Molecular Biology Reports

, 35:163

Strand compositional asymmetries in vertebrate large genes

Article

Abstract

Both transcription-associated and replication-associated strand compositional asymmetries have recently been shown in vertebrate genomes. In this paper, we illustrate that transcription-associated strand compositional asymmetries and replication-associated ones coexist in most vertebrate large genes, although in most case the former conceals the latter. Furthermore, we found that the transcription-associated strand compositional asymmetries of housekeeping genes are stronger than those of somatic cell expressed genes. Together with other evidence, we suggest that germline transcription-associated strand asymmetric mutations may be the main cause of the transcription-associated strand compositional asymmetries.

Keywords

Cumulative skew diagram Illegitimate transcription Replication Transcription 

Abbreviations

CSD

Cumulative skew diagram

CSDD

Cumulative skew difference diagram

Supplementary material

11033_2007_9066_MOESM1_ESM.pdf (635 kb)
ESM1 (PDF 635 kb)
11033_2007_9066_MOESM2_ESM.pdf (297 kb)
ESM3 (PDF 297 kb)
11033_2007_9066_MOESM3_ESM.pdf (553 kb)
ESM1 (PDF 553 kb)

References

  1. 1.
    Lobry JR (1996) Asymmetric substitution patterns in the two DNA strands of bacteria. Mol Biol Evol 13(5):660–665PubMedGoogle Scholar
  2. 2.
    Francino MP, Ochman H (1997) Strand asymmetries in DNA evolution. Trends Genet 13(6):240–245PubMedCrossRefGoogle Scholar
  3. 3.
    Grigoriev A (1998) Analyzing genomes with cumulative skew diagrams. Nucleic Acids Res 26(10):2286–2290PubMedCrossRefGoogle Scholar
  4. 4.
    Mrazek J, Karlin S (1998) Strand compositional asymmetry in bacterial and large viral genomes. Proc Natl Acad Sci USA 95(7):3720–3725PubMedCrossRefGoogle Scholar
  5. 5.
    Reyes A, Gissi C, Pesole G, Saccone C (1998) Asymmetrical directional mutation pressure in the mitochondrial genome of mammals. Mol Biol Evol 15(8):957–966PubMedGoogle Scholar
  6. 6.
    Frank AC, Lobry JR (1999) Asymmetric substitution patterns: A review of possible underlying mutational or selective mechanisms. Gene 238(1):65–77PubMedCrossRefGoogle Scholar
  7. 7.
    Grigoriev A (1999) Strand-specific compositional asymmetries in double-stranded DNA viruses. Virus Res 60(1):1–19PubMedCrossRefGoogle Scholar
  8. 8.
    Rocha EPC, Danchin A, Viari A (1999) Universal replication biases in bacteria Mol Microbiol 32(1):11–16PubMedCrossRefGoogle Scholar
  9. 9.
    Lobry JR, Sueoka N (2002) Asymmetric directional mutation pressures in bacteria. Genome Biol 3(10): research0058.0051–0058.0014Google Scholar
  10. 10.
    Tillier ERM, Collins RA (2000) The contributions of replication orientation, gene direction, and signal sequences to base-composition asymmetries in bacterial genomes. J Mol Evol 50(3):249–257PubMedGoogle Scholar
  11. 11.
    Kowalczuk M, Mackiewicz P, Mackiewicz D, Nowicka A, Dudkiewicz M, Dudek MR, Cebrat S (2001) DNA asymmetry and the replicational mutational pressure. J Appl Genet 42(4):553–577PubMedGoogle Scholar
  12. 12.
    Beletskii A, Bhagwat AS (1998) Correlation between transcription and C to T mutations in the non-transcribed DNA strand. Biol Chem 379(4–5):549–551PubMedGoogle Scholar
  13. 13.
    Francino MP, Ochman H (2001) Deamination as the basis of strand-asymmetric evolution in transcribed Escherichia coli sequences. Mol Biol Evol 18(6):1147–1150PubMedGoogle Scholar
  14. 14.
    Zeigler DR, Dean DH (1990) Orientation of genes in the Bacillus subtilis chromosome. Genetics 125(4):703–708PubMedGoogle Scholar
  15. 15.
    McLean MJ, Wolfe KH, Devine KM (1998) Base composition skews, replication orientation, and gene orientation in 12 prokaryote genomes. J Mol Evol 47(6):691–696PubMedCrossRefGoogle Scholar
  16. 16.
    Rocha EP, Danchin A (2003) Essentiality, not expressiveness, drives gene-strand bias in bacteria. Nat Genet 34(4):377–378PubMedCrossRefGoogle Scholar
  17. 17.
    Baran RH, Ko H (2006) An Ising model of transcription polarity in bacterial chromosomes. Physica A 362(2):403–422CrossRefGoogle Scholar
  18. 18.
    Nikolaou C, Almirantis Y (2005) A study on the correlation of nucleotide skews and the positioning of the origin of replication: different modes of replication in bacterial species. Nucleic Acids Res 33(21):6816–6822PubMedCrossRefGoogle Scholar
  19. 19.
    Baran RH, Ko H, Jernigan RW (2003) Methods for comparing sources of strand compositional asymmetry in microbial chromosomes. DNA Res 10(3):85–95PubMedCrossRefGoogle Scholar
  20. 20.
    Green P, Ewing B, Miller W, Thomas PJ, Green ED (2003) Transcription-associated mutational asymmetry in mammalian evolution. Nat Genet 33(4):514–517PubMedCrossRefGoogle Scholar
