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. 1998 Sep;150(1):157–171. doi: 10.1093/genetics/150.1.157

Molecular evolution of the Cecropin multigene family in Drosophila. functional genes vs. pseudogenes.

S Ramos-Onsins 1, M Aguadé 1
PMCID: PMC1460299  PMID: 9725836

Abstract

Approximately 4 kb of the Cecropin cluster region have been sequenced in nine lines of Drosophila melanogaster and one line of the sibling species D. simulans, D. mauritiana, and D. sechellia. This region includes three functional genes (CecA1, CecA2, and CecB), which are involved in the insect immune response, and two pseudogenes (CecPsi1 and CecPsi2). The level of silent polymorphism in the three Cec genes is rather high (0.028), and there is no excess of nonsynonymous polymorphism. There is no evidence of gene conversion in the history of these genes. The interspecific comparison has revealed that in the three species of the simulans cluster the CecA2 gene is partially deleted and has therefore lost its function and become a pseudogene; in each of the species, subsequent deletions have accumulated. Divergence estimates indicate that the CecPsi1 and CecPsi2 pseudogenes are highly diverged, both between themselves and relative to the other three Cec genes. However, both CecPsi1 and CecPsi2 have conserved transcriptional signals and splice sites, and they present an open reading frame; also, correctly spliced transcripts have been detected for both CecPsi1 and CecPsi2. The data support that these genes are either active genes with some null alleles or young pseudogenes.

