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The life cycle of Drosophila orphan genes.

Palmieri N, Kosiol C, Schlötterer C - Elife (2014)

Bottom Line: Interestingly, recently emerged orphans are more likely to be lost than older ones.Furthermore, highly expressed orphans with a strong male-bias are more likely to be retained.Since both lost and retained orphans show similar evolutionary signatures of functional conservation, we propose that orphan loss is not driven by high rates of sequence evolution, but reflects lineage-specific functional requirements.

View Article: PubMed Central - PubMed

Affiliation: Institut für Populationsgenetik, Vetmeduni Vienna, Vienna, Austria.

ABSTRACT
Orphans are genes restricted to a single phylogenetic lineage and emerge at high rates. While this predicts an accumulation of genes, the gene number has remained remarkably constant through evolution. This paradox has not yet been resolved. Because orphan genes have been mainly analyzed over long evolutionary time scales, orphan loss has remained unexplored. Here we study the patterns of orphan turnover among close relatives in the Drosophila obscura group. We show that orphans are not only emerging at a high rate, but that they are also rapidly lost. Interestingly, recently emerged orphans are more likely to be lost than older ones. Furthermore, highly expressed orphans with a strong male-bias are more likely to be retained. Since both lost and retained orphans show similar evolutionary signatures of functional conservation, we propose that orphan loss is not driven by high rates of sequence evolution, but reflects lineage-specific functional requirements. DOI: http://dx.doi.org/10.7554/eLife.01311.001.

No MeSH data available.


Related in: MedlinePlus

Orphans predating the XL-XR fusion are preferentially lost on the neo-X.For three terminal branches (D. lowei, D. miranda, and D. persimilis) the fraction of lost genes for each age class is shown. Each autosome and both X-chromosome arms are shown in different color. At node 4, where the neo-X originated, we observed the highest rate of orphan pseudogenization on the neo-X (A). Notably, this effect is not seen for younger orphans (B and C) neither for old genes (D).DOI:http://dx.doi.org/10.7554/eLife.01311.013
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fig8: Orphans predating the XL-XR fusion are preferentially lost on the neo-X.For three terminal branches (D. lowei, D. miranda, and D. persimilis) the fraction of lost genes for each age class is shown. Each autosome and both X-chromosome arms are shown in different color. At node 4, where the neo-X originated, we observed the highest rate of orphan pseudogenization on the neo-X (A). Notably, this effect is not seen for younger orphans (B and C) neither for old genes (D).DOI:http://dx.doi.org/10.7554/eLife.01311.013

Mentions: The analysis of orphans that have putatively lost their function via the acquisition of a stop codon or a frame shift causing insertion/deletion (pseudogenized/lost orphans) reveals another interesting feature of the XL–XR fusion. The oldest orphans in our dataset (age class 4) show a pronounced excess of pseudogenized orphans on XR in D. affinis and D. miranda (Figure 8A). This trend was not observed for orphans that emerged on XR after the XL–XR fusion (Figure 8B,C), nor for old genes (Figure 8D) and is not due to an increased rate of orphan gain on XR (Figure 9). Since the oldest orphans (age class 4) on XR are a mixture of autosomal (i.e., before the fusion) and sex-chromosomal (i.e., after the fusion) orphans, we speculate that the high rate of pseudogenization of orphans on the XR may reflect the new X-linkage of previously autosomal orphans. A previous study (Meisel et al., 2009) found that the XR chromosome has experienced a burst of gene duplications to autosomes after its creation. It is plausible that after the conversion of the XR from autosome to sex-chromosome, orphans might have been duplicated to autosomes, whereas the XR ancestral copy would have become pseudogenized. To test this hypothesis, we looked for evidence of gene duplications for the orphans lost on the XR at node 4 (Figure 6). We aligned the sequences of these genes in D. lowei and D. miranda to the respective genomes using BLASTN (cutoff 10−5). Upon manual inspection of the alignments, we found that only 1 out of 21 genes in D. miranda (gene ID: GA23486) and 1 out of 14 genes in D. lowei (gene ID: GA23807) had a second hit on an autosome covering at least 50% of the length of the query gene. Other genes either produced a single best hit on the XR chromosome or spurious short hits on other chromosomes (data not shown). Thus, we conclude that duplication of orphans cannot explain the excess of pseudogenized orphans on XR. Nevertheless, our analysis clearly indicates that the emergence of the neo-X chromosome influenced the orphan dynamics on XR, affecting rates of both gain and loss, thus we excluded this chromosome arm for our analyses of the rate of orphan turnover.10.7554/eLife.01311.013Figure 8.Orphans predating the XL-XR fusion are preferentially lost on the neo-X.


The life cycle of Drosophila orphan genes.

