Skip to main content
Genetics logoLink to Genetics
. 1997 Dec;147(4):1899–1914. doi: 10.1093/genetics/147.4.1899

DNA Polymorphism at the Pgi Locus of a Wild Yam, Dioscorea Tokoro

R Terauchi 1, T Terachi 1, N T Miyashita 1
PMCID: PMC1208355  PMID: 9409845

Abstract

To study the origin and maintenance mechanisms of the PGI allozyme polymorphism of a wild plant, Dioscorea tokoro, DNA sequences of the entire coding region (1701 bp) and two intronic regions (total 2049 bp) of the Pgi gene as well as a part of the Adh gene (590 bp) were analyzed. Two replacement substitutions were revealed to be responsible for the differentiation of three allozymes alleles (Pgi-a, Pgi-b and Pgi-c) that occur in natural population in intermediate frequencies. Interspecific comparison of DNA sequences identified Pgi-b as the oldest allele, from which two other alleles were derived probably within the last 150,000 years. The level of DNA polymorphism at D. tokoro Pgi locus was low. No elevated level of DNA polymorphism was detected in the close vicinity of the two replacement sites differentiating the three allozymes. Departures from the neutral mutation hypothesis were detected by Fu and Li's and MK tests. The observed patterns of DNA polymorphism are explainable by both (1) the neutral mutation hypothesis with an assumption of small effective size of D. tokoro population, and (2) the positive selection hypothesis that the allele frequencies of Pgi-a and Pgi-c have increased in a short time by their selective advantages.

Full Text

The Full Text of this article is available as a PDF (1.6 MB).

