Transcriptome-based identification of ABC transporters in the western tarnished plant bug lygus hesperus

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Hull, J Joe ^a   Chaney, Kendrick ^a   Geib, Scott M ^a   Fabrick, Jeffrey A ^a   Brent, Colin S ^a   Walsh, Douglas ^b   Lavine, Laura Corley ^b  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; MULTIDRUG RESISTANCE PROTEIN; TRANSCRIPTOME;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTHROPOD; ARTICLE; CONTROLLED STUDY; ENZYME SPECIFICITY; EXPRESSED SEQUENCE TAG; GENE AMPLIFICATION; GENE DUPLICATION; GENE EXPRESSION PROFILING; GENETIC CONSERVATION; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HYDROPHOBICITY; LYGUS HESPERUS; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; OXIDATIVE STRESS; PHYLOGENETIC TREE; PHYLOGENY; PHYTOCHEMISTRY; POLYMERASE CHAIN REACTION; PROTEIN DOMAIN; PROTEIN EXPRESSION; RNA SEQUENCE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; SEXUAL MATURATION; SPERMATOZOON; STOP CODON; TRANSCRIPTOMICS; UNINDEXED SEQUENCE; ANIMAL; GENETICS; HETEROPTERA;

HEXAPODA; LYGUS; LYGUS HESPERUS; LYGUS LINEOLARIS; VERTEBRATA;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; HETEROPTERA; PHYLOGENY; TRANSCRIPTOME;

EID: 84912141750     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0113046     Document Type: Article

References (162)

1. Oldham ML, Davidson AL, Chen J (2008) Structural insights into ABC transporter mechanism. Curr Opin Struct Biol 18: 726-733.
2. Rees DC, Johnson E, Lewinson O (2009) ABC transporters: the power to change. Nature 10: 218-227.
3. Jones PM, O'Mara ML, George AM (2009) ABC transporters: a riddle wrapped in a mystery inside an enigma. Trends Biochem Sci 34: 520-531.
4. George AM, Jones PM (2012) Perspectives on the structure-function of ABC transporters: the Switch and Constant Contact models. Prog Biophys Mol Biol 109: 95-107.
5. Kartner N, Riordan JR, Ling V (1983) Cell surface P-glycoprotein associated with multidrug resistance in mammalian cell lines. Science 221: 1285-1288.
6. Lage H (2003) ABC-transporters: implications on drug resistance from microorganisms to human cancers. Int J Antimicrob Agents 22: 188-199.
7. Leprohon P, Légaré D, Ouellette M (2011) ABC transporters involved in drug resistance in human parasites. Essays Biochem 50: 121-144.
8. Dermauw W, Van Leeuwen T (2014) The ABC gene family in arthropods: Comparative genomics and role in insecticide transport and resistance. Insect Biochem Mol Biol 45: 89-110.
9. Bisbal C, Martinand C, Silhol M, Lebleu B, Salehzada T (1995) Cloning and characterization of a RNAse L inhibitor. A new component of the interferonregulated 2-5A pathway. J Biol Chem 270: 13308-13317.
10. Tyzack JK, Wang X, Belsham GJ, Proud CG (2000) ABC50 interacts with eukaryotic initiation factor 2 and associates with the ribosome in an ATPdependent manner. J Biol Chem 275: 34131-34139.
11. Dong J, Lai R, Nielsen K, Fekete CA, Qiu H, et al. (2004) The essential ATPbinding cassette protein RLI1 functions in translation by promoting preinitiation complex assembly. J Biol Chem 279: 42157-42168.
12. Paytubi S, Wang X, Lam YW, Izquierdo L, Hunter MJ, et al. (2009) ABC50 promotes translation initiation in mammalian cells. J Biol Chem 284: 24061-24073.
13. Barthelme D, Dinkelaker S, Albers S-V, Londei P, Ermler U, et al. (2011) Ribosome recycling depends on a mechanistic link between the FeS cluster domain and a conformational switch of the twin-ATPase ABCE1. Proc Natl Acad Sci USA 108: 3228-3233.
14. Dean M, Annilo T (2005) Evolution of the ATP-binding cassette (ABC) transporter superfamily in vertebrates. Annu Rev Genomics Hum Genet 6: 123-142.
15. Popovic M, Zaja R, Loncar J, Smital T (2010) A novel ABC transporter: the first insight into zebrafish (Danio rerio) ABCH1. Mar Environ Res 69 Suppl: S11-S13.
