The female-specific Doublesex isoform regulates pleiotropic transcription factors to pattern genital development in Drosophila

Development

Volumn 138, Issue 6, 2011, Pages 1099-1109

  Chatterjee, Sujash S ^a   Uppendahl, Locke D ^a,b   Chowdhury, Moinuddin A ^a   Ip, Pui Leng ^a   Siegal, Mark L ^a  

^a NEW YORK UNIVERSITY   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

Drosophila; Genitalia; Pattern formation; Sexual differentiation

Indexed keywords

PROTEIN AP 2; PROTEIN BRANCHLESS; PROTEIN DOUBLESEX; PROTEIN DROP; PROTEIN DSXF; PROTEIN LZ; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BINDING SITE; DROSOPHILA; DROSOPHILA MELANOGASTER; FEMALE; GENETIC ASSOCIATION; GENITAL SYSTEM; MALE; NONHUMAN; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; SEX DETERMINATION; SEX DIFFERENCE; SPERMATHECA;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BODY PATTERNING; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; GENITALIA; MALE; ORGANOGENESIS; PROTEIN ISOFORMS; SEX CHARACTERISTICS; TRANSCRIPTION FACTORS;

ANIMALIA; DROSOPHILA MELANOGASTER;

EID: 79955134790     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.055731     Document Type: Article

References (89)

