The fruitless gene in nasonia displays complex sex-specific splicing and contains new zinc finger domains

Molecular Biology and Evolution

Volumn 26, Issue 7, 2009, Pages 1557-1569

  Bertossa, Rinaldo C ^a,b   Van De Zande, Louis ^a   Beukeboom, Leo W ^a  

^a Centre for Ecological and Evolutionary Studies   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Alternative splicing; C2H2 zinc finger; Fruitless; Hymenoptera; Nasonia vitripennis; Sex determination

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FRUITLESS; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ARTICLE; BINDING SITE; FLY; GENE FUNCTION; GENE LOCUS; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HONEYBEE; HYMENOPTERA; NASONIA VITRIPENNIS; NONHUMAN; SEXUAL BEHAVIOR; SPECIES DIFFERENCE; WASP; ZINC FINGER MOTIF;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; EVOLUTION, MOLECULAR; FEMALE; INSECT PROTEINS; INSECTS; MALE; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA SPLICING; SEX CHARACTERISTICS; TRANSCRIPTION FACTORS; WASPS;

APIS MELLIFERA; DIPTERA; DROSOPHILIDAE; HEXAPODA; HYMENOPTERA; NASONIA; NASONIA VITRIPENNIS;

EID: 67649349611     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msp067     Document Type: Article

References (62)

