Distinct frequency-distributions of homopolymeric DNA tracts in different genomes (original) (raw)

Abstract

The unusual base composition of the genome of the human malaria parasite Plasmodium falciparum prompted us to systematically investigate the occurrence of homopolymeric DNA tracts in the P. falciparum genome and, for comparison, in the genomes of Homo sapiens , Saccharomyces cerevisiae , Caenorhabditis elegans , Arabidopsis thaliana , Escherichia coli and Mycobacterium tuberculosis. Comparison of theobserved frequencies with the frequencies as expected for random DNA revealed that homopolymeric (dA:dT) tracts occur well above chance in the eukaryotic genome. In the majority of these genomes, (dA:dT) tract overrepresentation proved to be an exponential function of the tract length. (dG:dC) tract overrepresentation was absent or less pronounced in both prokaryotic and eukaryotic genomes. On the basis of our results, we propose that homopolymeric (dA:dT) tracts are expanded via replication slippage. This slippage-mediated expansion does not operate on tracts with lengths below a critical threshold of 7-10 bp.

Full Text

The Full Text of this article is available as a PDF (114.2 KB).

Selected References

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

  1. Bates G., Lehrach H. Trinucleotide repeat expansions and human genetic disease. Bioessays. 1994 Apr;16(4):277–284. doi: 10.1002/bies.950160411. [DOI] [PubMed] [Google Scholar]
  2. Blattner F. R., Plunkett G., 3rd, Bloch C. A., Perna N. T., Burland V., Riley M., Collado-Vides J., Glasner J. D., Rode C. K., Mayhew G. F. The complete genome sequence of Escherichia coli K-12. Science. 1997 Sep 5;277(5331):1453–1462. doi: 10.1126/science.277.5331.1453. [DOI] [PubMed] [Google Scholar]
  3. Cox R., Mirkin S. M. Characteristic enrichment of DNA repeats in different genomes. Proc Natl Acad Sci U S A. 1997 May 13;94(10):5237–5242. doi: 10.1073/pnas.94.10.5237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cress W. D., Nevins J. R. A role for a bent DNA structure in E2F-mediated transcription activation. Mol Cell Biol. 1996 May;16(5):2119–2127. doi: 10.1128/mcb.16.5.2119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dame J. B., Arnot D. E., Bourke P. F., Chakrabarti D., Christodoulou Z., Coppel R. L., Cowman A. F., Craig A. G., Fischer K., Foster J. Current status of the Plasmodium falciparum genome project. Mol Biochem Parasitol. 1996 Jul;79(1):1–12. doi: 10.1016/0166-6851(96)02641-2. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Doolittle W. F., Sapienza C. Selfish genes, the phenotype paradigm and genome evolution. Nature. 1980 Apr 17;284(5757):601–603. doi: 10.1038/284601a0. [DOI] [PubMed] [Google Scholar]
  8. Farber R. A., Petes T. D., Dominska M., Hudgens S. S., Liskay R. M. Instability of simple sequence repeats in a mammalian cell line. Hum Mol Genet. 1994 Feb;3(2):253–256. doi: 10.1093/hmg/3.2.253. [DOI] [PubMed] [Google Scholar]
  9. Gasser S. M., Laemmli U. K. Cohabitation of scaffold binding regions with upstream/enhancer elements of three developmentally regulated genes of D. melanogaster. Cell. 1986 Aug 15;46(4):521–530. doi: 10.1016/0092-8674(86)90877-9. [DOI] [PubMed] [Google Scholar]
  10. Goodsell D. S., Kaczor-Grzeskowiak M., Dickerson R. E. The crystal structure of C-C-A-T-T-A-A-T-G-G. Implications for bending of B-DNA at T-A steps. J Mol Biol. 1994 May 27;239(1):79–96. doi: 10.1006/jmbi.1994.1352. [DOI] [PubMed] [Google Scholar]
  11. Hancock J. M. Evolution of sequence repetition and gene duplications in the TATA-binding protein TBP (TFIID). Nucleic Acids Res. 1993 Jun 25;21(12):2823–2830. doi: 10.1093/nar/21.12.2823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hancock J. M. Simple sequences and the expanding genome. Bioessays. 1996 May;18(5):421–425. doi: 10.1002/bies.950180512. [DOI] [PubMed] [Google Scholar]
