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MBE Advance Access originally published online on January 6, 2009
Molecular Biology and Evolution 2009 26(4):729-741; doi:10.1093/molbev/msn303
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© The Author 2009. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Research Articles

The Relationship between DNA Replication and Human Genome Organization

Anamaria Necsulea*, Claire Guillet*, Jean-Charles Cadoret{dagger}, Marie-Noëlle Prioleau{dagger} and Laurent Duret*

* Université de Lyon, Lyon; Université Lyon 1; CNRS, UMR 5558, Laboratoire de Biométrie et Biologie Évolutive, Villeurbanne, France; HELIX, Unité de recherche INRIA
{dagger} Institut Jacques Monod, CNRS, Université Paris7, Université Pierre et Marie Curie, Paris, France

E-mail: duret{at}biomserv.univ-lyon1.fr.

Accepted for publication December 22, 2008.

Assessment of the impact of DNA replication on genome architecture in Eukaryotes has long been hampered by the scarcity of experimental data. Recent work, relying on computational predictions of origins of replication, suggested that replication might be a major determinant of gene organization in human (Huvet et al. 2007. Human gene organization driven by the coordination of replication and transcription. Genome Res. 17:1278–1285). Here, we address this question by analyzing the first large-scale data set of experimentally determined origins of replication in human: 283 origins identified in HeLa cells, in 1% of the genome covered by ENCODE regions (Cadoret et al. 2008. Genome-wide studies highlight indirect links between human replication origins and gene regulation. Proc Natl Acad Sci USA. 105:15837–15842). We show that origins of replication are not randomly distributed as they display significant overlap with promoter regions and CpG islands. The hypothesis of a selective pressure to avoid frontal collisions between replication and transcription polymerases is not supported by experimental data as we find no evidence for gene orientation bias in the proximity of origins of replication. The lack of a significant orientation bias remains manifest even when considering only genes expressed at a high rate, or in a wide number of tissues, and is not affected by the regional replication timing. Gene expression breadth does not appear to be correlated with the distance from the origins of replication. We conclude that the impact of DNA replication on human genome organization is considerably weaker than previously proposed.

Key Words: origin of replication • genome organization • transcription • nucleotide composition • polymerase collision

Aoife McLysaght, Associate Editor


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