Buffering of genetic regulatory networks in Drosophila melanogaster

Genetics

Volumn 203, Issue 3, 2016, Pages 1177-1190

  Fear, Justin M ^a   León Novelo, Luis G ^b   Morse, Alison M ^a   Gerken, Alison R ^a   Van Lehmann, Kjong ^c   Tower, John ^d   Nuzhdin, Sergey V ^a,d   McIntyre, Lauren M ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF TEXAS SCHOOL OF PUBLIC HEALTH   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Allele specific expression; Cis or trans effects; Drosophila; Genetic variation; Purifying selection; Regulatory mutations; Transcription

Indexed keywords

ALLELIC IMBALANCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BAYES THEOREM; DROSOPHILA MELANOGASTER; ENVIRONMENTAL CHANGE; EXON; FEMALE; GENE; GENE EXPRESSION REGULATION; GENE MUTATION; GENE REGULATORY NETWORK; GENETIC ASSOCIATION; GENETIC REGULATION; GENETIC TRANSCRIPTION; GENETIC VARIATION; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; RNA SEQUENCE; ALLELE; ANIMAL; GENETICS; GENOTYPE ENVIRONMENT INTERACTION; HIGH THROUGHPUT SEQUENCING; MOLECULAR EVOLUTION;

ALLELES; ALLELIC IMBALANCE; ANIMALS; BAYES THEOREM; DROSOPHILA MELANOGASTER; EVOLUTION, MOLECULAR; EXONS; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; GENE-ENVIRONMENT INTERACTION; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; TRANSCRIPTION, GENETIC;

EID: 84979900313     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.116.188797     Document Type: Article

References (126)

1. Albergante, L., J. J. Blow, and T. J. Newman, 2014 Buffered qualitative stability explains the robustness and evolvability of transcriptional networks. eLife 3: e02863.
2. Anders, S., A. Reyes, and W. Huber, 2012 Detecting differential usage of exons from RNA-seq data. Genome Res. 22: 2008– 2017.
3. Artieri, C. G., and H. B. Fraser, 2014 Evolution at two levels of gene expression in yeast. Genome Res. 24: 411–421.
4. Bader, D. M., S. Wilkening, G. Lin, M. M. Tekkedil, K. Dietrich et al., 2015 Negative feedback buffers effects of regulatory variants. Mol. Syst. Biol. 11: 785.
5. Barone, M. C., G. P. Sykiotis, and D. Bohmann, 2011 Genetic activation of Nrf2 signaling is sufficient to ameliorate neurodegenerative phenotypes in a Drosophila model of Parkinson’s disease. Dis. Model. Mech. 4: 701–707.
6. Benjamini, Y., and Y. Hochberg, 1995 Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57: 289–300.
7. Berger, R. L., 1997 Likelihood Ratio Tests and Intersection-Union Tests, pp. 225–237 in Advances in Statistical Decision Theory and Applications, edited by S. Panchapakesan and N. Balakrishnan. Birkhäuser Boston, Boston, MA.
8. Berger, R. L., and D. D. Boos, 1999 Confidence limits for the onset and duration of treatment effect. Biom. J. 41: 517–531.
9. Boltz, K. A., L. L. Ellis, and G. E. Carney, 2007 Drosophila melanogaster p24 genes have developmental, tissue-specific, and sexspecific expression patterns and functions. Dev. Dyn. 236: 544–555.
10. Brem, R. B., G. Yvert, R. Clinton, and L. Kruglyak, 2002 Genetic dissection of transcriptional regulation in budding yeast. Science 296: 752–755.
11. Campo, D., K. Lehmann, C. Fjeldsted, T. Souaiaia, J. Kao et al., 2013 Whole-genome sequencing of two North American Drosophila melanogaster populations reveals genetic differentiation and positive selection. Mol. Ecol. 22: 5084–5097.
12. Castel, S. E., A. Levy-Moonshine, P. Mohammadi, E. Banks, and T. Lappalainen, 2015 Tools and best practices for data processing in allelic expression analysis. Genome Biol. 16: 195.
