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MBE Advance Access published online on April 24, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn101
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© The Author 2008. 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

Co-expression of Linked Genes in Mammalian Genomes is Generally Disadvantageous

Ben-Yang Liao and Jianzhi Zhang*

Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA

* Correspondence to: Jianzhi Zhang, Department of Ecology and Evolutionary Biology ,University of Michigan, 1075 Natural Science Building, 830 North University Avenue, Ann Arbor, MI 48109, Phone: 734-763-0527, Fax: 734-763-0544, Email: jianzhi{at}umich.edu

Received for publication February 8, 2008. Revision received March 23, 2008. Accepted for publication April 19, 2008.

Similarity in gene expression pattern between closely linked genes is known in several eukaryotes. Two models have been proposed to explain the presence of such co-expression patterns. The adaptive model assumes that co-expression is advantageous and is established by relocation of initially unlinked but co-expressed genes, whereas the neutral model asserts that co-expression is a type of leaky expression due to similar expressional environments of linked genes, but is neither advantageous nor detrimental. However, these models are incompatible with several empirical observations. Here, we propose that co-expression of linked genes is a form of transcriptional interference that is disadvantageous to the organism. We show that even distantly linked genes that are tens of megabases away exhibit significant co-expression in the human genome. However, the linkage is more likely to be broken during evolution between genes of high co-expression than those of low co-expression and the breakage of linkage reduces gene co-expression. These results support our hypothesis that co-expression of linked genes in mammalian genomes is generally disadvantageous, implying that many mammalian genes may never reach their optimal expression pattern due to the interference of their genomic environment and that such transcriptional interference may be a force promoting recurrent relocation of genes in the genome.

Key Words: gene order • linkage • gene expression • co-expression • evolution • mammals


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