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Non-allelic gene conversion enables rapid evolutionary change at multiple regulatory sites encoded by transposable elements.

Ellison CE, Bachtrog D - Elife (2015)

Bottom Line: Selection has increased the frequency of this derived haplotype in the population, which is fixed at 30% of ISX insertions and polymorphic among another 41%.Sharing of this haplotype indicates that high levels of gene conversion among ISX elements allow them to 'crowd-source' refining mutations, and a refining mutation that occurs at any single ISX element can spread in two dimensions: horizontally across insertion sites by non-allelic gene conversion, and vertically through the population by natural selection.These results describe a novel route by which fully functional regulatory elements can arise rapidly from TEs and implicate non-allelic gene conversion as having an important role in accelerating the evolutionary fine-tuning of regulatory networks.

View Article: PubMed Central - PubMed

Affiliation: Department of Integrative Biology, University of California, Berkeley, Berkeley, United States.

ABSTRACT
Transposable elements (TEs) allow rewiring of regulatory networks, and the recent amplification of the ISX element dispersed 77 functional but suboptimal binding sites for the dosage compensation complex to a newly formed X chromosome in Drosophila. Here we identify two linked refining mutations within ISX that interact epistatically to increase binding affinity to the dosage compensation complex. Selection has increased the frequency of this derived haplotype in the population, which is fixed at 30% of ISX insertions and polymorphic among another 41%. Sharing of this haplotype indicates that high levels of gene conversion among ISX elements allow them to 'crowd-source' refining mutations, and a refining mutation that occurs at any single ISX element can spread in two dimensions: horizontally across insertion sites by non-allelic gene conversion, and vertically through the population by natural selection. These results describe a novel route by which fully functional regulatory elements can arise rapidly from TEs and implicate non-allelic gene conversion as having an important role in accelerating the evolutionary fine-tuning of regulatory networks.

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Alignment of ISY elements from the D. miranda MSH22 genome assembly.139 ISY elements from the MSH22 neo-X chromosome were identified and 200 basepairs from their 5′ flanks were aligned. The black arrows point to the sites where the derived ‘T’ alleles are common among ISX elements. In contrast, only a single ISY element from the neo-X chromosome harbors the TT haplotype.DOI:http://dx.doi.org/10.7554/eLife.05899.004
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fig1s1: Alignment of ISY elements from the D. miranda MSH22 genome assembly.139 ISY elements from the MSH22 neo-X chromosome were identified and 200 basepairs from their 5′ flanks were aligned. The black arrows point to the sites where the derived ‘T’ alleles are common among ISX elements. In contrast, only a single ISY element from the neo-X chromosome harbors the TT haplotype.DOI:http://dx.doi.org/10.7554/eLife.05899.004

Mentions: (A) The MSL recognition motif (MRE) plus 20 basepairs of flanking sequence were extracted from all 77 ISX transposable elements located on the neo-X chromosome in the MSH22 reference genome assembly. The multiple sequence alignment of these 77 sequence regions (arranged from top-to-bottom in the order in which they are found on the chromosome) shows that there is sequence variation among elements both within and adjacent to the 21 basepair MRE motif. Each variant has been classified as ancestral or derived based on its frequency in the ISX progenitor element, ISY. The derived allele frequency for each variant in this region is shown for ISX as well as 139 ISY elements from the neo-X chromosome (see Figure 1—figure supplement 1 for ISY alignment). Red arrows point to the derived TT haplotype that is common among ISX elements but rare in ISY. (B) Barplot showing the frequencies of all haplotypes at the GA/TT sites, for ISY and ISX elements separately. Two haplotypes are present within ISX elements (GA and TT) and the two alleles within each haplotype are in perfect linkage disequilibrium. In contrast, the majority of ISY elements harbor the GA haplotype, but these two alleles are not in perfect linkage disequilibrium among ISY elements. Rather, five additional allelic combinations are present at low frequencies in this location among ISY, but not ISX elements.


