Support for multiple classes of local expression clusters in Drosophila melanogaster, but no evidence for gene order conservation

Background: Gene order in eukaryotic genomes is not random, with genes with similar expression profiles tending to cluster. In yeasts, the model taxon for gene order analysis, such syntenic clusters of non-homologous genes tend to be conserved over evolutionary time. Whether similar clusters show gene order conservation in other lineages is, however, undecided. Here, we examine this issue in Drosophila melanogaster using high-resolution chromosome rearrangement data. Results: We show that D. melanogaster has at least three classes of expression clusters: first, as observed in mammals, large clusters of functionally unrelated housekeeping genes; second, small clusters of functionally related highly co-expressed genes; and finally, as previously defined by Spellman and Rubin, larger domains of co-expressed but functionally unrelated genes. The latter are, however, not independent of the small co-expression clusters and likely reflect a methodological artifact. While the small co-expression and housekeeping/essential gene clusters resemble those observed in yeast, in contrast to yeast, we see no evidence that any of the three cluster types are preserved as synteny blocks. If anything, adjacent co-expressed genes are more likely to become rearranged than expected. Again in contrast to yeast, in D. melanogaster, gene pairs with short intergene distance or in divergent orientations tend to have higher rearrangement rates. These findings are consistent with co-expression being partly due to shared chromatin environment. Conclusions: We conclude that, while similar in terms of cluster types, gene order evolution has strikingly different patterns in yeasts and in D. melanogaster, although recombination is associated with gene order rearrangement in both.