1. Ahmad, S. M. and Baker, B. S. (2002). Sex-specific deployment of FGF signaling in Drosophila recruits mesodermal cells into the male genital imaginal disc. Cell 109, 651-661.
2. An, W. and Wensink, P. C. (1995). Integrating sex-and tissue-specific regulation within a single Drosophila enhancer. Genes Dev. 9, 256-266.
3. Anderson, R. C. (1945). A study of the factors affecting fertility of lozenge females of Drosophila melanogaster. Genetics 30, 280-296.
4. Arbeitman, M. N., Fleming, A. A., Siegal, M. L., Null, B. H. and Baker, B. S. (2004). A genomic analysis of Drosophila somatic sexual differentiation and its regulation. Development 131, 2007-2021.
5. Arbeitman, M. N., Kopp, A., Siegal, M. L. and Van Doren, M. (2010). Everything you always wanted to know about sex... in flies. Sex. Dev. 4, 315-320.
6. Artero, R., Furlong, E. E., Beckett, K., Scott, M. P. and Baylies, M. (2003). Notch and Ras signaling pathway effector genes expressed in fusion competent and founder cells during Drosophila myogenesis. Development 130, 6257-6272.
7. Bainbridge, S. P. and Bownes, M. (1981). Staging the metamorphosis of Drosophila melanogaster. J. Embryol. Exp. Morphol. 66, 57-80.
8. Bashaw, G. J. and Baker, B. S. (1997). The regulation of the Drosophila msl-2 gene reveals a function for Sex-lethal in translational control. Cell 89, 789-798.
9. Boll, W. and Noll, M. (2002). The Drosophila Pox neuro gene: control of male courtship behavior and fertility as revealed by a complete dissection of all enhancers. Development 129, 5667-5681.
10. Bownes, M. (1994). The regulation of the yolk protein genes, a family of sex differentiation genes in Drosophila melanogaster. BioEssays 16, 745-752.
11. Brennan, J. and Capel, B. (2004). One tissue, two fates: molecular genetic events that underlie testis versus ovary development. Nat. Rev. Genet. 5, 509-521.
12. Bryant, P. J. (1978). Pattern formation in imaginal discs. In The Genetics and Biology of Drosophila, Vol. 2c (ed. M. Ashburner and T. R. F. Wright), pp. 229-335. New York: Academic Press.
13. Burtis, K. C., Coschigano, K. T., Baker, B. S. and Wensink, P. C. (1991). The doublesex proteins of Drosophila melanogaster bind directly to a sex-specific yolk protein gene enhancer. EMBO J. 10, 2577-2582.
14. Camara, N., Whitworth, C. and Van Doren, M. (2008). The creation of sexual dimorphism in the Drosophila soma. Curr. Top. Dev. Biol. 83, 65-107.
15. Campbell, G., Weaver, T. and Tomlinson, A. (1993). Axis specification in the developing Drosophila appendage: the role of wingless, decapentaplegic, and the homeobox gene aristaless. Cell 74, 1113-1123.
16. Canon, J. and Banerjee, U. (2000). Runt and lozenge function in Drosophila development. Semin. Cell Dev. Biol. 11, 327-336.
17. Carroll, S. B., Grenier, J. K. and Weatherbee, S. D. (2001). From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design. Malden, MA: Blackwell Science.
18. Casares, F., Sánchez, L., Guerrero, I. and Sánchez-Herrero, E. (1997). The genital disc of Drosophila melanogaster. I. Segmental and compartmental organization. Dev. Genes Evol. 207, 216-228.
19. Chen, E. H. and Baker, B. S. (1997). Compartmental organization of the Drosophila genital imaginal discs. Development 124, 205-218.
20. Chen, E. H., Christiansen, A. E. and Baker, B. S. (2005). Allocation and specification of the genital disc precursor cells in Drosophila. Dev. Biol. 281, 270-285.
21. Christiansen, A. E., Keisman, E. L., Ahmad, S. M. and Baker, B. S. (2002). Sex comes in from the cold: the integration of sex and pattern. Trends Genet. 18, 510-516.
22. Cline, T. W. and Meyer, B. J. (1996). Vive la difference: males vs females in flies vs worms. Annu. Rev. Genet. 30, 637-702.
23. Coelho, D. J., Sims, D. J., Ruegg, P. J., Minn, I., Muench, A. R. and Mitchell, P. J. (2005). Cell type-specific and sexually dimorphic expression of transcription factor AP-2 in the adult mouse brain. Neuroscience 134, 907-919.