13. Chapman, T., L. F. Liddle, J. M. Kalb, M. F. Wolfner, and L. Partridge, 1995 Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373: 241–244.
14. Coffman, C. J., R. W. Doerge, M. L. Wayne, and L. M. McIntyre, 2003 Intersection tests for single marker QTL analysis can be more powerful than two marker QTL analysis. BMC Genet. 4: 10.
15. Coolon, J. D., C. J. McManus, K. R. Stevenson, B. R. Graveley, and P. J. Wittkopp, 2014 Tempo and mode of regulatory evolution in Drosophila. Genome Res. 24: 797–808.
16. Coolon, J. D., K. R. Stevenson, C. J. McManus, B. Yang, B. R. Graveley et al., 2015 Molecular mechanisms and evolutionary processes contributing to accelerated divergence of gene expression on the Drosophila X chromosome. Mol. Biol. Evol. 32: 2605–2615.
17. Cowles, C. R., J. N. Hirschhorn, D. Altshuler, and E. S. Lander, 2002 Detection of regulatory variation in mouse genes. Nat. Genet. 32: 432–437.
18. Crowley, J. J., V. Zhabotynsky, W. Sun, S. Huang, I. K. Pakatci et al., 2015 Analyses of allele-specific gene expression in highly divergent mouse crosses identifies pervasive allelic imbalance. Nat. Genet. 47: 353–360.
19. Cubillos, F. A., O. Stegle, C. Grondin, M. Canut, S. Tisne et al., 2014 Extensive cis-regulatory variation robust to environmental perturbation in Arabidopsis. Plant Cell 26: 4298–4310.
20. Dalton, J. E., T. S. Kacheria, S. R. Knott, M. S. Lebo, A. Nishitani et al., 2010 Dynamic, mating-induced gene expression changes in female head and brain tissues of Drosophila melanogaster. BMC Genomics 11: 541.
21. Degner, J. F., J. C. Marioni, A. A. Pai, J. K. Pickrell, E. Nkadori et al., 2009 Effect of read-mapping biases on detecting allele-specific expression from RNA-sequencing data. Bioinformatics 25: 3207–3212.
22. Denby, C. M., J. H. Im, R. C. Yu, C. G. Pesce and R. B. Brem, 2012 Negative feedback confers mutational robustness in yeast transcription factor regulation. Proc. Natl. Acad. Sci. USA 109: 3874–3878.
23. Emerson, J. J., L. C. Hsieh, H. M. Sung, T. Y. Wang, C. J. Huang et al., 2010 Natural selection on cis and trans regulation in yeasts. Genome Res. 20: 826–836.
24. Fear, J. M., M. N. Arbeitman, M. P. Salomon, J. E. Dalton, J. Tower et al., 2015 The Wright stuff: reimagining path analysis reveals novel components of the sex determination hierarchy in Drosophila melanogaster. BMC Syst. Biol. 9: 1.
25. Flatt, T., 2011 Survival costs of reproduction in Drosophila. Exp. Gerontol. 46: 369–375.
26. Fontanillas, P., C. R. Landry, P. J. Wittkopp, C. Russ, J. D. Gruber et al., 2010 Key considerations for measuring allelic expression on a genomic scale using high‐throughput sequencing. Mol. Ecol. 19: 212–227.
27. Frith, M. C., R. Wan, and P. Horton, 2010 Incorporating sequence quality data into alignment improves DNA read mapping. Nucleic Acids Res. 38: e100.
28. Genissel, A., L. M. McIntyre, M. L. Wayne, and S. V. Nuzhdin, 2008 Cis and trans regulatory effects contribute to natural variation in transcriptome of Drosophila melanogaster. Mol. Biol. Evol. 25: 101–110.
29. Gibson, G., and I. Dworkin, 2004 Uncovering cryptic genetic variation. Nat. Rev. Genet. 5: 681–690.
30. 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.
31. Gioti, A., S. Wigby, B. Wertheim, E. Schuster, P. Martinez et al., 2012 Sex peptide of Drosophila melanogaster males is a global regulator of reproductive processes in females. Proc. Biol. Sci. 279: 4423–4432.
