Academic journal article Genetics

Inferring the History of Interchromosomal Gene Transposition in Drosophila Using N-Dimensional Parsimony

Academic journal article Genetics

Inferring the History of Interchromosomal Gene Transposition in Drosophila Using N-Dimensional Parsimony

Article excerpt

ABSTRACT Gene transposition puts a new gene copy in a novel genomic environment. Moreover, genes moving between the autosomes and the X chromosome experience change in several evolutionary parameters. Previous studies of gene transposition have not utilized the phylogenetic framework that becomes possible with the availability of whole genomes from multiple species. Here we used parsimonious reconstruction on the genomic distribution of gene families to analyze interchromosomal gene transposition in Drosophila. We identified 782 genes that have moved chromosomes within the phylogeny of 10 Drosophila species, including 87 gene families with multiple independent movements on different branches of the phylogeny. Using this large catalog of transposed genes, we detected accelerated sequence evolution in duplicated genes that transposed when compared to the parental copy at the original locus. We also observed a more refined picture of the biased movement of genes from the X chromosome to the autosomes. The bias of X-to-autosome movement was significantly stronger for RNA-based movements than for DNA-based movements, and among DNAbased movements there was an excess of genes moving onto the X chromosome as well. Genes involved in female-specific functions moved onto the X chromosome while genes with male-specific functions moved off the X. There was a significant overrepresentation of proteins involving chromosomal function among transposed genes, suggesting that genetic conflict between sexes and among chromosomes may be a driving force behind gene transposition in Drosophila.

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INTERCHROMOSOMAL gene transposition, the movement of genes between chromosome arms, has historically been regarded as relatively rare in Drosophila, on the basis of the observation that homology of the chromosome arms (referred to as "Muller elements") is generally maintained among the species within the genus (Muller 1940). This observation has been upheld by the mapping of molecular markers between different species (Ranz et al. 2003) and borne out again by a comparison of orthologs across the 12 completed genomes (Bhutkar et al. 2007). Nonetheless, specific instances of genes apparently moving between chromosomes have been reported since the 1970s (Ranz et al. 2003), including the recent report of a gene movement that has contributed to reproductive isolation between Drosophila melanogaster and D. simulans (Masly et al. 2006).

Gene transpositions occur through gene duplication, either by a DNA-based mechanism (ectopic recombination) or by an RNA-based mechanism (retrotransposition by reverse transcription of an mRNA). Once a duplicate has arisen in a new location, the original copy can be maintained or the original copy can be lost, resulting in an apparent map change of the locus. Hereafter, we refer to the former case as duplicative transpositions and the latter as relocations (Meisel et al. 2009).

With the sequencing of the genomes of 12 Drosophila species (Clark et al. 2007), transpositions could finally be systematically identified at gene-by-gene resolution. Several studies that looked at gene transpositions at a genome-wide scale have since been published. Bhutkar et al. (2007) found 500 positionally relocated genes, although these amounted to ,5% of all orthologs. Bai et al. (2007) focused on duplicated retrogenes that changed chromosome arms and found 0.5 retrogenes transposed per million years. More recently, Meisel et al. (2009) studied gene duplicates created by all mechanisms and found 368 duplicative transpositions and 195 relocations. Although these studies have expanded the knowledge of gene transpositions considerably, they are limited to gene families with simple lineagespecific transposition events. This is because they considered only the movement of single-copy orthologs (relocations) or unambiguous gains along only a single lineage (e.g., changes from one to two copies, where all other species have one copy). …

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