24. Cohen, S. M. (1993). Imaginal disc development. In The Development of Drosophila melanogaster (ed. M. Bate and A. Martinez-Arias), pp. 747-842. Plainview, NY: Cold Spring Harbor Laboratory Press.
25. Couderc, J. L., Godt, D., Zollman, S., Chen, J., Li, M., Tiong, S., Cramton, S. E., Sahut-Barnola, I. and Laski, F. A. (2002). The bric a brac locus consists of two paralogous genes encoding BTB/POZ domain proteins and acts as a homeotic and morphogenetic regulator of imaginal development in Drosophila. Development 129, 2419-2433.
26. Coyne, J. A. (1983). Genetic basis of differences in genital morphology among three sibling species of Drosophila. Evolution 37, 1101-1118.
27. Da Lage, J. L., Renard, E., Chartois, F., Lemeunier, F. and Cariou, M. L. (1998). Amyrel, a paralogous gene of the amylase gene family in Drosophila melanogaster and the Sophophora subgenus. Proc. Natl. Acad. Sci. USA 95, 6848-6853.
28. Dietzl, G., Chen, D., Schnorrer, F., Su, K. C., Barinova, Y., Fellner, M., Gasser, B., Kinsey, K., Oppel, S., Scheiblauer, S. et al. (2007). A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448, 151-156.
29. Dong, P. D., Todi, S. V., Eberl, D. F. and Boekhoff-Falk, G. (2003). Drosophila spalt/spalt-related mutants exhibit Townes-Brocks' syndrome phenotypes. Proc. Natl. Acad. Sci. USA 100, 10293-10298.
30. Dorus, S., Busby, S. A., Gerike, U., Shabanowitz, J., Hunt, D. F. and Karr, T. L. (2006). Genomic and functional evolution of the Drosophila melanogaster sperm proteome. Nat. Genet. 38, 1440-1445.
31. Epper, F. (1983). The evagination of the genital imaginal discs of Drosophila melanogaster. I. Morphogenesis of the female genital disc. Rouxs Arch. Dev. Biol. 192, 275-279.
32. Erdman, S. E., Chen, H. J. and Burtis, K. C. (1996). Functional and genetic characterization of the oligomerization and DNA binding properties of the Drosophila doublesex proteins. Genetics 144, 1639-1652.
33. Estrada, B., Casares, F. and Sanchez-Herrero, E. (2003). Development of the genitalia in Drosophila melanogaster. Differentiation 71, 299-310.
34. Ferveur, J. F., Stortkuhl, K. F., Stocker, R. F. and Greenspan, R. J. (1995). Genetic feminization of brain structures and changed sexual orientation in male Drosophila. Science 267, 902-905.
35. Fortier, E. and Belote, J. M. (2000). Temperature-dependent gene silencing by an expressed inverted repeat in Drosophila. Genesis 26, 240-244.
36. Freeland, D. E. and Kuhn, D. T. (1996). Expression patterns of developmental genes reveal segment and parasegment organization of D. melanogaster genital discs. Mech. Dev. 56, 61-72.
37. Furlong, E. E. (2004). Integrating transcriptional and signalling networks during muscle development. Curr. Opin. Genet. Dev. 14, 343-350.
38. Gentleman, R. C., Carey, V. J., Bates, D. M., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J. et al. (2004). Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80.
39. Goldman, T. D. and Arbeitman, M. N. (2007). Genomic and functional studies of Drosophila sex hierarchy regulated gene expression in adult head and nervous system tissues. PLoS Genet. 3, e216.
40. Gorfinkiel, N., Sanchez, L. and Guerrero, I. (1999). Drosophila terminalia as an appendage-like structure. Mech. Dev. 86, 113-123.
41. Ha, Y., Tsukada, A., Saito, N., Zadworny, D. and Shimada, K. (2008). Identification of differentially expressed genes involved in the regression and development of the chicken Mullerian duct. Int. J. Dev. Biol. 52, 1135-1141.
42. Hempel, L. U. and Oliver, B. (2007). Sex-specific DoublesexM expression in subsets of Drosophila somatic gonad cells. BMC Dev. Biol. 7, 113.
43. Hildreth, P. E. (1965). Doublesex, recessive gene that transforms both males and females of Drosophila into intersexes. Genetics 51, 659-678.
44. Irizarry, R. A., Bolstad, B. M., Collin, F., Cope, L. M., Hobbs, B. and Speed, T. P. (2003). Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31, e15.