32. Goncalves, A., S. Leigh-Brown, D. Thybert, K. Stefflova, E. Turro et al., 2012 Extensive compensatory cis-trans regulation in the evolution of mouse gene expression. Genome Res. 22: 2376– 2384.
33. Graze, R. M., L. M. McIntyre, B. J. Main, M. L. Wayne and S. V. Nuzhdin, 2009 Regulatory divergence in Drosophila melanogaster and D. simulans, a genome-wide analysis of allele-specific expression. Genetics 183: 547–561.
34. Graze, R. M., L. L. Novelo, V. Amin, J. M. Fear, G. Casella et al., 2012 Allelic imbalance in Drosophila hybrid heads: exons, isoforms, and evolution. Mol. Biol. Evol. 29: 1521–1532.
35. Graze, R. M., L. M. McIntyre, A. M. Morse, B. M. Boyd, S. V. Nuzhdin et al., 2014 What the X has to do with it: differences in regulatory variability between the sexes in Drosophila simulans. Genome Biol. Evol. 6: 818–829.
36. Greer, C. L., A. Grygoruk, D. E. Patton, B. Ley, R. Romero-Calderon et al., 2005 A splice variant of the Drosophila vesicular monoamine transporter contains a conserved trafficking domain and functions in the storage of dopamine, serotonin, and octopamine. J. Neurobiol. 64: 239–258.
37. Guichet, A., F. Peri, and S. Roth, 2001 Stable anterior anchoring of the oocyte nucleus is required to establish dorsoventral polarity of the Drosophila egg. Dev. Biol. 237: 93–106.
38. Guo, M., S. Yang, M. Rupe, B. Hu, D. R. Bickel et al., 2008a Genome-wide allele-specific expression analysis using Massively Parallel Signature Sequencing (MPSS) reveals cis- and trans-effects on gene expression in maize hybrid meristem tissue. Plant Mol. Biol. 66: 551–563.
39. Guo, Y., T. C. Walther, M. Rao, N. Stuurman, G. Goshima et al., 2008b Functional genomic screen reveals genes involved in lipid-droplet formation and utilization. Nature 453: 657–661.
40. Hodgins-Davis, A., D. P. Rice, and J. P. Townsend, 2015 Gene expression evolves under a house-of-cards model of stabilizing selection. Mol. Biol. Evol. 32: 2130–2140.
41. Huang, W., M. A. Carbone, M. M. Magwire, J. A. Peiffer, R. F. Lyman et al., 2015 Genetic basis of transcriptome diversity in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 112: E6010–E6019.
42. Hughes, K. A., J. F. Ayroles, M. M. Reedy, J. M. Drnevich, K. C. Rowe et al., 2006 Segregating variation in the transcriptome: cis regulation and additivity of effects. Genetics 173: 1347– 1355.
43. Hutter, S., S. S. Saminadin-Peter, W. Stephan, and J. Parsch, 2008 Gene expression variation in African and European populations of Drosophila melanogaster. Genome Biol. 9: R12.
44. Jin, W., R. M. Riley, R. D. Wolfinger, K. P. White, G. Passador Gurgel et al., 2001 The contributions of sex, genotype and age to transcriptional variance in Drosophila melanogaster. Nat. Genet. 29: 389–395.
45. Karim, M. R., H. Taniguchi, and A. Kobayashi, 2015 Constitutive activation of Drosophila CncC transcription factor reduces lipid formation in the fat body. Biochem. Biophys. Res. Commun. 463: 693–698.
46. King, E. G., C. M. Merkes, C. L. McNeil, S. R. Hoofer, S. Sen et al., 2012 Genetic dissection of a model complex trait using the Drosophila Synthetic Population Resource. Genome Res. 22: 1558–1566.
47. King, E. G., B. J. Sanderson, C. L. McNeil, A. D. Long, and S. J. Macdonald, 2014 Genetic dissection of the Drosophila mela nogaster female head transcriptome reveals widespread allelic heterogeneity. PLoS Genet. 10: e1004322.
