Identification and characterization of the doublesex gene of Nasonia

Insect Molecular Biology

Volumn 18, Issue 3, 2009, Pages 315-324

  Oliveira, D C S G ^a   Werren, J H ^a   Verhulst, E C ^b   Giebel, J D ^a   Kamping, A ^b   Beukeboom, L W ^b   Van De Zande, L ^b  

^a UNIVERSITY OF ROCHESTER   (United States)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

DM domain genes; Doublesex; Haplodiploidy; Hymenoptera; Sex determination

Indexed keywords

DNA BINDING PROTEIN; DROSOPHILA PROTEIN; DSX PROTEIN, DROSOPHILA; INSECT PROTEIN; MESSENGER RNA;

ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; ANIMAL; ARTICLE; FEMALE; GENDER AND SEX; GENETICS; HAPLOIDY; MALE; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; SEQUENCE HOMOLOGY; WASP;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; DNA-BINDING PROTEINS; DROSOPHILA PROTEINS; EVOLUTION, MOLECULAR; FEMALE; HAPLOIDY; INSECT PROTEINS; MALE; MOLECULAR SEQUENCE DATA; RNA, MESSENGER; SEQUENCE HOMOLOGY, AMINO ACID; SEX DETERMINATION (GENETICS); WASPS;

APIS; DIPTERA; HEXAPODA; HYMENOPTERA; LEPIDOPTERA; NASONIA; NASONIA VITRIPENNIS; VESPOIDEA;

EID: 67249156187     PISSN: 09621075     EISSN: 13652583     Source Type: Journal    
DOI: 10.1111/j.1365-2583.2009.00874.x     Document Type: Article

References (45)