16. Broehan G, Kroeger T, Lorenzen M, Merzendorfer H (2013) Functional analysis of the ATP-binding cassette (ABC) transporter gene family of Tribolium castaneum . BMC Genomics 14: 6.
17. Ewart GD, Cannell D, Cox GB, Howells AJ (1994) Mutational analysis of the traffic ATPase (ABC) transporters involved in uptake of eye pigment precursors in Drosophila melanogaster. Implications for structure-function relationships. J Biol Chem 269: 10370-10377.
18. Mackenzie SM, Brooker MR, Gill TR, Cox GB, Howells AJ, et al. (1999) Mutations in the white gene of Drosophila melanogaster affecting ABC transporters that determine eye colouration. Biochim Biophys Acta 1419: 173-185.
19. Kômoto N, Quan G-X, Sezutsu H, Tamura T (2009) A single-base deletion in an ABC transporter gene causes white eyes, white eggs, and translucent larval skin in the silkworm w-3(oe) mutant. Insect Biochem Mol Biol 39: 152-156.
20. Wang L, Kiuchi T, Fujii T, Daimon T, Li M, et al. (2013) Mutation of a novel ABC transporter gene is responsible for the failure to incorporate uric acid in the epidermis of ok mutants of the silkworm, Bombyx mori. Insect Biochem Mol Biol 43: 562-571.
21. Ricardo S, Lehmann R (2009) An ABC transporter controls export of a Drosophila germ cell attractant. Science 323: 943-946.
22. Itoh TQ, Tanimura T, Matsumoto A (2011) Membrane-bound transporter controls the circadian transcription of clock genes in Drosophila. Genes Cells 16: 1159-1167.
23. Strauss AS, Peters S, Boland W, Burse A (2013) ABC transporter functions as a pacemaker for the sequestration of plant glucosides in leaf beetles. eLife 2: e01096.
24. Borycz J, Borycz JA, Kubow A, Lloyd V, Meinertzhagen IA (2008) Drosophila ABC transporter mutants white, brown and scarlet have altered contents and distribution of biogenic amines in the brain. J Exp Biol 211: 3454-3466.
25. Buss DS, Callaghan A (2008) Interaction of pesticides with p-glycoprotein and other ABC proteins: A survey of the possible importance to insecticide, herbicide and fungicide resistance. Pest Biochem Physiol 90: 141-153.
26. Gahan LJ, Pauchet Y, Vogel H, Heckel DG (2010) An ABC transporter mutation is correlated with insect resistance to Bacillus thuringiensis Cry1Ac toxin. PLoS Genet 6: e1001248.
27. Baxter SW, Badenes-Perez FR, Morrison A, Vogel H, Crickmore N, et al. (2011) Parallel evolution of Bacillus thuringiensis toxin resistance in Lepidoptera. Genetics 189: 675-679.
28. Atsumi S, Miyamoto K, Yamamoto K, Narukawa J, Kawai S, et al. (2012) Single amino acid mutation in an ATP-binding cassette transporter gene causes resistance to Bt toxin Cry1Ab in the silkworm, Bombyx mori. Proc Natl Acad Sci USA 109: E1591-E1598.
29. Heckel DG (2012) Learning the ABCs of Bt: ABC transporters and insect resistance to Bacillus thuringiensis provide clues to a crucial step in toxin mode of action. Pest Biochem Physiol 104: 103-110.
30. Lei Y, Zhu X, Xie W, Wu Q, Wang S, et al. (2014) Midgut transcriptome response to a Cry toxin in the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). Gene 533: 180-187.
31. Park Y, González-Martínez RM, Navarro-Cerrillo G, Chakroun M, Kim Y, et al. (2014) ABCC transporters mediate insect resistance to multiple Bt toxins revealed by bulk segregant analysis. BMC Biology 12: 46.
32. Sturm A, Cunningham P, Dean M (2009) The ABC transporter gene family of Daphnia pulex. BMC Genomics 10: 170.
33. Dermauw W, Osborne EJ, Clark RM, Grbić M, Tirry L, et al. (2013) A burst of ABC genes in the genome of the polyphagous spider mite Tetranychus urticae. BMC Genomics 14: 317.
34. Dean M, Rzhetsky A, Allikmets R (2001) The human ATP-binding cassette (ABC) transporter superfamily. Genome Res 11: 1156-1166.
