Fine-Mapping Nicotine Resistance Loci in Drosophila Using a Multiparent Advanced Generation Inter-Cross Population

Genetics

Volumn 198, Issue 1, 2014, Pages 45-57

  Marriage, Tara N ^a   King, Elizabeth G ^b   Long, Anthony D ^b   Macdonald, Stuart J ^a  

^a UNIVERSITY OF KANSAS   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME P450; CYTOCHROME P450 28D1; CYTOCHROME P450 28D2; GLUCURONOSYLTRANSFERASE; NICOTINE; RNA; UDP GLUCURONOSYLTRANSFERASE UGT86DD; UNCLASSIFIED DRUG; GLYCOSYLTRANSFERASE;

ADVANCED INTERCROSS LINE; ALLELE; ARTICLE; CONTROLLED STUDY; DETOXIFICATION; DROSOPHILA MELANOGASTER; GENE EXPRESSION; GENE LOCUS; GENE MAPPING; GENETIC RESISTANCE; GENETIC VARIABILITY; HERITABILITY; NONHUMAN; QUANTITATIVE TRAIT LOCUS; QUANTITATIVE TRAIT LOCUS MAPPING; RNA SEQUENCE; TOXICOGENETICS; ANIMAL; CHROMOSOME MAP; DRUG EFFECTS; DRUG RESISTANCE; GENETICS; INBREEDING;

ANIMALS; CHROMOSOME MAPPING; CYTOCHROME P-450 ENZYME SYSTEM; DROSOPHILA MELANOGASTER; DRUG RESISTANCE; GLYCOSYLTRANSFERASES; INBREEDING; NICOTINE; QUANTITATIVE TRAIT LOCI;

EID: 84907978425     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.114.162107     Document Type: Article

References (82)

