Skip to main content
PMC home page
Genetics logoLink to Genetics
. 2003 Jul;164(3):977–988. doi: 10.1093/genetics/164.3.977

Dntf-2r, a young Drosophila retroposed gene with specific male expression under positive Darwinian selection.

Esther Betrán 1, Manyuan Long 1
PMCID: PMC1462638  PMID: 12871908

Abstract

A direct approach to investigating new gene origination is to examine recently evolved genes. We report a new gene in the Drosophila melanogaster subgroup, Drosophila nuclear transport factor-2-related (Dntf-2r). Its sequence features and phylogenetic distribution indicate that Dntf-2r is a retroposed functional gene and originated in the common ancestor of D. melanogaster, D. simulans, D. sechellia, and D. mauritiana, within the past 3-12 million years (MY). Dntf-2r evolved more rapidly than the parental gene, under positive Darwinian selection as revealed by the McDonald-Kreitman test and other evolutionary analyses. Comparative expression analysis shows that Dntf-2r is male specific whereas the parental gene, Dntf-2, is widely expressed in D. melanogaster. In agreement with its new expression pattern, the Dntf-2r putative promoter sequence is similar to the late testis promoter of beta2-tubulin. We discuss the possibility that the action of positive selection in Dntf-2r is related to its putative male-specific functions.

