Journal of Molecular Evolution

, Volume 66, Issue 4, pp 325–332 | Cite as

High Incidence of Interchromosomal Transpositions in the Evolutionary History of a Subset of Or Genes in Drosophila

Article

Abstract

In insects, the odorant receptor (Or) multigene family is an intermediate-sized family with genes present in all chromosomes, indicating that duplication followed by interchromosomal transposition played an important role in the early stages of the family evolution. Here, we have explored the occurrence of interchromosomal transpositions in more recent stages through the comparative analysis of a subset of Or genes in Drosophila, where the gene content of chromosomal arms is highly conserved. The studied subset consisted of 11 Or genes located on the left arm of chromosome 3 (Muller’s D element) in D. melanogaster. Our study focused on the number and chromosomal arm location of these members of the family across the 12 Drosophila species with complete genome sequences. In contrast to previous results from in situ hybridization comparative mapping that were mainly based on single-copy genes, our study, based on members of a multigene family of moderate size, revealed repeated interchromosomal transposition events and a complex history of some of the studied genes.

Keywords

Olfaction Olfactory receptor Genome evolution Gene transposition 

Supplementary material

239_2008_9071_MOESM1_ESM.doc (66 kb)
(DOC 67 kb)

References

  1. Ayala F (1997) Vagaries of the molecular clock. Proc Natl Acad Sci USA 94:7776–7783PubMedCrossRefGoogle Scholar
  2. Bartolomé C, Charlesworth B (2006) Rates and patterns of chromosomal evolution in Drosophila pseudoobscura and D. miranda. Genetics 173:779–791PubMedCrossRefGoogle Scholar
  3. Bergman CM, Pfeiffer BD, Rincon-Limas DE, Hoskins RA, Gnirke A, Mungall CJ, Wang AM, Kronmiller B, Pacleb J, Park S, Stapleton M, Wan K, George RA, de Jong PJ, Botas J, Rubin GM, Celniker SE (2002) Assessing the impact of comparative genomic sequence data on the functional annotation of the Drosophila genome. Genome Biol 3:research0086Google Scholar
  4. Bhutkar A, Russo SM, Smith TF, Gelbart WM (2007) Genome-scale analysis of positionally relocated genes. Genome Res 17:1880–1887PubMedCrossRefGoogle Scholar
  5. Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175–187PubMedCrossRefGoogle Scholar
  6. Burland TG (2000) DNASTAR’s Lasergene sequence analysis software. Methods Mol Biol 132:71–91PubMedGoogle Scholar
  7. Clyne PJ, Warr CG, Freeman MR, Lessing D, Kim J, Carlson JR (1999) A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22:327–338 PubMedCrossRefGoogle Scholar
  8. Coghlan A, Wolfe KH (2002) Fourfold faster rate of genome rearrangement in nematodes than in Drosophila. Genome Res 12:857–867PubMedCrossRefGoogle Scholar
  9. Crosby MA, Goodman JL, Strelets VB, Zhang P, Gelbart WM (2007) FlyBase: genomes by the dozen. Nucleic Acids Res 35:D486–D491PubMedCrossRefGoogle Scholar
  10. Do CB, Mahabhashyam MS, Brudno M, Batzoglou S (2005) ProbCons: Probabilistic consistency-based multiple sequence alignment. Genome Res 15:330–340PubMedCrossRefGoogle Scholar
  11. Drosophila 12 Genome Consortium (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450:203–218CrossRefGoogle Scholar
  12. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797PubMedCrossRefGoogle Scholar
  13. Gao Q, Chess A (1999) Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. Genomics 60:31–39PubMedCrossRefGoogle Scholar
  14. Glusman G, Yanai I, Rubin I, Lancet D (2001) The complete human olfactory subgenome. Genome Res 11:685–702PubMedCrossRefGoogle Scholar