  13. Hancock J. M. The contribution of slippage-like processes to genome evolution. J Mol Evol. 1995 Dec;41(6):1038–1047. doi: 10.1007/BF00173185. [DOI] [PubMed] [Google Scholar]
  14. Henderson S. T., Petes T. D. Instability of simple sequence DNA in Saccharomyces cerevisiae. Mol Cell Biol. 1992 Jun;12(6):2749–2757. doi: 10.1128/mcb.12.6.2749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hodgkin J., Plasterk R. H., Waterston R. H. The nematode Caenorhabditis elegans and its genome. Science. 1995 Oct 20;270(5235):410–414. doi: 10.1126/science.270.5235.410. [DOI] [PubMed] [Google Scholar]
  16. Hyde J. E., Sims P. F. Anomalous dinucleotide frequencies in both coding and non-coding regions from the genome of the human malaria parasite Plasmodium falciparum. Gene. 1987;61(2):177–187. doi: 10.1016/0378-1119(87)90112-0. [DOI] [PubMed] [Google Scholar]
  17. Iyer V., Struhl K. Poly(dA:dT), a ubiquitous promoter element that stimulates transcription via its intrinsic DNA structure. EMBO J. 1995 Jun 1;14(11):2570–2579. doi: 10.1002/j.1460-2075.1995.tb07255.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Koo H. S., Wu H. M., Crothers D. M. DNA bending at adenine . thymine tracts. Nature. 1986 Apr 10;320(6062):501–506. doi: 10.1038/320501a0. [DOI] [PubMed] [Google Scholar]
  19. Käs E., Izaurralde E., Laemmli U. K. Specific inhibition of DNA binding to nuclear scaffolds and histone H1 by distamycin. The role of oligo(dA).oligo(dT) tracts. J Mol Biol. 1989 Dec 5;210(3):587–599. doi: 10.1016/0022-2836(89)90134-4. [DOI] [PubMed] [Google Scholar]
  20. Käs E., Laemmli U. K. In vivo topoisomerase II cleavage of the Drosophila histone and satellite III repeats: DNA sequence and structural characteristics. EMBO J. 1992 Feb;11(2):705–716. doi: 10.1002/j.1460-2075.1992.tb05103.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lanzer M., de Bruin D., Ravetch J. V. Transcriptional differences in polymorphic and conserved domains of a complete cloned P. falciparum chromosome. Nature. 1993 Feb 18;361(6413):654–657. doi: 10.1038/361654a0. [DOI] [PubMed] [Google Scholar]
  22. Levinson G., Gutman G. A. Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol Biol Evol. 1987 May;4(3):203–221. doi: 10.1093/oxfordjournals.molbev.a040442. [DOI] [PubMed] [Google Scholar]
  23. Marini J. C., Levene S. D., Crothers D. M., Englund P. T. Bent helical structure in kinetoplast DNA. Proc Natl Acad Sci U S A. 1982 Dec;79(24):7664–7668. doi: 10.1073/pnas.79.24.7664. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Marx K. A., Hess S. T., Blake R. D. Characteristics of the large (dA).(dT) homopolymer tracts in D. discoideum gene flanking and intron sequences. J Biomol Struct Dyn. 1993 Aug;11(1):57–66. doi: 10.1080/07391102.1993.10508709. [DOI] [PubMed] [Google Scholar]
  25. McCutchan T. F., Dame J. B., Miller L. H., Barnwell J. Evolutionary relatedness of Plasmodium species as determined by the structure of DNA. Science. 1984 Aug 24;225(4664):808–811. doi: 10.1126/science.6382604. [DOI] [PubMed] [Google Scholar]
  26. Miassod R., Razin S. V., Hancock R. Distribution of topoisomerase II-mediated cleavage sites and relation to structural and functional landmarks in 830 kb of Drosophila DNA. Nucleic Acids Res. 1997 Jun 1;25(11):2041–2046. doi: 10.1093/nar/25.11.2041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Musto H., Rodriguez-Maseda H., Bernardi G. Compositional properties of nuclear genes from Plasmodium falciparum. Gene. 1995 Jan 11;152(1):127–132. doi: 10.1016/0378-1119(94)00708-z. [DOI] [PubMed] [Google Scholar]
  28. Nelson H. C., Finch J. T., Luisi B. F., Klug A. The structure of an oligo(dA).oligo(dT) tract and its biological implications. Nature. 1987 Nov 19;330(6145):221–226. doi: 10.1038/330221a0. [DOI] [PubMed] [Google Scholar]