35. Pavlidi N, Dermauw W, Rombauts S, Chrisargiris A, Van Leeuwen T, et al. (2013) Analysis of the olive fruit fly Bactrocera oleae transcriptome and phylogenetic classification of the major detoxification gene families. PLoS ONE 8: e66533.
36. Roth CW, Holm I, Graille M, Dehoux P, Rzhetsky A, et al. (2003) Identification of the Anopheles gambiae ATP-binding cassette transporter superfamily genes. Mol Cells 15: 150-158.
37. Liu S, Zhou S, Tian L, Guo E, Luan Y, et al. (2011) Genome-wide identification and characterization of ATP-binding cassette transporters in the silkworm, Bombyx mori. BMC Genomics 12: 491.
38. Xie X, Cheng T, Wang G, Duan J, Niu W, et al. (2012) Genome-wide analysis of the ATP-binding cassette (ABC) transporter gene family in the silkworm, Bombyx mori. Mol Biol Rep 39: 7281-7291.
39. Strauss AS, Wang D, Stock M, Gretscher RR, Groth M, et al. (2014) Tissuespecific transcript profiling for ABC transporters in the sequestering larvae of the phytophagous leaf beetle Chrysomela populi. PLoS ONE 9: e98637.
40. International Aphid Genomics Consortium (2010) Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biol 8: e1000313.
41. Ye X-D, Su Y-L, Zhao Q-Y, Xia W-Q, Liu S-S, et al. (2014) Transcriptomic analyses reveal the adaptive features and biological differences of guts from two invasive whitefly species. BMC Genomics 15: 370.
42. Yang N, Xie W, Jones CM, Bass C, Jiao X, et al. (2013) Transcriptome profiling of the whitefly Bemisia tabaci reveals stage-specific gene expression signatures for thiamethoxam resistance. Insect Mol Biol 22: 485-496.
43. Xia J, Zhang C-R, Zhang S, Li F-F, Feng M-G, et al. (2013) Analysis of whitefly transcriptional responses to Beauveria bassiana infection reveals new insights into insect-fungus interactions. PLoS ONE 8: e68185.
44. Mamidala P, Wijeratne AJ, Wijeratne S, Kornacker K, Sudhamalla B, et al. (2012) RNA-Seq and molecular docking reveal multi-level pesticide resistance in the bed bug. BMC Genomics 13: 6.
45. Bao Y-Y, Li B-L, Liu Z-B, Xue J, Zhu Z-R, et al. (2010) Triazophos upregulated gene expression in the female brown planthopper, Nilaparvata lugens. J Insect Physiol 56: 1087-1094.
46. Scott DR (1977) An annotated listing of host plants of Lygus hesperus Knight. Entomol Soc Am Bull 23: 19-22.
47. Young OP (1986) Host plants of the tarnished plant bug, Lygus lineolaris (Heteroptera: Miridae). Ann Entomol Soc Am 79: 747-762.
48. Wheeler AG (2001) Biology of the plant bugs (Hemiptera: Miridae): pests, predators, opportunists. Ithaca, NY: Comstock Publishing Associates. 528 p.
49. Snodgrass GL (1996) Insecticide resistance in field populations of the tarnished plant bug (Heteroptera: Miridae) in cotton in the Mississippi Delta. J Econ Entomol 89: 783-790.
50. Snodgrass G, Scott W (2002) Tolerance to acephate in tarnished plant bug (Heteroptera: Miridae) populations in the Mississippi river delta. Southwestern Entomologist 27: 191-199.
51. Snodgrass G, Gore J, Abel C, Jackson R (2009) Acephate resistance in populations of the tarnished plant bug (Heteroptera: Miridae) from the Mississippi River Delta. J Econ Entomol 102: 699-707.
52. Hull JJ, Geib SM, Fabrick JA, Brent CS (2013) Sequencing and de novo assembly of the western tarnished plant bug (Lygus hesperus) transcriptome. PLoS ONE 8: e55105.
53. Tapadia MG, Lakhotia SC (2005) Expression of mdr49 and mdr65 multidrug resistance genes in larval tissues of Drosophila melanogaster under normal and stress conditions. Cell Stress Chaperones 10: 7-11.
54. de Boussac H, Orbán TI, Várady G, Tihanyi B, Bacquet C, et al. (2012) Stimulus-induced expression of the ABCG2 multidrug transporter in HepG2 hepatocarcinoma model cells involves the ERK1/2 cascade and alternative promoters. Biochem Biophys Res Commun 426: 172-176.