Selected References

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

  1. Achari A., Marshall S. E., Muirhead H., Palmieri R. H., Noltmann E. A. Glucose-6-phosphate isomerase. Philos Trans R Soc Lond B Biol Sci. 1981 Jun 26;293(1063):145–157. doi: 10.1098/rstb.1981.0068. [DOI] [PubMed] [Google Scholar]
  2. Aquadro C. F., Lado K. M., Noon W. A. The rosy region of Drosophila melanogaster and Drosophila simulans. I. Contrasting levels of naturally occurring DNA restriction map variation and divergence. Genetics. 1988 Aug;119(4):875–888. doi: 10.1093/genetics/119.4.875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. Chang C., Meyerowitz E. M. Molecular cloning and DNA sequence of the Arabidopsis thaliana alcohol dehydrogenase gene. Proc Natl Acad Sci U S A. 1986 Mar;83(5):1408–1412. doi: 10.1073/pnas.83.5.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chaput M., Claes V., Portetelle D., Cludts I., Cravador A., Burny A., Gras H., Tartar A. The neurotrophic factor neuroleukin is 90% homologous with phosphohexose isomerase. Nature. 1988 Mar 31;332(6163):454–455. doi: 10.1038/332454a0. [DOI] [PubMed] [Google Scholar]
  6. Charlesworth B. The effect of background selection against deleterious mutations on weakly selected, linked variants. Genet Res. 1994 Jun;63(3):213–227. doi: 10.1017/s0016672300032365. [DOI] [PubMed] [Google Scholar]
  7. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Frohman M. A., Dush M. K., Martin G. R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998–9002. doi: 10.1073/pnas.85.23.8998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gaut B. S., Clegg M. T. Molecular evolution of alcohol dehydrogenase 1 in members of the grass family. Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2060–2064. doi: 10.1073/pnas.88.6.2060. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gaut B. S., Clegg M. T. Nucleotide polymorphism in the Adh1 locus of pearl millet (Pennisetum glaucum) (Poaceae). Genetics. 1993 Dec;135(4):1091–1097. doi: 10.1093/genetics/135.4.1091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Green J. B., Wright A. P., Cheung W. Y., Lancashire W. E., Hartley B. S. The structure and regulation of phosphoglucose isomerase in Saccharomyces cerevisiae. Mol Gen Genet. 1988 Dec;215(1):100–106. doi: 10.1007/BF00331310. [DOI] [PubMed] [Google Scholar]
  13. Hall J. G. Temperature-related kinetic differentiation of glucosephosphate isomerase alleloenzymes isolated from the blue mussel, Mytilus edulis. Biochem Genet. 1985 Oct;23(9-10):705–728. [PubMed] [Google Scholar]
  14. Hanfstingl U., Berry A., Kellogg E. A., Costa J. T., 3rd, Rüdiger W., Ausubel F. M. Haplotypic divergence coupled with lack of diversity at the Arabidopsis thaliana alcohol dehydrogenase locus: roles for both balancing and directional selection? Genetics. 1994 Nov;138(3):811–828. doi: 10.1093/genetics/138.3.811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hoffmann R. J. Evolutionary genetics of Metridium senile. I. Kinetic differences in phosphoglucose isomerase allozymes. Biochem Genet. 1981 Feb;19(1-2):129–144. doi: 10.1007/BF00486143. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Hudson R. R. How can the low levels of DNA sequence variation in regions of the drosophila genome with low recombination rates be explained? Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):6815–6818. doi: 10.1073/pnas.91.15.6815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. Hudson R. R., Kaplan N. L. The coalescent process in models with selection and recombination. Genetics. 1988 Nov;120(3):831–840. doi: 10.1093/genetics/120.3.831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Innan H., Tajima F., Terauchi R., Miyashita N. T. Intragenic recombination in the Adh locus of the wild plant Arabidopsis thaliana. Genetics. 1996 Aug;143(4):1761–1770. doi: 10.1093/genetics/143.4.1761. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Lal S. K., Sachs M. M. Cloning and characterization of an anaerobically induced cDNA encoding glucose-6-phosphate isomerase from maize. Plant Physiol. 1995 Jul;108(3):1295–1296. doi: 10.1104/pp.108.3.1295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Miyashita N. T., Innan H., Terauchi R. Intra- and interspecific variation of the alcohol dehydrogenase locus region in wild plants Arabis gemmifera and Arabidopsis thaliana. Mol Biol Evol. 1996 Feb;13(2):433–436. doi: 10.1093/oxfordjournals.molbev.a025603. [DOI] [PubMed] [Google Scholar]
  26. Miyata T., Miyazawa S., Yasunaga T. Two types of amino acid substitutions in protein evolution. J Mol Evol. 1979 Mar 15;12(3):219–236. doi: 10.1007/BF01732340. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Nei M. Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci U S A. 1973 Dec;70(12):3321–3323. doi: 10.1073/pnas.70.12.3321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Nozue F., Umeda M., Nagamura Y., Minobe Y., Uchimiya H. Characterization of cDNA encoding for phosphoglucose isomerase of rice (Oryza sativa L.). DNA Seq. 1996;6(3):127–135. doi: 10.3109/10425179609010200. [DOI] [PubMed] [Google Scholar]
  31. Ohta T. Role of very slightly deleterious mutations in molecular evolution and polymorphism. Theor Popul Biol. 1976 Dec;10(3):254–275. doi: 10.1016/0040-5809(76)90019-8. [DOI] [PubMed] [Google Scholar]
  32. Sharp P. M., Li W. H. On the rate of DNA sequence evolution in Drosophila. J Mol Evol. 1989 May;28(5):398–402. doi: 10.1007/BF02603075. [DOI] [PubMed] [Google Scholar]
  33. Sharp P. M., Matassi G. Codon usage and genome evolution. Curr Opin Genet Dev. 1994 Dec;4(6):851–860. doi: 10.1016/0959-437x(94)90070-1. [DOI] [PubMed] [Google Scholar]
  34. Shaw P. J., Muirhead H. Crystallographic structure analysis of glucose 6-phosphate isomerase at 3-5 A resolution. J Mol Biol. 1977 Jan 25;109(3):475–485. doi: 10.1016/s0022-2836(77)80025-9. [DOI] [PubMed] [Google Scholar]
  35. Shields D. C., Sharp P. M., Higgins D. G., Wright F. "Silent" sites in Drosophila genes are not neutral: evidence of selection among synonymous codons. Mol Biol Evol. 1988 Nov;5(6):704–716. doi: 10.1093/oxfordjournals.molbev.a040525. [DOI] [PubMed] [Google Scholar]
  36. Stephens J. C. Statistical methods of DNA sequence analysis: detection of intragenic recombination or gene conversion. Mol Biol Evol. 1985 Nov;2(6):539–556. doi: 10.1093/oxfordjournals.molbev.a040371. [DOI] [PubMed] [Google Scholar]
  37. Strobeck C. Expected linkage disequilibrium for a neutral locus linked to a chromosomal arrangement. Genetics. 1983 Mar;103(3):545–555. doi: 10.1093/genetics/103.3.545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. 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]
  39. Tajima F. The effect of change in population size on DNA polymorphism. Genetics. 1989 Nov;123(3):597–601. doi: 10.1093/genetics/123.3.597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Terauchi R., Konuma A. Microsatellite polymorphism in Dioscorea tokoro, a wild yam species. Genome. 1994 Oct;37(5):794–801. doi: 10.1139/g94-113. [DOI] [PubMed] [Google Scholar]
  41. Thomas B. R., Ford V. S., Pichersky E., Gottlieb L. D. Molecular characterization of duplicate cytosolic phosphoglucose isomerase genes in Clarkia and comparison to the single gene in Arabidopsis. Genetics. 1993 Nov;135(3):895–905. doi: 10.1093/genetics/135.3.895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Thomas B. R., Laudencia-Chingcuanco D., Gottlieb L. D. Molecular analysis of the plant gene encoding cytosolic phosphoglucose isomerase. Plant Mol Biol. 1992 Aug;19(5):745–757. doi: 10.1007/BF00027071. [DOI] [PubMed] [Google Scholar]
  43. Watt W. B. Adaptation at specific loci. I. Natural selection on phosphoglucose isomerase of Colias butterflies: Biochemical and population aspects. Genetics. 1977 Sep;87(1):177–194. doi: 10.1093/genetics/87.1.177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. 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]
  45. Watterson G. A. The homozygosity test of neutrality. Genetics. 1978 Feb;88(2):405–417. doi: 10.1093/genetics/88.2.405. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES