Linking the DNA strand asymmetry to the spatio-temporal replication program

I. About the role of the replication fork polarity in genome evolution
  • A. Baker
  • H. Julienne
  • C. L. Chen
  • B. Audit
  • Y. d’Aubenton-Carafa
  • C. Thermes
  • A. Arneodo
Open Access
Regular Article

Abstract

Two key cellular processes, namely transcription and replication, require the opening of the DNA double helix and act differently on the two DNA strands, generating different mutational patterns (mutational asymmetry) that may result, after long evolutionary time, in different nucleotide compositions on the two DNA strands (compositional asymmetry). We elaborate on the simplest model of neutral substitution rates that takes into account the strand asymmetries generated by the transcription and replication processes. Using perturbation theory, we then solve the time evolution of the DNA composition under strand-asymmetric substitution rates. In our minimal model, the compositional and substitutional asymmetries are predicted to decompose into a transcription- and a replication-associated components. The transcription-associated asymmetry increases in magnitude with transcription rate and changes sign with gene orientation while the replication-associated asymmetry is proportional to the replication fork polarity. These results are confirmed experimentally in the human genome, using substitution rates obtained by aligning the human and chimpanzee genomes using macaca and orangutan as outgroups, and replication fork polarity determined in the HeLa cell line as estimated from the derivative of the mean replication timing. When further investigating the dynamics of compositional skew evolution, we show that it is not at equilibrium yet and that its evolution is an extremely slow process with characteristic time scales of several hundred Myrs.

