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. 1996 Dec;144(4):1511–1518. doi: 10.1093/genetics/144.4.1511

Is Esterase-P Encoded by a Cryptic Pseudogene in Drosophila Melanogaster?

E S Balakirev 1, F J Ayala 1
PMCID: PMC1207704  PMID: 8978040

Abstract

We have amplified and sequenced the gene encoding Esterase-P (Est-P) in 10 strains of Drosophila melanogaster. Three premature termination codons occur in the coding region of the gene in two strains. This observation, together with other indirect evidence, leads us to propose that Est-P may be a pseudogene in D. melanogaster. Est-P would be a ``cryptic'' pseudogene, in the sense that it retains intact the coding sequence (without stop codons and other alterations usually observed in pseudogenes) in most D. melanogaster strains. We conjecture that the β-esterase cluster may consist in other Drosophila species of functional and nonfunctional genes. We also conjecture that the rarity of detected pseudogenes in Drosophila may be due to the difficulty of discovering them, because most of them are cryptic.

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Selected References

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  1. Aronshtam A. A., Kuzin B. A. Stanovlenie polovogo dimorfizma po vyrazheniiu gena Est-6 v ontogeneze Drosophila melanogaster i Drosophila simulans. Zh Obshch Biol. 1974 Nov-Dec;35(6):926–933. [PubMed] [Google Scholar]
  2. Atkinson P. W., Mills L. E., Starmer W. T., Sullivan D. T. Structure and evolution of the Adh genes of Drosophila mojavensis. Genetics. 1988 Nov;120(3):713–723. doi: 10.1093/genetics/120.3.713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Aubert D., Bisanz-Seyer C., Herzog M. Mitochondrial rps14 is a transcribed and edited pseudogene in Arabidopsis thaliana. Plant Mol Biol. 1992 Dec;20(6):1169–1174. doi: 10.1007/BF00028903. [DOI] [PubMed] [Google Scholar]
  4. Brady J. P., Richmond R. C., Oakeshott J. G. Cloning of the esterase-5 locus from Drosophila pseudoobscura and comparison with its homologue in D. melanogaster. Mol Biol Evol. 1990 Nov;7(6):525–546. doi: 10.1093/oxfordjournals.molbev.a040624. [DOI] [PubMed] [Google Scholar]
  5. Carter P., Wells J. A. Dissecting the catalytic triad of a serine protease. Nature. 1988 Apr 7;332(6164):564–568. doi: 10.1038/332564a0. [DOI] [PubMed] [Google Scholar]
  6. Collet C., Nielsen K. M., Russell R. J., Karl M., Oakeshott J. G., Richmond R. C. Molecular analysis of duplicated esterase genes in Drosophila melanogaster. Mol Biol Evol. 1990 Jan;7(1):9–28. doi: 10.1093/oxfordjournals.molbev.a040582. [DOI] [PubMed] [Google Scholar]
  7. Currie P. D., Sullivan D. T. Structure, expression and duplication of genes which encode phosphoglyceromutase of Drosophila melanogaster. Genetics. 1994 Oct;138(2):352–363. [PMC free article] [PubMed] [Google Scholar]
  8. Enikolopov G. N., Malevanchuk O. A., Peunova N. I., Sergeev P. V., Georgiev G. P. Lokus est Drosophila virilis soderzhit dva rodstvennykh gena. Dokl Akad Nauk SSSR. 1989;306(5):1247–1249. [PubMed] [Google Scholar]
  9. Fedoroff N. V., Brown D. D. The nucleotide sequence of the repeating unit in the oocyte 5S ribosomal DNA of Xenopus laevis. Cold Spring Harb Symp Quant Biol. 1978;42(Pt 2):1195–1200. doi: 10.1101/sqb.1978.042.01.120. [DOI] [PubMed] [Google Scholar]
  10. Fischer J. A., Maniatis T. Structure and transcription of the Drosophila mulleri alcohol dehydrogenase genes. Nucleic Acids Res. 1985 Oct 11;13(19):6899–6917. doi: 10.1093/nar/13.19.6899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fürbass R., Vanselow J. An aromatase pseudogene is transcribed in the bovine placenta. Gene. 1995 Mar 10;154(2):287–291. doi: 10.1016/0378-1119(94)00754-g. [DOI] [PubMed] [Google Scholar]
  12. Georgiev P., Yelagin V. Super-unstable mutations associated with P-M hybrid dysgenesis in Drosophila melanogaster. Genetica. 1992;87(1):17–29. doi: 10.1007/BF00128769. [DOI] [PubMed] [Google Scholar]
  13. Healy M. J., Dumancic M. M., Oakeshott J. G. Biochemical and physiological studies of soluble esterases from Drosophila melanogaster. Biochem Genet. 1991 Aug;29(7-8):365–388. doi: 10.1007/BF00554144. [DOI] [PubMed] [Google Scholar]
  14. Hickey D. A., Bally-Cuif L., Abukashawa S., Payant V., Benkel B. F. Concerted evolution of duplicated protein-coding genes in Drosophila. Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1611–1615. doi: 10.1073/pnas.88.5.1611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Jacq C., Miller J. R., Brownlee G. G. A pseudogene structure in 5S DNA of Xenopus laevis. Cell. 1977 Sep;12(1):109–120. doi: 10.1016/0092-8674(77)90189-1. [DOI] [PubMed] [Google Scholar]