Full Text

The Full Text of this article is available as a PDF (358.2 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aguadé M. Positive selection drives the evolution of the Acp29AB accessory gland protein in Drosophila. Genetics. 1999 Jun;152(2):543–551. doi: 10.1093/genetics/152.2.543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Arabidopsis Genome Initiative Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature. 2000 Dec 14;408(6814):796–815. doi: 10.1038/35048692. [DOI] [PubMed] [Google Scholar]
  3. Ball C. A., Cherry J. M. Genome comparisons highlight similarity and diversity within the eukaryotic kingdoms. Curr Opin Chem Biol. 2001 Feb;5(1):86–89. doi: 10.1016/s1367-5931(00)00172-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Begun D. J. Origin and evolution of a new gene descended from alcohol dehydrogenase in Drosophila. Genetics. 1997 Feb;145(2):375–382. doi: 10.1093/genetics/145.2.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Betrán Esther, Long Manyuan. Expansion of genome coding regions by acquisition of new genes. Genetica. 2002 May;115(1):65–80. doi: 10.1023/a:1016024131097. [DOI] [PubMed] [Google Scholar]
  6. Betrán Esther, Thornton Kevin, Long Manyuan. Retroposed new genes out of the X in Drosophila. Genome Res. 2002 Dec;12(12):1854–1859. doi: 10.1101/gr.604902. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bhattacharya Ananya, Steward Ruth. The Drosophila homolog of NTF-2, the nuclear transport factor-2, is essential for immune response. EMBO Rep. 2002 Apr;3(4):378–383. doi: 10.1093/embo-reports/kvf072. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Blanc G., Barakat A., Guyot R., Cooke R., Delseny M. Extensive duplication and reshuffling in the Arabidopsis genome. Plant Cell. 2000 Jul;12(7):1093–1101. doi: 10.1105/tpc.12.7.1093. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Davidson M. H., Stein E. A., Hunninghake D. B., Ose L., Dujovne C. A., Insull W., Jr, Bertolami M., Weiss S. R., Kastelein J. J., Scott R. S. Lipid-altering efficacy and safety of simvastatin 80 mg/day: worldwide long-term experience in patients with hypercholesterolemia. Nutr Metab Cardiovasc Dis. 2000 Oct;10(5):253–262. [PubMed] [Google Scholar]
  10. Fay J. C., Wu C. I. Hitchhiking under positive Darwinian selection. Genetics. 2000 Jul;155(3):1405–1413. doi: 10.1093/genetics/155.3.1405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Goldman N., Yang Z. A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol. 1994 Sep;11(5):725–736. doi: 10.1093/oxfordjournals.molbev.a040153. [DOI] [PubMed] [Google Scholar]
  12. Jeffs P., Ashburner M. Processed pseudogenes in Drosophila. Proc Biol Sci. 1991 May 22;244(1310):151–159. doi: 10.1098/rspb.1991.0064. [DOI] [PubMed] [Google Scholar]
  13. Lemeunier F., Ashburner M. A. Relationships within the melanogaster species subgroup of the genus Drosophila (Sophophora). II. Phylogenetic relationships between six species based upon polytene chromosome banding sequences. Proc R Soc Lond B Biol Sci. 1976 May 18;193(1112):275–294. doi: 10.1098/rspb.1976.0046. [DOI] [PubMed] [Google Scholar]
  14. Li W. H., Gu Z., Wang H., Nekrutenko A. Evolutionary analyses of the human genome. Nature. 2001 Feb 15;409(6822):847–849. doi: 10.1038/35057039. [DOI] [PubMed] [Google Scholar]
  15. Llopart Ana, Comeron Josep M., Brunet Frédéric G., Lachaise Daniel, Long Manyuan. Intron presence-absence polymorphism in Drosophila driven by positive Darwinian selection. Proc Natl Acad Sci U S A. 2002 Jun 11;99(12):8121–8126. doi: 10.1073/pnas.122570299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Long M. Evolution of novel genes. Curr Opin Genet Dev. 2001 Dec;11(6):673–680. doi: 10.1016/s0959-437x(00)00252-5. [DOI] [PubMed] [Google Scholar]
  17. Long M., Langley C. H. Natural selection and the origin of jingwei, a chimeric processed functional gene in Drosophila. Science. 1993 Apr 2;260(5104):91–95. doi: 10.1126/science.7682012. [DOI] [PubMed] [Google Scholar]
  18. McDonald J. H., Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 1991 Jun 20;351(6328):652–654. doi: 10.1038/351652a0. [DOI] [PubMed] [Google Scholar]
  19. Metz E. C., Palumbi S. R. Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin. Mol Biol Evol. 1996 Feb;13(2):397–406. doi: 10.1093/oxfordjournals.molbev.a025598. [DOI] [PubMed] [Google Scholar]
  20. Michiels F., Gasch A., Kaltschmidt B., Renkawitz-Pohl R. A 14 bp promoter element directs the testis specificity of the Drosophila beta 2 tubulin gene. EMBO J. 1989 May;8(5):1559–1565. doi: 10.1002/j.1460-2075.1989.tb03540.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nurminsky D. I., Nurminskaya M. V., De Aguiar D., Hartl D. L. Selective sweep of a newly evolved sperm-specific gene in Drosophila. Nature. 1998 Dec 10;396(6711):572–575. doi: 10.1038/25126. [DOI] [PubMed] [Google Scholar]
  22. Nurminsky D., Aguiar D. D., Bustamante C. D., Hartl D. L. Chromosomal effects of rapid gene evolution in Drosophila melanogaster. Science. 2001 Jan 5;291(5501):128–130. doi: 10.1126/science.291.5501.128. [DOI] [PubMed] [Google Scholar]
  23. Otto S. P. Detecting the form of selection from DNA sequence data. Trends Genet. 2000 Dec;16(12):526–529. doi: 10.1016/s0168-9525(00)02141-7. [DOI] [PubMed] [Google Scholar]
  24. Rozas J., Rozas R. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics. 1999 Feb;15(2):174–175. doi: 10.1093/bioinformatics/15.2.174. [DOI] [PubMed] [Google Scholar]
  25. Rubin G. M., Yandell M. D., Wortman J. R., Gabor Miklos G. L., Nelson C. R., Hariharan I. K., Fortini M. E., Li P. W., Apweiler R., Fleischmann W. Comparative genomics of the eukaryotes. Science. 2000 Mar 24;287(5461):2204–2215. doi: 10.1126/science.287.5461.2204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Simonsen K. L., Churchill G. A., Aquadro C. F. Properties of statistical tests of neutrality for DNA polymorphism data. Genetics. 1995 Sep;141(1):413–429. doi: 10.1093/genetics/141.1.413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Swanson W. J., Aquadro C. F., Vacquier V. D. Polymorphism in abalone fertilization proteins is consistent with the neutral evolution of the egg's receptor for lysin (VERL) and positive darwinian selection of sperm lysin. Mol Biol Evol. 2001 Mar;18(3):376–383. doi: 10.1093/oxfordjournals.molbev.a003813. [DOI] [PubMed] [Google Scholar]
  28. Swanson W. J., Clark A. G., Waldrip-Dail H. M., Wolfner M. F., Aquadro C. F. Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila. Proc Natl Acad Sci U S A. 2001 Jun 12;98(13):7375–7379. doi: 10.1073/pnas.131568198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Thompson J. D., Higgins D. G., Gibson T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994 Nov 11;22(22):4673–4680. doi: 10.1093/nar/22.22.4673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Ting C. T., Tsaur S. C., Wu C. I. The phylogeny of closely related species as revealed by the genealogy of a speciation gene, Odysseus. Proc Natl Acad Sci U S A. 2000 May 9;97(10):5313–5316. doi: 10.1073/pnas.090541597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Ting C. T., Tsaur S. C., Wu M. L., Wu C. I. A rapidly evolving homeobox at the site of a hybrid sterility gene. Science. 1998 Nov 20;282(5393):1501–1504. doi: 10.1126/science.282.5393.1501. [DOI] [PubMed] [Google Scholar]
  32. Tsaur S. C., Ting C. T., Wu C. I. Positive selection driving the evolution of a gene of male reproduction, Acp26Aa, of Drosophila: II. Divergence versus polymorphism. Mol Biol Evol. 1998 Aug;15(8):1040–1046. doi: 10.1093/oxfordjournals.molbev.a026002. [DOI] [PubMed] [Google Scholar]
  33. Wang W., Zhang J., Alvarez C., Llopart A., Long M. The origin of the Jingwei gene and the complex modular structure of its parental gene, yellow emperor, in Drosophila melanogaster. Mol Biol Evol. 2000 Sep;17(9):1294–1301. doi: 10.1093/oxfordjournals.molbev.a026413. [DOI] [PubMed] [Google Scholar]
  34. Watterson G. A. On the number of segregating sites in genetical models without recombination. Theor Popul Biol. 1975 Apr;7(2):256–276. doi: 10.1016/0040-5809(75)90020-9. [DOI] [PubMed] [Google Scholar]
  35. Wyckoff G. J., Wang W., Wu C. I. Rapid evolution of male reproductive genes in the descent of man. Nature. 2000 Jan 20;403(6767):304–309. doi: 10.1038/35002070. [DOI] [PubMed] [Google Scholar]
  36. Yang Z. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol. 1998 May;15(5):568–573. doi: 10.1093/oxfordjournals.molbev.a025957. [DOI] [PubMed] [Google Scholar]
  37. Yang Z. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci. 1997 Oct;13(5):555–556. doi: 10.1093/bioinformatics/13.5.555. [DOI] [PubMed] [Google Scholar]
  38. Yi S., Charlesworth B. A selective sweep associated with a recent gene transposition in Drosophila miranda. Genetics. 2000 Dec;156(4):1753–1763. doi: 10.1093/genetics/156.4.1753. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES