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MBE Advance Access published online on January 6, 2009
Molecular Biology and Evolution, 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 Article

The relationship between DNA replication and human genome organization

Anamaria Necsulea1, Claire Guillet1, Jean-Charles Cadoret2, Marie-Noëlle Prioleau2 and Laurent Duret1

1 Université de Lyon, F-69000, Lyon; Université Lyon 1; CNRS, UMR 5558, Laboratoire de Biométrie et Biologie Évolutive, F-69622, Villeurbanne, France; HELIX, Unité de recherche INRIA
2 Institut Jacques Monod, CNRS, Université Paris7, Université Pierre et Marie Curie, 75005 Paris, France

Laurent Duret (duret{at}biomserv.univ-lyon1.fr), Laboratoire de Biométrie et Biologie Évolutive, Université Claude Bernard Lyon 1, 43 Bd. du 11 Novembre 1918, Bâtiment Gregor Mendel, 69622 Villeurbanne CEDEX, FRANCE, Phone: +33 (0)4 72 44 62 97, Fax: +33 (0)4 72 43 13 88

Received for publication November 7, 2008. Revision received December 16, 2008. 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). Here, we address this question by analyzing the first large-scale dataset 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). 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


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