Skip to main content
PMC home page
Genetics logoLink to Genetics
. 2000 Dec;156(4):1737–1752. doi: 10.1093/genetics/156.4.1737

Extensive amino acid polymorphism at the pgm locus is consistent with adaptive protein evolution in Drosophila melanogaster.

B C Verrelli 1, W F Eanes 1
PMCID: PMC1461360  PMID: 11102370

Abstract

PGM plays a central role in the glycolytic pathway at the branch point leading to glycogen metabolism and is highly polymorphic in allozyme studies of many species. We have characterized the nucleotide diversity across the Pgm gene in Drosophila melanogaster and D. simulans to investigate the role that protein polymorphism plays at this crucial metabolic branch point shared with several other enzymes. Although D. melanogaster and D. simulans share common allozyme mobility alleles, we find these allozymes are the result of many different amino acid changes at the nucleotide level. In addition, specific allozyme classes within species contain several amino acid changes, which may explain the absence of latitudinal clines for PGM allozyme alleles, the lack of association of PGM allozymes with the cosmopolitan In(3L)P inversion, and the failure to detect differences between PGM allozymes in functional studies. We find a significant excess of amino acid polymorphisms within D. melanogaster when compared to the complete absence of fixed replacements with D. simulans. There is also strong linkage disequilibrium across the 2354 bp of the Pgm locus, which may be explained by a specific amino acid haplotype that is high in frequency yet contains an excess of singleton polymorphisms. Like G6pd, Pgm shows strong evidence for a branch point enzyme that exhibits adaptive protein evolution.

Full Text

The Full Text of this article is available as a PDF (335.7 KB).