55. de Araujo Leite JC, de Vasconcelos RB, da Silva SG, de Siqueira-Junior JP, Marques-Santos LF (2013) ATP-binding cassette transporters protect sea urchin gametes and embryonic cells against the harmful effects of ultraviolet light. Mol Reprod Dev 81: 66-83.
56. Kim Y, Park S-Y, Kim D, Choi J, Lee Y-H, et al. (2013) Genome-scale analysis of ABC transporter genes and characterization of the ABCC type transporter genes in Magnaporthe oryzae. Genomics 101: 354-361.
57. Kulkarni SR, Donepudi AC, Xu J, Wei W, Cheng QC, et al. (2014) Fasting induces nuclear factor E2-related factor 2 and ATP-binding cassette transporters via protein kinase A and sirtuin-1 in mouse and human. Antioxid Redox Signal 20: 15-30.
58. Peelman F, Labeur C, Vanloo B, Roosbeek S, Devaud C, et al. (2003) Characterization of the ABCA transporter subfamily: identification of prokaryotic and eukaryotic members, phylogeny and topology. J Mol Biol 325: 259-274.
59. Beers MF, Hawkins A, Shuman H, Zhao M, Newitt JL, et al. (2011) A novel conserved targeting motif found in ABCA transporters mediates trafficking to early post-Golgi compartments. J Lipid Res 52: 1471-1482.
60. Kaminski WE, Piehler A, Wenzel JJ (2006) ABC A-subfamily transporters: Structure, function and disease. Biochim Biophys Acta 1762: 510-524.
61. Albrecht C, Viturro E (2007) The ABCA subfamily-gene and protein structures, functions and associated hereditary diseases. Pflugers Arch 453: 581-589.
62. Akiyama M, Sugiyama-Nakagiri Y, Sakai K, McMillan JR, Goto M, et al. (2005) Mutations in lipid transporter ABCA12 in harlequin ichthyosis and functional recovery by corrective gene transfer. J Clin Invest 115: 1777-1784.
63. Bain LJ, LeBlanc GA (1996) Interaction of structurally diverse pesticides with the human MDR1 gene product P-glycoprotein. Toxicol Appl Pharmacol 141: 288-298.
64. Gottesman MM, Fojo T, Bates SE (2002) Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer 2: 48-58.
65. Szakács G, Annereau J-P, Lababidi S, Shankavaram U, Arciello A, et al. (2004) Predicting drug sensitivity and resistance: profiling ABC transporter genes in cancer cells. Cancer Cell 6: 129-137.
66. Yasui K, Mihara S, Zhao C, Okamoto H, Saito-Ohara F, et al. (2004) Alteration in copy numbers of genes as a mechanism for acquired drug resistance. Cancer Res 64: 1403-1410.
67. Sooksa-Nguan T, Yakubov B, Kozlovskyy VI, Barkume CM, Howe KJ, et al. (2009) Drosophila ABC transporter, DmHMT-1, confers tolerance to cadmium. DmHMT-1 and its yeast homolog, SpHMT-1, are not essential for vacuolar phytochelatin sequestration. J Biol Chem 284: 354-362.
68. Bariami V, Jones CM, Poupardin R, Vontas J, Ranson H (2012) Gene amplification, ABC transporters and cytochrome P450s: unraveling the molecular basis of pyrethroid resistance in the dengue vector, Aedes aegypti. PLoS Negl Trop Dis 6: e1692.
69. Telonis-Scott M, Hallas R, McKechnie SW, Wee CW, Hoffmann AA (2009) Selection for cold resistance alters gene transcript levels in Drosophila melanogaster. J Insect Physiol 55: 549-555.
70. Parcej D, Tampé R (2010) ABC proteins in antigen translocation and viral inhibition. Nature Chemical Biology 6: 572-580.
71. Abele R, Tampé R (2011) The TAP translocation machinery in adaptive immunity and viral escape mechanisms. Essays Biochem 50: 249-264.
72. Wu CT, Budding M, Griffin MS, Croop JM (1991) Isolation and characterization of Drosophila multidrug resistance gene homologs. Mol Cell Biol 11: 3940-3948.
73. Vache C, Camares O, Cardoso-Ferreira M-C, Dastugue B, Creveaux I, et al. (2007) A potential genomic biomarker for the detection of polycyclic aromatic hydrocarbon pollutants: multidrug resistance gene 49 in Drosophila melanogaster. Environ Toxicol Chem 26: 1418-1424.
74. Azad P, Zhou D, Russo E, Haddad GG (2009) Distinct mechanisms underlying tolerance to intermittent and constant hypoxia in Drosophila melanogaster. PLoS ONE 4: e5371.
75. Chahine S, O'Donnell MJ (2009) Physiological and molecular characterization of methotrexate transport by Malpighian tubules of adult Drosophila melanogaster. J Insect Physiol 55: 927-935.
76. Figueira-Mansur J, Ferreira-Pereira A, Mansur JF, Franco TA, Alvarenga ESL, et al. (2013) Silencing of P-glycoprotein increases mortality in temephos-treated Aedes aegypti larvae. Insect Mol Biol 22: 648-658.
77. Tian L, Yang J, Hou W, Xu B, Xie W, et al. (2013) Molecular cloning and characterization of a P-glycoprotein from the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). Intl J Mol Sci 14: 22891-22905.
78. Luo L, Sun Y-J, Wu Y-J (2013) Abamectin resistance in Drosophila is related to increased expression of P-glycoprotein via the dEGFR and dAkt pathways. Insect Biochem Mol Biol 43: 627-634.
79. Toyoda Y, Hagiya Y, Adachi T, Hoshijima K, Kuo MT, et al. (2008) MRP class of human ATP binding cassette (ABC) transporters: historical background and new research directions. Xenobiotica 38: 833-862.
80. Keppler D (2010) Multidrug Resistance Proteins (MRPs, ABCCs): importance for pathophysiology and drug therapy. Drug Transporters. Handbook of Experimental Pharmacology. Berlin, Heidelberg: Springer Berlin Heidelberg, Vol. 201. 299-323.
81. Slot AJ, Molinski SV, Cole SPC (2011) Mammalian multidrug-resistance proteins (MRPs). Essays Biochem 50: 179-207.
82. Dassa E, Bouige P (2001) The ABC of ABCs: a phylogenetic and functional classification of ABC systems in living organisms. Res Microbiol 152: 211-229.
83. Grailles M, Brey PT, Roth CW (2003) The Drosophila melanogaster multidrugresistance protein 1 (MRP1) homolog has a novel gene structure containing two variable internal exons. Gene 307: 41-50.
84. Labbé R, Caveney S, Donly C (2011) Genetic analysis of the xenobiotic resistance-associated ABC gene subfamilies of the Lepidoptera. Insect Mol Biol 20: 243-256.
85. Chahine S, O'Donnell MJ (2011) Interactions between detoxification mechanisms and excretion in Malpighian tubules of Drosophila melanogaster. J Exp Biol 214: 462-468.
86. Luckenbach T, Epel D (2008) ABCB- and ABCC-type transporters confer multixenobiotic resistance and form an environment-tissue barrier in bivalve gills. Am J Physiol Regul Integr Comp Physiol 294: R1919-R1929.
87. Kruh GD, Guo Y, Hopper-Borge E, Belinsky MG, Chen Z-S (2006) ABCC10, ABCC11, and ABCC12. Pflugers Arch 453: 675-684.
88. Beckstead RB, Lam G, Thummel CS (2007) Specific transcriptional responses to juvenile hormone and ecdysone in Drosophila. Insect Biochem Mol Biol 37: 570-578.
89. Vodovar N, Vinals M, Liehl P, Basset A, Degrouard J, et al. (2005) Drosophila host defense after oral infection by an entomopathogenic Pseudomonas species. Proc Natl Acad Sci USA 102: 11414-11419.
90. Yepiskoposyan H, Egli D, Fergestad T, Selvaraj A, Treiber C, et al. (2006) Transcriptome response to heavy metal stress in Drosophila reveals a new zinc transporter that confers resistance to zinc. Nucleic Acids Res 34: 4866-4877.
91. Morozova TV, Anholt RRH, Mackay TFC (2006) Transcriptional response to alcohol exposure in Drosophila melanogaster. Genome Biol 7: R95.
92. Monnier V, Girardot F, Cheret C, Andres O, Tricoire H (2002) Modulation of oxidative stress resistance in Drosophila melanogaster by gene overexpression. Genesis 34: 76-79.
93. Huang H, Haddad GG (2007) Drosophila dMRP4 regulates responsiveness to O2 deprivation and development under hypoxia. Physiol Genomics 29: 260-266.
94. Fernández-Ayala DJ, Chen S, Kemppainen E, O'Dell KMC, Jacobs HT (2010) Gene expression in a Drosophila model of mitochondrial disease. PLoS ONE 5: e8549.