1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol. 215:403-410.
2. Anand A, Villella A, Ryner LC, et al. (11 co-authors). 2001. Molecular genetic dissection of the sex-specific and vital functions of the Drosophila melanogaster sex determination gene fruitless. Genetics. 158:1569-1595.
3. Ausubel FM, Bensong Chanda V, Brent R, Kingston RE, Seidman JG, Struhl K, Moore DD. 2003. Current protocols in molecular biology. New York: John Wiley & Sons, Inc.
4. Baker BS, Taylor BJ, Hall JC. 2001. Are complex behaviors specified by dedicated regulatory genes? Reasoning from Drosophila. Cell. 105:13-24.
5. Bertossa RC. 2005. Evolution of behaviour: bridging the gap between evolutionary and developmental genetics. Bioessays. 27:1303-1304.
6. Beukeboom LW, Desplan C. 2003. Quick guide: Nasonia. Curr Biol. 13:R860.
7. Beukeboom LW, Kamping A, van de Zande L. 2007. Sex determination in the haplodiploid wasp Nasonia vitripennis (Hymenoptera: Chalcidoidea): a critical consideration of models and evidence. Semin Cell Dev Biol. 18:371-378.
8. Beukeboom LW, van den Assem J. 2001. Courtship and mating behaviour of interspecific Nasonia hybrids (Hymenoptera, Pteromalidae): a grandfather effect. Behav Genet. 31:167-177.
9. Beye M, Hasselmann M, Fondrk MK, Page RE Jr., Omholt SW. 2003. The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell. 114:419-429.
10. Billeter JC, Goodwin SF, O'Dell KM. 2002. Genes mediating sex-specific behaviors in Drosophila. Adv Genet. 47:87-116.
11. Billeter JC, Rideout EJ, Dornan AJ, Goodwin SF. 2006. Control of male sexual behavior in Drosophila by the sex determination pathway. Curr Biol. 16:R766-R776.
12. Billeter JC, Villella A, Allendorfer JB, Dornan AJ, Richardson M, Gailey DA, Goodwin SF. 2006. Isoformspecific control of male neuronal differentiation and behavior in Drosophila by the fruitless gene. Curr Biol. 16:1063-1076.
13. Cho S, Huang ZY, Zhang J. 2007. Sex-specific splicing of the honey bee doublesex gene reveals 300 million years of evolution at the bottom of the insect sex-determination pathway. Genetics. 177:1733-1741.
14. Crooks GE, Hon G, Chandonia JM, Brenner SE. 2004. WebLogo: a sequence logo generator. Genome Res. 14:1188-1190.
15. Davis T, Hiroki I. 2001. Genomic structure of the sexual behaviour gene fruitless. Dros Inf Ser. 84:65-66.
16. Davis T, Kurihara J, Yoshino E, Yamamoto D. 2000. Genomic organisation of the neural sex determination gene fruitless (fru) in the Hawaiian species Drosophila silvestris and the conservation of the fru BTB protein-protein-binding domain throughout evolution. Hereditas. 132:67-78.
17. Demir E, Dickson BJ. 2005. fruitless splicing specifies male courtship behavior in Drosophila. Cell. 121:785-794.
18. Dornan AJ, Gailey DA, Goodwin SF. 2005. GAL4 enhancer trap targeting of the Drosophila sex determination gene fruitless. Genesis. 42:236-246.
19. Drosophila 12 Genomes Consortium, Clark AG, Eisen MB, et al. (415 co-authors). 2007. Evolution of genes and genomes on the Drosophila phylogeny. Nature. 450:203-218.
20. Ferri SL, Bohm RA, Lincicome HE, Hall JC, Villella A. 2008. fruitless gene products truncated of their male-like qualities promote neural and behavioral maleness in Drosophila if these proteins are produced in the right places at the right times. J Neurogenet. 22:17-55.
21. Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J. 1999. Preservation of duplicate genes by complementary, degenerative mutations. Genetics. 151:1531-1545.
22. Gailey DA, Billeter JC, Liu JH, Bauzon F, Allendorfer JB, Goodwin SF. 2006. Functional conservation of the fruitless male sex-determination gene across 250 Myr of insect evolution. Mol Biol Evol. 23:633-643.
23. Goodwin SF, Taylor BJ, Villella A, Foss M, Ryner LC, Baker BS, Hall JC. 2000. Aberrant splicing and altered spatial expression patterns in fruitless mutants of Drosophila melanogaster. Genetics. 154:725-745.
24. Hedley ML, Maniatis T. 1991. Sex-specific splicing and polyadenylation of dsx pre-mRNA requires a sequence that binds specifically to tra-2 protein in vitro. Cell. 65:579-586.
25. Heinrichs V, Ryner LC, Baker BS. 1998. Regulation of sexspecific selection of fruitless 5′ splice sites by transformer and transformer-2. Mol Cell Biol. 18:450-458.
26. Holt RA, Subramanian GM, Halpern A, et al. (120 co-authors). 2002. The genome sequence of the malaria mosquito Anopheles gambiae. Science. 298:129-49.
27. Honeybee Genome Sequencing Consortium. 2006. Insights into social insects from the genome of the honeybee Apis mellifera. Nature. 443:931-949.
28. Ito H, Fujitani K, Usui K, Shimizu-Nishikawa K, Tanaka S, Yamamoto D. 1996. Sexual orientation in Drosophila is altered by the satori mutation in the sex-determination gene fruitless that encodes a zinc finger protein with a BTB domain. Proc Natl Acad Sci USA. 93:9687-9692.
29. Kamping A, Katju V, Beukeboom LW, Werren JH. 2007. Inheritance of gynandromorphism in the parasitic wasp Nasonia vitripennis. Genetics. 175:1321-1333.
30. Kopelman NM, Lancet D, Yanai I. 2005. Alternative splicing and gene duplication are inversely correlated evolutionary mechanisms. Nat Genet. 37:588-589.