1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215 : 403 410.
2. Baker, B.S. Ridge, K. (1980) Sex and the single cell: On the action of major loci affecting sex determination in Drosophila melanogaster. Genetics 94 : 383 423. (Pubitemid 11014207)
3. Baker, B.S. Wolfner, M.F. (1988) A molecular analysis of doublesex, a bifunctional gene that controls both male and female sexual differentiation in Drosophila melanogaster. Genes Dev 2 : 477 489.
4. Bayrer, J.R., Zhang, W. Weiss, M.A. (2005) Dimerization of doublesex is mediated by a cryptic ubiquitin-associated domain fold: implications for sex-specific gene regulation. J Biol Chem 280 : 32989 32996. (Pubitemid 41368348)
5. Beukeboom, L.W. (1995) Sex determination in Hymenoptera: a need for genetic and molecular studies. Bioessays 17 : 813 817.
6. Beukeboom, L. Desplan, C. (2003) Nasonia. Curr Biol 13 : R860.
7. Beukeboom, L.W. Kamping, A. (2006) No patrigenes required for femaleness in the haplodiploid wasp Nasonia vitripennis. Genetics 172 : 981 989. (Pubitemid 43345433)
8. Beukeboom, L.W., Kamping, A., Louter, M., Pijnacker, L.P., Katju, V., Ferree, P.M. et al 2007a) Haploid females in the parasitic wasp Nasonia vitripennis. Science 315 : 206. (Pubitemid 46166359)
9. Beukeboom, L., Kamping, A. van de Zande, L. (2007b) Sex determination in the haplodiploid wasp Nasonia vitripennis (Hymenoptera: Chalcidoidea): A critical consideration of models and evidence. Semin Cell Dev Biol 18 : 371 378. (Pubitemid 47211979)
10. Beye, M., Hasselmann, M., Fondrk, M.K., Page, R.E. Omholt, S.W. (2003) The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell 114 : 419 429. (Pubitemid 37100991)
11. Cho, S., Huang, Z.Y. 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. (Pubitemid 350277066)
12. Cook, J.M. (1993) Sex determination in the Hymenoptera: a review of models and evidence. Heredity 71 : 421 435.
13. Crozier, R.H. (1971) Heterozygosity and sex determination in haplodiploidy. Am Nat 105 : 399 412.
14. Erickson, J.W. Quintero, J.J. (2007) Indirect effects of ploidy suggest X chromosome dosage, not the X:A ratio, signals sex in Drosophila. PLoS Biol 5 : 2821 2830. (Pubitemid 351159710)
15. Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39 : 783 791.
16. Ferree, P.M., McDonald, K., Fasulo, B. Sullivan, W. (2006) The origin of centrosomes in parthenogenetic hymenopteran insects. Curr Biol 16 : 801 807.
17. Finn, R.D., Mistry, J., Schuster-Böckler, B., Griffiths-Jones, S., Hollich, V., Lassmann, T. et al 2006) Pfam: clans, web tools and services. Nucl Acids Res 34 : D247 D251.
18. Hasselmann, M., Gempe, T., Schiott, M., Nunes-Silva, C.G., Otte, M. Beye, M. (2008) Evidence for the evolutionary nascence of a novel sex determination pathway in honeybees. Nature 454 : 519 522.
19. Hediger, M., Burghardt, G., Siegenthaler, C., Buser, N., Hilfiker-Kleiner, D., Dübendorfer, A. 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. (Pubitemid 38196114)
20. Inoue, K., Hoshijima, K., Higuchi, I., Sakamoto, H. Shimura, Y. (1992) 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 USA 89 : 8092 8096.
21. Kamping, A., Katju, V., Beukeboom, L.W. Werren, J.H. (2007) Inheritance of gynandromorphism in the parasitic wasp Nasonia vitripennis. Genetics 175 : 1321 1333. (Pubitemid 46798233)
22. Lynch, J.A., Brent, A.E., Leaf, D.S., Pultz, M.A. Desplan, C. (2006) Localized maternal orthodenticle patterns anterior and posterior in the long germ wasp Nasonia. Nature 439 : 728 732. (Pubitemid 43237619)
23. Maddison, D.R. Maddison, W.P. (2000) MacClade: analysis of phylogeny and character evolution, version 4.0. Sinauer Associates Sunderland, Massachusetts.
24. Ohbayashi, F.M., Suzuki, M.G., 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 B Biochem Mol Biol 1 : 145 158. (Pubitemid 32157505)
25. Pultz, M.A. Leaf, D.S. (2003) The jewel wasp Nasonia: querying the genome with haplo-diploid genetics. Genesis 35 : 185 191. (Pubitemid 36396892)
26. Raymond, C.S., Shamu, C.S., Shen, M.M., Selfert, K.J., Hirsch, B., Hodgkin, J. et al 1998) Evidence for evolutionary conservation of sex-determining genes. Nature 391 : 691 695. (Pubitemid 28113214)
27. Raymond, C.S., Murphy, M.W., O′Sullivan, M.G., Bardwell, V.J. Zarkower, D. (2000) Dmrt1, a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation. Genes Dev 14 : 2587 2595.
28. Ruiz, M.F., Stefani, R.N., Mascarenhas, R.O., Perondine, A.L., Selivon, D. Sánchez, L. (2005) The gene doublesex of the fruit fly Anastrepha obliqua (Diptera, Tephritidae). Genetics 171 : 849 854. (Pubitemid 43156472)
29. 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. (Pubitemid 41571750)
30. Sherman, D.C. Frommer, M. (1998) The Bactrocera tryoni homologue of the Drosophila melanogaster sex-determining gene doublesex. Insect Mol Biol 7 : 355 366. (Pubitemid 28371564)
31. Shuker, D., Lynch, J. Peire Morais, A. (2003) Moving from model to non-model organisms? Lessons from Nasonia wasps. Bioessays 25 : 1247 1248. (Pubitemid 37499325)
32. Skinner, S.W. Werren, J.H. (1980) The genetics of sex determination in Nasonia vitripennis (Hymenoptera, Pteromalidae). Genetics 94 : s98.
33. Suzuki, M.G., Ohbayashi F., Mita, K. Shimada, T. (2001) The mechanism of sex-specific splicing at the doublesex is different between Drosophila melanogaster and Bombyx mori. Insect Biochem Mol Biol 31 : 1201 1211. (Pubitemid 33032530)
34. Suzuki, M.G., Funaguma S., Kanda, T., Tamura, T. Shimada, T. (2005) Role of the male BmDSX protein in the sexual differentiation of Bombyx mori. Evol Dev 7 : 58 68. (Pubitemid 40210833)
35. Swofford, D.L. (2002) PAUP*: phylogenetic analysis using parsimony (and other methods), version 4.0 beta. Smithsonian Institution, Washington, DC.
36. Trent, C., Crosby, C. Eavey, J. (2006) Additional evidence for the genomic imprinting model of sex determination in the haplodiploid wasp Nasonia vitripennis: isolation of biparental diploid males after X-ray mutagenesis. Heredity 96 : 368 376. (Pubitemid 43670400)
37. van Wilgenburg, E., Driessen, G. Beukeboom, L.W. (2006) Single locus complementary sex determination in Hymenoptera: an 'unintelligent' design? Front Zool 3 : 1 15. (Pubitemid 43186022)
38. Werren, J.H. Beukeboom, L. (1998) Sex determination, sex ratios and genetic conflict. Annu Rev Ecol Syst 29 : 233 261. (Pubitemid 29033032)
39. Werren, J.H. Stouthamer, R. (2002) PSR (Paternal Sex Ratio) chromosomes: The ultimate selfish genetic elements. Genetica 117 : 85 101.
40. Werren, J.H., Gadau, J., Beukeboom, L., Desplan, C., Lynch, J., Rivers, R. et al 2004) Proposal to sequence the Nasonia genome. http://www.genome.gov/ Pages/Research/Sequencing/SeqProposals/NasoniaSeq.pdf.
41. Whiting, A.R. (1967) The biology of the parasitic wasp Mormoniella vitripennis. [= Nasonia brevicornis] (Walker). Q Rev Biol 42 : 333 406.
42. Whiting, P.W. (1943) Multiple alleles in complementary sex determination of Habrobracon. Genetics 28 : 365 382.
43. Wilkins, A.S. (1995) Moving up the hierarchy. A hypothesis on the evolution of a genetic sex determination pathway. Bioessays 17 : 71 77.
44. Yang, Y., Zhang, W., Bayrer, J.R. Weiss, M.A. (2008) Doublesex and the regulation of sexual dimorphism in Drosophila melanogaster: structure, function, and mutagenesis of the female-specific domain. J Biochem Chem 283 : 7280 7292.
45. Zhu, L., Wilken, J., Phillips, N.B., Narendra, U., Chan, G., Stratton, S.M. et al 2000) Sexual dimorphism in diverse metazoans is regulated by a novel class of intertwined zinc fingers. Genes Dev 14 : 1750 1764. (Pubitemid 30602994)