95. Shah S, Yarrow C, Dunning R, Cheek B, Vass S, et al. (2011) Insecticide detoxification indicator strains as tools for enhancing chemical discovery screens. Pest Manag Sci 68: 38-48.
96. Tanaka S, Miyamoto K, Noda H, Jurat-Fuentes JL, Yoshizawa Y, et al. (2013) The ATP-binding cassette transporter subfamily C member 2 in Bombyx mori larvae is a functional receptor for Cry toxins from Bacillus thuringiensis. FEBS J 280: 1782-1794.
97. Baum JA, Sukuru UR, Penn SR, Meyer SE, Subbarao S, et al. (2012) Cotton plants expressing a hemipteran-active Bacillus thuringiensis crystal protein impact the development and survival of Lygus hesperus (Hemiptera: Miridae) nymphs. J Econ Entomol 105: 616-624.
98. Aittoniemi J, Fotinou C, Craig TJ, de Wet H, Proks P, et al. (2009) SUR1: a unique ATP-binding cassette protein that functions as an ion channel regulator. Philos Trans R Soc Lond B Biol Sci 364: 257-267.
99. Kim SK, Rulifson EJ (2004) Conserved mechanisms of glucose sensing and regulation by Drosophila corpora cardiaca cells. Nature 431: 316-320.
100. Akasaka T, Klinedinst S, Ocorr K, Bustamante EL, Kim SK, et al. (2006) The ATP-sensitive potassium (KATP) channel-encoded dSUR gene is required for Drosophila heart function and is regulated by tinman. Proc Natl Acad Sci USA 103: 11999-12004.
101. Li Y, Qin Y, Yang N, Sun Y, Yang X, et al. (2013) Studies on insecticidal activities and action mechanism of novel benzoylphenylurea candidate NK-17. PLoS ONE 8: e66251.
102. Merzendorfer H, Kim HS, Chaudhari SS, Kumari M, Specht CA, et al. (2012) Genomic and proteomic studies on the effects of the insect growth regulator diflubenzuron in the model beetle species Tribolium castaneum. Insect Biochem Mol Biol 42: 264-276.
103. Meyer F, Flötenmeyer M, Moussian B (2013) The sulfonylurea receptor Sur is dispensable for chitin synthesis in Drosophila melanogaster embryos. Pest Manag Sci 69: 1136-1140.
104. Jordan IK, Kota KC, Cui G, Thompson CH, McCarty NA (2008) Evolutionary and functional divergence between the cystic fibrosis transmembrane conductance regulator and related ATP-binding cassette transporters. Proc Natl Acad Sci USA 105: 18865-18870.
105. Wanders RJ, Visser WF, van Roermund CWT, Kemp S, Waterham HR (2007) The peroxisomal ABC transporter family. Pflugers Arch 453: 719-734.
106. Morita M, Imanaka T (2012) Peroxisomal ABC transporters: structure, function and role in disease. Biochim Biophys Acta 1822: 1387-1396.
107. Shani N, Sapag A, Valle D (1996) Characterization and analysis of conserved motifs in a peroxisomal ATP-binding cassette transporter. J Biol Chem 271: 8725-8730.
108. Mosallanejad H, Badisco L, Swevers L, Soin T, Knapen D, et al. (2010) Ecdysone signaling and transcript signature in Drosophila cells resistant against methoxyfenozide. J Insect Physiol 56: 1973-1985.
109. Khoshnevis S, Gross T, Rotte C, Baierlein C, Ficner R, et al. (2010) The ironsulphur protein RNase L inhibitor functions in translation termination. EMBO Reports 11: 214-219.
110. Liu S, Li Q, Liu Z (2013) Genome-wide identification, characterization and phylogenetic analysis of 50 catfish ATP-binding cassette (ABC) transporter genes. PLoS ONE 8: e63895.
111. Abruzzi KC, Rodriguez J, Menet JS, Desrochers J, Zadina A, et al. (2011) Drosophila CLOCK target gene characterization: implications for circadian tissue-specific gene expression. Genes Dev 25: 2374-2386.
112. Tarr PT, Tarling EJ, Bojanic DD, Edwards PA, Baldán A (2009) Emerging new paradigms for ABCG transporters. Biochim Biophys Acta 1791: 584-593.
113. Kerr ID, Haider AJ, Gelissen IC (2011) The ABCG family of membraneassociated transporters: you don't have to be big to be mighty. Br J Pharmacol 164: 1767-1779.
