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PLOS ONE  2009 

Effect of the Gene doublesex of Anastrepha on the Somatic Sexual Development of Drosophila

DOI: 10.1371/journal.pone.0005141

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Background The gene doublesex (dsx) is at the bottom of the sex determination genetic cascade and is transcribed in both sexes, but gives rise to two different proteins, DsxF and DsxM, which impose female and male sexual development respectively via the sex-specific regulation of the so-called sexual cyto-differentiation genes. The present manuscript addressed the question about the functional conservation of the tephritid Anastrepha DsxF and DsxM proteins to direct the sexual development in Drosophila (Drosophilidae). Methodology To express these proteins in Drosophila, the GAL4-UAS system was used. The effect of these proteins was monitored in the sexually dimorphic regions of the fly: the foreleg basitarsus, the 5th, 6th and 7th tergites, and the external terminalia. In addition, we analysed the effect of Anastrepha DsxF and DsxM proteins on the regulation of Drosophila yolk protein genes, which are expressed in the fat body of adult females under the control of dsx. Conclusions The Anastrepha DsxF and DsxM proteins transformed doublesex intersexual Drosophila flies into females and males respectively, though this transformation was incomplete and the extent of their influence varied in the different sexually dimorphic regions of the adult fly. The Anastrepha DsxF and DsxM proteins also behaved as activators and repressors, respectively, of the Drosophila yolk protein genes, as do the DsxF and DsxM proteins of Drosophila itself. Finally, the Anastrepha DsxF and DsxM proteins were found to counteract the functions of Drosophila DsxM and DsxF respectively, reflecting the normal behaviour of the latter proteins towards one another. Collectively, these results indicate that the Anastrepha DsxF and DsxM proteins show conserved female and male sex-determination function respectively in Drosophila, though it appears that they cannot fully substitute the latter's own Dsx proteins. This incomplete function might be partly due to a reduced capacity of the Anastrepha Dsx proteins to completely control the Drosophila sexual cyto-differentiation genes, a consequence of the accumulation of divergence between these species resulting in the formation of different co-adapted complexes between the Dsx proteins and their target genes.


