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Toward a General Model for the Evolution of DNA Replication in Three Domains of Life

Published online by Cambridge University Press:  28 May 2014

R. Retkute
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Abstract

Nothing is more fundamental to life than the ability to reproduce and duplicate the information cells store in their genomes. The mechanism of duplication of DNA has been conserved from prokaryotes to eukaryotes. The aim of the study was to quantify which evolutionary forces could produce the pattern of genome replication architecture observed in present-day organisms. This was achieved using an evolutionary simulation, combining random genome sequence shuffling, mutation, selection and the mathematical modeling of DNA replication. We have found parameter values which explained evolutionary pressures of DNA replication in E.coli, P.calidifontis and S. cerevisae. Surprisingly, the results of the evolutionary simulation suggests that for a fixed cost per replication origin it is more advantageous for genomes to reduce the number of replication origins under increasing uncertainty in origin activation timing.

Keywords

DNA replicationmodeling biological evolutionmutationselectionfitness
Type
Research Article
Information
Mathematical Modelling of Natural Phenomena , Volume 9 , Issue 3: Biological evolution , 2014 , pp. 96 - 106
Copyright
© EDP Sciences, 2014

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References

Baker, A., Audit, B., Yang, S. C. H., Bechhoefer, J., Arneodo, A.. Inferring Where and When Replication Initiates from Genome-Wide Replication Timing Data. Phys. Rev. Let., 108 (2012), 268101, 1–5. CrossRefGoogle ScholarPubMed
Baker, A., Chen, C. L., Julienne, H., Audit, B., dÕAubenton-Carafa, Y., Thermes, C., Arneodo, A.. Linking the DNA strand asymmetry to the spatio-temporal replication program I. About the role of the replication fork polarity in genome evolution. Europ. Phys. J. E, 35 (2012), 92, 1–25. Google Scholar
Baker, A., Julienne, H., Chen, C. L., Audit, B., dÕAubenton-Carafa, Y., Thermes, C., Arneodo, A.. Linking the DNA strand asymmetry to the spatio-temporal replication program II. Accounting for neighbor-dependent substitution rates. Europ. Phys. J. E, 35 (2012), 123, 1–12. Google Scholar
Bechhoefer, J., Rhind, N.. Replication timing and its emergence from stochastic processes. Tren. in Gen., 28 (2012), 374–381. CrossRefGoogle ScholarPubMed
Besnard, E., Babied, A., Lapasset, L., Milhavet, O., Parrinello, H., Dantec, C., Marin, J. M., Lemaitre, J.M.. Unraveling cell type-specific and reprogrammable human replication origin signatures associated with G-quadruplex consensus motifs. Nat. Struct. & Mol. Biol., 19 (2012), 837–844. CrossRefGoogle ScholarPubMed
Brodie of Brodie, E.B., Nicolay, S., Touchon, M., Audit, B., d’Aubenton-Carafa, Y., Thermes, C., Arneodo, A.. From DNA sequence analysis to modeling replication in the human genome. Phys. Rev. Let., 94 (2005), 248103, 1–4. CrossRefGoogle ScholarPubMed
Cayrou, C., Coulombe, P., Vigneron, A., Stanojcic, S., Ganier, O., Peiffer, I., Puy, A., Laurent-Chabalier, S., Desprat, R., Mechali, M.. Genome-scale analysis of metazoan replication origins reveals their organization in specific but flexible sites defined by conserved features. Gen. Res., 21 (2011), 1438–1449. CrossRefGoogle ScholarPubMed
Cayrou, C., Coulombe, P., Puy, A., Rialle, S., Kaplan, N., Segal, E., Mechali, M.. New insights into replication origin characteristics in metazoans. Cell Cycl., 11 (2012), 658–667. CrossRefGoogle ScholarPubMed
Clement, Y., Arndt, P. F.. Meiotic Recombination Strongly Influences GC-Content Evolution in Short Regions in the Mouse Genome. Mol. Biol. & Evol., 30 (2013), 2612–2618. CrossRefGoogle Scholar
Costas, C., Sanchez, M. D., Stroud, H., Yu, Y., Oliveros, J. C., Feng, S., Benguria, A., Lopez-Vidriero, I., Zhang, X., Solano, R., Jacobsen, S. E., Gutierrez, C.. Genome-wide mapping of Arabidopsis thaliana origins of DNA replication and their associated epigenetic marks. Nat. Struct. & Mol. Biol., 18 (2011), 395–U190. CrossRefGoogle ScholarPubMed
