High Incidence of Interchromosomal Transpositions in the Evolutionary History of a Subset of Or Genes in Drosophila

Departament de Genètica, Universitat de Barcelona, Av. Diagonal, 645, Barcelona 08028, Spain.
Journal of Molecular Evolution (Impact Factor: 1.68). 05/2008; 66(4):325-32. DOI: 10.1007/s00239-008-9071-y
Source: PubMed


In insects, the odorant receptor (Or) multigene family is an intermediate-sized family with genes present in all chromosomes, indicating that duplication followed by interchromosomal transposition played an important role in the early stages of the family evolution. Here, we have explored the occurrence of interchromosomal transpositions in more recent stages through the comparative analysis of a subset of Or genes in Drosophila, where the gene content of chromosomal arms is highly conserved. The studied subset consisted of 11 Or genes located on the left arm of chromosome 3 (Muller's D element) in D. melanogaster. Our study focused on the number and chromosomal arm location of these members of the family across the 12 Drosophila species with complete genome sequences. In contrast to previous results from in situ hybridization comparative mapping that were mainly based on single-copy genes, our study, based on members of a multigene family of moderate size, revealed repeated interchromosomal transposition events and a complex history of some of the studied genes.

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    • "This precludes the explanation via retrotransposition because such mechanism mostly creates single-exon duplogs (see, e.g., Babushok et al. 2007), unless premature long RNA transcripts were reverse-transcribed. Pattern (iii) is consistent with the classical view of tandem duplication followed by genomic rearrangements (e.g., Friedman and Hughes 2003, 2004; Conceic xã o and Aguadé 2008; Hu et al. 2008). In contrast, it is difficult to explain patterns (i), (ii), and (iv) with this classical view. "
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    ABSTRACT: Duplogs, or intraspecies paralogs, constitute the important portion of eukaryote genomes and serve as a major source of functional innovation. We conducted detailed analyses of recently emerged animal duplogs. Genome data of three vertebrate species (Homo sapiens, Mus musculus, and Danio rerio), Caenorhabditis elegans, and two Drosophila species (Drosophila melanogaster and D. pseudoobscura) were used. Duplication events were divided into six age-groups according to the synonymous distance (dS) up to 0.6. Duplogs were classified into four equal-sized classes on physical distances and into three classes on relative orientations. We observed the following shared characteristics among intrachromosomal multiexon duplogs: 1) inverted duplogs account for 20-50%, and about a half of the physically most distant 25%; 2) except for C. elegans, the composition of physical distances, that of relative orientations, and the proportion of inverted duplogs in each physical distance category are more or less uniform; 3) except for C. elegans, the characteristics of the youngest (dS < 0.01) duplogs are similar to the overall characteristics of the entire set. These results suggest that intrachromosomal duplogs with fairly long physical distances were generated at once, rather than resulting from tandem duplications and subsequent genomic rearrangements. This is different from the three well-known modes of gene duplication: tandem duplication, retrotransposition, and genome duplication. We termed this new mode as "drift" duplication. The drift duplication has been producing duplicate copies at paces comparable with tandem duplications since the common ancestor of vertebrates, and it may have already operated in the common ancestor of bilateral animals.
    Genome Biology and Evolution 08/2011; 3(1):1119-35. DOI:10.1093/gbe/evr074 · 4.23 Impact Factor
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    • "Drosophila OR and GR genes, on the other hand, appear more scattered throughout the genome, having only a few clusters (Robertson et al., 2003); this distribution differs from other insects where the receptor genes are arranged in a number of clusters (Robertson and Wanner, 2006; Bohbot et al., 2007; Engsontia et al., 2008). Indeed, the chromosomal distribution of OR genes have revealed repeated inter-chromosomal translocation events across the Drosophila phylogeny; these evolutionary events seem to be more frequent in this receptor family than in the OBP family (Guo and Kim, 2007; Conceição and Aguadé, 2008). The distinct gene expression patterns of the OBP and OR/GR families might account for these differences. "
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    ABSTRACT: Chemoreception is a crucial biological process that is essential for the survival of animals. In insects, olfaction allows the organism to recognise volatile cues that allow the detection of food, predators and mates, whereas the sense of taste commonly allows the discrimination of soluble stimulants that elicit feeding behaviours and can also initiate innate sexual and reproductive responses. The most important proteins involved in the recognition of chemical cues comprise moderately sized multigene families. These families include odorant-binding proteins (OBPs) and chemosensory proteins (CSPs), which are involved in peripheral olfactory processing, and the chemoreceptor superfamily formed by the olfactory receptor (OR) and gustatory receptor (GR) families. Here, we review some recent evolutionary genomic studies of chemosensory gene families using the data from fully sequenced insect genomes, especially from the 12 newly available Drosophila genomes. Overall, the results clearly support the birth-and-death model as the major mechanism of evolution in these gene families. Namely, new members arise by tandem gene duplication, progressively diverge in sequence and function, and can eventually be lost from the genome by a deletion or pseudogenisation event. Adaptive changes fostered by environmental shifts are also observed in the evolution of chemosensory families in insects and likely involve reproductive, ecological or behavioural traits. Consequently, the current size of these gene families is mainly a result of random gene gain and loss events. This dynamic process may represent a major source of genetic variation, providing opportunities for FUTURE specific adaptations.
    Heredity 06/2009; 103(3):208-16. DOI:10.1038/hdy.2009.55 · 3.81 Impact Factor
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    ABSTRACT: In Drosophila, odorant receptors are encoded by an old and moderately sized multigene family. Or22a and Or22b are two tandemly arranged genes of this family that have proved to be the result of a rather young duplication. Nucleotide variation in the region spanning both duplicates was surveyed in four natural populations (two African and two non-African) of Drosophila melanogaster and also analyzed in species of the melanogaster subgroup. The intraspecific survey revealed a particular copy-number polymorphism in some of the studied populations, with the two genes (Or22a and Or22b) present in the long variant and a single chimeric gene (Or22ab) present in the short variant. Estimated nucleotide diversity was higher in the short than in the long variant, despite the ancestral character of the latter variant in D. melanogaster. The general skew toward low-frequency variants detected in the non-African long variant and its reduced level of silent polymorphism relative to divergence is consistent with the recent fixation of an advantageous mutation at, or nearby, the Or22 long variant region. The nonnegligible frequency of the short variant and the presence of a highly divergent haplotype in the East African sample would point to direct or indirect selection for its maintenance in the species. There was evidence for a generally more rapid evolution of the Or22b copy at both synonymous and nonsynonymous sites. However, an excess of nonsynonymous substitutions was only detected in the early history of this copy.
    Molecular Biology and Evolution 11/2008; 26(1):61-70. DOI:10.1093/molbev/msn227 · 9.11 Impact Factor
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