45. Ito, K., Awano, W., Suzuki, K., Hiromi, Y. and Yamamoto, D. (1997). The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurones and glial cells. Development 124, 761-771.
46. Kaufman, L. and Rousseeuw, P. J. (1990). Partitioning around medoids (Program PAM). In Finding Groups in Data: An Introduction to Cluster Analysis, pp. 68-125. New York, NY: Wiley.
47. Keisman, E. L. and Baker, B. S. (2001). The Drosophila sex determination hierarchy modulates wingless and decapentaplegic signaling to deploy dachshund sex-specifically in the genital imaginal disc. Development 128, 1643-1656.
48. Keisman, E. L., Christiansen, A. E. and Baker, B. S. (2001). The sex determination gene doublesex regulates the A/P organizer to direct sex-specific patterns of growth in the Drosophila genital imaginal disc. Dev. Cell 1, 215-225.
49. Kiger, J. A., Jr, Natzle, J. E., Kimbrell, D. A., Paddy, M. R., Kleinhesselink, K. and Green, M. M. (2007). Tissue remodeling during maturation of the Drosophila wing. Dev. Biol. 301, 178-191.
50. Kopp, A., Duncan, I., Godt, D. and Carroll, S. B. (2000). Genetic control and evolution of sexually dimorphic characters in Drosophila. Nature 408, 553-559.
51. Kosman, D., Mizutani, C. M., Lemons, D., Cox, W. G., McGinnis, W. and Bier, E. (2004). Multiplex detection of RNA expression in Drosophila embryos. Science 305, 846.
52. Kozopas, K. M., Samos, C. H. and Nusse, R. (1998). DWnt-2, a Drosophila Wnt gene required for the development of the male reproductive tract, specifies a sexually dimorphic cell fate. Genes Dev. 12, 1155-1165.
53. Lebo, M. S., Sanders, L. E., Sun, F. and Arbeitman, M. N. (2009). Somatic, germline and sex hierarchy regulated gene expression during Drosophila metamorphosis. BMC Genomics 10, 80.
54. MacKenzie, A., Purdie, L., Davidson, D., Collinson, M. and Hill, R. E. (1997). Two enhancer domains control early aspects of the complex expression pattern of Msx1. Mech. Dev. 62, 29-40.
55. Manolakou, P., Lavranos, G. and Angelopoulou, R. (2006). Molecular patterns of sex determination in the animal kingdom: a comparative study of the biology of reproduction. Reprod. Biol. Endocrinol. 4, 59.
56. Marín, I. and Baker, B. S. (1998). The evolutionary dynamics of sex determination. Science 281, 1990-1994.
57. Milán, M., Weihe, U., Tiong, S., Bender, W. and Cohen, S. M. (2001). msh specifies dorsal cell fate in the Drosophila wing. Development 128, 3263-3268.
58. Monge, I., Krishnamurthy, R., Sims, D., Hirth, F., Spengler, M., Kammermeier, L., Reichert, H. and Mitchell, P. J. (2001). Drosophila transcription factor AP-2 in proboscis, leg and brain central complex development. Development 128, 1239-1252.
59. Nöthiger, R., Dübendorfer, A. and Epper, F. (1977). Gynandromorphs reveal two separate primordia for male and female genitalia. Rouxs Arch. Dev. Biol. 181, 367-373.
60. Parks, A. L., Cook, K. R., Belvin, M., Dompe, N. A., Fawcett, R., Huppert, K., Tan, L. R., Winter, C. G., Bogart, K. P., Deal, J. E. et al. (2004). Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nat. Genet. 36, 288-292.
61. Pignoni, F. and Zipursky, S. L. (1997). Induction of Drosophila eye development by decapentaplegic. Development 124, 271-278.
62. Pitnick, S., Markow, T. and Spicer, G. S. (1999). Evolution of multiple kinds of female sperm-storage organs in Drosophila. Evolution 53, 1804-1822.
63. Ramos, C. and Robert, B. (2005). msh/Msx gene family in neural development. Trends Genet. 21, 624-632.
64. Robinett, C. C., Vaughan, A. G., Knapp, J. M. and Baker, B. S. (2010). Sex and the single cell. II. There is a time and place for sex. PLoS Biol. 8, e1000365.
65. Schüpbach, T., Wieschaus, E. and Nöthiger, R. (1978). The embryonic organization of the genital disc studied in genetic mosaics of Drosophila melanogaster. Rouxs Arch. Dev. Biol. 185, 249-270.
66. Shen-Orr, S. S., Milo, R., Mangan, S. and Alon, U. (2002). Network motifs in the transcriptional regulation network of Escherichia coli. Nat. Genet. 31, 64-68.
67. Shirangi, T. R., Dufour, H. D., Williams, T. M. and Carroll, S. B. (2009). Rapid evolution of sex pheromone-producing enzyme expression in Drosophila. PLoS Biol. 7, e1000168.
68. Siegal, M. L. and Baker, B. S. (2005). Functional conservation and divergence of intersex, a gene required for female differentiation in Drosophila melanogaster. Dev. Genes Evol. 215, 1-12.
69. Simeone, A., Daga, A. and Calabi, F. (1995). Expression of runt in the mouse embryo. Dev. Dyn. 203, 61-70.
70. Skeath, J. B. and Carroll, S. B. (1991). Regulation of achaete-scute gene expression and sensory organ pattern formation in the Drosophila wing. Genes Dev. 5, 984-995.
71. Sosinsky, A., Bonin, C. P., Mann, R. S. and Honig, B. (2003). Target explorer: An automated tool for the identification of new target genes for a specified set of transcription factors. Nucleic Acids Res. 31, 3589-3592.
72. Spéder, P., Ádám, G. and Noselli, S. (2006). Type ID unconventional myosin controls left-right asymmetry in Drosophila. Nature 440, 803-807.
73. Stern, C. (1941a). The growth of the testes in Drosophila. I. The relation between vas deferens and testis within various species. J. Exp. Zool. 87, 113-158.
74. Stern, C. (1941b). The growth of the testes in Drosophila. II. The nature of interspecific differences. J. Exp. Zool. 87, 159-180.
75. Stieper, B. C., Kupershtok, M., Driscoll, M. V. and Shingleton, A. W. (2008). Imaginal discs regulate developmental timing in Drosophila melanogaster. Dev. Biol. 321, 18-26.
76. Sullivan, W., Ashburner, M. and Hawley, R. S. (2000). Drosophila Protocols. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
77. Suzanne, M., Petzoldt, A. G., Spéder, P., Coutelis, J. B., Steller, H. and Noselli, S. (2010). Coupling of apoptosis and L/R patterning controls stepwise organ looping. Curr. Biol. 20, 1773-1778.
78. Takemori, N. and Yamamoto, M. T. (2009). Proteome mapping of the Drosophila melanogaster male reproductive system. Proteomics 9, 2484-2493.
79. Tusher, V. G., Tibshirani, R. and Chu, G. (2001). Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. USA 98, 5116-5121.
80. Tweedie, S., Ashburner, M., Falls, K., Leyland, P., McQuilton, P., Marygold, S., Millburn, G., Osumi-Sutherland, D., Schroeder, A., Seal, R. et al. (2009). FlyBase: enhancing Drosophila gene ontology annotations. Nucleic Acids Res. 37, D555-D559.
81. van der Laan, M. J., Pollard, K. S. and Bryan, J. (2003). A new partitioning around medoids algorithm. J. Stat. Comput. Simul. 73, 575-584.
82. von Ohlen, T. and Doe, C. Q. (2000). Convergence of dorsal, dpp, and egfr signaling pathways subdivides the drosophila neuroectoderm into three dorsalventral columns. Dev. Biol. 224, 362-372.
83. Williams, T. M. and Carroll, S. B. (2009). Genetic and molecular insights into the development and evolution of sexual dimorphism. Nat. Rev. Genet. 10, 797-804.
84. Williams, T. M., Selegue, J. E., Werner, T., Gompel, N., Kopp, A. and Carroll, S. B. (2008). The regulation and evolution of a genetic switch controlling sexually dimorphic traits in Drosophila. Cell 134, 610-623.
85. Xu, T. and Rubin, G. M. (1993). Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223-1237.
86. Xue, L. and Noll, M. (2002). Dual role of the Pax gene paired in accessory gland development of Drosophila. Development 129, 339-346.
87. Yao, J. G., Weasner, B. M., Wang, L. H., Jang, C. C., Weasner, B., Tang, C. Y., Salzer, C. L., Chen, C. H., Hay, B., Sun, Y. H. et al. (2008). Differential requirements for the Pax6(5a) genes eyegone and twin of eyegone during eye development in Drosophila. Dev. Biol. 315, 535-551.
88. Yin, Y., Lin, C. and Ma, L. (2006). MSX2 promotes vaginal epithelial differentiation and Wolffian duct regression and dampens the vaginal response to diethylstilbestrol. Mol. Endocrinol. 20, 1535-1546.
89. Zarkower, D. (2002). Invertebrates may not be so different after all. Novartis Found. Symp. 244, 115-135.