48. Kirst, M., C. J. Basten, A. A. Myburg, Z. B. Zeng, and R. R. Sederoff, 2005 Genetic architecture of transcript-level variation in differentiating xylem of a eucalyptus hybrid. Genetics 169: 2295– 2303.
49. Kocher, S. D., F. J. Richard, D. R. Tarpy, and C. M. Grozinger, 2008 Genomic analysis of post-mating changes in the honey bee queen (Apis mellifera). BMC Genomics 9: 232.
50. Kurmangaliyev, Y. Z., A. V. Favorov, N. M. Osman, K. V. Lehmann, D. Campo et al., 2015 Natural variation of gene models in Drosophila melanogaster. BMC Genomics 16: 198.
51. Kvitek, D. J., J. L. Will, and A. P. Gasch, 2008 Variations in stress sensitivity and genomic expression in diverse S. cerevisiae isolates. PLoS Genet. 4: e1000223.
52. Landis, G. N., M. P. Salomon, D. Keroles, N. Brookes, T. Sekimura et al., 2015 The progesterone antagonist mifepristone/RU486 blocks the negative effect on life span caused by mating in female Drosophila. Aging 7: 53–69.
53. Landry, C. R., P. J. Wittkopp, C. H. Taubes, J. M. Ranz, A. G. Clark et al., 2005 Compensatory cis–trans evolution and the dysregulation of gene expression in interspecific hybrids of Drosophila. Genetics 171: 1813–1822.
54. Langmead, B., C. Trapnell, M. Pop, and S. L. Salzberg, 2009 Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10: R25.
55. Lawniczak, M. K., and D. J. Begun, 2004 A genome-wide analysis of courting and mating responses in Drosophila melanogaster females. Genome 47: 900–910.
56. Lawniczak, M. K., A. I. Barnes, J. R. Linklater, J. M. Boone, S. Wigby et al., 2007 Mating and immunity in invertebrates. Trends Ecol. Evol. 22: 48–55.
57. Lebo, M. S., L. E. Sanders, F. Sun, and M. N. Arbeitman, 2009 Somatic, germline and sex hierarchy regulated gene expression during Drosophila metamorphosis. BMC Genomics 10: 80.
58. Lee, T. I., and R. A. Young, 2013 Transcriptional regulation and its misregulation in disease. Cell 152: 1237–1251.
59. Lee, Y. S., S. Pressman, A. P. Andress, K. Kim, J. L. White et al., 2009 Silencing by small RNAs is linked to endosomal trafficking. Nat. Cell Biol. 11: 1150–1156.
60. Lemos, B., L. O. Araripe, P. Fontanillas, and D. L. Hartl, 2008 Dominance and the evolutionary accumulation of cis- and trans-effects on gene expression. Proc. Natl. Acad. Sci. USA 105: 14471–14476.
61. Leon-Novelo, L. G., L. M. McIntyre, J. M. Fear, and R. M. Graze, 2014 A flexible Bayesian method for detecting allelic imbalance in RNA-seq data. BMC Genomics 15: 920.
62. Lo, H. S., Z. Wang, Y. Hu, H. H. Yang, S. Gere et al., 2003 Allelic variation in gene expression is common in the human genome. Genome Res. 13: 1855–1862.
63. Mack, P. D., A. Kapelnikov, Y. Heifetz, and M. Bender, 2006 Mating-responsive genes in reproductive tissues of female Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 103: 10358–10363.
64. Mackay, T. F., E. A. Stone, and J. F. Ayroles, 2009 The genetics of quantitative traits: challenges and prospects. Nat. Rev. Genet. 10: 565–577.
65. 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.
66. Massouras, A., S. M. Waszak, M. Albarca-Aguilera, K. Hens, W. Holcombe et al., 2012 Genomic variation and its impact on gene expression in Drosophila melanogaster. PLoS Genet. 8: e1003055.
67. McGraw, L. A., G. Gibson, A. G. Clark, and M. F. Wolfner, 2004 Genes regulated by mating, sperm, or seminal proteins in mated female Drosophila melanogaster. Curr. Biol. 14: 1509–1514.