114. Weber AL, Khan GF, Magwire MM, Tabor CL, Mackay TFC, et al. (2012) Genome-wide association analysis of oxidative stress resistance in Drosophila melanogaster. PLoS ONE 7: e34745.
115. Buchmann J, Meyer C, Neschen S, Augustin R, Schmolz K, et al. (2007) Ablation of the cholesterol transporter adenosine triphosphate-binding cassette transporter G1 reduces adipose cell size and protects against diet-induced obesity. Endocrinology 148: 1561-1573.
116. Morozova TV, Anholt RRH, Mackay TFC (2007) Phenotypic and transcriptional response to selection for alcohol sensitivity in Drosophila melanogaster. Genome Biol 8: R231.
117. Hock T, Cottrill T, Keegan J, Garza D (2000) The E23 early gene of Drosophila encodes an ecdysone-inducible ATP-binding cassette transporter capable of repressing ecdysone-mediated gene activation. Proc Natl Acad Sci USA 97: 9519-9524.
118. Tan A, Palli SR (2008) Edysone receptor isoforms play distinct roles in controlling molting and metamorphosis in the red flour beetle, Tribolium castaneum. Mol Cell Endocrinol 291: 42-49.
119. Bryon A, Wybouw N, Dermauw W, Tirry L, Van Leeuwen T (2013) Genome wide gene-expression analysis of facultative reproductive diapause in the twospotted spider mite Tetranychus urticae. BMC Genomics 14: 815.
120. Abraham EG, Sezutsu H, Kanda T, Sugasaki T, Shimada T, et al. (2000) Identification and characterisation of a silkworm ABC transporter gene homologous to Drosophila white. Mol Gen Genet 264: 11-19.
121. Tatematsu K-I, Yamamoto K, Uchino K, Narukawa J, Iizuka T, et al. (2011) Positional cloning of silkworm white egg 2 (w-2) locus shows functional conservation and diversification of ABC transporters for pigmentation in insects. Genes Cells 16: 331-342.
122. Anaka M, MacDonald CD, Barkova E, Simon K, Rostom R, et al. (2008) The white gene of Drosophila melanogaster encodes a protein with a role in courtship behavior. J Neurogenet 22: 243-276.
123. Snodgrass GL (2002) Characteristics of a red-eye mutant of the tarnished plant bug (Heteroptera: Miridae). Ann Entomol Soc Am 95: 366-369.
124. Allen ML (2013) Genetics of a sex-linked recessive red eye color mutant of the tarnished plant bug, Lygus lineolaris. Open J Anim Sci 3: 1-9.
125. Liu S-H, Yao J, Yao H-W, Jiang P-L, Yang B-J, et al. (2014) Biological and biochemical characterization of a red-eye mutant in Nilaparvata lugens (Hemiptera: Delphacidae). Insect Science 21: 469-476.
126. Seo BY, Jung JK, Kim Y (2011) An orange-eye mutant of the brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae). J Asia-Pacific Entomol 14: 469-472.
127. Annilo T, Chen Z-Q, Shulenin S, Costantino J, Thomas L, et al. (2006) Evolution of the vertebrate ABC gene family: analysis of gene birth and death. Genomics 88: 1-11.
128. Mummery-Widmer JL, Yamazaki M, Stoeger T, Novatchkova M, Bhalerao S, et al. (2009) Genome-wide analysis of Notch signalling in Drosophila by transgenic RNAi. Nature 458: 987-992.
129. Zhang S, Feany MB, Saraswati S, Littleton JT, Perrimon N (2009) Inactivation of Drosophila Huntingtin affects long-term adult functioning and the pathogenesis of a Huntington's disease model. Dis Model Mech 2: 247-266.
130. Qin W, Neal SJ, Robertson RM, Westwood JT, Walker VK (2005) Cold hardening and transcriptional change in Drosophila melanogaster. Insect Mol Biol 14: 607-613.
131. You M, Yue Z, He W, Yang X, Yang G, et al. (2013) A heterozygous moth genome provides insights into herbivory and detoxification. Nat Genet 45: 220-225.
132. Robinson SW, Herzyk P, Dow JAT, Leader DP (2012) FlyAtlas: database of gene expression in the tissues of Drosophila melanogaster. Nucleic Acids Res 41: D744-D750.
133. Sullivan DT, Bell LA, Paton DR, Sullivan MC (1980) Genetic and functional analysis of tryptophan transport in Malpighian tubules of Drosophila. Biochem Genet 18: 1109-1130.