  15. González J, Casals F, Ruiz A (2004) Duplicative and conservative transpositions of larval serum protein 1 genes in the genus Drosophila. Genetics 168:253–264PubMedCrossRefGoogle Scholar
  16. Guo S, Kim J (2007) Molecular evolution of Drosophila odorant receptor genes. Mol Biol Evol 24:1198–1207PubMedCrossRefGoogle Scholar
  17. Jones WD, Nguyen TA, Kloss B, Lee KJ, Vosshall LB (2005) Functional conservation of an insect odorant receptor gene across 250 million years of evolution. Curr Biol 15:R119–R121PubMedCrossRefGoogle Scholar
  18. Krieger J, Klink O, Mohl C, Raming K, Breer H (2003) A candidate olfactory receptor subtype highly conserved across different insect orders. J Comp Physiol A 189:519–526CrossRefGoogle Scholar
  19. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163PubMedCrossRefGoogle Scholar
  20. Labandeira CC, Sepkoski JJ Jr (1993) Insect diversity in the fossil record. Science 261:310–315PubMedCrossRefGoogle Scholar
  21. McBride CS, Arguello JR (2007) Five Drosophila genomes reveal nonneutral evolution and the signature of host specialization in the chemoreceptor superfamily. Genetics 177:1395–1416PubMedCrossRefGoogle Scholar
  22. Muller JH (1940) Bearings of the Drosophila work on systematics. In: Huxley J (ed) New systematics. Claredon Press, Oxford, pp 185–268Google Scholar
  23. Niimura Y, Nei M (2006) Evolutionary dynamics of olfactory and other chemosensory receptor genes in vertebrates. J Hum Genet 51:505–517 PubMedCrossRefGoogle Scholar
  24. Nozawa M, Nei M (2007) Evolutionary dynamics of olfactory receptor genes in Drosophila species. Proc Natl Acad Sci USA 104:7122–7127PubMedCrossRefGoogle Scholar
  25. Ramos-Onsins S, Aguadé M (1998) Molecular evolution of the Cecropin multigene family in Drosophila. Functional genes vs. pseudogenes. Genetics 150:157–171PubMedGoogle Scholar
  26. Ranz JM, Casals F, Ruiz A (2001) How malleable is the eukaryotic genome? Extreme rate of chromosomal rearrangement in the genus Drosophila. Genome Res 11:230–239PubMedCrossRefGoogle Scholar
  27. Ranz JM, González J, Casals F, Ruiz A (2003) Low occurrence of gene transposition events during the evolution of the genus Drosophila. Evol Int J Org Evol 57:1325–1335 Google Scholar
  28. Ranz JM, Maurin D, Chan YS, von Grotthuss M, Hillier LW, Roote J, Ashburner M, Bergman CM (2007) Principles of genome evolution in the Drosophila melanogaster species group. PLoS Biol 5:e152PubMedCrossRefGoogle Scholar
  29. Robertson HM, Warr CG, Carlson JR (2003) Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc Natl Acad Sci USA 100(Suppl 2):14537–14542PubMedCrossRefGoogle Scholar
  30. Russo CA, Takezaki N, Nei M (1995) Molecular phylogeny and divergence times of drosophilid species. Mol Biol Evol 12:391–404PubMedGoogle Scholar
  31. Segarra C, Aguadé M (1992) Molecular organization of the X chromosome in different species of the obscura group of Drosophila. Genetics 130:513–521PubMedGoogle Scholar
  32. Segarra C, Lozovskaya ER, Ribó G, Aguadé M, Hartl DL (1995) P1 clones from Drosophila melanogaster as markers to study the chromosomal evolution of Muller’s A element in two species of the obscura group of Drosophila. Chromosoma 104:129–136PubMedGoogle Scholar
  33. Segarra C, Ribó G, Aguadé M (1996) Differentiation of Muller’s chromosomal elements D and E in the obscura group of Drosophila. Genetics 144:139–146PubMedGoogle Scholar
  34. Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R (1999) A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96:725–736PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  1. 1.Departament de GenèticaUniversitat de BarcelonaBarcelonaSpain

Personalised recommendations