68. McGraw, L. A., A. G. Clark, and M. F. Wolfner, 2008 Postmating gene expression profiles of female Drosophila melanogaster in response to time and to four male accessory gland proteins. Genetics 179: 1395–1408.
69. McManus, C. J., J. D. Coolon, M. O. Duff, J. Eipper-Mains, B. R. Graveley et al., 2010 Regulatory divergence in Drosophila revealed by mRNA-seq. Genome Res. 20: 816–825.
70. McManus, C. J., J. D. Coolon, J. Eipper-Mains, P. J. Wittkopp, and B. R. Graveley, 2014 Evolution of splicing regulatory networks in Drosophila. Genome Res. 24: 786–796.
71. Meiklejohn, C. D., J. D. Coolon, D. L. Hartl, and P. J. Wittkopp, 2014 The roles of cis- and trans-regulation in the evolution of regulatory incompatibilities and sexually dimorphic gene expression. Genome Res. 24: 84–95.
72. Mendell, J. T., and H. C. Dietz, 2001 When the message goes awry: disease-producing mutations that influence mRNA content and performance. Cell 107: 411–414.
73. Michalak, P., and M. A. Noor, 2003 Genome-wide patterns of expression in Drosophila pure species and hybrid males. Mol. Biol. Evol. 20: 1070–1076.
74. Michalak, P., and M. A. Noor, 2004 Association of misexpression with sterility in hybrids of Drosophila simulans and D. mauritiana. J. Mol. Evol. 59: 277–282.
75. 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.
76. Morrow, E. H., and P. Innocenti, 2012 Female postmating immune responses, immune system evolution and immunogenic males. Biol. Rev. Camb. Philos. Soc. 87: 631–638.
77. Mugat, B., A. Akkouche, V. Serrano, C. Armenise, B. Li et al., 2015 MicroRNA-dependent transcriptional silencing of transposable elements in Drosophila follicle cells. PLoS Genet. 11: e1005194.
78. Munger, S. C., N. Raghupathy, K. Choi, A. K. Simons, D. M. Gatti et al., 2014 RNA-Seq alignment to individualized genomes improves transcript abundance estimates in multiparent populations. Genetics 198: 59–73.
79. Nothnagel, M., A. Wolf, A. Herrmann, K. Szafranski, I. Vater et al., 2011 Statistical inference of allelic imbalance from transcriptome data. Hum. Mutat. 32: 98–106.
80. Nuzhdin, S. V., M. L. Wayne, K. L. Harmon, and L. M. McIntyre, 2004 Common pattern of evolution of gene expression level and protein sequence in Drosophila. Mol. Biol. Evol. 21: 1308– 1317.
81. Nuzhdin, S. V., M. L. Friesen, and L. M. McIntyre, 2012 Genotypephenotype mapping in a post-GWAS world. Trends Genet. 28: 421–426.
82. Obata, F., and M. Miura, 2015 Enhancing S-adenosyl-methionine catabolism extends Drosophila lifespan. Nat. Commun. 6: 8332.
83. Ortiz-Barrientos, D., B. A. Counterman, and M. A. Noor, 2007 Gene expression divergence and the origin of hybrid dysfunctions. Genetica 129: 71–81.
84. Paaby, A. B., and M. V. Rockman, 2014 Cryptic genetic variation: evolution’s hidden substrate. Nat. Rev. Genet. 15: 247–258.
85. Pastinen, T., 2010 Genome-wide allele-specific analysis: insights into regulatory variation. Nat. Rev. Genet. 11: 533–538.
86. Peng, J., P. Zipperlen, and E. Kubli, 2005 Drosophila sex-peptide stimulates female innate immune system after mating via the Toll and Imd pathways. Curr. Biol. 15: 1690–1694.
87. Pickering, A. M., T. A. Staab, J. Tower, D. Sieburth, and K. J. Davies, 2013 A conserved role for the 20S proteasome and Nrf2 transcription factor in oxidative stress adaptation in mammals, Caenorhabditis elegans and Drosophila melanogaster. J. Exp. Biol. 216: 543–553.
