The wright stuff: Reimagining path analysis reveals novel components of the sex determination hierarchy in drosophila melanogaster

BMC Systems Biology

Volumn 9, Issue 1, 2015, Pages

  Fear, Justin M ^a   Arbeitman, Michelle N ^b   Salomon, Matthew P ^c   Dalton, Justin E ^b   Tower, John ^c   Nuzhdin, Sergey V ^c   McIntyre, Lauren M ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b FLORIDA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; DROSOPHILA PROTEIN; DSX PROTEIN, DROSOPHILA; MESSENGER RNA; NUCLEAR PROTEIN; TRANSFORMER PROTEIN, DROSOPHILA;

ANIMAL; BIOLOGICAL MODEL; BIOLOGY; DROSOPHILA MELANOGASTER; FEMALE; GENE REGULATORY NETWORK; GENETICS; MALE; METABOLISM; PROCEDURES; SEX DETERMINATION PROCESS; SUPERVISED MACHINE LEARNING; UNSUPERVISED MACHINE LEARNING;

ANIMALS; COMPUTATIONAL BIOLOGY; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE REGULATORY NETWORKS; MALE; MODELS, GENETIC; NUCLEAR PROTEINS; RNA, MESSENGER; SEX DETERMINATION PROCESSES; SUPERVISED MACHINE LEARNING; UNSUPERVISED MACHINE LEARNING;

EID: 84941260299     PISSN: None     EISSN: 17520509     Source Type: Journal    
DOI: 10.1186/s12918-015-0200-0     Document Type: Article

References (129)

1. Christiansen AE, Keisman EL, Ahmad SM, Baker BS. Sex comes in from the cold: the integration of sex and pattern. Trends Genet. 2002;18:510-6.
2. Kelley RL, Wang J, Bell L, Kuroda MI. Sex lethal controls dosage compensation in Drosophila by a non-splicing mechanism. Nature. 1997;387:195-9.
3. Yamamoto D. The neural and genetic substrates of sexual behavior in Drosophila. Adv Genet. 2007;59:39-66.
4. Villella A, Hall JC. Neurogenetics of courtship and mating in Drosophila. Adv Genet. 2008;62:67-184.
5. Bell LR, Horabin JI, Schedl P, Cline TW. Positive autoregulation of sex-lethal by alternative splicing maintains the female determined state in Drosophila. Cell. 1991;65:229-39.
6. Boggs RT, Gregor P, Idriss S, Belote JM, McKeown M. Regulation of sexual differentiation in D. melanogaster via alternative splicing of RNA from the transformer gene. Cell. 1987;50:739-47.
7. Baker BS, Ridge KA. Sex and the single cell. I. On the action of major loci affecting sex determination in Drosophila melanogaster. Genetics. 1980;94:383-423.
8. Ryner LC, Goodwin SF, Castrillon DH, Anand A, Villella A, Baker BS, et al. Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell. 1996;87:1079-89.
9. Salz HK, Erickson JW. Sex determination in Drosophila: The view from the top. Fly (Austin). 2010;4:60-70.
10. Granadino B, Campuzano S, Sánchez L. The Drosophila melanogaster fl(2)d gene is needed for the female-specific splicing of Sex-lethal RNA. EMBO J. 1990;9:2597-602.
11. Acharyya M, Chatterjee R. Genetic analysis of an intersex allele (ix5) that regulates sexual phenotype of both female and male Drosophila melanogaster. Genet Res. 2002;80:7-14.
12. Chandler DS, McGuffin ME, Mattox W. Functionally antagonistic sequences are required for normal autoregulation of Drosophila tra-2 pre-mRNA splicing. Nucleic Acids Res. 2001;29:3012-9.
13. Cline T. A male-specific lethal mutation in Drosophila melanogaster that transforms sex. Dev Biol. 1979;72:266-75.
14. Goodwin SF, Taylor BJ, Villella A, Foss M, Ryner LC, Baker BS, et al. Aberrant splicing and altered spatial expression patterns in fruitless mutants of Drosophila melanogaster. Genetics. 2000;154:725-45.
15. Hildreth PE. Doublesex, recessive gene that transforms both males and females of Drosophila into intersexes. Genetics. 1965;51:659-78.
16. Erdman SE, Chen HJ, Burtis KC. Functional and genetic characterization of the oligomerization and DNA binding properties of the Drosophila doublesex proteins. Genetics. 1996;144:1639-52.
17. Chang PL, Dunham JP, Nuzhdin SV, Arbeitman MN. Somatic sex-specific transcriptome differences in Drosophila revealed by whole transcriptome sequencing. BMC Genomics. 2011;12:364.
18. Lebo MS, Sanders LE, Sun F, Arbeitman MN. Somatic, germline and sex hierarchy regulated gene expression during Drosophila metamorphosis. BMC Genomics. 2009;10:80.
19. Goldman TD, Arbeitman MN. Genomic and functional studies of Drosophila sex hierarchy regulated gene expression in adult head and nervous system tissues. PLoS Genet. 2007;3:e216.
20. Dalton JE, Fear JM, Knott S, Baker BS, McIntyre LM, Arbeitman MN. Male-specific Fruitless isoforms have different regulatory roles conferred by distinct zinc finger DNA binding domains. BMC Genomics. 2013;14:659.
21. Dalton JE, Lebo MS, Sanders LE, Sun F, Arbeitman MN. Ecdysone receptor acts in fruitless- expressing neurons to mediate drosophila courtship behaviors. Curr Biol. 2009;19:1447-52.
22. Arbeitman MN, Fleming AA, Siegal ML, Null BH, Baker BS. A genomic analysis of Drosophila somatic sexual differentiation and its regulation. Development. 2004;131:2007-21.
23. Rockman MV, Kruglyak L. Genetics of global gene expression. Nat Rev Genet. 2006;7:862-72.
24. Rockman MV. Reverse engineering the genotype-phenotype map with natural genetic variation. Nature. 2008;456:738-44.
25. Nuzhdin SV, Friesen ML, McIntyre LM. Genotype-phenotype mapping in a post-GWAS world. Trends Genet. 2012;28:421-6.
26. Tarone AM, Nasser YM, Nuzhdin SV. Genetic variation for expression of the sex determination pathway genes in Drosophila melanogaster. Genet Res. 2005;86:31-40.
27. Hilfiker A, Amrein H, Dübendorfer A, Schneiter R, Nöthiger R. The gene virilizer is required for female-specific splicing controlled by Sxl, the master gene for sexual development in Drosophila. Development. 1995;121:4017-26.
28. Sosnowski B, Belote J, McKeown M. Sex-specific alternative splicing of RNA from the transformer gene results from sequence-dependent splice site blockage. Cell. 1989;59:449-59.
29. Gailey DA, Hall JC. Behavior and cytogenetics of fruitless in Drosophila melanogaster: different courtship defects caused by separate, closely linked lesions. Genetics. 1989;121:773-85.
30. Tarone AM, McIntyre LM, Harshman LG, Nuzhdin SV. Genetic variation in the Yolk protein expression network of Drosophila melanogaster: sex-biased negative correlations with longevity. Heredity (Edinb). 2012;109:226-34.
31. Coffman CJ, Wayne ML, Nuzhdin SV, Higgins LA, McIntyre LM. Identification of co-regulated transcripts affecting male body size in Drosophila. Genome Biol. 2005;6:R53.
32. King EG, Sanderson BJ, McNeil CL, Long AD, Macdonald SJ. Genetic dissection of the Drosophila melanogaster female head transcriptome reveals widespread allelic heterogeneity. PLoS Genet. 2014;10:e1004322.
33. Kurmangaliyev YZ, Favorov AV, Osman NM, Lehmann K-V, Campo D, Salomon MP, et al. Natural variation of gene models in Drosophila melanogaster. BMC Genomics. 2015;16:198.
34. Mackay TFC, Richards S, Stone E a, Barbadilla A, Ayroles JF, Zhu D, et al. The Drosophila melanogaster Genetic Reference Panel. Nature. 2012;482:173-8.
35. Campo D, Lehmann K, Fjeldsted C, Souaiaia T, Kao J, Nuzhdin SV. Whole-genome sequencing of two North American Drosophila melanogaster populations reveals genetic differentiation and positive selection. Mol Ecol. 2013;22:5084-97.
36. Reverter A, Chan EKF. Combining partial correlation and an information theory approach to the reversed engineering of gene co-expression networks. Bioinformatics. 2008;24:2491-7.
37. de la Fuente A, Bing N, Hoeschele I, Mendes P. Discovery of meaningful associations in genomic data using partial correlation coefficients. Bioinformatics. 2004;20:3565-74.
