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Genetics. Nov 2003; 165(3): 1279–1288.
PMCID: PMC1462860

Patterns of nucleotide polymorphism and divergence in the odorant-binding protein genes OS-E and OS-F: analysis in the melanogaster species subgroup of Drosophila.

Abstract

The Olfactory Specific-E and -F genes (OS-E and OS-F) belong to the odorant-binding protein gene family, which includes the general odorant-binding proteins and the pheromone-binding proteins. In Drosophila melanogaster, these genes are arranged in tandem in a genomic region near the centromere of chromosome arm 3R. We examined the pattern of DNA sequence variation in an approximately 7-kb genomic region encompassing the two OS genes in four species of the melanogaster subgroup of Drosophila and in a population sample of D. melanogaster. We found that both the OS-E and the OS-F gene are present in all surveyed species. Nucleotide divergence estimates would support that the two genes are functional, although they diverge in their functional constraint. The pattern of nucleotide variation in D. melanogaster also differed between genes. Variation in the OS-E gene region exhibited an unusual and distinctive pattern: (i) a relatively high number of fixed amino acid replacements in the encoded protein and (ii) a peak of nucleotide polymorphism around the OS-E gene. These results are unlikely under the neutral model and suggest the action of natural selection in the evolution of the two odorant-binding protein genes.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Andolfatto P, Przeworski M. A genome-wide departure from the standard neutral model in natural populations of Drosophila. Genetics. 2000 Sep;156(1):257–268. [PMC free article] [PubMed]
  • Begun DJ, Aquadro CF. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature. 1992 Apr 9;356(6369):519–520. [PubMed]
  • Bingham PM, Levis R, Rubin GM. Cloning of DNA sequences from the white locus of D. melanogaster by a novel and general method. Cell. 1981 Sep;25(3):693–704. [PubMed]
  • Buck L, Axel R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell. 1991 Apr 5;65(1):175–187. [PubMed]
  • Campanacci V, Longhi S, Nagnan-Le Meillour P, Cambillau C, Tegoni M. Recombinant pheromone binding protein 1 from Mamestra brassicae (MbraPBP1). Functional and structural characterization. Eur J Biochem. 1999 Sep;264(3):707–716. [PubMed]
  • Charlesworth B, Morgan MT, Charlesworth D. The effect of deleterious mutations on neutral molecular variation. Genetics. 1993 Aug;134(4):1289–1303. [PMC free article] [PubMed]
  • Cirera S, Aguadé M. Evolutionary history of the sex-peptide (Acp70A) gene region in Drosophila melanogaster. Genetics. 1997 Sep;147(1):189–197. [PMC free article] [PubMed]
  • Comeron JM, Kreitman M, Aguadé M. Natural selection on synonymous sites is correlated with gene length and recombination in Drosophila. Genetics. 1999 Jan;151(1):239–249. [PMC free article] [PubMed]
  • Danty E, Briand L, Michard-Vanhée C, Perez V, Arnold G, Gaudemer O, Huet D, Huet JC, Ouali C, Masson C, et al. Cloning and expression of a queen pheromone-binding protein in the honeybee: an olfactory-specific, developmentally regulated protein. J Neurosci. 1999 Sep 1;19(17):7468–7475. [PubMed]
  • Pelosi P, Maida R. Odorant-binding proteins in insects. Comp Biochem Physiol B Biochem Mol Biol. 1995 Jul;111(3):503–514. [PubMed]
  • Peng G, Leal WS. Identification and cloning of a pheromone-binding protein from the Oriental beetle, Exomala orientalis. J Chem Ecol. 2001 Nov;27(11):2183–2192. [PubMed]
  • Pikielny CW, Hasan G, Rouyer F, Rosbash M. Members of a family of Drosophila putative odorant-binding proteins are expressed in different subsets of olfactory hairs. Neuron. 1994 Jan;12(1):35–49. [PubMed]
  • Galindo K, Smith DP. A large family of divergent Drosophila odorant-binding proteins expressed in gustatory and olfactory sensilla. Genetics. 2001 Nov;159(3):1059–1072. [PMC free article] [PubMed]
  • Plettner E, Lazar J, Prestwich EG, Prestwich GD. Discrimination of pheromone enantiomers by two pheromone binding proteins from the gypsy moth Lymantria dispar. Biochemistry. 2000 Aug 1;39(30):8953–8962. [PubMed]
  • 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. [PubMed]
  • Ramos-Onsins S, Aguadé M. Molecular evolution of the Cecropin multigene family in Drosophila. functional genes vs. pseudogenes. Genetics. 1998 Sep;150(1):157–171. [PMC free article] [PubMed]
  • Hekmat-Scafe DS, Dorit RL, Carlson JR. Molecular evolution of odorant-binding protein genes OS-E and OS-F in Drosophila. Genetics. 2000 May;155(1):117–127. [PMC free article] [PubMed]
  • Rost B. Review: protein secondary structure prediction continues to rise. J Struct Biol. 2001 May-Jun;134(2-3):204–218. [PubMed]
  • Rozas J, Gullaud M, Blandin G, Aguadé M. DNA variation at the rp49 gene region of Drosophila simulans: evolutionary inferences from an unusual haplotype structure. Genetics. 2001 Jul;158(3):1147–1155. [PMC free article] [PubMed]
  • Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KB, Erlich HA. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. [PubMed]
  • Minutes of meeting of the Human Gene Therapy Subcommittee, 30 Mar 1990. Hum Gene Ther. 1990 Winter;1(4):481–491. [PubMed]
  • Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. [PubMed]
  • Hudson RR, Kaplan NL. Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics. 1985 Sep;111(1):147–164. [PMC free article] [PubMed]
  • Sandler BH, Nikonova L, Leal WS, Clardy J. Sexual attraction in the silkworm moth: structure of the pheromone-binding-protein-bombykol complex. Chem Biol. 2000 Feb;7(2):143–151. [PubMed]
  • Hudson RR, Kreitman M, Aguadé M. A test of neutral molecular evolution based on nucleotide data. Genetics. 1987 May;116(1):153–159. [PMC free article] [PubMed]
  • Scaloni A, Monti M, Angeli S, Pelosi P. Structural analysis and disulfide-bridge pairing of two odorant-binding proteins from Bombyx mori. Biochem Biophys Res Commun. 1999 Dec 20;266(2):386–391. [PubMed]
  • Kelly JK. A test of neutrality based on interlocus associations. Genetics. 1997 Jul;146(3):1197–1206. [PMC free article] [PubMed]
  • Steinbrecht RA. Are odorant-binding proteins involved in odorant discrimination? Chem Senses. 1996 Dec;21(6):719–727. [PubMed]
  • Kirby DA, Stephan W. Multi-locus selection and the structure of variation at the white gene of Drosophila melanogaster. Genetics. 1996 Oct;144(2):635–645. [PMC free article] [PubMed]
  • Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989 Nov;123(3):585–595. [PMC free article] [PubMed]
  • Kreitman M, Aguadé M. Genetic uniformity in two populations of Drosophila melanogaster as revealed by filter hybridization of four-nucleotide-recognizing restriction enzyme digests. Proc Natl Acad Sci U S A. 1986 May;83(10):3562–3566. [PMC free article] [PubMed]
  • Vogt RG, Riddiford LM. Pheromone binding and inactivation by moth antennae. Nature. 1981 Sep 10;293(5828):161–163. [PubMed]
  • Vogt Richard G, Rogers Matthew E, Franco Marie-dominique, Sun Ming. A comparative study of odorant binding protein genes: differential expression of the PBP1-GOBP2 gene cluster in Manduca sexta (Lepidoptera) and the organization of OBP genes in Drosophila melanogaster (Diptera). J Exp Biol. 2002 Mar;205(Pt 6):719–744. [PubMed]
  • Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R. A spatial map of olfactory receptor expression in the Drosophila antenna. Cell. 1999 Mar 5;96(5):725–736. [PubMed]
  • McDonald JH. Improved tests for heterogeneity across a region of DNA sequence in the ratio of polymorphism to divergence. Mol Biol Evol. 1998 Apr;15(4):377–384. [PubMed]
  • Vosshall LB, Wong AM, Axel R. An olfactory sensory map in the fly brain. Cell. 2000 Jul 21;102(2):147–159. [PubMed]
  • McKenna MP, Hekmat-Scafe DS, Gaines P, Carlson JR. Putative Drosophila pheromone-binding proteins expressed in a subregion of the olfactory system. J Biol Chem. 1994 Jun 10;269(23):16340–16347. [PubMed]
  • Watterson GA. On the number of segregating sites in genetical models without recombination. Theor Popul Biol. 1975 Apr;7(2):256–276. [PubMed]
  • Moriyama EN, Powell JR. Intraspecific nuclear DNA variation in Drosophila. Mol Biol Evol. 1996 Jan;13(1):261–277. [PubMed]
  • Willett CS. Evidence for directional selection acting on pheromone-binding proteins in the genus Choristoneura. Mol Biol Evol. 2000 Apr;17(4):553–562. [PubMed]
  • Yang Z. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci. 1997 Oct;13(5):555–556. [PubMed]
  • Yang Z, Kumar S, Nei M. A new method of inference of ancestral nucleotide and amino acid sequences. Genetics. 1995 Dec;141(4):1641–1650. [PMC free article] [PubMed]
  • Wu CI, Li WH. Evidence for higher rates of nucleotide substitution in rodents than in man. Proc Natl Acad Sci U S A. 1985 Mar;82(6):1741–1745. [PMC free article] [PubMed]

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