Non-allelic gene conversion enables rapid evolutionary change at multiple regulatory sites encoded by transposable elements.

Ellison CE, Bachtrog D - Elife (2015)

Alignment of ISY elements from the D. miranda MSH22 genome assembly.139 ISY elements from the MSH22 neo-X chromosome were identified and 200 basepairs from their 5′ flanks were aligned. The black arrows point to the sites where the derived ‘T’ alleles are common among ISX elements. In contrast, only a single ISY element from the neo-X chromosome harbors the TT haplotype.DOI:http://dx.doi.org/10.7554/eLife.05899.004
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4384637&req=5

fig1s1: Alignment of ISY elements from the D. miranda MSH22 genome assembly.139 ISY elements from the MSH22 neo-X chromosome were identified and 200 basepairs from their 5′ flanks were aligned. The black arrows point to the sites where the derived ‘T’ alleles are common among ISX elements. In contrast, only a single ISY element from the neo-X chromosome harbors the TT haplotype.DOI:http://dx.doi.org/10.7554/eLife.05899.004
Mentions: (A) The MSL recognition motif (MRE) plus 20 basepairs of flanking sequence were extracted from all 77 ISX transposable elements located on the neo-X chromosome in the MSH22 reference genome assembly. The multiple sequence alignment of these 77 sequence regions (arranged from top-to-bottom in the order in which they are found on the chromosome) shows that there is sequence variation among elements both within and adjacent to the 21 basepair MRE motif. Each variant has been classified as ancestral or derived based on its frequency in the ISX progenitor element, ISY. The derived allele frequency for each variant in this region is shown for ISX as well as 139 ISY elements from the neo-X chromosome (see Figure 1—figure supplement 1 for ISY alignment). Red arrows point to the derived TT haplotype that is common among ISX elements but rare in ISY. (B) Barplot showing the frequencies of all haplotypes at the GA/TT sites, for ISY and ISX elements separately. Two haplotypes are present within ISX elements (GA and TT) and the two alleles within each haplotype are in perfect linkage disequilibrium. In contrast, the majority of ISY elements harbor the GA haplotype, but these two alleles are not in perfect linkage disequilibrium among ISY elements. Rather, five additional allelic combinations are present at low frequencies in this location among ISY, but not ISX elements.

Bottom Line: Selection has increased the frequency of this derived haplotype in the population, which is fixed at 30% of ISX insertions and polymorphic among another 41%.Sharing of this haplotype indicates that high levels of gene conversion among ISX elements allow them to 'crowd-source' refining mutations, and a refining mutation that occurs at any single ISX element can spread in two dimensions: horizontally across insertion sites by non-allelic gene conversion, and vertically through the population by natural selection.These results describe a novel route by which fully functional regulatory elements can arise rapidly from TEs and implicate non-allelic gene conversion as having an important role in accelerating the evolutionary fine-tuning of regulatory networks.

View Article: PubMed Central - PubMed

Affiliation: Department of Integrative Biology, University of California, Berkeley, Berkeley, United States.

ABSTRACT
Transposable elements (TEs) allow rewiring of regulatory networks, and the recent amplification of the ISX element dispersed 77 functional but suboptimal binding sites for the dosage compensation complex to a newly formed X chromosome in Drosophila. Here we identify two linked refining mutations within ISX that interact epistatically to increase binding affinity to the dosage compensation complex. Selection has increased the frequency of this derived haplotype in the population, which is fixed at 30% of ISX insertions and polymorphic among another 41%. Sharing of this haplotype indicates that high levels of gene conversion among ISX elements allow them to 'crowd-source' refining mutations, and a refining mutation that occurs at any single ISX element can spread in two dimensions: horizontally across insertion sites by non-allelic gene conversion, and vertically through the population by natural selection. These results describe a novel route by which fully functional regulatory elements can arise rapidly from TEs and implicate non-allelic gene conversion as having an important role in accelerating the evolutionary fine-tuning of regulatory networks.

Show MeSH