  17. Jeffs P. S., Holmes E. C., Ashburner M. The molecular evolution of the alcohol dehydrogenase and alcohol dehydrogenase-related genes in the Drosophila melanogaster species subgroup. Mol Biol Evol. 1994 Mar;11(2):287–304. doi: 10.1093/oxfordjournals.molbev.a040110. [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. Korochkin L. I., Aronshtam A. A., Matveeva N. M. Genetics of esterases in Drosophila. III. Influence of different chromosomes on esterase pattern in Drosophila. Biochem Genet. 1974 Jul;12(1):9–24. doi: 10.1007/BF00487524. [DOI] [PubMed] [Google Scholar]
  20. Korochkin L., Ludwig M., Tamarina N., Uspensky I., Yenikolopov G., Khechumijan R., Kopantseva M., Evgeniev M., Kuzin B., Bakayeva T. Molecular genetic mechanisms of tissue-specific esterase isozymes and protein expression in Drosophila. Prog Clin Biol Res. 1990;344:399–440. [PubMed] [Google Scholar]
  21. Kwiatowski J., Skarecky D., Bailey K., Ayala F. J. Phylogeny of Drosophila and related genera inferred from the nucleotide sequence of the Cu,Zn Sod gene. J Mol Evol. 1994 May;38(5):443–454. doi: 10.1007/BF00178844. [DOI] [PubMed] [Google Scholar]
  22. Kwiatowski J., Skarecky D., Hernandez S., Pham D., Quijas F., Ayala F. J. High fidelity of the polymerase chain reaction. Mol Biol Evol. 1991 Nov;8(6):884–887. doi: 10.1093/oxfordjournals.molbev.a040693. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Langley C. H., Voelker R. A., Brown A. J., Ohnishi S., Dickson B., Montgomery E. Null allele frequencies at allozyme loci in natural populations of Drosophila melanogaster. Genetics. 1981 Sep;99(1):151–156. doi: 10.1093/genetics/99.1.151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Li W. H., Gojobori T., Nei M. Pseudogenes as a paradigm of neutral evolution. Nature. 1981 Jul 16;292(5820):237–239. doi: 10.1038/292237a0. [DOI] [PubMed] [Google Scholar]
  26. Li W. H. Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J Mol Evol. 1993 Jan;36(1):96–99. doi: 10.1007/BF02407308. [DOI] [PubMed] [Google Scholar]
  27. Li W. H., Wu C. I., Luo C. C. A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes. Mol Biol Evol. 1985 Mar;2(2):150–174. doi: 10.1093/oxfordjournals.molbev.a040343. [DOI] [PubMed] [Google Scholar]
  28. Ludwig M. Z., Tamarina N. A., Richmond R. C. Localization of sequences controlling the spatial, temporal, and sex-specific expression of the esterase 6 locus in Drosophila melanogaster adults. Proc Natl Acad Sci U S A. 1993 Jul 1;90(13):6233–6237. doi: 10.1073/pnas.90.13.6233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Mane S. D., Tepper C. S., Richmond R. C. Studies of esterase 6 in Drosophila melanogaster. XIII. Purification and characterization of the two major isozymes. Biochem Genet. 1983 Oct;21(9-10):1019–1040. doi: 10.1007/BF00483957. [DOI] [PubMed] [Google Scholar]
  30. Matters G. L., Goodenough U. W. A gene/pseudogene tandem duplication encodes a cysteine-rich protein expressed during zygote development in Chlamydomonas reinhardtii. Mol Gen Genet. 1992 Mar;232(1):81–88. doi: 10.1007/BF00299140. [DOI] [PubMed] [Google Scholar]
  31. McCarrey J. R., Thomas K. Human testis-specific PGK gene lacks introns and possesses characteristics of a processed gene. Nature. 1987 Apr 2;326(6112):501–505. doi: 10.1038/326501a0. [DOI] [PubMed] [Google Scholar]
  32. Menotti-Raymond M., Starmer W. T., Sullivan D. T. Characterization of the structure and evolution of the Adh region of Drosophila hydei. Genetics. 1991 Feb;127(2):355–366. doi: 10.1093/genetics/127.2.355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Miyata T., Hayashida H. Extraordinarily high evolutionary rate of pseudogenes: evidence for the presence of selective pressure against changes between synonymous codons. Proc Natl Acad Sci U S A. 1981 Sep;78(9):5739–5743. doi: 10.1073/pnas.78.9.5739. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Modiano G., Battistuzzi G., Motulsky A. G. Nonrandom patterns of codon usage and of nucleotide substitutions in human alpha- and beta-globin genes: an evolutionary strategy reducing the rate of mutations with drastic effects? Proc Natl Acad Sci U S A. 1981 Feb;78(2):1110–1114. doi: 10.1073/pnas.78.2.1110. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Myers M., Richmond R. C., Oakeshott J. G. On the origins of esterases. Mol Biol Evol. 1988 Mar;5(2):113–119. doi: 10.1093/oxfordjournals.molbev.a040485. [DOI] [PubMed] [Google Scholar]