31. Lee G, Foss M, Goodwin SF, Carlo T, Taylor BJ, Hall JC. 2000. Spatial, temporal, and sexually dimorphic expression patterns of the fruitless gene in the Drosophila central nervous system. J Neurobiol. 43:404-426.
32. Lee G, Hall JC. 2001. Abnormalities of male-specific FRU protein and serotonin expression in the CNS of fruitless mutants in Drosophila. J Neurosci. 21:513-526.
33. Lee G, Villella A, Taylor BJ, Hall JC. 2001. New reproductive anomalies in fruitless-mutant Drosophila males: extreme lengthening of mating durations and infertility correlated with defective serotonergic innervation of reproductive organs. J Neurobiol. 47:121-149.
34. Lynch JA, Brent AE, Leaf DS, Pultz MA, Desplan C. 2006. Localized maternal orthodenticle patterns anterior and posterior in the long germ wasp Nasonia. Nature. 439:728-732.
35. Marchler-Bauer A, Anderson JB, Derbyshire MK, et al. (25 coauthors). 2007.CDD: a conserved domain database for interactive domain family analysis. Nucleic Acids Res. 35:D237-D240.
36. Oliveira DCSG, Werren JH, Verhulst EC, Giebel JD, Kamping A, Beukeboom LW, van de Zande L. 2009. Identification and characterization of the doublesex gene of Nasonia. Insect Mol Biol. Forthcoming.
37. Posada D, Crandall KA. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics. 14:817-818.
38. Pultz MA, Leaf DS. 2003. The jewel wasp Nasonia: querying the genome with haplo-diploid genetics. Genesis. 35:185-191.
39. Ramakers C, Ruijter JM, Deprez RH, Moorman AF. 2003. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett. 339:62-66.
40. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 19:1572-1574.
41. Ryner LC, Goodwin SF, Castrillon DH, Anand A, Villella A, Baker BS, Hall JC, Taylor BJ, Wasserman SA. 1996. Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell. 87:1079-1089.
42. Salvemini M, Robertson M, Aronson B, Atkinson P, Polito LC, Saccone G. 2009. Ceratitis capitata transformer-2 gene is required to establish and maintain the autoregulation of Cctra, the master gene for female sex determination. Int J Dev Biol. 53:109-120.
43. Savard J, Tautz D, Richards S, Weinstock GM, Gibbs RA, Werren JH, Tettelin H, Lercher MJ. 2006. Phylogenomic analysis reveals bees and wasps (Hymenoptera) at the base of the radiation of Holometabolous insects. Genome Res. 16:1334-1338.
44. Solovyev V, Kosarev P, Seledsov I, Vorobyev D. 2006. Automatic annotation of eukaryotic genes, pseudogenes and promoters. Genome Biol. 7(Suppl 1:S10):11-12.
45. Song HJ, Billeter JC, Reynaud E, Carlo T, Spana EP, Perrimon N, Goodwin SF, Baker BS, Taylor BJ. 2002. The fruitless gene is required for the proper formation of axonal tracts in the embryonic central nervous system of Drosophila. Genetics. 162:1703-1724.
46. Spokony RF, Restifo LL. 2007. Anciently duplicated Broad Complex exons have distinct temporal functions during tissue morphogenesis. Dev Genes Evol. 217:499-513.
47. Stogios PJ, Downs GS, Jauhal JJ, Nandra SK, Prive GG. 2005. Sequence and structural analysis of BTB domain proteins. Genome Biol. 6:R82.
48. 2-zinc finger genes and subfamilies in mammals: speciesspecific duplication and loss of clusters, genes and effector domains. BMC Evol Biol. 8:176.
49. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol. 24:1596-1599.
50. Tribolium Genome Sequencing Consortium, Richards S, Gibbs RA, et al. (189 co-authors). 2008. The genome of the model beetle and pest Tribolium castaneum. Nature. 452:949-955.
51. Ustinova J,Mayer F. 2006. Alternative starts of transcription, several paralogues, and almost-fixed interspecific differences of the gene fruitless in a hemimetabolous insect. J Mol Evol. 63:788-800.
52. Usui-Aoki K, Ito H, Ui-Tei K, et al. (11 co-authors). 2000. Formation of the male-specific muscle in female Drosophila by ectopic fruitless expression. Nat Cell Biol. 2:500-506.
53. van den Assem J, Jachmann F. 1999. Changes in male perseverance in courtship and female readiness to mate in a strain of the parasitic wasp Nasonia vitripennis over a period of 20 years. Neth J Zool. 49:125-137.
54. van den Assem J, Werren JH. 1994. A comparison of the courtship and mating-behavior of three species of Nasonia (Hymenoptera, Pteromalidae). J Insect Behav. 7:53-66.
55. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3:RESEARCH0034. 1-0034.12.
56. Villella A, Gailey DA, Berwald B, Ohshima S, Barnes PT, Hall JC. 1997. Extended reproductive roles of the fruitless gene in Drosophila melanogaster revealed by behavioral analysis of new fru mutants. Genetics. 147: 1107-1130.
57. Vrontou E, Nilsen SP, Demir E, Kravitz EA, Dickson BJ. 2006. fruitless regulates aggression and dominance in Drosophila. Nat Neurosci. 9:1469-1471.
58. Wilgenbusch JC, Swofford D. 2003. Inferring evolutionary trees with PAUP*. Curr Protoc Bioinformatics. Chapter 6:Unit 6 4.
59. Wilkins AS. 1995. Moving up the hierarchy: a hypothesis on the evolution of a genetic sex determination pathway. Bioessays. 17:71-77.
60. Xia Q, Zhou Z, Lu C, et al. (80 co-authors). 2004. A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science. 306:1937-1940.
61. Yamamoto D. 2007. The neural and genetic substrates of sexual behavior in Drosophila. Adv Genet. 59:39-66.
62. Yu JY, Dickson BJ. 2006. Sexual behaviour: do a few dead neurons make the difference? Curr Biol. 16:R23-R25.