38. Schäfer J, Opgen-Rhein R, Strimmer K. Reverse engineering genetic networks using the GeneNet package. J Acoust Soc Am. 2001;6(December):2004-7.
39. Friedman N, Linial M, Nachman I, Pe'er D. Using Bayesian networks to analyze expression data. J Comput Biol. 2000;7:601-20.
40. Zhu J, Lum PY, Lamb J, GuhaThakurta D, Edwards SW, Thieringer R, et al. An integrative genomics approach to the reconstruction of gene networks in segregating populations. Cytogenet Genome Res. 2004;105:363-74.
41. Schadt EE, Lamb J, Yang X, Zhu J, Edwards S, Guhathakurta D, et al. An integrative genomics approach to infer causal associations between gene expression and disease. Nat Genet. 2005;37:710-7.
42. Keurentjes JJB, Fu J, Terpstra IR, Garcia JM, van den Ackerveken G, Snoek LB, et al. Regulatory network construction in Arabidopsis by using genome-wide gene expression quantitative trait loci. Proc Natl Acad Sci U S A. 2007;104:1708-13.
43. Chaibub Neto E, Keller MP, Attie AD, Yandell BS. Causal graphical models in systems genetics: A unified framework for joint inference of causal network and genetic architecture for correlated phenotypes. Ann Appl Stat. 2010;4:320-39.
44. Logsdon BA, Mezey J. Gene expression network reconstruction by convex feature selection when incorporating genetic perturbations. PLoS Comput Biol. 2010;6:e1001014.
45. Chipman KC, Singh AK. Using stochastic causal trees to augment Bayesian networks for modeling eQTL datasets. BMC Bioinformatics. 2011;12:7.
46. Hageman RS, Leduc MS, Korstanje R, Paigen B, Churchill GA. A Bayesian framework for inference of the genotype-phenotype map for segregating populations. Genetics. 2011;187:1163-70.
47. Bollen K. Structural Equations with Latent Variables. New York: JOHN WILEY & SONS INC; 1989.
48. Wright S. The Method of Path Coefficients. Ann Math Stat. 1934;5:161-215.
49. Wright S. Correlation and causation. J Agric Res. 1921;20:557-8.
50. Gove RP, Chen W, Zweber NB, Erwin R, Rychtá J, Remington DL. Effects of causal networks on the structure and stability of resource allocation trait correlations. J Theor Biol. 2012;293:1-14.
51. Mi X, Eskridge K, Wang D, Baenziger PS, Campbell BT, Gill KS, et al. Regression-based multi-trait QTL mapping using a structural equation model. Stat Appl Genet Mol Biol. 2010;9:Article38.
52. Remington DL. Effects of genetic and environmental factors on trait network predictions from quantitative trait locus data. Genetics. 2009;181:1087-99.
53. Li R, Tsaih S-W, Shockley K, Stylianou IM, Wergedal J, Paigen B, et al. Structural model analysis of multiple quantitative traits. PLoS Genet. 2006;2:1046-57.
54. Kim J, Namkung J, Lee S, Park T. Application of Structural Equation Models to Genome-wide Association Analysis. Genomics Inform. 2010;8:150-8.
55. Rosa GJM, Valente BD, de los Campos G, Wu X-L, Gianola D, Silva MA. Inferring causal phenotype networks using structural equation models. Genet Sel Evol. 2011;43:6.
56. Liu B, de la Fuente A, Hoeschele I. Gene network inference via structural equation modeling in genetical genomics experiments. Genetics. 2008;178:1763-76.
57. Cai X, Bazerque JA, Giannakis GB. Inference of gene regulatory networks with sparse structural equation models exploiting genetic perturbations. PLoS Comput Biol. 2013;9:e1003068.
58. Aburatani S. Application of structure equation modeling for inferring a serial transcriptional regulation in yeast. Gene Regul Syst Bio. 2011;5:75-88.
59. Shieh GS, Chen C-M, Yu C-Y, Huang J, Wang W-F, Lo Y-C. Inferring transcriptional compensation interactions in yeast via stepwise structure equation modeling. BMC Bioinformatics. 2008;9:134.
60. Aburatani S. Network inference of pal-1 lineage-specific regulation in the C. elegans embryo by structural equation modeling. Bioinformation. 2012;8:652-7.