88. Pinter, S. F., D. Colognori, B. J. Beliveau, R. I. Sadreyev, B. Payer et al., 2015 Allelic imbalance is a prevalent and tissue-specific feature of the mouse transcriptome. Genetics 200: 537–549.
89. Pool, J. E., R. B. Corbett-Detig, R. P. Sugino, K. A. Stevens, C. M. Cardeno et al., 2012 Population genomics of sub-Saharan Drosophila melanogaster: African diversity and non-African admixture. PLoS Genet. 8: e1003080.
90. Ranz, J. M., K. Namgyal, G. Gibson, and D. L. Hartl, 2004 Anomalies in the expression profile of interspecific hybrids of Drosophila melanogaster and Drosophila simulans. Genome Res. 14: 373–379.
91. Rezaval, C., T. Nojima, M. C. Neville, A. C. Lin, and S. F. Goodwin, 2014 Sexually dimorphic octopaminergic neurons modulate female postmating behaviors in Drosophila. Curr. Biol. 24: 725–730.
92. Rockman, M. V., and L. Kruglyak, 2006 Genetics of global gene expression. Nat. Rev. Genet. 7: 862–872.
93. Ronald, J., J. M. Akey, J. Whittle, E. N. Smith, G. Yvert et al., 2005 Simultaneous genotyping, gene-expression measurement, and detection of allele-specific expression with oligonucleotide arrays. Genome Res. 15: 284–291.
94. Rozowsky, J., A. Abyzov, J. Wang, P. Alves, D. Raha et al., 2011 AlleleSeq: analysis of allele-specific expression and binding in a network framework. Mol. Syst. Biol. 7: 522.
95. Saito, K., S. Inagaki, T. Mituyama, Y. Kawamura, Y. Ono et al., 2009 A regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila. Nature 461: 1296–1299.
96. Saleem, S., C. C. Schwedes, L. L. Ellis, S. T. Grady, R. L. Adams et al., 2012 Drosophila melanogaster p24 trafficking proteins have vital roles in development and reproduction. Mech. Dev. 129: 177–191.
97. Seshaiah, P., B. Miller, M. M. Myat, and D. J. Andrew, 2001 pasilla, the Drosophila homologue of the human Nova1 and Nova-2 proteins, is required for normal secretion in the salivary gland. Dev. Biol. 239: 309–322.
98. Skelly, D. A., M. Johansson, J. Madeoy, J. Wakefield, and J. M. Akey, 2011 A powerful and flexible statistical framework for testing hypotheses of allele-specific gene expression from RNA-seq data. Genome Res. 21: 1728–1737.
99. Smith, E. N., and L. Kruglyak, 2008 Gene-environment interaction in yeast gene expression. PLoS Biol. 6: e83.
100. Smith, G., Y. Fang, X. Liu, J. Kenny, A. R. Cossins et al., 2013 Transcriptome-wide expression variation associated with environmental plasticity and mating success in cactophilic Drosophila mojavensis. Evolution 67: 1950–1963.
101. Springer, N. M., and R. M. Stupar, 2007 Allele-specific expression patterns reveal biases and embryo-specific parent-of-origin effects in hybrid maize. Plant Cell 19: 2391–2402.
102. Stauffer, D. R., T. L. Howard, T. Nyun, and S. M. Hollenberg, 2001 CHMP1 is a novel nuclear matrix protein affecting chromatin structure and cell-cycle progression. J. Cell Sci. 114: 2383–2393.
103. Stell, R., J. Torrie, and D. Dickey, 1980 Principles and Procedures of Statistics: A Biometrical Approach. MacGraw-Hill, New York.
104. Stevenson, K. R., J. D. Coolon, and P. J. Wittkopp, 2013 Sources of bias in measures of allele-specific expression derived from RNA-sequence data aligned to a single reference genome. BMC Genomics 14: 536.
105. Sykiotis, G. P., I. G. Habeos, A. V. Samuelson, and D. Bohmann, 2011 The role of the antioxidant and longevity-promoting Nrf2 pathway in metabolic regulation. Curr. Opin. Clin. Nutr. Metab. Care 14: 41–48.
