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Repetitive element-mediated recombination as a mechanism for new gene origination in Drosophila.

Yang S, Arguello JR, Li X, Ding Y, Zhou Q, Chen Y, Zhang Y, Zhao R, Brunet F, Peng L, Long M, Wang W - PLoS Genet. (2007)

Bottom Line: Lack of a dataset comprising experimentally verified young duplicates has hampered an effective examination of these models as well as an investigation of sequence features that mediate the rearrangements.Examination of their flanking sequences revealed an excess of repetitive sequences, with the majority belonging to the transposable element DNAREP1 family, associated with the new genes.Our dataset strongly suggests an important role for REs in the generation of chimeric genes within these species.

View Article: PubMed Central - PubMed

Affiliation: Chinese Academy of Sciences-Max Planck Junior Research Group, Key Laboratory of Cellular and Molecular Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China.

ABSTRACT
Previous studies of repetitive elements (REs) have implicated a mechanistic role in generating new chimerical genes. Such examples are consistent with the classic model for exon shuffling, which relies on non-homologous recombination. However, recent data for chromosomal aberrations in model organisms suggest that ectopic homology-dependent recombination may also be important. Lack of a dataset comprising experimentally verified young duplicates has hampered an effective examination of these models as well as an investigation of sequence features that mediate the rearrangements. Here we use approximately 7,000 cDNA probes (approximately 112,000 primary images) to screen eight species within the Drosophila melanogaster subgroup and identify 17 duplicates that were generated through ectopic recombination within the last 12 mys. Most of these are functional and have evolved divergent expression patterns and novel chimeric structures. Examination of their flanking sequences revealed an excess of repetitive sequences, with the majority belonging to the transposable element DNAREP1 family, associated with the new genes. Our dataset strongly suggests an important role for REs in the generation of chimeric genes within these species.

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Related in: MedlinePlus

A Simplified Schematic of the Repetitive Sequence Flanking New Genes and Their Distribution over the D. melanogaster Subgroup PhylogenyLeft panel displays the varying degrees of identity and degeneration between flanking regions of paralogs, with the right panel displaying the branches in which they are found; 1: (CG2952:CG2952-r), (kep1: CG4021), (kep1:CG9337), (CG9902:CG7692), (kep1:CG3875); 2: (CG3875-CG3927); 3: (CG9337-CG9337-r); 4: (mkgr-mkgr2); 5: (CR9337-CR33318); 6: (CG3101-CG3101-r). The red blocks in the left panel indicate alignable regions of the TEs and other repeat sequences. The black boxes represent sequences of TEs and other repeats; fragmented black boxes represent RE fragments. The long boxes in various colors represent the identified new genes. See also Figure S1, for the alignments.
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pgen-0040003-g005: A Simplified Schematic of the Repetitive Sequence Flanking New Genes and Their Distribution over the D. melanogaster Subgroup PhylogenyLeft panel displays the varying degrees of identity and degeneration between flanking regions of paralogs, with the right panel displaying the branches in which they are found; 1: (CG2952:CG2952-r), (kep1: CG4021), (kep1:CG9337), (CG9902:CG7692), (kep1:CG3875); 2: (CG3875-CG3927); 3: (CG9337-CG9337-r); 4: (mkgr-mkgr2); 5: (CR9337-CR33318); 6: (CG3101-CG3101-r). The red blocks in the left panel indicate alignable regions of the TEs and other repeat sequences. The black boxes represent sequences of TEs and other repeats; fragmented black boxes represent RE fragments. The long boxes in various colors represent the identified new genes. See also Figure S1, for the alignments.

Mentions: Four lines of evidence indicate that this association has not been observed by chance. The first is based on orthology assignments available from current genome databases, indicating that all ten in our set are euchromatic and not on the 4th chromosome. High-resolution analyses of D. melanogaster TEs have verified that the paracentromeric regions of the major chromosome arms and chromosome 4 harbor the highest densities of TEs [44]. Second, simulations show that the probability that the number of genes flanked by TEs ≥7 given the sample size of seven genes (with 14 breakpoints) is low (p < 0.05) given a TE-free region (TFR) of ∼15 kb or larger (Figure S2; Materials and Methods). Despite TE differences between species, 15 kb is less than half the mean TFR found in D. melanogaster [44]. Given that the TEs in our dataset are comprised primarily of DNAREP1 family members, the distance is even greater. Furthermore, the probability that both paralogs contain the same TE sequence in their flanking regions, as three (and possibly four) do in our dataset, is much lower (Table 2; Figure S1). Finally, our data reveal a gradation of degeneration in the TEs and other REs with the ages of the gene duplicates that the repeats flank (Figure 5). This gradation is consistent with observed degeneration rate of functionless elements in Drosophila [30], as well as any potential internal deletions that could be part of a self-regulation system as seen in D. melanogaster TEs [45].


