MBE Advance Access published online on June 19, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn136
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RESEARCH ARTICLE |
Evolution of closely linked gene pairs in vertebrate genomes
a Biomolecular Chemistry, 271 NCMLS, Radboud University Nijmegen, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands
b Centre for Molecular and Biomolecular Informatics, NCMLS, Radboud University Nijmegen Medical Centre, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands
c Current address: Animal Breeding and Genetics Group, University of Wageningen, P.O. Box 338, 6700 AH, Wageningen, The Netherlands
* corresponding author: Biomolecular Chemistry, 271 NCMLS, Radboud University Nijmegen, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands. Email: N.Lubsen{at}science.ru.nl. Tel.: +31-24-3616850; FAX: +31-24-3540525
Received for publication January 11, 2008. Revision received June 11, 2008. Accepted for publication June 12, 2008.
The orientation of closely linked genes in mammalian genomes is not random: there are more head-to-head (h2h) gene pairs than expected. To understand the origin of this enrichment in h2h gene pairs, we have analyzed the phylogenetic distribution of gene pairs separated by less than 600 bp of intergenic DNA ("gene duos"). We show here that a lack of head-to-tail (h2t) gene duos is an even more distinctive characteristic of mammalian genomes, with the platypus genome as the only exception. In non-mammalian vertebrate and in non-vertebrate genomes the frequency of h2h, h2t and tail-to-tail (t2t) gene duos is close to random. In tetrapod genomes the h2t and t2t gene duos are more likely to be part of a larger gene cluster of closely spaced genes than h2h gene duos; in fish and urochordate genomes the reverse is seen. In human and mouse tissues the expression profiles of gene duos were skewed toward positive co-expression, irrespective of orientation. The organization of orthologs of both members of about 40% of the human gene duos could be traced in other species, enabling a prediction of the organization at the branch points of gnathostomes, tetrapods, amniotes and euarchontoglires. The accumulation of h2h gene duos started in tetrapods, while that of h2t and t2t gene duos only started in amniotes. The apparent lack of evolutionary conservation of h2t and t2t gene duos relative to that of h2h gene duos is thus a result of their relatively late origin in the lineage leading to mammals; we show that once they are formed h2t and t2t gene duos are as stable as h2h gene duos.
Key Words: head-to-head gene • bidirectional promoter • coordinate expression
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