Keywords

Living systems: Structure and Function 

References

  1. 1.
    R. Berezney, D.D. Dubey, J.A. Huberman, Chromosoma 108, 471 (2000)CrossRefGoogle Scholar
  2. 2.
    D.M. Gilbert, Science 294, 96 (2001)ADSCrossRefGoogle Scholar
  3. 3.
    M. Méchali, Nat. Rev. Genet. 2, 640 (2001)CrossRefGoogle Scholar
  4. 4.
    S.P. Bell, A. Dutta, Annu. Rev. Biochem. 71, 333 (2002)CrossRefGoogle Scholar
  5. 5.
    A.J. McNairn, D.M. Gilbert, Bioessays 25, 647 (2003)CrossRefGoogle Scholar
  6. 6.
    M.I. Aladjem, Nat. Rev. Genet. 8, 588 (2007)CrossRefGoogle Scholar
  7. 7.
    S. Courbet, S. Gay, N. Arnoult, G. Wronka, M. Anglana, O. Brison, M. Debatisse, Nature 455, 557 (2008)ADSCrossRefGoogle Scholar
  8. 8.
    J.L. Hamlin, L.D. Mesner, O. Lar, R. Torres, S.V. Chodaparambil, L. Wang, J. Cell. Biochem. 105, 321 (2008)CrossRefGoogle Scholar
  9. 9.
    M. Méchali, Nat. Rev. Mol. Cell Biol. 11, 728 (2010)CrossRefGoogle Scholar
  10. 10.
    D.M. Gilbert, Nat. Rev. Genet. 11, 673 (2010)CrossRefGoogle Scholar
  11. 11.
    J.R. Lobry, Mol. Biol. Evol. 13, 660 (1996)CrossRefGoogle Scholar
  12. 12.
    J. Mrázek, S. Karlin, Proc. Natl. Acad. Sci. U.S.A. 95, 3720 (1998)ADSCrossRefGoogle Scholar
  13. 13.
    C.L. Chen, L. Duquenne, B. Audit, G. Guilbaud, A. Rappailles, A. Baker, M. Huvet, Y. d’Aubenton Carafa, O. Hyrien, A. Arneodo et al., Mol. Biol. Evol. 28, 2327 (2011)CrossRefGoogle Scholar
  14. 14.
    B. Alberts, A. Jonhson, J. Lewis, M. Raff, K. Roberts, P. Walter, Molecular Biology of the Cell, 5th edition (Garland Publishing, New York, 2008)Google Scholar
  15. 15.
    M.L. DePamphilis (Editor), DNA Replication and Human Disease (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 2006)Google Scholar
  16. 16.
    B. Audit, S. Nicolay, M. Huvet, M. Touchon, Y. d’Aubenton-Carafa, C. Thermes, A. Arneodo, Phys. Rev. Lett. 99, 248102 (2007)ADSCrossRefGoogle Scholar
  17. 17.
    A. Baker, B. Audit, C. Chen, B. Moindrot, A. Leleu, G. Guilbaud, A. Rappailles, C. Vaillant, A. Goldar, F. Mongelard et al., PLoS Comput. Biol. 8, e1002443 (2012)CrossRefGoogle Scholar
  18. 18.
    M. Touchon, S. Nicolay, B. Audit, E.B. Brodie of Brodie, Y. d’Aubenton-Carafa, A. Arneodo, C. Thermes, Proc. Natl. Acad. Sci. U.S.A. 102, 9836 (2005)ADSCrossRefGoogle Scholar
  19. 19.
    E.B. Brodie of Brodie, S. Nicolay, M. Touchon, B. Audit, Y. d’Aubenton-Carafa, C. Thermes, A. Arneodo, Phys. Rev. Lett. 94, 248103 (2005)ADSCrossRefGoogle Scholar
  20. 20.
    S. Nicolay, PhD Thesis, University of Liège, Belgium (2006)Google Scholar
  21. 21.
    M. Huvet, S. Nicolay, M. Touchon, B. Audit, Y. d’Aubenton-Carafa, A. Arneodo, C. Thermes, Genome Res. 17, 1278 (2007)CrossRefGoogle Scholar
  22. 22.
    B. Audit, L. Zaghloul, C. Vaillant, G. Chevereau, Y. d’Aubenton Carafa, C. Thermes, A. Arneodo, Nucl. Acids Res. 37, 6064 (2009)CrossRefGoogle Scholar
  23. 23.
    C. Lemaitre, L. Zaghloul, M.F. Sagot, C. Gautier, A. Arneodo, E. Tannier, B. Audit, BMC Genomics 10, 335 (2009)CrossRefGoogle Scholar
  24. 24.
    L. Zaghloul, PhD Thesis, ENS de Lyon, France (2009)Google Scholar
  25. 25.
    R.S. Hansen, S. Thomas, R. Sandstrom, T.K. Canfield, R.E. Thurman, M. Weaver, M.O. Dorschner, S.M. Gartler, J.A. Stamatoyannopoulos, Proc. Natl. Acad. Sci. U.S.A. 107, 139 (2010)ADSCrossRefGoogle Scholar
  26. 26.
    M. Touchon, S. Nicolay, A. Arneodo, Y. d’Aubenton-Carafa, C. Thermes, FEBS Lett. 555, 579 (2003)CrossRefGoogle Scholar
  27. 27.
    M. Touchon, A. Arneodo, Y. d’Aubenton-Carafa, C. Thermes, Nucl. Acids Res. 32, 4969 (2004)CrossRefGoogle Scholar
  28. 28.