Donley, N., Thayer, M. J.. DNA replication timing, genome stability and cancer. Late and/or delayed DNA replication timing is associated with increased genomic instability. Sem. in Canc. Biol., 23 (2013), 80–89. CrossRefGoogle Scholar
de Moura, A. P. S., Retkute, R., Hawkins, M., Nieduszynski, C. A.. Mathematical modelling of whole chromosome replication. NAR, 38 (2010), 5623–5633. CrossRefGoogle Scholar
dos Reis, M., Wernisch, L.. Estimating Translational Selection in Eukaryotic Genomes. Mol. Biol. & Evol., 26 (2009), 451–461. CrossRefGoogle Scholar
Gao, F., Luo, H., Zhang, C. T.. DeOri: a database of eukaryotic DNA replication origins. Bioinformatics, 28 (2012), 1551–1552. CrossRefGoogle ScholarPubMed
Gao, F., Luo, H., Zhang, C. T.. DoriC 5.0: an updated database of oriC regions in both bacterial and archaeal genomes. NAR, 41 (2013), 90–93. CrossRefGoogle ScholarPubMed
Gauthier, M. G., Norio, P., Bechhoefer, J.. Modeling Inhomogeneous DNA Replication Kinetics, PLoS one, 7 (2012), e32053-1–13. CrossRefGoogle ScholarPubMed
Gierlik, A., Kowalczuk, M., Mackiewicz, P., Dudek, M. R., Cebrat, S.. Is there replication-associated mutational pressure in the Saccharomyces cerevisiae genome?. J. Theor. Biol., 202 (2000), 305–314. CrossRefGoogle Scholar
Green, P., Ewing, B., Miller, W., Thomas, P., Green, E.. Transcription-associated mutational asymmetry in mammalian evolution. Nat. Gen., 33 (2003), 14–517. CrossRefGoogle ScholarPubMed
Hayashi, M., Katou, Y., Itoh, T., Tazumi, M., Yamada, Y., Takahashi, T., Nakagawa, T., Shirahige, K., Masukata, H.. Genome-wide localization of pre-RC sites and identification of replication origins in fission yeast. EMBO J., 26 (2007), 1327–1339. CrossRefGoogle ScholarPubMed
Hyrien, O., Rappailles, A., Guilbaud, G., Baker, A., Chen, C. L., Goldar, A., Petryk, N., Kahli, M., Ma, E., d’Aubenton-Carafa, Y., Audit, B., Thermes, C., Arneodo, A.. From Simple Bacterial and Archaeal Replicons to Replication N/U-Domains. J. Mol. Biol., 425 (2013), 4673–89. CrossRefGoogle ScholarPubMed
Kellis, M., Birren, B. W., Lander, E. S.. Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature, 428 (2008), 617–624. CrossRefGoogle Scholar
M. L. DePamphilis. DNA replication and human disease. Cold Spring Harbor monograph series.
Lang, G. I., Murray, A. W.. Mutation Rates across Budding Yeast Chromosome VI Are Correlated with Replication Timing. Gen. Biol. & Evol., 3 (2011), 799–811. CrossRefGoogle ScholarPubMed
Leonard, A. C., Mechali, M.. DNA Replication Origins. Cold Spring Harbor Persp. Biol., 5 (2013), a010116, 1–18. Google ScholarPubMed
Liachko, I., Bhaskar, A., Lee, C., Chung, S. C. C., Tye, B. K., Keich, U.. A Comprehensive genome-wide map of autonomously replicating sequences in a naive genome. PLoS Gen., 6 (2010), e1000946, 1–12. CrossRefGoogle Scholar
Liu, L., De, S., Michor, F.. DNA replication timing and higher-order nuclear organization determine single-nucleotide substitution patterns in cancer genomes. Nat. Comm., 4 (2013), 1502, 1–10. Google ScholarPubMed
Lundgren, M., Andersson, A., Chen, L. M., Nilsson, P., Bernander, R.. Three replication origins in Sulfolobus species: Synchronous initiation of chromosome replication and asynchronous termination. PNAS, 101 (2004), 7046–7051. CrossRefGoogle ScholarPubMed
Luo, H. E., Li, J. T., Eshaghi, M., Liu, J. H., Karuturi, R. K. M.. Genome-wide estimation of firing efficiencies of origins of DNA replication from time-course copy number variation data. BMC Bioinf., 11 (2010), 1–15. CrossRefGoogle ScholarPubMed
Lygeros, J., Koutroumpas, K., Dimopoulos, S., Legouras, I., Kouretas, P., Heichinger, C., Nurse, P., Lygerou, Z.. Stochastic hybrid modeling of DNA replication across a complete genome. PNAS, 105 (2008), 12295–12300. CrossRefGoogle ScholarPubMed
M. Lynch. The origins of the genome architecture. Sinauer Associates Inc Publishers, Massachusetts.
Lynch, M.. Evolution of the mutation rate. Tr. Gen., 26 (2010), 345–52. CrossRefGoogle ScholarPubMed