Selected References

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

  1. Aguadé M., Miyashita N., Langley C. H. Polymorphism and divergence in the Mst26A male accessory gland gene region in Drosophila. Genetics. 1992 Nov;132(3):755–770. doi: 10.1093/genetics/132.3.755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Akashi H. Inferring the fitness effects of DNA mutations from polymorphism and divergence data: statistical power to detect directional selection under stationarity and free recombination. Genetics. 1999 Jan;151(1):221–238. doi: 10.1093/genetics/151.1.221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Akashi H. Inferring weak selection from patterns of polymorphism and divergence at "silent" sites in Drosophila DNA. Genetics. 1995 Feb;139(2):1067–1076. doi: 10.1093/genetics/139.2.1067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Akashi H. Molecular evolution between Drosophila melanogaster and D. simulans: reduced codon bias, faster rates of amino acid substitution, and larger proteins in D. melanogaster. Genetics. 1996 Nov;144(3):1297–1307. doi: 10.1093/genetics/144.3.1297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Argos P., Rossman M. G., Grau U. M., Zuber H., Frank G., Tratschin J. D. Thermal stability and protein structure. Biochemistry. 1979 Dec 11;18(25):5698–5703. doi: 10.1021/bi00592a028. [DOI] [PubMed] [Google Scholar]
  6. Ayala F. J., Hartl D. L. Molecular drift of the bride of sevenless (boss) gene in Drosophila. Mol Biol Evol. 1993 Sep;10(5):1030–1040. doi: 10.1093/oxfordjournals.molbev.a040052. [DOI] [PubMed] [Google Scholar]
  7. Ballard J. W., Kreitman M. Unraveling selection in the mitochondrial genome of Drosophila. Genetics. 1994 Nov;138(3):757–772. doi: 10.1093/genetics/138.3.757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Begun D. J., Betancourt A. J., Langley C. H., Stephan W. Is the fast/slow allozyme variation at the Adh locus of Drosophila melanogaster an ancient balanced polymorphism? Mol Biol Evol. 1999 Dec;16(12):1816–1819. doi: 10.1093/oxfordjournals.molbev.a026095. [DOI] [PubMed] [Google Scholar]
  9. Braverman J. M., Hudson R. R., Kaplan N. L., Langley C. H., Stephan W. The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics. 1995 Jun;140(2):783–796. doi: 10.1093/genetics/140.2.783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Burkhart B. D., Montgomery E., Langley C. H., Voelker R. A. Characterization of Allozyme Null and Low Activity Alleles from Two Natural Populations of DROSOPHILA MELANOGASTER. Genetics. 1984 Jun;107(2):295–306. doi: 10.1093/genetics/107.2.295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Carfagna M., Fucci L., Gaudio L., Pontecorvo G., Rubino R. Adaptive value of PGM polymorphism in laboratory populations of Drosophila melanogaster. Genet Res. 1980 Dec;36(3):265–276. doi: 10.1017/s0016672300019881. [DOI] [PubMed] [Google Scholar]
  12. Chakrabartty A., Schellman J. A., Baldwin R. L. Large differences in the helix propensities of alanine and glycine. Nature. 1991 Jun 13;351(6327):586–588. doi: 10.1038/351586a0. [DOI] [PubMed] [Google Scholar]
  13. Cooke P. H., Oakeshott J. G. Amino acid polymorphisms for esterase-6 in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1989 Feb;86(4):1426–1430. doi: 10.1073/pnas.86.4.1426. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dai J. B., Liu Y., Ray W. J., Jr, Konno M. The crystal structure of muscle phosphoglucomutase refined at 2.7-angstrom resolution. J Biol Chem. 1992 Mar 25;267(9):6322–6337. [PubMed] [Google Scholar]
  15. David J. R., Capy P. Genetic variation of Drosophila melanogaster natural populations. Trends Genet. 1988 Apr;4(4):106–111. doi: 10.1016/0168-9525(88)90098-4. [DOI] [PubMed] [Google Scholar]