61. Xiong M, Li J, Fang X. Identification of genetic networks. Genetics. 2004;166:1037-52.
62. Pepe D, Grassi M. Investigating perturbed pathway modules from gene expression data via structural equation models. BMC Bioinformatics. 2014;15:132.
63. Lee G, Hall JC, Park JH. Doublesex gene expression in the central nervous system of Drosophila melanogaster. J Neurogenet. 2002;16:229-48.
64. Sanders LE, Arbeitman MN. Doublesex establishes sexual dimorphism in the Drosophila central nervous system in an isoform-dependent manner by directing cell number. Dev Biol. 2008;320:378-90.
65. Rideout EJ, Dornan AJ, Neville MC, Eadie S, Goodwin SF. Control of sexual differentiation and behavior by the doublesex gene in Drosophila melanogaster. Nat Neurosci. 2010;13:458-66.
66. Zhou C, Pan Y, Robinett CC, Meissner GW, Baker BS. Central brain neurons expressing doublesex regulate female receptivity in Drosophila. Neuron. 2014;83:149-63.
67. Garrett-Engele CM, Siegal ML, Manoli DS, Williams BC, Li H, Baker BS. intersex, a gene required for female sexual development in Drosophila, is expressed in both sexes and functions together with doublesex to regulate terminal differentiation. Development. 2002;129:4661-75.
68. Margolin AA, Nemenman I, Basso K, Wiggins C, Stolovitzky G, Dalla Favera R, et al. ARACNE: an algorithm for the reconstruction of gene regulatory networks in a mammalian cellular context. BMC Bioinformatics. 2006;1(7 Suppl):S7.
69. Aluru M, Zola J, Nettleton D, Aluru S. Reverse engineering and analysis of large genome-scale gene networks. Nucleic Acids Res. 2013;41:e24.
70. Opgen-Rhein R, Strimmer K. From correlation to causation networks: a simple approximate learning algorithm and its application to high-dimensional plant gene expression data. BMC Syst Biol. 2007;1:37.
71. Inoue K, Hoshijima K, Higuchi I, Sakamoto H, Shimura Y. Binding of the Drosophila transformer and transformer-2 proteins to the regulatory elements of doublesex primary transcript for sex-specific RNA processing. Proc Natl Acad Sci U S A. 1992;89:8092-6.
72. Begun DJ, Holloway AK, Stevens K, Hillier LW, Poh Y-P, Hahn MW, et al. Population genomics: whole-genome analysis of polymorphism and divergence in Drosophila simulans. PLoS Biol. 2007;5:e310.
73. Ranz JM, Castillo-Davis CI, Meiklejohn CD, Hartl DL. Sex-dependent gene expression and evolution of the Drosophila transcriptome. Science. 2003;300:1742-5.
74. Nuzhdin SV, Wayne ML, Harmon KL, McIntyre LM. Common pattern of evolution of gene expression level and protein sequence in Drosophila. Mol Biol Evol. 2004;21:1308-17.
75. Gibson G, Riley-Berger R, Harshman L, Kopp A, Vacha S, Nuzhdin S, et al. Extensive sex-specific nonadditivity of gene expression in Drosophila melanogaster. Genetics. 2004;167:1791-9.
76. Wayne ML, Pan Y-J, Nuzhdin SV, McIntyre LM. Additivity and trans-acting effects on gene expression in male Drosophila simulans. Genetics. 2004;168:1413-20.
77. Wayne ML, Telonis-Scott M, Bono LM, Harshman L, Kopp A, Nuzhdin SV, et al. Simpler mode of inheritance of transcriptional variation in male Drosophila melanogaster. Proc Natl Acad Sci U S A. 2007;104:18577-82.
78. Wayne ML, Pienaar J, Telonis-Scott M, Sylvestre L-S, Nuzhdin SV, McIntyre LM. Expression of defense genes in Drosophila evolves under a different selective regime from expression of other genes. Evolution. 2011;65:1068-78.
79. Catalán A, Hutter S, Parsch J. Population and sex differences in Drosophila melanogaster brain gene expression. BMC Genomics. 2012;13:654.
80. Schadt EE, Molony C, Chudin E, Hao K, Yang X, Lum PY, et al. Mapping the genetic architecture of gene expression in human liver. PLoS Biol. 2008;6:e107.
81. Cooper GM, Shendure J. Needles in stacks of needles: finding disease-causal variants in a wealth of genomic data. Nat Rev Genet. 2011;12:628-40.