Repetitive element-mediated recombination as a mechanism for new gene origination in Drosophila.

Yang S, Arguello JR, Li X, Ding Y, Zhou Q, Chen Y, Zhang Y, Zhao R, Brunet F, Peng L, Long M, Wang W - PLoS Genet. (2007)

A Simplified Schematic of the Repetitive Sequence Flanking New Genes and Their Distribution over the D. melanogaster Subgroup PhylogenyLeft panel displays the varying degrees of identity and degeneration between flanking regions of paralogs, with the right panel displaying the branches in which they are found; 1: (CG2952:CG2952-r), (kep1: CG4021), (kep1:CG9337), (CG9902:CG7692), (kep1:CG3875); 2: (CG3875-CG3927); 3: (CG9337-CG9337-r); 4: (mkgr-mkgr2); 5: (CR9337-CR33318); 6: (CG3101-CG3101-r). The red blocks in the left panel indicate alignable regions of the TEs and other repeat sequences. The black boxes represent sequences of TEs and other repeats; fragmented black boxes represent RE fragments. The long boxes in various colors represent the identified new genes. See also Figure S1, for the alignments.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2211543&req=5

pgen-0040003-g005: A Simplified Schematic of the Repetitive Sequence Flanking New Genes and Their Distribution over the D. melanogaster Subgroup PhylogenyLeft panel displays the varying degrees of identity and degeneration between flanking regions of paralogs, with the right panel displaying the branches in which they are found; 1: (CG2952:CG2952-r), (kep1: CG4021), (kep1:CG9337), (CG9902:CG7692), (kep1:CG3875); 2: (CG3875-CG3927); 3: (CG9337-CG9337-r); 4: (mkgr-mkgr2); 5: (CR9337-CR33318); 6: (CG3101-CG3101-r). The red blocks in the left panel indicate alignable regions of the TEs and other repeat sequences. The black boxes represent sequences of TEs and other repeats; fragmented black boxes represent RE fragments. The long boxes in various colors represent the identified new genes. See also Figure S1, for the alignments.
Mentions: Four lines of evidence indicate that this association has not been observed by chance. The first is based on orthology assignments available from current genome databases, indicating that all ten in our set are euchromatic and not on the 4th chromosome. High-resolution analyses of D. melanogaster TEs have verified that the paracentromeric regions of the major chromosome arms and chromosome 4 harbor the highest densities of TEs [44]. Second, simulations show that the probability that the number of genes flanked by TEs ≥7 given the sample size of seven genes (with 14 breakpoints) is low (p < 0.05) given a TE-free region (TFR) of ∼15 kb or larger (Figure S2; Materials and Methods). Despite TE differences between species, 15 kb is less than half the mean TFR found in D. melanogaster [44]. Given that the TEs in our dataset are comprised primarily of DNAREP1 family members, the distance is even greater. Furthermore, the probability that both paralogs contain the same TE sequence in their flanking regions, as three (and possibly four) do in our dataset, is much lower (Table 2; Figure S1). Finally, our data reveal a gradation of degeneration in the TEs and other REs with the ages of the gene duplicates that the repeats flank (Figure 5). This gradation is consistent with observed degeneration rate of functionless elements in Drosophila [30], as well as any potential internal deletions that could be part of a self-regulation system as seen in D. melanogaster TEs [45].

Bottom Line: Lack of a dataset comprising experimentally verified young duplicates has hampered an effective examination of these models as well as an investigation of sequence features that mediate the rearrangements.Examination of their flanking sequences revealed an excess of repetitive sequences, with the majority belonging to the transposable element DNAREP1 family, associated with the new genes.Our dataset strongly suggests an important role for REs in the generation of chimeric genes within these species.

View Article: PubMed Central - PubMed

Affiliation: Chinese Academy of Sciences-Max Planck Junior Research Group, Key Laboratory of Cellular and Molecular Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China.

ABSTRACT
Previous studies of repetitive elements (REs) have implicated a mechanistic role in generating new chimerical genes. Such examples are consistent with the classic model for exon shuffling, which relies on non-homologous recombination. However, recent data for chromosomal aberrations in model organisms suggest that ectopic homology-dependent recombination may also be important. Lack of a dataset comprising experimentally verified young duplicates has hampered an effective examination of these models as well as an investigation of sequence features that mediate the rearrangements. Here we use approximately 7,000 cDNA probes (approximately 112,000 primary images) to screen eight species within the Drosophila melanogaster subgroup and identify 17 duplicates that were generated through ectopic recombination within the last 12 mys. Most of these are functional and have evolved divergent expression patterns and novel chimeric structures. Examination of their flanking sequences revealed an excess of repetitive sequences, with the majority belonging to the transposable element DNAREP1 family, associated with the new genes. Our dataset strongly suggests an important role for REs in the generation of chimeric genes within these species.

Show MeSH
Related in: MedlinePlus