  29. Newfeld S. J., Tachida H., Yedvobnick B. Drive-selection equilibrium: homopolymer evolution in the Drosophila gene mastermind. J Mol Evol. 1994 Jun;38(6):637–641. doi: 10.1007/BF00175884. [DOI] [PubMed] [Google Scholar]
  30. Parvin J. D., McCormick R. J., Sharp P. A., Fisher D. E. Pre-bending of a promoter sequence enhances affinity for the TATA-binding factor. Nature. 1995 Feb 23;373(6516):724–727. doi: 10.1038/373724a0. [DOI] [PubMed] [Google Scholar]
  31. Pollack Y., Katzen A. L., Spira D. T., Golenser J. The genome of Plasmodium falciparum. I: DNA base composition. Nucleic Acids Res. 1982 Jan 22;10(2):539–546. doi: 10.1093/nar/10.2.539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Pologe L. G., de Bruin D., Ravetch J. V. A and T homopolymeric stretches mediate a DNA inversion in Plasmodium falciparum which results in loss of gene expression. Mol Cell Biol. 1990 Jun;10(6):3243–3246. doi: 10.1128/mcb.10.6.3243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Richards R. I., Sutherland G. R. Simple repeat DNA is not replicated simply. Nat Genet. 1994 Feb;6(2):114–116. doi: 10.1038/ng0294-114. [DOI] [PubMed] [Google Scholar]
  34. Saitoh N., Goldberg I., Earnshaw W. C. The SMC proteins and the coming of age of the chromosome scaffold hypothesis. Bioessays. 1995 Sep;17(9):759–766. doi: 10.1002/bies.950170905. [DOI] [PubMed] [Google Scholar]
  35. Schlötterer C., Tautz D. Slippage synthesis of simple sequence DNA. Nucleic Acids Res. 1992 Jan 25;20(2):211–215. doi: 10.1093/nar/20.2.211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Schmidt R., West J., Love K., Lenehan Z., Lister C., Thompson H., Bouchez D., Dean C. Physical map and organization of Arabidopsis thaliana chromosome 4. Science. 1995 Oct 20;270(5235):480–483. doi: 10.1126/science.270.5235.480. [DOI] [PubMed] [Google Scholar]
  37. Struhl K. Naturally occurring poly(dA-dT) sequences are upstream promoter elements for constitutive transcription in yeast. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8419–8423. doi: 10.1073/pnas.82.24.8419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Tachida H., Iizuka M. Persistence of repeated sequences that evolve by replication slippage. Genetics. 1992 Jun;131(2):471–478. doi: 10.1093/genetics/131.2.471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Tautz D., Trick M., Dover G. A. Cryptic simplicity in DNA is a major source of genetic variation. Nature. 1986 Aug 14;322(6080):652–656. doi: 10.1038/322652a0. [DOI] [PubMed] [Google Scholar]
  40. Tran H. T., Degtyareva N. P., Koloteva N. N., Sugino A., Masumoto H., Gordenin D. A., Resnick M. A. Replication slippage between distant short repeats in Saccharomyces cerevisiae depends on the direction of replication and the RAD50 and RAD52 genes. Mol Cell Biol. 1995 Oct;15(10):5607–5617. doi: 10.1128/mcb.15.10.5607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Treier M., Pfeifle C., Tautz D. Comparison of the gap segmentation gene hunchback between Drosophila melanogaster and Drosophila virilis reveals novel modes of evolutionary change. EMBO J. 1989 May;8(5):1517–1525. doi: 10.1002/j.1460-2075.1989.tb03536.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Walsh J. B. Persistence of tandem arrays: implications for satellite and simple-sequence DNAs. Genetics. 1987 Mar;115(3):553–567. doi: 10.1093/genetics/115.3.553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Weber J. L. Molecular biology of malaria parasites. Exp Parasitol. 1988 Aug;66(2):143–170. doi: 10.1016/0014-4894(88)90087-2. [DOI] [PubMed] [Google Scholar]
  44. Zhu Z., Thiele D. J. A specialized nucleosome modulates transcription factor access to a C. glabrata metal responsive promoter. Cell. 1996 Nov 1;87(3):459–470. doi: 10.1016/s0092-8674(00)81366-5. [DOI] [PubMed] [Google Scholar]