82. Schadt EE, Lum PY. Thematic review series: systems biology approaches to metabolic and cardiovascular disorders. Reverse engineering gene networks to identify key drivers of complex disease phenotypes. J Lipid Res. 2006;47:2601-13.
83. Schadt EE, Friend SH, Shaywitz DA. A network view of disease and compound screening. Nat Rev Drug Discov. 2009;8:286-95.
84. Jansen RC. Studying complex biological systems using multifactorial perturbation. Nat Rev Genet. 2003;4:145-51.
85. Jansen RC, Tesson BM, Fu J, Yang Y, McIntyre LM. Defining gene and QTL networks. Curr Opin Plant Biol. 2009;12:241-6.
86. Graze RM, McIntyre LM, Morse AM, Boyd BM, Nuzhdin SV, Wayne ML. What the X has to do with it: differences in regulatory variability between the sexes in Drosophila simulans. Genome Biol Evol. 2014;6:818-29.
87. Genissel A, McIntyre LM, Wayne ML, Nuzhdin SV. Cis and trans regulatory effects contribute to natural variation in transcriptome of Drosophila melanogaster. Mol Biol Evol. 2008;25:101-10.
88. Bashaw GJ, Baker BS. The regulation of the Drosophila msl-2 gene reveals a function for Sex-lethal in translational control. Cell. 1997;89:789-98.
89. McIntyre LM, Bono LM, Genissel A, Westerman R, Junk D, Telonis-Scott M, et al. Sex-specific expression of alternative transcripts in Drosophila. Genome Biol. 2006;7:R79.
90. Kim S, Shi H, Lee DK, Lis JT. Specific SR protein-dependent splicing substrates identified through genomic SELEX. Nucleic Acids Res. 2003;31:1955-61.
91. Conrad T, Akhtar A. Dosage compensation in Drosophila melanogaster: epigenetic fine-tuning of chromosome-wide transcription. Nat Rev Genet. 2011;13:123-34.
92. Sun L, Fernandez HR, Donohue RC, Li J, Cheng J, Birchler JA. Male-specific lethal complex in Drosophila counteracts histone acetylation and does not mediate dosage compensation. Proc Natl Acad Sci U S A. 2013;110:E808-17.
93. Kiuchi T, Koga H, Kawamoto M, Shoji K, Sakai H, Arai Y, et al. A single female-specific piRNA is the primary determiner of sex in the silkworm. Nature. 2014;509:633-6.
94. Metzstein MM, Krasnow MA. Functions of the nonsense-mediated mRNA decay pathway in Drosophila development. PLoS Genet. 2006;2:e180.
95. Luo SD, Shi GW, Baker BS. Direct targets of the D. melanogaster DSXF protein and the evolution of sexual development. Development. 2011;138:2761-71.
96. Cléry A, Blatter M, Allain FH-T. RNA recognition motifs: boring? Not quite. Curr Opin Struct Biol. 2008;18:290-8.
97. Testa ND, Ghosh SM, Shingleton AW. Sex-specific weight loss mediates sexual size dimorphism in Drosophila melanogaster. PLoS One. 2013;8:e58936.
98. Wigby S, Slack C, Grönke S, Martinez P, Calboli FCF, Chapman T, et al. Insulin signalling regulates remating in female Drosophila. Proc Biol Sci. 2011;278:424-31.
99. Lazareva AA, Roman G, Mattox W, Hardin PE, Dauwalder B. A role for the adult fat body in Drosophila male courtship behavior. PLoS Genet. 2007;3:e16.
100. Al-Anzi B, Sapin V, Waters C, Zinn K, Wyman RJ, Benzer S. Obesity-blocking neurons in Drosophila. Neuron. 2009;63:329-41.
101. Bentley DL. Coupling mRNA processing with transcription in time and space. Nat Rev Genet. 2014;15:163-75.
102. Ho JWK, Jung YL, Liu T, Alver BH, Lee S, Ikegami K, et al. Comparative analysis ofmetazoan chromatin organization. Nature. 2014;512:449-52.
103. King EG, Merkes CM, McNeil CL, Hoofer SR, Sen S, Broman KW, et al. Genetic dissection of a model complex trait using the Drosophila Synthetic Population Resource. Genome Res. 2012;22(8):1558-66.
