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Nucleic Acids Research 2005 33(10):3224-3234; doi:10.1093/nar/gki638
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Published online 7 June 2005

© The Author 2005. Published by Oxford University Press. All rights reserved
The online version of this article has been published under an open access model. Users are entitled to use, reproduce, disseminate, or display the open access version of this article for non-commercial purposes provided that: the original authorship is properly and fully attributed; the Journal and Oxford University Press are attributed as the original place of publication with the correct citation details given; if an article is subsequently reproduced or disseminated not in its entirety but only in part or as a derivative work this must be clearly indicated. For commercial re-use, please contact journals.permissions{at}oupjournals.org

Article

Interruptions in gene expression drive highly expressed operons to the leading strand of DNA replication

Morgan N. Price1, Eric J. Alm1,* and Adam P. Arkin1,2,3

1Lawrence Berkeley National Lab 1 Cyclotron Road, Mailstop 977-152, Berkeley, CA 94720, USA 2Howard Hughes Medical Institute Berkeley CA, USA 3Department of Bioengineering, University of California Berkeley CA, USA

*To whom correspondence should be addressed. Tel: +1 510 486 6899; Fax: +1 510 486 6219; Email: ejalm{at}lbl.gov

Received February 24, 2005. Revised April 22, 2005. Accepted May 16, 2005.

In bacteria, most genes are on the leading strand of replication, a phenomenon attributed to collisions between the DNA and RNA polymerases. In Escherichia coli, these collisions slow the movement of the replication fork through actively transcribed genes only if they are coded on the lagging strand. For genes on both strands, however, these collisions sever nascent transcripts and interrupt gene expression. Based on these observations, we propose a new theory to explain strand bias: genes whose expression is important for fitness are selected to the leading strand because this reduces the duration of these interruptions. Our theory predicts that multi-gene operons, which are subject to longer interruptions, should be more strongly selected to the leading strand than singleton transcripts. We show that this is true even after controlling for the tendency for essential genes, which are strongly biased to the leading strand, to occur in operons. Our theory also predicts that other factors that are associated with strand bias should have stronger effects for genes that are in operons. We find that expression level and phylogenetic ubiquity are correlated with strand bias for both essential and non-essential genes, but only for genes in operons.


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