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Selected References

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

  1. Baeuerle P. A., Henkel T. Function and activation of NF-kappa B in the immune system. Annu Rev Immunol. 1994;12:141–179. doi: 10.1146/annurev.iy.12.040194.001041. [DOI] [PubMed] [Google Scholar]
  2. Balakirev E. S., Ayala F. J. Is esterase-P encoded by a cryptic pseudogene in Drosophila melanogaster? Genetics. 1996 Dec;144(4):1511–1518. doi: 10.1093/genetics/144.4.1511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. Bingham P. M., Levis R., Rubin G. M. Cloning of DNA sequences from the white locus of D. melanogaster by a novel and general method. Cell. 1981 Sep;25(3):693–704. doi: 10.1016/0092-8674(81)90176-8. [DOI] [PubMed] [Google Scholar]
  5. Cabot E. L., Beckenbach A. T. Simultaneous editing of multiple nucleic acid and protein sequences with ESEE. Comput Appl Biosci. 1989 Jul;5(3):233–234. doi: 10.1093/bioinformatics/5.3.233. [DOI] [PubMed] [Google Scholar]
  6. Cirera S., Aguadé M. Evolutionary history of the sex-peptide (Acp70A) gene region in Drosophila melanogaster. Genetics. 1997 Sep;147(1):189–197. doi: 10.1093/genetics/147.1.189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Clark A. G., Wang L. Molecular population genetics of Drosophila immune system genes. Genetics. 1997 Oct;147(2):713–724. doi: 10.1093/genetics/147.2.713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hey J., Kliman R. M. Population genetics and phylogenetics of DNA sequence variation at multiple loci within the Drosophila melanogaster species complex. Mol Biol Evol. 1993 Jul;10(4):804–822. doi: 10.1093/oxfordjournals.molbev.a040044. [DOI] [PubMed] [Google Scholar]
  10. Higuchi R. G., Ochman H. Production of single-stranded DNA templates by exonuclease digestion following the polymerase chain reaction. Nucleic Acids Res. 1989 Jul 25;17(14):5865–5865. doi: 10.1093/nar/17.14.5865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hudson R. R., Bailey K., Skarecky D., Kwiatowski J., Ayala F. J. Evidence for positive selection in the superoxide dismutase (Sod) region of Drosophila melanogaster. Genetics. 1994 Apr;136(4):1329–1340. doi: 10.1093/genetics/136.4.1329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hudson R. R. Estimating the recombination parameter of a finite population model without selection. Genet Res. 1987 Dec;50(3):245–250. doi: 10.1017/s0016672300023776. [DOI] [PubMed] [Google Scholar]
  13. Hudson R. R., Kaplan N. L. Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics. 1985 Sep;111(1):147–164. doi: 10.1093/genetics/111.1.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hudson R. R., Kreitman M., Aguadé M. A test of neutral molecular evolution based on nucleotide data. Genetics. 1987 May;116(1):153–159. doi: 10.1093/genetics/116.1.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hudson R. R. Properties of a neutral allele model with intragenic recombination. Theor Popul Biol. 1983 Apr;23(2):183–201. doi: 10.1016/0040-5809(83)90013-8. [DOI] [PubMed] [Google Scholar]
  16. Hughes A. L., Nei M. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature. 1988 Sep 8;335(6186):167–170. doi: 10.1038/335167a0. [DOI] [PubMed] [Google Scholar]
  17. Hultmark D. Immune reactions in Drosophila and other insects: a model for innate immunity. Trends Genet. 1993 May;9(5):178–183. doi: 10.1016/0168-9525(93)90165-e. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Kliman R. M., Hey J. DNA sequence variation at the period locus within and among species of the Drosophila melanogaster complex. Genetics. 1993 Feb;133(2):375–387. doi: 10.1093/genetics/133.2.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kliman R. M., Hey J. Reduced natural selection associated with low recombination in Drosophila melanogaster. Mol Biol Evol. 1993 Nov;10(6):1239–1258. doi: 10.1093/oxfordjournals.molbev.a040074. [DOI] [PubMed] [Google Scholar]
  21. Kumar S., Tamura K., Nei M. MEGA: Molecular Evolutionary Genetics Analysis software for microcomputers. Comput Appl Biosci. 1994 Apr;10(2):189–191. doi: 10.1093/bioinformatics/10.2.189. [DOI] [PubMed] [Google Scholar]
  22. Kylsten P., Samakovlis C., Hultmark D. The cecropin locus in Drosophila; a compact gene cluster involved in the response to infection. EMBO J. 1990 Jan;9(1):217–224. doi: 10.1002/j.1460-2075.1990.tb08098.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lewontin R. C. The detection of linkage disequilibrium in molecular sequence data. Genetics. 1995 May;140(1):377–388. doi: 10.1093/genetics/140.1.377. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. Meister M., Lemaitre B., Hoffmann J. A. Antimicrobial peptide defense in Drosophila. Bioessays. 1997 Nov;19(11):1019–1026. doi: 10.1002/bies.950191112. [DOI] [PubMed] [Google Scholar]
  27. Nei M., Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 1986 Sep;3(5):418–426. doi: 10.1093/oxfordjournals.molbev.a040410. [DOI] [PubMed] [Google Scholar]
  28. Ohta T. Further examples of evolution by gene duplication revealed through DNA sequence comparisons. Genetics. 1994 Dec;138(4):1331–1337. doi: 10.1093/genetics/138.4.1331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Petrov D. A., Lozovskaya E. R., Hartl D. L. High intrinsic rate of DNA loss in Drosophila. Nature. 1996 Nov 28;384(6607):346–349. doi: 10.1038/384346a0. [DOI] [PubMed] [Google Scholar]
  30. Pritchard J. K., Schaeffer S. W. Polymorphism and divergence at a Drosophila pseudogene locus. Genetics. 1997 Sep;147(1):199–208. doi: 10.1093/genetics/147.1.199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  32. Simon M. C. Gotta have GATA. Nat Genet. 1995 Sep;11(1):9–11. doi: 10.1038/ng0995-9. [DOI] [PubMed] [Google Scholar]
  33. Tryselius Y., Samakovlis C., Kimbrell D. A., Hultmark D. CecC, a cecropin gene expressed during metamorphosis in Drosophila pupae. Eur J Biochem. 1992 Feb 15;204(1):395–399. doi: 10.1111/j.1432-1033.1992.tb16648.x. [DOI] [PubMed] [Google Scholar]
  34. Voelker R. A., Langley C. H., Brown A. J., Ohnishi S., Dickson B., Montgomery E., Smith S. C. Enzyme null alleles in natural populations of Drosophila melanogaster: Frequencies in a North Carolina population. Proc Natl Acad Sci U S A. 1980 Feb;77(2):1091–1095. doi: 10.1073/pnas.77.2.1091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Walsh J. B. How often do duplicated genes evolve new functions? Genetics. 1995 Jan;139(1):421–428. doi: 10.1093/genetics/139.1.421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Walsh J. B. Sequence-dependent gene conversion: can duplicated genes diverge fast enough to escape conversion? Genetics. 1987 Nov;117(3):543–557. doi: 10.1093/genetics/117.3.543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. 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]
  38. von Heijne G. A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 1986 Jun 11;14(11):4683–4690. doi: 10.1093/nar/14.11.4683. [DOI] [PMC free article] [PubMed] [Google Scholar]

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