104. DSPR Available Data. http://wfitch.bio.uci.edu/~dspr/Data/index.html . Accessed August 14, 2014.
105. Stone EA, Ayroles JF. Modulated modularity clustering as an exploratory tool for functional genomic inference. PLoS Genet. 2009;5:e1000479.
106. Kline RB: Principle and Practice of Structural Equation Modeling. 3rd ed. New York: The Gulliford Press; 2010.
107. Zwiener I, Frisch B, Binder H. Transforming RNA-Seq data to improve the performance of prognostic gene signatures. PLoS One. 2014;9:e85150.
108. Soneson C, Delorenzi M. A comparison of methods for differential expression analysis of RNA-seq data. BMC Bioinformatics. 2013;14:91.
109. Law CW, Chen Y, Shi W, Smyth GK. voom: Precision weights unlock linear model analysis tools for RNA-seq read counts. Genome Biol. 2014;15:R29.
110. Hoyle RH. Handbook of Structural Equation Modeling. New York: The Guilford Press; 2012.
111. Akaike H: Information theory and an extension of the maximum likelihood principle. In: Parzen E, Tanabe K, Kitagawa G, editors. Selected Papers of Hirotugu Akaike. New York: Springer; 1998. p. 199-213.
112. Sugiura N. Further analysis of the data by Akaike's Information Criterion and the finite corrections. Commun Stat - Theory Methods. 1978;A7:13-26.
113. Smiesko V, Khayutin VM, Kozík J, Rogoza AN. Flow-induced dilation of the dog gracilis muscle artery. Physiol Bohemoslov. 1987;36:289-300.
114. Burnham KP, Anderson DR: Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. 2nd ed. New York: Springer; 2002.
115. Rosseel Y: lavaan: An R package for structural equation modeling. J Stat Softw 2012.
116. Schoemann A: Using Monte Carlo simulations to determine power and sample size for planned missing designs. Int J ... 2014.
117. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B. 1995;57:289-300.
118. Yin J, Li H. A sparse conditional Gaussian graphical model for analysis of genetical genomics data. Ann Appl Stat. 2011;5:2630-50.
119. Krumsiek J, Suhre K, Illig T, Adamski J, Theis FJ. Gaussian graphical modeling reconstructs pathway reactions from high-throughput metabolomics data. BMC Syst Biol. 2011;5:21.
120. Takahashi H, Bhumiratana S, Cheevadhanarak S, Netrphan S, Tanticharoen M, Ingkasuwan P, et al. Inferring transcriptional gene regulation network of starch metabolism in Arabidopsis thaliana leaves using graphical gaussian model. BMC Syst Biol. 2012;100.
121. Ma S, Gong Q, Bohnert HJ. An Arabidopsis gene network based on the graphical Gaussian model. Genome Res. 2007;17:1614-25.
122. Lallena MJ, Chalmers KJ, Llamazares S, Lamond AI, Valcárcel J. Splicing regulation at the second catalytic step by Sex-lethal involves 3' splice site recognition by SPF45. Cell. 2002;109:285-96.
123. Flickinger TW, Salz HK. The Drosophila sex determination gene snf encodes a nuclear protein with sequence and functional similarity to the mammalian U1A snRNP protein. Genes Dev. 1994;8:914-25.
124. Inoue K, Hoshijima K, Sakamoto H, Shimura Y. Binding of the Drosophila sex-lethal gene product to the alternative splice site of transformer primary transcript. Nature. 1990;344:461-3.
125. Gebauer F, Merendino L, Hentze MW, Valcárcel J. The Drosophila splicing regulator sex-lethal directly inhibits translation of male-specific-lethal 2 mRNA. RNA. 1998;4:142-50.
126. Granadino B, Penalva LO, Sánchez L. The gene fl(2)d is needed for the sex-specific splicing of transformer pre-mRNA but not for double-sex pre-mRNA in Drosophila melanogaster. Mol Gen Genet. 1996;253:26-31.
127. An W, Wensink PC. Three protein binding sites form an enhancer that regulates sex- and fat body-specific transcription of Drosophila yolk protein genes. EMBO J. 1995;14:1221-30.
128. Burtis KC, Coschigano KT, Baker BS, Wensink PC. The doublesex proteins of Drosophila melanogaster bind directly to a sex-specific yolk protein gene enhancer. EMBO J. 1991;10:2577-82.
129. Li H, Baker B. hermaphrodite and doublesex function both dependently and independently to control various aspects of sexual differentiation in Drosophila. Development. 1998;125:2641-51.