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Selective maintenance of Drosophila tandemly arranged duplicated genes during evolution

Carlos Quijano12, Pavel Tomancak3, Jesus Lopez-Marti2, Mikita Suyama48, Peer Bork4, Marco Milan5, David Torrents46* and Miguel Manzanares17*

Author Affiliations

1 Instituto de Investigaciones Biomédicas CSIC-UAM, Arturo Duperier 4, 28029 Madrid, Spain

2 Barcelona Supercomputing Center, Jordi Girona 31, 08034 Barcelona, Spain

3 Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, D-01307 Dresden, Germany

4 European Molecular Biology Laboratory, Meyerhofstrasse 1, 69117 Heidelberg, Germany

5 ICREA and Institute for Research in Biomedicine (IRB), Parc Científic de Barcelona, Josep Samitier 1-5, 08028 Barcelona, Spain

6 ICREA and Barcelona Supercomputing Center, Jordi Girona 31, 08034 Barcelona, Spain

7 Centro Nacional de Investigaciones Cardiovasculares (CNIC), Melchor Fernandez Almagro 3, 28029 Madrid, Spain

8 Current address: Center for Genomic Medicine, Kyoto University Graduate School of Medicine, Kyoto 606-8501 Japan

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Genome Biology 2008, 9:R176  doi:10.1186/gb-2008-9-12-r176

Published: 16 December 2008

Abstract

Background

The physical organization and chromosomal localization of genes within genomes is known to play an important role in their function. Most genes arise by duplication and move along the genome by random shuffling of DNA segments. Higher order structuring of the genome occurs in eukaryotes, where groups of physically linked genes are co-expressed. However, the contribution of gene duplication to gene order has not been analyzed in detail, as it is believed that co-expression due to recent duplicates would obscure other domains of co-expression.

Results

We have catalogued ordered duplicated genes in Drosophila melanogaster, and found that one in five of all genes is organized as tandem arrays. Furthermore, among arrays that have been spatially conserved over longer periods than would be expected on the basis of random shuffling, a disproportionate number contain genes encoding developmental regulators. Using in situ gene expression data for more than half of the Drosophila genome, we find that genes in these conserved clusters are co-expressed to a much higher extent than other duplicated genes.

Conclusions

These results reveal the existence of functional constraints in insects that retain copies of genes encoding developmental and regulatory proteins as neighbors, allowing their co-expression. This co-expression may be the result of shared cis-regulatory elements or a shared need for a specific chromatin structure. Our results highlight the association between genome architecture and the gene regulatory networks involved in the construction of the body plan.