  36. Oakeshott J. G., Cooke P. H., Richmond R. C., Bortoli A., Game A. Y., Labate J. Molecular population genetics of structural variants of esterase 6 in Drosophila melanogaster. Genome. 1989;31(2):788–796. doi: 10.1139/g89-139. [DOI] [PubMed] [Google Scholar]
  37. Ohta T. Some models of gene conversion for treating the evolution of multigene families. Genetics. 1984 Mar;106(3):517–528. doi: 10.1093/genetics/106.3.517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Procunier W. S., Smith J. J., Richmond R. C. Physical mapping of the Esterase-6 locus of Drosophila melanogaster. Genetica. 1991;84(3):203–208. doi: 10.1007/BF00127248. [DOI] [PubMed] [Google Scholar]
  39. Prudhommeau C., Proust J. I-R hybrid dysgenesis in Drosophila melanogaster: nature and site specificity of induced recessive lethals. Mutat Res. 1990 Jun;230(2):135–157. doi: 10.1016/0027-5107(90)90052-6. [DOI] [PubMed] [Google Scholar]
  40. Richmond R. C., Gilbert D. G., Sheehan K. B., Gromko M. H., Butterworth F. M. Esterase 6 and reproduction in Drosophila melanogaster. Science. 1980 Mar 28;207(4438):1483–1485. doi: 10.1126/science.6767273. [DOI] [PubMed] [Google Scholar]
  41. Saad M., Game A. Y., Healy M. J., Oakeshott J. G. Associations of esterase 6 allozyme and activity variation with reproductive fitness in Drosophila melanogaster. Genetica. 1994;94(1):43–56. doi: 10.1007/BF01429219. [DOI] [PubMed] [Google Scholar]
  42. 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]
  43. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Satta Y. How the ratio of nonsynonymous to synonymous pseudogene substitutions can be less than one. Immunogenetics. 1993;38(6):450–454. doi: 10.1007/BF00184527. [DOI] [PubMed] [Google Scholar]
  45. Schrag J. D., Li Y. G., Wu S., Cygler M. Ser-His-Glu triad forms the catalytic site of the lipase from Geotrichum candidum. Nature. 1991 Jun 27;351(6329):761–764. doi: 10.1038/351761a0. [DOI] [PubMed] [Google Scholar]
  46. Seager R. D., Ayala F. J. Chromosome interactions in Drosophila melanogaster. I. Viability studies. Genetics. 1982 Nov;102(3):467–483. doi: 10.1093/genetics/102.3.467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Sibbald P. R., Blencowe B. J. A completely conserved rat U6 snRNA pseudogene coding sequence is sandwiched between a cytochrome c retropseudogene and a LINE-like sequence. Nucleic Acids Res. 1990 Feb 25;18(4):1063–1063. doi: 10.1093/nar/18.4.1063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Sorge J., Gross E., West C., Beutler E. High level transcription of the glucocerebrosidase pseudogene in normal subjects and patients with Gaucher disease. J Clin Invest. 1990 Oct;86(4):1137–1141. doi: 10.1172/JCI114818. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Sullivan D. T., Starmer W. T., Curtiss S. W., Menotti-Raymond M., Yum J. Unusual molecular evolution of an Adh pseudogene in Drosophila. Mol Biol Evol. 1994 May;11(3):443–458. doi: 10.1093/oxfordjournals.molbev.a040125. [DOI] [PubMed] [Google Scholar]
  50. 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]
  51. Vanin E. F. Processed pseudogenes: characteristics and evolution. Annu Rev Genet. 1985;19:253–272. doi: 10.1146/annurev.ge.19.120185.001345. [DOI] [PubMed] [Google Scholar]
  52. 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]
  53. Weiner A. M., Deininger P. L., Efstratiadis A. Nonviral retroposons: genes, pseudogenes, and transposable elements generated by the reverse flow of genetic information. Annu Rev Biochem. 1986;55:631–661. doi: 10.1146/annurev.bi.55.070186.003215. [DOI] [PubMed] [Google Scholar]
  54. Yenikolopov G. N., Kuzin B. A., Evgen'ev N. B., Ludwig M. Z., Korochkin L. I., Georgiev G. P. The cloning and expression of the gene encoding organ-specific esterase S from the genome of Drosophila virilis. EMBO J. 1983;2(1):1–7. doi: 10.1002/j.1460-2075.1983.tb01371.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Yum J. S., Starmer W. T., Sullivan D. T. The structure of the Adh locus of Drosophila mettleri: an intermediate in the evolution of the Adh locus in the repleta group of Drosophila. Mol Biol Evol. 1991 Nov;8(6):857–867. doi: 10.1093/oxfordjournals.molbev.a040692. [DOI] [PubMed] [Google Scholar]

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