106. Takahasi, K. R., T. Matsuo, and T. Takano-Shimizu-Kouno, 2011 Two types of cis-trans compensation in the evolution of transcriptional regulation. Proc. Natl. Acad. Sci. USA 108: 15276–15281.
107. Telonis-Scott, M., A. Kopp, M. L. Wayne, S. V. Nuzhdin, and L. M. McIntyre, 2009 Sex-specific splicing in Drosophila: widespread occurrence, tissue specificity and evolutionary conservation. Genetics 181: 421–434.
108. Tirosh, I., S. Reikhav, A. A. Levy, and N. Barkai, 2009 A yeast hybrid provides insight into the evolution of gene expression regulation. Science 324: 659–662.
109. 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.
110. van de Geijn, B., G. McVicker, Y. Gilad, and J. Pritchard, 2015 WASP: allele-specific software for robust discovery of molecular quantitative trait loci. Nat. Methods 12: 1061–1063.
111. Wang, H.-Y., Y. Fu, M. S. McPeek, X. Lu, S. Nuzhdin et al., 2008 Complex genetic interactions underlying expression differences between Drosophila races: analysis of chromosome substitutions. Proc. Natl. Acad. Sci. USA 105: 6362–6367.
112. Wayne, M. L., Y. J. Pan, S. V. Nuzhdin, and L. M. McIntyre, 2004 Additivity and trans-acting effects on gene expression in male Drosophila simulans. Genetics 168: 1413–1420.
113. Wayne, M. L., M. Telonis-Scott, L. M. Bono, L. Harshman, A. Kopp et al., 2007 Simpler mode of inheritance of transcriptional variation in male Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 104: 18577–18582.
114. Winbush, A., D. Reed, P. L. Chang, S. V. Nuzhdin, L. C. Lyons et al., 2012 Identification of gene expression changes associated with long-term memory of courtship rejection in Drosophila males. G3 2: 1437–1445.
115. Wittkopp, P. J., and G. Kalay, 2012 Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat. Rev. Genet. 13: 59–69.
116. Wittkopp, P. J., B. K. Haerum, and A. G. Clark, 2004 Evolutionary changes in cis and trans gene regulation. Nature 430: 85–88.
117. Wittkopp, P. J., B. K. Haerum, and A. G. Clark, 2006 Parent-oforigin effects on mRNA expression in Drosophila melanogaster not caused by genomic imprinting. Genetics 173: 1817–1821.
118. Wittkopp, P. J., B. K. Haerum, and A. G. Clark, 2008a Independent effects of cis- and trans-regulatory variation on gene expression in Drosophila melanogaster. Genetics 178: 1831–1835.
119. Wittkopp, P. J., B. K. Haerum, and A. G. Clark, 2008b Regulatory changes underlying expression differences within and between Drosophila species. Nat. Genet. 40: 346–350.
120. Yan, H., W. Yuan, V. E. Velculescu, B. Vogelstein, and K. W. Kinzler, 2002 Allelic variation in human gene expression. Science 297: 1143.
121. Yasuyama, K., T. Kitamoto, and P. M. Salvaterra, 1995 Immunocytochemical study of choline acetyltransferase in Drosophila melanogaster: an analysis of cis-regulatory regions controlling expression in the brain of cDNA-transformed flies. J. Comp. Neurol. 361: 25–37.
122. Yuan, S., and Z. Qin, 2012 Read-mapping using personalized diploid reference genome for RNA sequencing data reduced bias for detecting allele-specific expression. IEEE Int. Conf. Bioinform. Biomed. Workshops 2012: 718–724.
123. Zhang, F., and J. R. Lupski, 2015 Non-coding genetic variants in human disease. Hum. Mol. Genet. 24: R102–R110.
124. Zhang, X., and J. O. Borevitz, 2009 Global analysis of allele-specific expression in Arabidopsis thaliana. Genetics 182: 943–954.
125. Zhou, S., T. Mackay, and R. R. Anholt, 2014 Transcriptional and epigenetic responses to mating and aging in Drosophila melanogaster. BMC Genomics 15: 927.
126. 1 reciprocal crosses and inbred lines. Genetics 197: 389–399.