Abstract
BackgroundGene order in eukaryotic chromosomes is not random and has been linked to coordination of gene expression, chromatin structure and also recombination rate. The evolution of recombination rate is especially relevant for genes involved in immunity because host-parasite co-evolution could select for increased recombination rate (Red Queen hypothesis). To identify patterns left by the intimate interaction between hosts and parasites, I analysed the genomic parameters of the immune genes from 24 gene families/groups of Drosophila melanogaster.Principal FindingsImmune genes that directly interact with the pathogen (i.e. recognition and effector genes) clustered in regions of higher recombination rates. Out of these, clustered effector genes were transcribed fastest indicating that transcriptional control might be one major cause for cluster formation. The relative position of clusters to each other, on the other hand, cannot be explained by transcriptional control per se. Drosophila immune genes that show epistatic interactions can be found at an average distance of 15.44±2.98 cM, which is considerably closer than genes that do not interact (30.64±1.95 cM).ConclusionsEpistatically interacting genes rarely belong to the same cluster, which supports recent models of optimal recombination rates between interacting genes in antagonistic host-parasite co-evolution. These patterns suggest that formation of local clusters might be a result of transcriptional control, but that in the condensed genome of D. melanogaster relative position of these clusters may be a result of selection for optimal rather than maximal recombination rates between these clusters.
Highlights
The sequence of genes in eukaryotic genomes is not random [1]
Epistatically interacting genes rarely belong to the same cluster, which supports recent models of optimal recombination rates between interacting genes in antagonistic host-parasite co-evolution
These patterns suggest that formation of local clusters might be a result of transcriptional control, but that in the condensed genome of D. melanogaster relative position of these clusters may be a result of selection for optimal rather than maximal recombination rates between these clusters
Summary
The sequence of genes in eukaryotic genomes is not random [1]. Several mechanisms could potentially account for the observed patterns, some of which are not a direct result from selection, while others bear signs of selection favouring clustered genes. In the C. elegans genome, for example, a major proportion of genes occurs in clusters [2]. This pattern is most likely a consequence of gene duplications placing homologous copies in close vicinity to each other rather than a direct consequence of selection. Essential genes for example cluster in regions with open chromatin structure to reduce noise in expression patterns [4]. Selection on transcription levels favouring local concentration is not restricted to essential genes but can be extended to other genes [5,6,7], which are often functionally related [8,9] and share chromatin organisation [10]. To identify patterns left by the intimate interaction between hosts and parasites, I analysed the genomic parameters of the immune genes from 24 gene families/groups of Drosophila melanogaster
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