  16. Depaulis F., Brazier L., Veuille M. Selective sweep at the Drosophila melanogaster Suppressor of Hairless locus and its association with the In(2L)t inversion polymorphism. Genetics. 1999 Jul;152(3):1017–1024. doi: 10.1093/genetics/152.3.1017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Eanes W. F., Kirchner M., Yoon J., Biermann C. H., Wang I. N., McCartney M. A., Verrelli B. C. Historical selection, amino acid polymorphism and lineage-specific divergence at the G6pd locus in Drosophila melanogaster and D. simulans. Genetics. 1996 Nov;144(3):1027–1041. doi: 10.1093/genetics/144.3.1027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Eanes W. F., Kirchner M., Yoon J. Evidence for adaptive evolution of the G6pd gene in the Drosophila melanogaster and Drosophila simulans lineages. Proc Natl Acad Sci U S A. 1993 Aug 15;90(16):7475–7479. doi: 10.1073/pnas.90.16.7475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Fu Y. X., Li W. H. Statistical tests of neutrality of mutations. Genetics. 1993 Mar;133(3):693–709. doi: 10.1093/genetics/133.3.693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Fucci L., Gaudio L., Rao R., Spanò A., Carfagna M. Properties of the two common electrophoretic variants of phosphoglucomutase in Drosophila melanogaster. Biochem Genet. 1979 Oct;17(9-10):825–836. doi: 10.1007/BF00504306. [DOI] [PubMed] [Google Scholar]
  21. Gillespie J. H. Junk ain't what junk does: neutral alleles in a selected context. Gene. 1997 Dec 31;205(1-2):291–299. doi: 10.1016/s0378-1119(97)00470-8. [DOI] [PubMed] [Google Scholar]
  22. Hamblin M. T., Aquadro C. F. Contrasting patterns of nucleotide sequence variation at the glucose dehydrogenase (Gld) locus in different populations of Drosophila melanogaster. Genetics. 1997 Apr;145(4):1053–1062. doi: 10.1093/genetics/145.4.1053. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hamblin M. T., Veuille M. Population structure among African and derived populations of Drosophila simulans: evidence for ancient subdivision and recent admixture. Genetics. 1999 Sep;153(1):305–317. doi: 10.1093/genetics/153.1.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hasegawa M., Cao Y., Yang Z. Preponderance of slightly deleterious polymorphism in mitochondrial DNA: nonsynonymous/synonymous rate ratio is much higher within species than between species. Mol Biol Evol. 1998 Nov;15(11):1499–1505. doi: 10.1093/oxfordjournals.molbev.a025877. [DOI] [PubMed] [Google Scholar]
  25. Hasson E., Eanes W. F. Contrasting histories of three gene regions associated with In(3L)Payne of Drosophila melanogaster. Genetics. 1996 Dec;144(4):1565–1575. doi: 10.1093/genetics/144.4.1565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hasson E., Wang I. N., Zeng L. W., Kreitman M., Eanes W. F. Nucleotide variation in the triosephosphate isomerase (Tpi) locus of Drosophila melanogaster and Drosophila simulans. Mol Biol Evol. 1998 Jun;15(6):756–769. doi: 10.1093/oxfordjournals.molbev.a025979. [DOI] [PubMed] [Google Scholar]
  27. Hentze M. W., Argos P. Homology between IRE-BP, a regulatory RNA-binding protein, aconitase, and isopropylmalate isomerase. Nucleic Acids Res. 1991 Apr 25;19(8):1739–1740. doi: 10.1093/nar/19.8.1739. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hirose M., Sugimoto E., Sasaki R., Chiaa H. Crystallization and reaction mechanism of yeast phosphoglucomutase. J Biochem. 1970 Oct;68(4):449–457. doi: 10.1093/oxfordjournals.jbchem.a129375. [DOI] [PubMed] [Google Scholar]
  29. Hjorth J. P. A phosphoglucomutase locus in Drosophila melanogaster. Hereditas. 1970;64(1):146–148. doi: 10.1111/j.1601-5223.1970.tb02284.x. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. 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]
  32. Hyytia P., Capy P., David J. R., Singh R. S. Enzymatic and quantitative variation in European and African populations of Drosophila simulans. Heredity (Edinb) 1985 Apr;54(Pt 2):209–217. doi: 10.1038/hdy.1985.28. [DOI] [PubMed] [Google Scholar]
  33. Inomata N., Shibata H., Okuyama E., Yamazaki T. Evolutionary relationships and sequence variation of alpha-amylase variants encoded by duplicated genes in the Amy locus of Drosophila melanogaster. Genetics. 1995 Sep;141(1):237–244. doi: 10.1093/genetics/141.1.237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Kaplan N. L., Darden T., Hudson R. R. The coalescent process in models with selection. Genetics. 1988 Nov;120(3):819–829. doi: 10.1093/genetics/120.3.819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Karotam J., Delves A. C., Oakeshott J. G. Conservation and change in structural and 5' flanking sequences of esterase 6 in sibling Drosophila species. Genetica. 1993;88(1):11–28. doi: 10.1007/BF02424448. [DOI] [PubMed] [Google Scholar]