[1]  Bull JB (1983) Evolution of sex determining mechanisms. Menlo Park, California, USA: The Benjamin/Cummings Publishing Company, Inc.
[2]  Marín I, Baker BS (1998) The evolutionary dynamics of sex determination. Science 281: 1990–1994.
[3]  Sánchez L (2008) Sex-determining mechanisms in insects. Int J Dev Biol 52: 837–856.
[4]  Sánchez L, Gorfinkiel N, Guerrero I (2005) Sex determination and the development of the genital disc. In: Gilbert LI, Iatrou K, Gill SS, editors. Comprehensive Molecular Insect Science, Vol. 1. Oxforf, UK: Elsevier Pergamon. pp. 1–38.
[5]  Sievert V, Kuhn S, Traut W (1997) Expression of the sex determination cascade genes Sex-lethal and doublesex in the phorid fly Megaselia scalaris. Genome 40: 211–214.
[6]  Kuhn S, Sievert V, Traut W (2000) The sex-determining gene doublesex in the fly Megaselia scalaris: conserved structure and sex-specific splicing. Genome 43: 1011–1020.
[7]  Hediger M, Burghardt G, Siegenthaler C, Buser N, Hilfiker-Kleiner D, et al. (2004) Sex determination in Drosophila melanogaster and Musca domestica converges at the level of the terminal regulator doublesex. Dev Genes Evol 214: 29–42.
[8]  Scali C, Catteruccia F, Li Q, Crisanti A (2005) Identification of sex-specific transcripts of the Anopheles gambiae doublesex gene. J Exp Biol 208: 3701–3709.
[9]  Shearman D, Frommer M (1998) The Bactrocera tryoni homologue of the Drosophila melanogaster sex determination gene doublesex. Insect Mol Biol 7: 355–366.
[10]  Lagos D, Ruiz MF, Sánchez L, Komitopoulou K (2005) Isolation and characterization of the Bactrocera oleae genes orthologous to the sex determining Sex-lethal and doublesex genes of Drosophila melanogaster. Gene 384: 111–121.
[11]  Chen SL, Dai SM, Lu KH, Chang Ch (2008) Female-specific doublesex dsRNA interrupts yolk protein gene expression and reproductive ability in oriental fruit fly, Bactrocera dorsalis (Hendel). Insect Bioch Mol Biol 38: 155–165.
[12]  Saccone G, Salvemini M, Pane A, Polito LC (2008) Masculinization of XX Drosophila transgenic flies expressing the Ceratitis capitata DoublsexM isoform. Int J Dev Biol 52: 1043–1050.
[13]  Ruiz MF, Stefani RN, Mascarenhas RO, Perondini ALP, Selivon D, et al. (2005) The gene doublesex of the fruit fly Anastrepha obliqua (Diptera, Tephritidae). Genetics 171: 849–854.
[14]  Ruiz MF, Eirín-López JM, Stefani RN, Perondini ALP, Selivon D, et al. (2007) The gene doublesex of Anastrepha fruit flies (Diptera, tephritidae) and its evolution in insects. Dev Genes Evol 217: 725–731.
[15]  Ohbayashi F, Suzuki M, Mita K, Okano K, Shimada T (2001) A homologue of the Drosophila doublesex gene is transcribed into sex-specific mRNA isoforms in the silkworm, Bombyx mori. Comp Biochem Physiol 128: 145–158.
[16]  Suzuki MG, Ohbayashi F, Mita K, Shimada T (2001) The mechanism of sex-specific splicing at the doublesex gene is different between Drosophila melanogaster and Bombyx mori. Insect Biochem Mol Biol 31: 1201–1211.
[17]  Cho S, Huang ZY, Zhang J (2007) Sex-Specific Splicing of the Honeybee doublesex Gene Reveals 300 Million Years of Evolution at the Bottom of the Insect Sex-Determination Pathway. Genetics 177: 1733–1741.
[18]  An W, Cho S, Ishii H, Wensink PC (1996) Sex-specific and non-sex-specific oligomerization domains in both of the Doublesex transcription factors from Drosophila melanogaster. Mol Cell Biol 16: 3106–3111.
[19]  Cho S, Wensink PC (1997) DNA binding by the male and female doublesex proteins of Drosophila melanogaster. J Biol Chem 272: 3185–3189.
[20]  Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401–415.
[21]  Jurnish VA, Burtis K (1993) A positive role in differentiation for the male doublesex protein of Drosophila. Dev Biol 155: 235–249.
[22]  Sánchez L, Guerrero I (2001) The development of the Drosophila genital disc. BioEssays 23: 698–707.
[23]  Christiansen AE, Keisman EL, Ahmad SM, Baker BS (2002) Sex comes in from the cold: the integration of sex and pattern. Trends in Genetics 18: 510–516.
[24]  Gowen JW (1942) Hermaphrodites in Drosophila melanogaster. Drosophila Inform Serv 16: 63.
[25]  Denell RE, Jackson J (1972) A genetic analysis of transformer-Dominant. Drosophila Inform Serv 48: 45.
[26]  Epper F (1981) Morphological analysis and fate map of the intersexual genital disc of the mutant doublesex-dominant in Drosophila melanogaster. Dev Biol 88: 104–14.
[27]  Baker B, Ridge K (1980) Sex and the single cell. I. On the action of the major loci affecting sex determination in Drosophila melanogaster. Genetics 94: 383–423.
[28]  N?thiger R, Leuthold M, Andersen N, Gerschwiler P, Gruter A, et al. (1987) Genetic and developmental analysis of the sex-determining gene doublesex (dsx) of Drosophila melanogaster. Genet Res 50: 113–123.
[29]  Bownes M (1994) The regulation of yolk protein genes, a family of sex differentiation genes in Drosophila melanogaster. BioEssays 16: 745–752.
[30]  Bownes M, Steinmann-Zwicky M, N?thiger R (1990) Differential control of yolk protein gene expression in fat bodies and gonads by the sex-determining gene tra-2 of Drosophila. EMBO J 9: 3975–3980.
[31]  Bownes M, N?thiger R (1981) Sex determining genes and vitellogenin synthesis in Drosophila melanogaster. Mol Gen Genet 182: 222–228.
[32]  Ramos-Onsins S, Segarra C, Rozas J, Aguadé M (1998) Molecular and chromosomal phylogeny in the obscura group of Drosophila inferred from sequences of the rp49 gene region. Mol Phylo Evol 9: 33–41.
[33]  Kopp A, Duncan I, Carroll SB (2000) Genetic control and evolution of sexually dimorphic characters in Drosophila. Nature 408: 553–559.
[34]  Williams TM, Selegue JE, Werner T, Gompel N, Kopp A, et al. (2008) The Regulation and evolution of a genetic switch controlling sexually dimorphic traits in Drosophila. Cell 134: 610–623.
[35]  Sánchez L, Gorfinkiel N, Guerrero I (2001) Sex determination genes control the development of the Drosophila genital disc modulating the response to Hedgehog, Wingless, and Decapentaplegic signals. Development 128: 1033–1043.
[36]  Keisman EL, Baker BS (2001) The Drosophila sex determination hierarchy modulates wingless and decapentaplegic signaling to deploy dachshund sex-specifically in the genital imaginal disc. Development 128: 1643–56.
[37]  Estrada B, Sánchez-Herrero E (2001) The Hox gene Abdominal-B antagonizes appendage development in the genital disc of Drosophila. Development 128: 331–339.
[38]  Gorfinkiel N, et al. (1999) Drosophila terminalia as an appendage-like structure. Mech Dev 86: 113–23.
[39]  Moreno E, Morata G (1999) Caudal is the Hox gene that specifies the most posterior Drosophila segment. Nature 400: 873–877.
[40]  Chase BA, Baker BS (1995) A genetic analysis of intersex, a gene regulating sexual differentiation in Drosophila melanogaster females. Genetics 139: 1649–61.
[41]  Waterbury JA, Jackson LL, Schedl P (1999) Analysis of the doublesex female protein in Drosophila melanogaster: role on sexual differentiation and behavior and dependence on intersex. Genetics 152: 1653–67.
[42]  Garrett-Engele CM, et al. (2002) 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 129: 4661–75.
[43]  Sánchez L, Santamaría P (1997) Reproductive isolation and morphogenetic evolution in Drosophila analyzed by breakage of ethological barriers. Genetics 147: 231–242.
[44]  Carroll SB (2008) Evo-Devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134: 25–36.
[45]  Lindsley DL, Zimm G (1992) The genome of Drosophila melanogaster. San Diego, California: Academic Press.


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