McGeoch, A. T., Bell, S.D.. Extra-chromosomal elements and the evolution of cellular DNA replication machineries. Nat. Rev. Mol. Cell Biol., 9 (2008), 569–574. CrossRefGoogle ScholarPubMed
Mechali, M., Yoshida, K., Coulombe, P., Pasero, P.. Genetic and epigenetic determinants of DNA replication origins, position and activation. Curr. Op. Gen., & Dev., 23 (2013), 124–31. CrossRefGoogle ScholarPubMed
Muller, C. A., Nieduszynski, C. A.. Conservation of replication timing reveals global and local regulation of replication origin activity. Gen. Res., 22 (2012), 1953–1962. CrossRefGoogle Scholar
Nowak, M. A., Ohtsuki, H.. Prevolutionary dynamics and the origin of evolution. PNAS, 105 (2008), 14924–14927. CrossRefGoogle Scholar
S.Ohno. Evolution by Gene Duplication. Springer-Verlag, London.
Pelve, E. A., Lindas, A. C., Knoppel, A., Mira, A., Bernander, R.. Four chromosome replication origins in the archaeon Pyrobaculum calidifontis. Mol. Microbiol., 85 (2012), 986–995. CrossRefGoogle Scholar
Pohl, T. J., Kolor, K., Fangman, W. L., Brewer, B. J., Raghuraman, M. K.. A DNA Sequence Element That Advances Replication Origin Activation Time in Saccharomyces cerevisiae. G3, 3 (2013), 1955–1963. CrossRefGoogle ScholarPubMed
Pope, B. D., Gilbert, D. M.. The Replication Domain Model: Regulating Replicon Firing in the Context of Large-Scale Chromosome Architecture. J. Mol. Biol., 425 (2013), 4690–4695. CrossRefGoogle Scholar
Prendergast, J. G. D., Campbell, H., Gilbert, N., Dunlop, M. G., Bickmore, W. A., Semple, C. A. M.. Chromatin structure and evolution in the human genome. BMC Evol. Biol., 7 (2007), 1–12. CrossRefGoogle ScholarPubMed
Rocha, E. P. C.. The Organization of the Bacterial Genome. Ann. Rev. Gen., 42 (2008), 211–233. CrossRefGoogle ScholarPubMed
Robinson, N. P., Bell, S. D.. Origins of DNA replication in the three domains of life. FEBS J., 272 (2005), 3757–3766. CrossRefGoogle ScholarPubMed
Siow, C. C., Nieduszynska, S. R., Muller, C. A., Nieduszynski, C. A.. OriDB, the DNA replication origin database updated and extended. NAR, 40 (2012), D682–D686. CrossRefGoogle Scholar
Skarstad, K., Steen, H. B., Boye, E.. Cell Cycle Parameters of Slowly Growing Escherichia coli B/r Studied by Flow Cytometry. J. Bacteriol., 124 (1983), 656–662. Google Scholar
Skovgaard, O., Bak, M., Lobner-Olesen, A., Tommerup, N.. Genome-wide detection of chromosomal rearrangements, indels, and mutations in circular chromosomes by short read sequencing. Gen. Res., 21 (2011), 1388–1393. CrossRefGoogle Scholar
Srivatsan, A., Tehranchi, A., MacAlpine, D. M., Wang, J. D.. Co-Orientation of Replication and Transcription Preserves Genome Integrity. PLoS Gen., 6 (2010), e1000810, 1–14. CrossRefGoogle ScholarPubMed
Stamatoyannopoulos, J. A., Adzhubei, I., Thurman, R. E., Kryukov, G. V., Mirkin, S. M., Sunyaev, S. R.. Human mutation rate associated with DNA replication timing. Nat. Gen., 41 (2009), 393–395. CrossRefGoogle Scholar
Tatarinova, T., Elhaik, E., Pellegrini, M.. Cross-Species Analysis of Genic GC(3) Content and DNA Methylation Patterns. Gen. Biol. & Evol., 5 (2013), 1443–1456. CrossRefGoogle Scholar
Yaffe, E., Farkash-Amar, S., Polten, A., Yakhini, Z., Tanay, A., Simon, I.. Comparative Analysis of DNA Replication Timing Reveals Conserved Large-Scale Chromosomal Architecture. PLoS Gen., 6 (2010), e1001011, 1–12. CrossRefGoogle ScholarPubMed
Yang, S. C. H., Rhind, N., Bechhoefer, J.. Modeling genome-wide replication kinetics reveals a mechanism for regulation of replication timing. Mol. Syst. Biol., 6 (2012), 404, 1–13. Google Scholar
Weber, C. C., Pink, C. J., Hurst, L. D.. Late-Replicating Domains Have Higher Divergence and Diversity in Drosophila melanogaster. Mol. Biol. & Evol., 29 (2012), 873–882. CrossRefGoogle ScholarPubMed
Worning, P., Jensen, L. J., Hallin, P. H., Staerfeldt, H. H., Ussery, D. W.. Origin of replication in circular prokaryotic chromosomes. Env. Biol., 8 (2006), 353–361. Google ScholarPubMed
Wu, Z., Liu, H., Hailong, , Liu, J., Liu, X. Q., Xiang, H.. Diversity and evolution of multiple orc/cdc6-adjacent replication origins in haloarchaea. BMC Gen., 13 (2012), 1–16. CrossRefGoogle ScholarPubMed