  36. Keightley P. D., Kacser H. Dominance, pleiotropy and metabolic structure. Genetics. 1987 Oct;117(2):319–329. doi: 10.1093/genetics/117.2.319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Keightley P. D. Models of quantitative variation of flux in metabolic pathways. Genetics. 1989 Apr;121(4):869–876. doi: 10.1093/genetics/121.4.869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Kennedy P., Nachman M. W. Deleterious mutations at the mitochondrial ND3 gene in South American marsh rats (Holochilus). Genetics. 1998 Sep;150(1):359–368. doi: 10.1093/genetics/150.1.359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. 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]
  40. 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]
  41. Knibb W. R., Oakeshott J. G., Gibson J. B. Chromosome Inversion Polymorphisms in DROSOPHILA MELANOGASTER. I. Latitudinal Clines and Associations between Inversions in Australasian Populations. Genetics. 1981 Aug;98(4):833–847. doi: 10.1093/genetics/98.4.833. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Kreitman M., Hudson R. R. Inferring the evolutionary histories of the Adh and Adh-dup loci in Drosophila melanogaster from patterns of polymorphism and divergence. Genetics. 1991 Mar;127(3):565–582. doi: 10.1093/genetics/127.3.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Kreitman M. Nucleotide polymorphism at the alcohol dehydrogenase locus of Drosophila melanogaster. Nature. 1983 Aug 4;304(5925):412–417. doi: 10.1038/304412a0. [DOI] [PubMed] [Google Scholar]
  44. LaPorte D. C., Walsh K., Koshland D. E., Jr The branch point effect. Ultrasensitivity and subsensitivity to metabolic control. J Biol Chem. 1984 Nov 25;259(22):14068–14075. [PubMed] [Google Scholar]
  45. Labate J. A., Biermann C. H., Eanes W. F. Nucleotide variation at the runt locus in Drosophila melanogaster and Drosophila simulans. Mol Biol Evol. 1999 Jun;16(6):724–731. doi: 10.1093/oxfordjournals.molbev.a026157. [DOI] [PubMed] [Google Scholar]
  46. Langley C. H., Ito K., Voelker R. A. Linkage disequilibrium in natural populations of Drosophila melanogaster Seasonal variation. Genetics. 1977 Jun;86(2 Pt 1):447–454. [PMC free article] [PubMed] [Google Scholar]
  47. Langley C. H., Tobari Y. N., Kojima K. I. Linkage disequilibrium in natural populations of Drosophila melanogaster. Genetics. 1974 Nov;78(3):921–936. doi: 10.1093/genetics/78.3.921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. 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]
  49. Leicht B. G., Muse S. V., Hanczyc M., Clark A. G. Constraints on intron evolution in the gene encoding the myosin alkali light chain in Drosophila. Genetics. 1995 Jan;139(1):299–308. doi: 10.1093/genetics/139.1.299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Liu Y., Ray W. J., Jr, Baranidharan S. Structure of rabbit muscle phosphoglucomutase refined at 2.4 A resolution. Acta Crystallogr D Biol Crystallogr. 1997 Jul 1;53(Pt 4):392–405. doi: 10.1107/S0907444997000875. [DOI] [PubMed] [Google Scholar]
  51. McDonald J. H. 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. doi: 10.1093/oxfordjournals.molbev.a025934. [DOI] [PubMed] [Google Scholar]
  52. 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]
  53. Mettler L. E., Voelker R. A., Mukai T. Inversion Clines in Populations of DROSOPHILA MELANOGASTER. Genetics. 1977 Sep;87(1):169–176. doi: 10.1093/genetics/87.1.169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Moriyama E. N., Powell J. R. Intraspecific nuclear DNA variation in Drosophila. Mol Biol Evol. 1996 Jan;13(1):261–277. doi: 10.1093/oxfordjournals.molbev.a025563. [DOI] [PubMed] [Google Scholar]
  55. Nachman M. W., Boyer S. N., Aquadro C. F. Nonneutral evolution at the mitochondrial NADH dehydrogenase subunit 3 gene in mice. Proc Natl Acad Sci U S A. 1994 Jul 5;91(14):6364–6368. doi: 10.1073/pnas.91.14.6364. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Neuhauser C., Krone S. M. The genealogy of samples in models with selection. Genetics. 1997 Feb;145(2):519–534. doi: 10.1093/genetics/145.2.519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Nielsen R., Weinreich D. M. The age of nonsynonymous and synonymous mutations in animal mtDNA and implications for the mildly deleterious theory. Genetics. 1999 Sep;153(1):497–506. doi: 10.1093/genetics/153.1.497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Oakeshott J. G., Chambers G. K., Gibson J. B., Willcocks D. A. Latitudinal relationships of esterase-6 and phosphoglucomutase gene frequencies in Drosophila melanogaster. Heredity (Edinb) 1981 Dec;47(Pt 3):385–396. doi: 10.1038/hdy.1981.99. [DOI] [PubMed] [Google Scholar]