Palmieri N, Kosiol C, Schlötterer C - Elife (2014)

Orphans predating the XL-XR fusion are preferentially lost on the neo-X.For three terminal branches (D. lowei, D. miranda, and D. persimilis) the fraction of lost genes for each age class is shown. Each autosome and both X-chromosome arms are shown in different color. At node 4, where the neo-X originated, we observed the highest rate of orphan pseudogenization on the neo-X (A). Notably, this effect is not seen for younger orphans (B and C) neither for old genes (D).DOI:http://dx.doi.org/10.7554/eLife.01311.013
© Copyright Policy - open-access
Related In: Results  -  Collection

License
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getmorefigures.php?uid=PMC3927632&req=5

fig8: Orphans predating the XL-XR fusion are preferentially lost on the neo-X.For three terminal branches (D. lowei, D. miranda, and D. persimilis) the fraction of lost genes for each age class is shown. Each autosome and both X-chromosome arms are shown in different color. At node 4, where the neo-X originated, we observed the highest rate of orphan pseudogenization on the neo-X (A). Notably, this effect is not seen for younger orphans (B and C) neither for old genes (D).DOI:http://dx.doi.org/10.7554/eLife.01311.013
Mentions: The analysis of orphans that have putatively lost their function via the acquisition of a stop codon or a frame shift causing insertion/deletion (pseudogenized/lost orphans) reveals another interesting feature of the XL–XR fusion. The oldest orphans in our dataset (age class 4) show a pronounced excess of pseudogenized orphans on XR in D. affinis and D. miranda (Figure 8A). This trend was not observed for orphans that emerged on XR after the XL–XR fusion (Figure 8B,C), nor for old genes (Figure 8D) and is not due to an increased rate of orphan gain on XR (Figure 9). Since the oldest orphans (age class 4) on XR are a mixture of autosomal (i.e., before the fusion) and sex-chromosomal (i.e., after the fusion) orphans, we speculate that the high rate of pseudogenization of orphans on the XR may reflect the new X-linkage of previously autosomal orphans. A previous study (Meisel et al., 2009) found that the XR chromosome has experienced a burst of gene duplications to autosomes after its creation. It is plausible that after the conversion of the XR from autosome to sex-chromosome, orphans might have been duplicated to autosomes, whereas the XR ancestral copy would have become pseudogenized. To test this hypothesis, we looked for evidence of gene duplications for the orphans lost on the XR at node 4 (Figure 6). We aligned the sequences of these genes in D. lowei and D. miranda to the respective genomes using BLASTN (cutoff 10−5). Upon manual inspection of the alignments, we found that only 1 out of 21 genes in D. miranda (gene ID: GA23486) and 1 out of 14 genes in D. lowei (gene ID: GA23807) had a second hit on an autosome covering at least 50% of the length of the query gene. Other genes either produced a single best hit on the XR chromosome or spurious short hits on other chromosomes (data not shown). Thus, we conclude that duplication of orphans cannot explain the excess of pseudogenized orphans on XR. Nevertheless, our analysis clearly indicates that the emergence of the neo-X chromosome influenced the orphan dynamics on XR, affecting rates of both gain and loss, thus we excluded this chromosome arm for our analyses of the rate of orphan turnover.10.7554/eLife.01311.013Figure 8.Orphans predating the XL-XR fusion are preferentially lost on the neo-X.

Bottom Line: Interestingly, recently emerged orphans are more likely to be lost than older ones.Furthermore, highly expressed orphans with a strong male-bias are more likely to be retained.Since both lost and retained orphans show similar evolutionary signatures of functional conservation, we propose that orphan loss is not driven by high rates of sequence evolution, but reflects lineage-specific functional requirements.

View Article: PubMed Central - PubMed

Affiliation: Institut für Populationsgenetik, Vetmeduni Vienna, Vienna, Austria.

ABSTRACT
Orphans are genes restricted to a single phylogenetic lineage and emerge at high rates. While this predicts an accumulation of genes, the gene number has remained remarkably constant through evolution. This paradox has not yet been resolved. Because orphan genes have been mainly analyzed over long evolutionary time scales, orphan loss has remained unexplored. Here we study the patterns of orphan turnover among close relatives in the Drosophila obscura group. We show that orphans are not only emerging at a high rate, but that they are also rapidly lost. Interestingly, recently emerged orphans are more likely to be lost than older ones. Furthermore, highly expressed orphans with a strong male-bias are more likely to be retained. Since both lost and retained orphans show similar evolutionary signatures of functional conservation, we propose that orphan loss is not driven by high rates of sequence evolution, but reflects lineage-specific functional requirements. DOI: http://dx.doi.org/10.7554/eLife.01311.001.

No MeSH data available.


Related in: MedlinePlus