  21. 21.
    Majewski J (2003) Dependence of mutational asymmetry on gene-expression levels in the human genome. Am J Hum Genet 73(3):688–692PubMedCrossRefGoogle Scholar
  22. 22.
    Niu DK, Lin K, Zhang DY (2003) Strand compositional asymmetries of nuclear DNA in eukaryotes. J Mol Evol 57(3):325–334PubMedCrossRefGoogle Scholar
  23. 23.
    Touchon M, Nicolay S, Audit B, Brodie of Brodie E-B, d’Aubenton-Carafa Y, Arneodo A, Thermes C (2005) Replication-associated strand asymmetries in mammalian genomes: toward detection of replication origins. Proc Natl Acad Sci USA 102(28):9836–9841PubMedCrossRefGoogle Scholar
  24. 24.
    Brodie of Brodie E-B, Nicolay S, Touchon M, Audit B, d’Aubenton-Carafa Y, Thermes C, Arneodo A (2005) From DNA sequence analysis to modeling replication in the human genome. Phys Rev Lett 9424(24):248103CrossRefGoogle Scholar
  25. 25.
    Hou WR, Wang HF, Niu DK (2006) Replication-associated strand asymmetries in vertebrate genomes and implications for replicon size, DNA replication origin, and termination. Biochem Biophys Res Commun 344(4):1258–1262PubMedCrossRefGoogle Scholar
  26. 26.
    Touchon M, Nicolay S, Arneodo A, d’Aubenton-Carafa Y, Thermes C (2003) Transcription-coupled TA and GC strand asymmetries in the human genome. FEBS Lett 555(3):579–582PubMedCrossRefGoogle Scholar
  27. 27.
    Touchon M, Arneodo A, d’Aubenton-Carafa Y, Thermes C (2004) Transcription-coupled and splicing-coupled strand asymmetries in eukaryotic genomes. Nucleic Acids Res 32(17):4969–4978PubMedCrossRefGoogle Scholar
  28. 28.
    Chamary JV, Parmley JL, Hurst LD (2006) Hearing silence: non-neutral evolution at synonymous sites in mammals. Nat Rev Genet 7(2):98–108PubMedCrossRefGoogle Scholar
  29. 29.
    Parmley JL, Chamary JV, Hurst LD (2006) Evidence for purifying selection against synonymous mutations in mammalian exonic splicing enhancers. Mol Biol Evol 23(2):301–309PubMedCrossRefGoogle Scholar
  30. 30.
    Pozzoli U, Riva L, Menozzi G, Cagliani R, Comi GP, Bresolin N, Giorda R, Sironi M (2004) Over-representation of exonic splicing enhancers in human intronless genes suggests multiple functions in mRNA processing. Biochem Biophys Res Commun 322(2):470–476PubMedCrossRefGoogle Scholar
  31. 31.
    Lobry JR (1996) A simple vectorial representation of DNA sequences for the detection of replication origins in bacteria. Biochimie 78(5):323–326PubMedCrossRefGoogle Scholar
  32. 32.
    Zhang R, Zhang C-T (2005) Identification of replication origins in archaeal genomes based on the Z-curve method. Archaea 1(5):335–346PubMedCrossRefGoogle Scholar
  33. 33.
    Lewin B (2004) Genes, VIII edn. Pearson Prentice Hall, Upper Saddle RiverGoogle Scholar
  34. 34.
    Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, Zhang J, Soden R, Hayakawa M, Kreiman G et al (2004) A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci USA 101(16):6062–6067PubMedCrossRefGoogle Scholar
  35. 35.
    Su AI, Cooke MP, Ching KA, Hakak Y, Walker JR, Wiltshire T, Orth AP, Vega RG, Sapinoso LM, Moqrich A et al (2002) Large-scale analysis of the human and mouse transcriptomes. Proc Natl Acad Sci USA 99(7):4465–4470PubMedCrossRefGoogle Scholar
  36. 36.
    Karlin S, Campbell AM, Mrazek J (1998) Comparative DNA analysis across diverse genomes. Annu Rev Genet 32:185–225PubMedCrossRefGoogle Scholar
  37. 37.
    Gierlik A, Kowalczuk M, Mackiewicz P, Dudek MR, Cebrat S (2000) Is there replication-associated mutational pressure in the Saccharomyces cerevisiae genome? J Theor Biol 202(4):305–314PubMedCrossRefGoogle Scholar
  38. 38.
    Chelly J, Concordet JP, Kaplan JC, Kahn A (1989) Illegitimate transcription: transcription of any gene in any cell type. Proc Natl Acad Sci USA 86(8): 2617–2621PubMedCrossRefGoogle Scholar
  39. 39.
    Kimoto Y (1998) A single human cell expresses all messenger ribonucleic acids: the arrow of time in a cell. Mol Gen Genet 258(3):233–239PubMedCrossRefGoogle Scholar
  40. 40.
    Sarkar G, Sommer SS (1989) Access to a messenger RNA sequence or its protein product is not limited by tissue or species specificity. Science 244(4902):331–334PubMedCrossRefGoogle Scholar
  41. 41.
    Niu D-K (2005) Low-level illegitimate transcription of genes may be to silence the genes. Biochem Biophys Res Commun 337(2):413–414PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2007

Authors and Affiliations

  1. 1.Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life SciencesBeijing Normal UniversityBeijingChina
  2. 2.National Institute of Biological SciencesBeijingChina

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