1. Adler, P. N., L. F. Sobala, D. Thom, and R. Nagaraj, 2013 duskylike is required to maintain the integrity and planar cell polarity of hairs during the development of the Drosophila wing. Dev. Biol. 379: 76-91.
2. Bastide, H., A. Betancourt, V. Nolte, R. Tobler, P. Stobe et al., 2013 A genome-wide, fine-scale map of natural pigmentation variation in Drosophila melanogaster. PLoS Genet. 9: e1003534.
3. Baud, A., R. Hermsen, V. Guryev, P. Stridh, D. Graham et al., 2013 Combined sequence-based and genetic mapping analysis of complex traits in outbred rats. Nat. Genet. 45: 767-775.
4. Beavis, W. D., 1994 The power and deceit of QTL experiments: lessons from comparative QTL studies. Proceedings of the 49th Annual Corn and Sorghum Industry Research Conference. American Seed Trade Association, Washington, DC, pp. 250-266.
5. Bergland, A. O., H. S. Chae, Y. J. Kim, and M. Tatar, 2012 Finescale mapping of natural variation in fly fecundity identifies neuronal domain of expression and function of an aquaporin. PLoS Genet. 8: e1002631.
6. Boyle, A. P., S. Davis, H. P. Shulha, P. Meltzer, E. H. Margulies et al., 2008 High-resolution mapping and characterization of open chromatin across the genome. Cell 132: 311-322.
7. Burke, M. K., J. P. Dunham, P. Shahrestani, K. R. Thornton, M. R. Rose et al., 2010 Genome-wide analysis of a long-term evolution experiment with Drosophila. Nature 467: 587-590.
8. Carrillo, R., and G. Gibson, 2002 Unusual genetic architecture of natural variation affecting drug resistance in Drosophila melanogaster. Genet. Res. 80: 205-213.
9. Cheng, R., J. E. Lim, K. E. Samocha, G. Sokoloff, M. Abney et al., 2010 Genome-wide association studies and the problem of relatedness among advanced intercross lines and other highly recombinant populations. Genetics 185: 1033-1044.
10. Chung, H., M. R. Bogwitz, C. McCart, and A. Andrianopoulos, R.H. Ffrench-Constant et al., 2007 Cis-regulatory elements in the Accord retrotransposon result in tissue-specific expression of the Drosophila melanogaster insecticide resistance gene Cyp6g1. Genetics 175: 1071-1077.
11. Chung, H., T. Sztal, S. Pasricha, M. Sridhar, P. Batterham et al., 2009 Characterization of Drosophila melanogaster cytochrome P450 genes. Proc. Natl. Acad. Sci. USA 106: 5731-5736.
12. Chung, H., A. Boey, C. Lumb, L. Willoughby, P. Batterham et al., 2011 Induction of a detoxification gene in Drosophila melanogaster requires an interaction between tissue specific enhancers and a novel cis-regulatory element. Insect Biochem. Mol. Biol. 41: 863-871.
13. Churchill, G. A., and R. W. Doerge, 1994 Empirical threshold values for quantitative trait mapping. Genetics 138: 963-971.
14. Churchill, G. A., D. C. Airey, H. Allayee, J. M. Angel, A. D. Attie et al., 2004 The Collaborative Cross, a community resource for the genetic analysis of complex traits. Nat. Genet. 36: 1133-1137.
15. Cingolani, P., A. Platts, L. L. Wang, M. Coon, T. Nguyen et al., 2012 A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly (Austin) 6: 80-92.
16. Cookson, W., L. Liang, G. R. Abecasis, M. Moffatt, and M. Lathrop, 2009 Mapping complex disease traits with global gene expression. Nat. Rev. Genet. 10: 184-194.
17. Cooper, G. M., J. A. Johnson, T. Y. Langaee, H. Feng, I. B. Stanaway et al., 2008 A genome-wide scan for common genetic variants with a large influence on warfarin maintenance dose. Blood 112: 1022-1027.
18. Cridland, J. M., S. J. Macdonald, A. D. Long, and K. R. Thornton, 2013 Abundance and distribution of transposable elements intwo Drosophila QTL mapping resources. Mol. Biol. Evol. 30: 2311-2327.
19. Crow, J. F., 1957 Genetics of insect resistance to chemicals. Annu. Rev. Entomol. 2: 227-246.
20. Daborn, P. J., J. L. Yen, M. R. Bogwitz, G. Le Goff, E. Feil et al., 2002 A single p450 allele associated with insecticide resistance in Drosophila. Science 297: 2253-2256.
21. Darvasi, A., and M. Soller, 1995 Advanced intercross lines, an experimental population for fine genetic mapping. Genetics 141: 1199-1207.
22. Degner, J. F., A. A. Pai, R. Pique-Regi, J. B. Veyrieras, D. J. Gaffney et al., 2012 DNase I sensitivity QTLs are a major determinant of human expression variation. Nature 482: 390-394.
23. Dombrowski, S. M., R. Krishnan, M. Witte, S. Maitra, C. Diesing et al., 1998 Constitutive and barbital-induced expression of the Cyp6a2 allele of a high producer strain of CYP6A2 in the genetic background of a low producer strain. Gene 221: 69-77.
24. Ffrench-Constant, R. H., 1994 The molecular and population genetics of cyclodiene insecticide resistance. Insect Biochem. Mol. Biol. 24: 335-345.
25. Ffrench-Constant, R. H., 2013 The molecular genetics of insecticide resistance. Genetics 194: 807-815.
26. Ffrench-Constant, R. H., D. P. Mortlock, C. D. Shaffer, R. J. MacIntyre, and R. T. Roush, 1991 Molecular cloning and transformation of cyclodiene resistance in Drosophila: an invertebrate g-aminobutyric acid subtype A receptor locus. Proc. Natl. Acad. Sci. USA 88: 7209-7213.
27. Gaffney, D. J., J. B. Veyrieras, J. F. Degner, R. Pique-Regi, A. A. Pai et al., 2012 Dissecting the regulatory architecture of gene expression QTLs. Genome Biol. 13: R7.
28. Gibson, G., and B. Weir, 2005 The quantitative genetics of transcription. Trends Genet. 21: 616-623.
29. Gilad, Y., S. A. Rifkin, and J. K. Pritchard, 2008 Revealing the architecture of gene regulation: the promise of eQTL studies. Trends Genet. 24: 408-415.
30. Glendinning, J. I., 2002 How do herbivorous insects cope with noxious secondary plant compounds in their diet? Entomol. Exp. Appl. 104: 15-25.
31. Glendinning, J. I., 2007 How do predators cope with chemically defended foods? Biol. Bull. 213: 252-266.
32. Goulson, D., 2013 An overview of the environmental risks posed by neonicotinoid insecticides. J. Appl. Ecol. 50: 977-987.
33. Gruber, J. D., A. Genissel, S. J. Macdonald, and A. D. Long, 2007 How repeatable are associations between polymorphisms in achaete-scute and bristle number variation in Drosophila? Genetics 175: 1987-1997.
34. Hall, L. M., R. W. Von Borstel, B. C. Osmond, S. D. Hoeltzli, and T. H. Hudson, 1978 Genetic variants in an acetylcholine receptor from Drosophila melanogaster. FEBS Lett. 95: 243-246.
35. Huang, W., S. Richards, M. A. Carbone, D. Zhu, R. R. Anholt et al., 2012 Epistasis dominates the genetic architecture of Drosophila quantitative traits. Proc. Natl. Acad. Sci. USA 109: 15553-15559.
36. Hungate, E. A., E. J. Earley, I. A. Boussy, D. A. Turissini, C. T. Ting et al., 2013 A locus in Drosophila sechellia affecting tolerance of a host plant toxin. Genetics 195: 1063-1075.
37. Jha, P., C. Ramasundarahettige, V. Landsman, B. Rostron, M. Thun et al., 2013 21st-century hazards of smoking and benefits of cessation in the United States. N. Engl. J. Med. 368: 341-350.
38. Kaun, K. R., A. V. Devineni, and U. Heberlein, 2012 Drosophila melanogaster as a model to study drug addiction. Hum. Genet. 131: 959-975.
39. Kim, D., G. Pertea, C. Trapnell, H. Pimentel, R. Kelley et al., 2013 TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14: R36.
40. King, E. G., C. M. Merkes, C. L. McNeil, S. R. Hoofer, S. Sen et al., 2012a Genetic dissection of a model complex trait using the Drosophila Synthetic Population Resource. Genome Res. 22: 1558-1566.
41. King, E. G., S. J. Macdonald, and A. D. Long, 2012b Properties and power of the Drosophila Synthetic Population Resource for the routine dissection of complex traits. Genetics 191: 935-949.
42. Kislukhin, G., E. G. King, K. N. Walters, S. J. Macdonald, and A. D. Long, 2013 The genetic architecture of methotrexate toxicity is similar in Drosophila melanogaster and humans. G3 (Bethesda) 3: 1301-1310.
43. Kover, P. X., W. Valdar, J. Trakalo, N. Scarcelli, I. M. Ehrenreich et al., 2009 A multiparent advanced generation inter-cross to fine-map quantitative traits in Arabidopsis thaliana. PLoS Genet. 5: e1000551.
44. Lai, C. Q., J. Leips, W. Zou, J. F. Roberts, K. R. Wollenberg et al., 2007 Speed-mapping quantitative trait loci using microarrays. Nat. Methods 4: 839-841.
45. Li, X., M. A. Schuler, and M. R. Berenbaum, 2007 Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu. Rev. Entomol. 52: 231-253.
46. Li, X., S. Bai, and B. N. Cass, 2012 Accord insertion in the 59 flanking region of CYP6G1 confers nicotine resistance in Drosophila melanogaster. Gene 502: 1-8.
47. Long, A. D., S. L. Mullaney, T. F. Mackay, and C. H. Langley, 1996 Genetic interactions between naturally occurring alleles at quantitative trait loci and mutant alleles at candidate loci affecting bristle number in Drosophila melanogaster. Genetics 144: 1497-1510.
48. Long, A. D., R. F. Lyman, A. H. Morgan, C. H. Langley, and T. F. Mackay, 2000 Both naturally occurring insertions of transposable elements and intermediate frequency polymorphisms at the achaete-scute complex are associated with variation in bristle number in Drosophila melanogaster. Genetics 154: 1255-1269.
49. Luque, T., and D. R. O’Reilly, 2002 Functional and phylogenetic analyses of a putative Drosophila melanogaster UDPglycosyltransferase gene. Insect Biochem. Mol. Biol. 32: 1597-1604.
50. Macdonald, S. J., and A. D. Long, 2007 Joint estimates of quantitative trait locus effect and frequency using synthetic recombinant populations of Drosophila melanogaster. Genetics 176: 1261-1281.
51. Mackay, T. F., and C. H. Langley, 1990 Molecular and phenotypic variation in the achaete-scute region of Drosophila melanogaster. Nature 348: 64-66.
52. Mackay, T. F., S. Richards, E. A. Stone, A. Barbadilla, J. F. Ayroles et al., 2012 The Drosophila melanogaster Genetic Reference Panel. Nature 482: 173-178.
53. Marygold, S. J., P. C. Leyland, R. L. Seal, J. L. Goodman, J. Thurmond et al., 2013 FlyBase: improvements to the bibliography. Nucleic Acids Res. 41: D751-D757.
54. Misra, J. R., M. A. Horner, G. Lam, and C. S. Thummel, 2011 Transcriptional regulation of xenobiotic detoxification in Drosophila. Genes Dev. 25: 1796-1806.
55. Mokdad, A. H., J. S. Marks, D. F. Stroup, and J. L. Gerberding, 2004 Actual causes of death in the United States, 2000. JAMA 291: 1238-1245.
56. Park, J. H., S. Wacholder, M. H. Gail, U. Peters, K. B. Jacobs et al., 2010 Estimation of effect size distribution from genome-wide association studies and implications for future discoveries. Nat. Genet. 42: 570-575.
57. Passador-Gurgel, G., W. P. Hsieh, P. Hunt, N. Deighton, and G. Gibson, 2007 Quantitative trait transcripts for nicotine resistance in Drosophila melanogaster. Nat. Genet. 39: 264-268.
58. Pasyukova, E. G., C. Vieira, and T. F. Mackay, 2000 Deficiency mapping of quantitative trait loci affecting longevity in Drosophila melanogaster. Genetics 156: 1129-1146.
59. Perry, T., P. Batterham, and P. J. Daborn, 2011 The biology of insecticidal activity and resistance. Insect Biochem. Mol. Biol. 41: 411-422.
60. Pinheiro, J., D. Bates, S. DebRoy, D. Sarkar; and R Development Core Team, 2011 nlme: linear and nonlinear mixed effects models. R package version 3.1-101.
61. Schmidt, J. M., R. T. Good, B. Appleton, J. Sherrard, G. C. Raymant et al., 2010 Copy number variation and transposable elements feature in recent, ongoing adaptation at the Cyp6g1 locus. PLoS Genet. 6: e1000998.
62. Shrimpton, A. E., T. F. Mackay, and A. J. Brown, 1990 Transposable element-induced response to artificial selection in Drosophila melanogaster: molecular analysis of selection lines. Genetics 125: 803-811.
63. Snyder, M. J., and J. I. Glendinning, 1996 Causal connection between detoxification enzyme activity and consumption of a toxic plant compound. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 179: 255-261.
64. Stamatoyannopoulos, J. A., 2004 The genomics of gene expression. Genomics 84: 449-457.
65. Steppuhn, A., K. Gase, B. Krock, R. Halitschke, and I. T. Baldwin, 2004 Nicotine’s defensive function in nature. PLoS Biol. 2: E217.
66. Strode, C., C. S. Wondji, J. P. David, N. J. Hawkes, N. Lumjuan et al., 2008 Genomic analysis of detoxification genes in the mosquito Aedes aegypti. Insect Biochem. Mol. Biol. 38: 113-123.
67. Svenson, K. L., D. M. Gatti, W. Valdar, C. E. Welsh, R. Cheng et al., 2012 High-resolution genetic mapping using the Mouse Diversity outbred population. Genetics 190: 437-447.
68. Takeuchi, F., R. McGinnis, S. Bourgeois, C. Barnes, N. Eriksson et al., 2009 A genome-wide association study confirms VKORC1, CYP2C9, and CYP4F2 as principal genetic determinants of warfarin dose. PLoS Genet. 5: e1000433.
69. Thomas, S., X. Y. Li, P. J. Sabo, R. Sandstrom, R. E. Thurman et al., 2011 Dynamic reprogramming of chromatin accessibility during Drosophila embryo development. Genome Biol. 12: R43.
70. Threadgill, D. W., and G. A. Churchill, 2012 Ten years of the collaborative cross. G3 (Bethesda) 2: 153-156.
71. Trapnell, C., L. Pachter, and S. L. Salzberg, 2009 TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111.
72. Trapnell, C., B. A. Williams, G. Pertea, A. Mortazavi, G. Kwan et al., 2010 Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28: 511-515.
73. Trapnell, C., D. G. Hendrickson, M. Sauvageau, L. Goff, J. L. Rinn et al., 2013 Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat. Biotechnol. 31: 46-53.
74. Turner, T. L., A. D. Stewart, A. T. Fields, W. R. Rice, and A. M. Tarone, 2011 Population-based resequencing of experimentally evolved populations reveals the genetic basis of body size variation in Drosophila melanogaster. PLoS Genet. 7: e1001336.
75. Turner, T. L., P. M. Miller, and V. A. Cochrane, 2013 Combining genome-wide methods to investigate the genetic complexity of courtship song variation in Drosophila melanogaster. Mol. Biol. Evol. 30: 2113-2120.
76. Wayne, M. L., and L. M. McIntyre, 2002 Combining mapping and arraying: an approach to candidate gene identification. Proc. Natl. Acad. Sci. USA 99: 14903-14906.
77. Willoughby, L., H. Chung, C. Lumb, C. Robin, P. Batterham et al., 2006 A comparison of Drosophila melanogaster detoxification gene induction responses for six insecticides, caffeine and phenobarbital. Insect Biochem. Mol. Biol. 36: 934-942.
78. Xu, S., 2003 Theoretical basis of the Beavis effect. Genetics 165: 2259-2268.
79. Xu, C., C. Y. Li, and A. N. Kong, 2005 Induction of phase I, II and III drug metabolism/transport by xenobiotics. Arch. Pharm. Res. 28: 249-268.
80. Yang, J., C. McCart, D. J. Woods, S. Terhzaz, K. G. Greenwood et al., 2007 A Drosophila systems approach to xenobiotic metabolism. Physiol. Genomics 30: 223-231.
81. Yang, J., B. Benyamin, B. P. McEvoy, S. Gordon, A. K. Henders et al., 2010 Common SNPs explain a large proportion of the heritability for human height. Nat. Genet. 42: 565-569.
82. You, M., Z. Yue, W. He, X. Yang, G. Yang et al., 2013 A heterozygous moth genome provides insights into herbivory and detoxification. Nat. Genet. 45: 220-225.