    C.L. Chen, A. Rappailles, L. Duquenne, M. Huvet, G. Guilbaud, L. Farinelli, B. Audit, Y. d’Aubenton-Carafa, A. Arneodo, O. Hyrien et al., Genome Res. 20, 447 (2010)CrossRefGoogle Scholar
  29. 29.
    G. Guilbaud, A. Rappailles, A. Baker, C.L. Chen, A. Arneodo, A. Goldar, Y. d’Aubenton-Carafa, C. Thermes, B. Audit, O. Hyrien, PLoS Comput. Biol. 7, e1002322 (2011)CrossRefGoogle Scholar
  30. 30.
    N. Sueoka, J. Mol. Evol. 40, 318 (1995)CrossRefGoogle Scholar
  31. 31.
    R. Rudner, J.D. Karkas, E. Chargaff, Proc. Natl. Acad. Sci. U.S.A. 60, 921 (1968)ADSCrossRefGoogle Scholar
  32. 32.
    J.R. Lobry, J. Mol. Evol. 40, 326 (1995)CrossRefGoogle Scholar
  33. 33.
    J.R. Lobry, C. Lobry, Mol. Biol. Evol. 16, 719 (1999)CrossRefGoogle Scholar
  34. 34.
    A. Arneodo, C. Vaillant, B. Audit, F. Argoul, Y. d’Aubenton-Carafa, C. Thermes, Phys. Rep. 498, 45 (2011)ADSCrossRefGoogle Scholar
  35. 35.
    M.P. Francino, H. Ochman, Trends Genet 13, 240 (1997)CrossRefGoogle Scholar
  36. 36.
    A.C. Frank, J.R. Lobry, Gene 238, 65 (1999)CrossRefGoogle Scholar
  37. 37.
    M.P. Francino, H. Ochman, Mol. Biol. Evol. 18, 1147 (2001)CrossRefGoogle Scholar
  38. 38.
    P. Green, B. Ewing, W. Miller, P.J. Thomas, E.D. Green, Nat. Genet. 33, 514 (2003)CrossRefGoogle Scholar
  39. 39.
    P. Polak, P.F. Arndt, Genome Res. 18, 1216 (2008)CrossRefGoogle Scholar
  40. 40.
    C.F. Mugal, H.H. von Grunberg, M. Peifer, Mol. Biol. Evol. 26, 131 (2009)CrossRefGoogle Scholar
  41. 41.
    A. Beletskii, A.S. Bhagwat, Proc. Natl. Acad. Sci. U.S.A. 93, 13919 (1996)ADSCrossRefGoogle Scholar
  42. 42.
    A. Beletskii, A.S. Bhagwat, Biol. Chem. 379, 549 (1998)Google Scholar
  43. 43.
    M.P. Francino, L. Chao, M.A. Riley, H. Ochman, Science 272, 107 (1996)ADSCrossRefGoogle Scholar
  44. 44.
    J.Q. Svejstrup, Nat. Rev. Mol. Cell Biol. 3, 21 (2002)CrossRefGoogle Scholar
  45. 45.
    S. Nicolay, F. Argoul, M. Touchon, Y. d’Aubenton-Carafa, C. Thermes, A. Arneodo, Phys. Rev. Lett. 93, 108101 (2004)ADSCrossRefGoogle Scholar
  46. 46.
    S. Nicolay, E.B. Brodie of Brodie, M. Touchon, B. Audit, Y. d’Aubenton-Carafa, C. Thermes, A. Arneodo, Phys. Rev. E 75, 032902 (2007)ADSCrossRefGoogle Scholar
  47. 47.
    E.P. Rocha, A. Danchin, A. Viari, Mol. Microbiol. 32, 11 (1999)CrossRefGoogle Scholar
  48. 48.
    E.P.C. Rocha, M. Touchon, E.J. Feil, Genome Res. 16, 1537 (2006)CrossRefGoogle Scholar
  49. 49.
    P. Polak, P.F. Arndt, Genome Biol. Evol. 1, 189 (2009)CrossRefGoogle Scholar
  50. 50.
    T.A. Kunkel, P.M. Burgers, Trends Cell Biol. 18, 521 (2008)CrossRefGoogle Scholar
  51. 51.
    J.R. Lobry, Science 272, 745 (1996)ADSCrossRefGoogle Scholar
  52. 52.
    E.R. Tillier, R.A. Collins, J. Mol. Evol. 50, 249 (2000)Google Scholar
  53. 53.
    A. Grigoriev, Virus Res. 60, 1 (1999)CrossRefGoogle Scholar
  54. 54.
    A. Gierlik, M. Kowalczuk, P. Mackiewicz, M.R. Dudek, S. Cebrat, J. Theor. Biol. 202, 305 (2000)CrossRefGoogle Scholar
  55. 55.
    A. Reyes, C. Gissi, G. Pesole, C. Saccone, Mol. Biol. Evol. 15, 957 (1998)CrossRefGoogle Scholar
  56. 56.
    M.C. Marsolier-Kergoat, A. Goldar, Mol. Biol. Evol. 29, 893 (2012)CrossRefGoogle Scholar
  57. 57.
    F. Jacob, S. Brenner, F. Cuzin, Cold Spring Harb. Symp. Quant. Biol. 28, 329 (1963)CrossRefGoogle Scholar
  58. 58.
    D. Graur, W.H. Li, Fundamentals of Molecular Evolution (Sinauer Associates, Sunderland, MA, 1999)Google Scholar
  59. 59.
    M. Kimura, Nature 217, 624 (1968)ADSCrossRefGoogle Scholar
  60. 60.
    N. Galtier, G. Piganeau, D. Mouchiroud, L. Duret, Genetics 159, 907 (2001)Google Scholar
  61. 61.
