of bifenazate: new evidence for a mitochondrial target site. Pestic. Biochem. Physiol. 104:88–95 [Google Scholar]
  145. VanEtten HD, Mansfield JW, Bailey JA, Farmer EE. 145.  1994. Two classes of plant antibiotics: “phytoalexins” versus “phytoanticipins.”. Plant Cell 6:1191–92 [Google Scholar]
  146. Walter DE, Proctor HC. 146.  2013. Mites: Ecology, Evolution & Behaviour. Dordrecht, Neth: Springer, 2nd ed..
  147. Wang R, Liu Z, Dong K, Elzen PJ, Pettis J, Huang Z. 147.  2002. Association of novel mutations in a sodium channel gene with fluvalinate resistance in the mite, Varroa destructor. J. Apic. Res. 41:17–25 [Google Scholar]
  148. Wu K, Hoy MA. 148.  2014. Oral delivery of double-stranded RNA induces prolonged and systemic gene knockdown in Metaseiulus occidentalis only after feeding on Tetranychus urticae. Exp. Appl. Acarol. 63:171–87 [Google Scholar]
  149. Wybouw N, Balabanidou V, Ballhorn DJ, Dermauw W, Grbić M. 149.  et al. 2012. A horizontally transferred cyanase gene in the spider mite Tetranychus urticae is involved in cyanate metabolism and is differentially expressed upon host plant change. Insect Biochem. Mol. Biol. 42:881–9 [Google Scholar]
  150. Wybouw N, Dermauw W, Tirry L, Stevens C, Grbić M. 150.  et al. 2014. A gene horizontally transferred from bacteria protects arthropods from host plant cyanide poisoning. eLife 3:e02365First demonstration of a horizontally transferred gene with a function in detoxification of plant defense compounds. [Google Scholar]
  151. Wybouw N, Zhurov V, Martel C, Bruinsma K, Hendrickx F. 151.  et al. 2015. Adaptation of a polyphagous herbivore to a novel host plant extensively shapes the transcriptome of herbivore and host. Mol. Ecol. 24:4647–63Adaptation to a novel host alters transcriptional plasticity in the herbivore and attenuates plant defenses. [Google Scholar]
  152. Zhang HG, ffrench-Constant RH, Jackson MB. 152.  1994. A unique amino acid of the Drosophila GABA receptor with influence on drug sensitivity by two mechanisms. J. Physiol. 479:65–75 [Google Scholar]
  153. Zhang Z-Q. 153.  2011. Animal Biodiversity: An Outline of Higher-Level Classification and Survey of Taxonomic Richness Auckland: Magnolia
  154. Zhurov V, Navarro M, Bruinsma KA, Arbona V, Estrella Santamaria M. 154.  et al. 2014. Reciprocal responses in the interaction between Arabidopsis and the cell-content-feeding chelicerate herbivore spider mite. Plant Physiol. 164:384–99Reciprocal transcriptome responses provide molecular insights into the nature of T. urticae herbivory. [Google Scholar]
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The Molecular Evolution of Xenobiotic Metabolism and Resistance in Chelicerate Mites
Annual Review of Entomology 61, 475 (2016); https://doi.org/10.1146/annurev-ento-010715-023907
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