  59. Oakeshott J. G., Wilson S. R., Knibb W. R. Selection affecting enzyme polymorphisms in enclosed Drosophila populations maintained in a natural environment. Proc Natl Acad Sci U S A. 1988 Jan;85(1):293–297. doi: 10.1073/pnas.85.1.293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Ohta T. The current significance and standing of neutral and neutral theories. Bioessays. 1996 Aug;18(8):673–683. doi: 10.1002/bies.950180811. [DOI] [PubMed] [Google Scholar]
  61. Przeworski M., Charlesworth B., Wall J. D. Genealogies and weak purifying selection. Mol Biol Evol. 1999 Feb;16(2):246–252. doi: 10.1093/oxfordjournals.molbev.a026106. [DOI] [PubMed] [Google Scholar]
  62. RAY W. J., Jr, ROSCELLI G. A. A KINETIC STUDY OF THE PHOSPHOGLUCOMUTASE PATHWAY. J Biol Chem. 1964 Apr;239:1228–1236. [PubMed] [Google Scholar]
  63. Rand D. M., Dorfsman M., Kann L. M. Neutral and non-neutral evolution of Drosophila mitochondrial DNA. Genetics. 1994 Nov;138(3):741–756. doi: 10.1093/genetics/138.3.741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Rand D. M., Kann L. M. Excess amino acid polymorphism in mitochondrial DNA: contrasts among genes from Drosophila, mice, and humans. Mol Biol Evol. 1996 Jul;13(6):735–748. doi: 10.1093/oxfordjournals.molbev.a025634. [DOI] [PubMed] [Google Scholar]
  65. Rozas J., Aguadé M. Gene conversion is involved in the transfer of genetic information between naturally occurring inversions of Drosophila. Proc Natl Acad Sci U S A. 1994 Nov 22;91(24):11517–11521. doi: 10.1073/pnas.91.24.11517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. 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]
  67. Rozas J., Segarra C., Ribó G., Aguadé M. Molecular population genetics of the rp49 gene region in different chromosomal inversions of Drosophila subobscura. Genetics. 1999 Jan;151(1):189–202. doi: 10.1093/genetics/151.1.189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. 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]
  69. Singh R. S., Rhomberg L. R. A Comprehensive Study of Genic Variation in Natural Populations of Drosophila melanogaster. II. Estimates of Heterozygosity and Patterns of Geographic Differentiation. Genetics. 1987 Oct;117(2):255–271. doi: 10.1093/genetics/117.2.255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Slatkin M., Rannala B. Estimating the age of alleles by use of intraallelic variability. Am J Hum Genet. 1997 Feb;60(2):447–458. [PMC free article] [PubMed] [Google Scholar]
  71. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989 Nov;123(3):585–595. doi: 10.1093/genetics/123.3.585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Trippa G., Catamo A., Lombardozzi A., Cicchetti R. A simple approach for discovering common nonelectrophoretic enzyme variability: a heat denaturation study in Drosophila melanogaster. Biochem Genet. 1978 Apr;16(3-4):299–305. doi: 10.1007/BF00484086. [DOI] [PubMed] [Google Scholar]
  73. Trippa G., Loverre A., Catamo A. Thermostability studies for investigating non-electrophoretic polymorphic alleles in Drosophila melanogaster. Nature. 1976 Mar 4;260(5546):42–44. doi: 10.1038/260042a0. [DOI] [PubMed] [Google Scholar]
  74. Trippa G., Santolamazza C., Scozzari R. Phosphoglucomutase (PGM) locus in Drosophila melanogaster: linkage and population data. Biochem Genet. 1970 Dec;4(6):665–667. doi: 10.1007/BF00486380. [DOI] [PubMed] [Google Scholar]
  75. 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]
  76. 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]
  77. Wayne M. L., Contamine D., Kreitman M. Molecular population genetics of ref(2)P, a locus which confers viral resistance in Drosophila. Mol Biol Evol. 1996 Jan;13(1):191–199. doi: 10.1093/oxfordjournals.molbev.a025555. [DOI] [PubMed] [Google Scholar]
  78. Wesley C. S., Eanes W. F. Isolation and analysis of the breakpoint sequences of chromosome inversion In(3L)Payne in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3132–3136. doi: 10.1073/pnas.91.8.3132. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Whitehouse D. B., Tomkins J., Lovegrove J. U., Hopkinson D. A., McMillan W. O. A phylogenetic approach to the identification of phosphoglucomutase genes. Mol Biol Evol. 1998 Apr;15(4):456–462. doi: 10.1093/oxfordjournals.molbev.a025942. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES