Origin and Evolution of a Chimeric Fusion Gene in Drosophila subobscura, D. madeirensis and D. guanche

Center for Population Biology, University of California, Davis, 95616, USA.
Genetics (Impact Factor: 5.96). 06/2005; 170(1):207-19. DOI: 10.1534/genetics.104.037283
Source: PubMed


An understanding of the mutational and evolutionary mechanisms underlying the emergence of novel genes is critical to studies of phenotypic and genomic evolution. Here we describe a new example of a recently formed chimeric fusion gene that occurs in Drosophila guanche, D. madeirensis, and D. subobscura. This new gene, which we name Adh-Twain, resulted from an Adh mRNA that retrotransposed into the Gapdh-like gene, CG9010. Adh-Twain is transcribed; its 5' promoters and transcription patterns appear similar to those of CG9010. Population genetic and phylogenetic analyses suggest that the amino acid sequence of Adh-Twain evolved rapidly via directional selection shortly after it arose. Its more recent history, however, is characterized by slower evolution consistent with increasing functional constraints. We present a model for the origin of this new gene and discuss genetic and evolutionary factors affecting the evolution of new genes and functions.

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    • "The probability that chimeric fusion genes are retained in the genome may be strongly influenced by their recombinational mode of origin and the nature of functional divergence between the parental genes (Katju and Lynch 2003, 2006; Jones and Begun 2005; Jones et al. 2005; Rogers et al. 2009, 2010; Kaessmann 2010; Katju 2012, 2013). Unequal crossing-over (nonallelic homologous recombination) between tandem gene duplicates represents a common mechanism for producing chimeric fusion genes in conjunction with changes in gene copy number (Holloway et al. 2006; Hoffmann et al. 2008b). "
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    ABSTRACT: The evolutionary fate of chimeric fusion genes may be strongly influenced by their recombinational mode of origin and the nature of functional divergence between the parental genes. In the β-globin gene family of placental mammals, the two postnatally expressed δ- and β-globin genes (HBD and HBB, respectively) have a propensity for recombinational exchange via gene conversion and unequal crossing-over. In the latter case, there are good reasons to expect differences in retention rates for the reciprocal HBB/HBD and HBD/HBB fusion genes due to thalassemia pathologies associated with the HBD/HBB “Lepore” deletion mutant in humans. Here, we report a comparative genomic analysis of the mammalian β-globin gene cluster, which revealed that chimeric HBB/HBD fusion genes originated independently in four separate lineages of laurasiatherian mammals: Eulipotyphlans (shrews, moles, and hedgehogs), carnivores, microchiropteran bats, and cetaceans. In cases where an independently derived “anti-Lepore” duplication mutant has become fixed, the parental HBD and/or HBB genes have typically been inactivated or deleted, so that the newly created HBB/HBD fusion gene is primarily responsible for synthesizing the β-type subunits of adult and fetal hemoglobin (Hb). Contrary to conventional wisdom that the HBD gene is a vestigial relict that is typically inactivated or expressed at negligible levels, we show that HBD-like genes often encode a substantial fraction (20–100%) of β-chain Hbs in laurasiatherian taxa. Our results indicate that the ascendancy or resuscitation of genes with HBD-like coding sequence requires the secondary acquisition of HBB-like promoter sequence via unequal crossing-over or interparalog gene conversion.
    Full-text · Article · May 2014 · Genome Biology and Evolution
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    • "Because of their unique origination, chimeric genes are unlikely to retain their parental characteristics and thus evolve novel functions. By surveying previous new genes detected in other organisms, it can be concluded that chimeric new genes account for a high percentage of total new genes identified in a variety of organisms ranging from mammals (Paulding et al. 2003; Sayah et al. 2004; Parker et al. 2009), to flies (Long and Langley 1993; Jones et al. 2005; Nozawa et al. 2005) and plants (Long et al. 1996; Wang et al. 2006; Fan et al. 2008). A recent investigation systematically searched through new genes using the Drosophila genome comparisons and found 30% of the new genes in the D. melanogaster species complex recruited various genomic sequences and formed chimeric gene structures. "
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    ABSTRACT: In an effort to identify newly evolved genes in rice, we searched the genomes of Asian-cultivated rice Oryza sativa ssp. japonica and its wild progenitors, looking for lineage-specific genes. Using genome pairwise comparison of approximately 20-Mb DNA sequences from the chromosome 3 short arm (Chr3s) in six rice species, O. sativa, O. nivara, O. rufipogon, O. glaberrima, O. barthii, and O. punctata, combined with synonymous substitution rate tests and other evidence, we were able to identify potential recently duplicated genes, which evolved within the last 1 Myr. We identified 28 functional O. sativa genes, which likely originated after O. sativa diverged from O. glaberrima. These genes account for around 1% (28/3,176) of all annotated genes on O. sativa’s Chr3s. Among the 28 new genes, two recently duplicated segments contained eight genes. Fourteen of the 28 new genes consist of chimeric gene structure derived from one or multiple parental genes and flanking targeting sequences. Although the majority of these 28 new genes were formed by single or segmental DNA-based gene duplication and recombination, we found two genes that were likely originated partially through exon shuffling. Sequence divergence tests between new genes and their putative progenitors indicated that new genes were most likely evolving under natural selection. We showed all 28 new genes appeared to be functional, as suggested by Ka/Ks analysis and the presence of RNA-seq, cDNA, expressed sequence tag, massively parallel signature sequencing, and/or small RNA data. The high rate of new gene origination and of chimeric gene formation in rice may demonstrate rice’s broad diversification, domestication, its environmental adaptation, and the role of new genes in rice speciation
    Full-text · Article · May 2013 · Genome Biology and Evolution
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    • "This result suggests that genes similar to those forming the TcPR-1 cluster fused with a kinase domain of a LecRLK, giving rise to PR-1RKs. The formation of new chimeric proteins has been related to molecular mechanisms, such as exon shuffling, gene duplication, retrotransposition or combinations of these (Jones et al., 2005; Long et al., 2003; Nisole et al., 2004; Wang et al., 2006). Therefore , we searched for retrotransposition marks in both LecRLK and PR-1 clusters, using RepeatMasker (A.F. "
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    ABSTRACT: Members of the pathogenesis-related protein 1 (PR-1) family are well-known markers of plant defence responses, forming part of the arsenal of the secreted proteins produced on pathogen recognition. Here, we report the identification of two cacao (Theobroma cacao L.) PR-1s that are fused to transmembrane regions and serine/threonine kinase domains, in a manner characteristic of receptor-like kinases (RLKs). These proteins (TcPR-1f and TcPR-1g) were named PR-1 receptor kinases (PR-1RKs). Phylogenetic analysis of RLKs and PR-1 proteins from cacao indicated that PR-1RKs originated from a fusion between sequences encoding PR-1 and the kinase domain of a LecRLK (Lectin Receptor-Like Kinase). Retrotransposition marks surround TcPR-1f, suggesting that retrotransposition was involved in the origin of PR-1RKs. Genes with a similar domain architecture to cacao PR-1RKs were found in rice (Oryza sativa), barrel medic (Medicago truncatula) and a nonphototrophic bacterium (Herpetosiphon aurantiacus). However, their kinase domains differed from those found in LecRLKs, indicating the occurrence of convergent evolution. TcPR-1g expression was up-regulated in the biotrophic stage of witches’ broom disease, suggesting a role for PR-1RKs during cacao defence responses.We hypothesize that PR-1RKs transduce a defence signal by interacting with a PR-1 ligand.
    Full-text · Article · Apr 2013 · Molecular Plant Pathology
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