134. Dow JAT, Davies S-A (2006) The Malpighian tubule: Rapid insights from postgenomic biology. J Insect Physiol 52: 365-378.
135. Dow JAT (2009) Insights into the Malpighian tubule from functional genomics. J Exp Biol 212: 435-445.
136. Wang J, Kean L, Yang J, Allan AK, Davies S-A, et al. (2004) Functioninformed transcriptome analysis of Drosophila renal tubule. Genome Biol 5: R69.
137. Yang J, McCart C, Woods DJ, Terhzaz S, Greenwood KG, et al. (2007) A Drosophila systems approach to xenobiotic metabolism. Physiol Genomics 30: 223-231.
138. Labbé R, Caveney S, Donly C (2011) Expression of multidrug resistance proteins is localized principally to the Malpighian tubules in larvae of the cabbage looper moth, Trichoplusia ni. J Exp Biol 214: 937-944.
139. Wasbrough ER, Dorus S, Hester S, Howard-Murkin J, Lilley K, et al. (2010) The Drosophila melanogaster sperm proteome-II (DmSP-II). J Proteomics 73: 2171-2185.
140. Jones SR, Cyr DG (2011) Regulation and characterization of the ATP-binding cassette transporter-B1 in the epididymis and epididymal spermatozoa of the rat. Toxicol Sci 119: 369-379.
141. Gillott C (2003) Male accessory gland secretions: modulators of female reproductive physiology and behavior. Annu Rev Entomol 48: 163-184.
142. Avila FW, Sirot LK, LaFlamme BA, Rubinstein CD, Wolfner MF (2011) Insect seminal fluid proteins: identification and function. Annu Rev Entomol 56: 21-40.
143. Quan GX, Kanda T, Tamura T (2002) Induction of the white egg 3 mutant phenotype by injection of the double-stranded RNA of the silkworm white gene. Insect Mol Biol 11: 217-222.
144. Martins GF, Ramalho-Ortigao JM (2012) Oenocytes in insects. Inver Surv J 9: 139-152.
145. Zhu F, Gujar H, Gordon JR, Haynes KF, Potter MF, et al. (2013) Bed bugs evolved unique adaptive strategy to resist pyrethroid insecticides. Sci Rep 3: 1456.
146. Debolt JW (1982) Meridic diet for rearing successive generations of Lygus hesperus. Ann Entomol Soc Am 75: 119-122.
147. Brent CS, Hull JJ (2014) Characterization of male-derived factors inhibiting female sexual receptivity in Lygus hesperus . J Insect Physiol 60: 104-110.
148. Lohse M, Bolger AM, Nagel A, Fernie AR, Lunn JE, et al. (2012) RobiNA: a user-friendly, integrated software solution for RNA-Seq-based transcriptomics. Nucleic Acids Res 40: W622-W627.
149. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, et al. (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nature Protocols 8: 1494-1512.
150. Eddy SR (2011) Accelerated profile HMM searches. PLoS Comput Biol 7: e1002195.
151. Sheps JA, Ralph S, Zhao Z, Baillie DL, Ling V (2004) The ABC transporter gene family of Caenorhabditis elegans has implications for the evolutionary dynamics of multidrug resistance in eukaryotes. Genome Biol 5: R15.
152. de Castro E, Sigrist CJA, Gattiker A, Bulliard V, Langendijk-Genevaux PS, et al. (2006) ScanProsite: detection of PROSITE signature matches and ProRuleassociated functional and structural residues in proteins. Nucleic Acids Res 34: W362-W365.
153. Sigrist CJA, Cerutti L, de Castro E, Langendijk-Genevaux PS, Bulliard V, et al. (2010) PROSITE, a protein domain database for functional characterization and annotation. Nucleic Acids Res 38: D161-D166.
154. Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39: W29-W37.
155. Horton P, Park K-J, Obayashi T, Fujita N, Harada H, et al. (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35: W585-W587.
156. Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567-580.
157. Bernsel A, Viklund H, Hennerdal A, Elofsson A (2009) TOPCONS: consensus prediction of membrane protein topology. Nucleic Acids Res 37: W465-W468.
158. von Heijne G (1992) Membrane protein structure prediction. Hydrophobicity analysis and the positive-inside rule. J Mol Biol 225: 487-494.
159. Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113.
160. Price MN, Dehal PS, Arkin AP (2010) FastTree 2- approximately maximumlikelihood trees for large alignments. PLoS ONE 5: e9490.
161. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
162. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8: 275-282.