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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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The Gene Structures of 16 New Duplicates Mapped on the Species PhylogenyCR33318 is not shown because it is a truncated copy without detectable expression and has frame shift mutations. Duplicated regions are indicated with vertical dash lines. Horizontal dash lines in CG7635-r, CG3101-r, d-r, and klg-r indicate that we only obtained partial coding regions with RT-PCR and longer coding regions may exist outward. Boxes are exon regions and lines indicate introns. Yellow boxes indicate recruited chimeric regions, green boxes indicate parental loci UTRs, and blue boxes indicate duplicate loci UTRs. Positions of start and stop codons are marked.
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pgen-0040003-g003: The Gene Structures of 16 New Duplicates Mapped on the Species PhylogenyCR33318 is not shown because it is a truncated copy without detectable expression and has frame shift mutations. Duplicated regions are indicated with vertical dash lines. Horizontal dash lines in CG7635-r, CG3101-r, d-r, and klg-r indicate that we only obtained partial coding regions with RT-PCR and longer coding regions may exist outward. Boxes are exon regions and lines indicate introns. Yellow boxes indicate recruited chimeric regions, green boxes indicate parental loci UTRs, and blue boxes indicate duplicate loci UTRs. Positions of start and stop codons are marked.

Mentions: To examine whether the new duplicates have evolved chimeric gene structures, we utilized previously reported cDNA sequences, RACE, or RT-PCR based on computationally predicted structures (Materials and Methods). Among the 17 new genes, 13 were found to have evolved chimeric gene sequences through the recruitment of flanking sequence near the insertion site or as the result of extensive deletions (CG5372, CG9902, CG4021, CG3875, CG3927, CR9337, CG7635-r, CG3101-r, CG3071-r, d-r, Dox-A3-r, Hun, and klg-r; Figure 3). Among these chimeric genes, 11 can encode chimeric proteins (CG5372, CG9902, CG4021, CG3875, CG3927, CR9337, CG7635-r, CG3101-r, CG3071-r, Hun and d-r). For example, d-r and CG9902 have both recruited novel coding regions following their duplications, and possibly in conjunction with their deletions events that followed (Figure 3). These observations reveal that the majority of young duplicated genes have evolved chimeric gene structures. In addition, it is notable that the chimeric genes that we have detected involve only the duplicated loci and integenic sequences. This suggests that for dispersed duplication events, the formation of chimeric genes by recombining two or more genic sequences may be relatively rare.


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)

The Gene Structures of 16 New Duplicates Mapped on the Species PhylogenyCR33318 is not shown because it is a truncated copy without detectable expression and has frame shift mutations. Duplicated regions are indicated with vertical dash lines. Horizontal dash lines in CG7635-r, CG3101-r, d-r, and klg-r indicate that we only obtained partial coding regions with RT-PCR and longer coding regions may exist outward. Boxes are exon regions and lines indicate introns. Yellow boxes indicate recruited chimeric regions, green boxes indicate parental loci UTRs, and blue boxes indicate duplicate loci UTRs. Positions of start and stop codons are marked.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-0040003-g003: The Gene Structures of 16 New Duplicates Mapped on the Species PhylogenyCR33318 is not shown because it is a truncated copy without detectable expression and has frame shift mutations. Duplicated regions are indicated with vertical dash lines. Horizontal dash lines in CG7635-r, CG3101-r, d-r, and klg-r indicate that we only obtained partial coding regions with RT-PCR and longer coding regions may exist outward. Boxes are exon regions and lines indicate introns. Yellow boxes indicate recruited chimeric regions, green boxes indicate parental loci UTRs, and blue boxes indicate duplicate loci UTRs. Positions of start and stop codons are marked.
Mentions: To examine whether the new duplicates have evolved chimeric gene structures, we utilized previously reported cDNA sequences, RACE, or RT-PCR based on computationally predicted structures (Materials and Methods). Among the 17 new genes, 13 were found to have evolved chimeric gene sequences through the recruitment of flanking sequence near the insertion site or as the result of extensive deletions (CG5372, CG9902, CG4021, CG3875, CG3927, CR9337, CG7635-r, CG3101-r, CG3071-r, d-r, Dox-A3-r, Hun, and klg-r; Figure 3). Among these chimeric genes, 11 can encode chimeric proteins (CG5372, CG9902, CG4021, CG3875, CG3927, CR9337, CG7635-r, CG3101-r, CG3071-r, Hun and d-r). For example, d-r and CG9902 have both recruited novel coding regions following their duplications, and possibly in conjunction with their deletions events that followed (Figure 3). These observations reveal that the majority of young duplicated genes have evolved chimeric gene structures. In addition, it is notable that the chimeric genes that we have detected involve only the duplicated loci and integenic sequences. This suggests that for dispersed duplication events, the formation of chimeric genes by recombining two or more genic sequences may be relatively rare.

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