    L. Duret, P.F. Arndt, PLoS Genet. 4, e1000071 (2008)CrossRefGoogle Scholar
  62. 62.
    L. Duret, N. Galtier, Annu. Rev. Genomics Hum. Genet. 10, 285 (2009)CrossRefGoogle Scholar
  63. 63.
    The ENCODE Project Consortium, Nature 447, 799 (2007)ADSCrossRefGoogle Scholar
  64. 64.
    J. Cheng, P. Kapranov, J. Drenkow, S. Dike, S. Brubaker, S. Patel, J. Long, D. Stern, H. Tammana, G. Helt et al., Science 308, 1149 (2005)ADSCrossRefGoogle Scholar
  65. 65.
    L.J. Core, J.J. Waterfall, J.T. Lis, Science 322, 1845 (2008)ADSCrossRefGoogle Scholar
  66. 66.
    Y. He, B. Vogelstein, V.E. Velculescu, N. Papadopoulos, K.W. Kinzler, Science 322, 1855 (2008)ADSCrossRefGoogle Scholar
  67. 67.
    P. Preker, J. Nielsen, S. Kammler, S. Lykke-Andersen, M.S. Christensen, C.K. Mapendano, M.H. Schierup, T.H. Jensen, Science 322, 1851 (2008)ADSCrossRefGoogle Scholar
  68. 68.
    A.C. Seila, J.M. Calabrese, S.S. Levine, G.W. Yeo, P.B. Rahl, R.A. Flynn, R.A. Young, P.A. Sharp, Science 322, 1849 (2008)ADSCrossRefGoogle Scholar
  69. 69.
    A. Necsulea, C. Guillet, J.C. Cadoret, M.N. Prioleau, L. Duret, Mol. Biol. Evol. 26, 729 (2009)CrossRefGoogle Scholar
  70. 70.
    A. Baker, PhD Thesis, University of Lyon, France (2011)Google Scholar
  71. 71.
    L.A. Frederico, T.A. Kunkel, B.R. Shaw, Biochemistry 29, 2532 (1990)CrossRefGoogle Scholar
  72. 72.
    J.A. Stamatoyannopoulos, I. Adzhubei, R.E. Thurman, G.V. Kryukov, S.M. Mirkin, S.R. Sunyaev, Nat. Genet. 41, 393 (2009)CrossRefGoogle Scholar
  73. 73.
    C.F. Mugal, J.B.W. Wolf, H.H. von Grunberg, H. Ellegren, Genome Biol. Evol. 2, 19 (2010)CrossRefGoogle Scholar
  74. 74.
    C.L. Chen, A. Baker, B. Audit, Y. d’Aubenton-Carafa, A. Arneodo, C. Thermes, in preparation (2012).Google Scholar
  75. 75.
    N. Van Kampen, Stochastic Processes in Physics and Chemistry, 3rd edition (North-Holland, Amsterdam, 2007)Google Scholar
  76. 76.
    T. Ryba, I. Hiratani, J. Lu, M. Itoh, M. Kulik, J. Zhang, T.C. Schulz, A.J. Robins, S. Dalton, D.M. Gilbert, Genome Res. 20, 761 (2010)CrossRefGoogle Scholar
  77. 77.
    E. Yaffe, S. Farkash-Amar, A. Polten, Z. Yakhini, A. Tanay, I. Simon, PLoS Genet. 6, e1001011 (2010)CrossRefGoogle Scholar
  78. 78.
    A. Baker, S. Nicolay, L. Zaghloul, Y. d’Aubenton-Carafa, C. Thermes, B. Audit, A. Arneodo, Appl. Comput. Harmon. Annal. 28, 150 (2010)MathSciNetMATHCrossRefGoogle Scholar
  79. 79.
    G. McVicker, P. Green, Genome Res. 20, 1503 (2010)CrossRefGoogle Scholar
  80. 80.
    J. Majewski, Am. J. Hum. Genet. 73, 688 (2003)CrossRefGoogle Scholar
  81. 81.
    J.M. Comeron, Genetics 167, 1293 (2004)CrossRefGoogle Scholar
  82. 82.
    L. Duret, Curr. Opin. Genet. Dev. 12, 640 (2002)CrossRefGoogle Scholar
  83. 83.
    D. Karolchik, R. Baertsch, M. Diekhans, T.S. Furey, A. Hinrichs, Y.T. Lu, K.M. Roskin, M. Schwartz, C.W. Sugnet, D.J. Thomas et al., Nucl. Acids Res. 31, 51 (2003)CrossRefGoogle Scholar
  84. 84.
    M.M. Suzuki, A. Bird, Nat. Rev. Genet. 9, 465 (2008)CrossRefGoogle Scholar
  85. 85.
    S.T. Hess, J.D. Blake, R.D. Blake, J. Mol. Biol. 236, 1022 (1994)CrossRefGoogle Scholar
  86. 86.
    P.F. Arndt, T. Hwa, Bioinformatics 21, 2322 (2005)CrossRefGoogle Scholar

Copyright information

© The Author(s) 2012

Authors and Affiliations

  • A. Baker
    • 1
    • 2
  • H. Julienne
    • 1
    • 2
  • C. L. Chen
    • 3
  • B. Audit
    • 1
    • 2
  • Y. d’Aubenton-Carafa
    • 3
  • C. Thermes
    • 3
  • A. Arneodo
    • 1
    • 2
  1. 1.Université de LyonLyonFrance
  2. 2.Laboratoire de PhysiqueENS Lyon, CNRSLyonFrance
  3. 3.Centre de Génétique MoléculaireCNRSGif-sur-YvetteFrance

Personalised recommendations