Gene expression, chromosome heterogeneity and the fast-X effect in mammals

Nguyen, Linh-Phuong; Galtier, Nicolas

doi:10.1098/rsbl.2015.0010

Cited by 18 publications

(12 citation statements)

References 16 publications

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“…Such negative correlations between substitution rates and expression levels have already been observed in several species ( Drummond et al. 2005 ; Nguyen et al. 2015 ; Zhang and Yang 2015 ).…”

Section: Discussionsupporting

confidence: 61%

Disentangling the Causes for Faster-X Evolution in Aphids

Jaquiéry

Peccoud

Ouisse

et al. 2018

Genome Biology and Evolution

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The faster evolution of X chromosomes has been documented in several species, and results from the increased efficiency of selection on recessive alleles in hemizygous males and/or from increased drift due to the smaller effective population size of X chromosomes. Aphids are excellent models for evaluating the importance of selection in faster-X evolution because their peculiar life cycle and unusual inheritance of sex chromosomes should generally lead to equivalent effective population sizes for X and autosomes. Because we lack a high-density genetic map for the pea aphid, whose complete genome has been sequenced, we first assigned its entire genome to the X or autosomes based on ratios of sequencing depth in males (X0) to females (XX). Then, we computed nonsynonymous to synonymous substitutions ratios (dN/dS) for the pea aphid gene set and found faster evolution of X-linked genes. Our analyses of substitution rates, together with polymorphism and expression data, showed that relaxed selection is likely to be the greatest contributor to faster-X because a large fraction of X-linked genes are expressed at low rates and thus escape selection. Yet, a minor role for positive selection is also suggested by the difference between substitution rates for X and autosomes for male-biased genes (but not for asexual female-biased genes) and by lower Tajima’s D for X-linked compared with autosomal genes with highly male-biased expression patterns. This study highlights the relevance of organisms displaying alternative chromosomal inheritance to the understanding of forces shaping genome evolution.

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Section: Discussionsupporting

confidence: 61%

Disentangling the Causes for Faster-X Evolution in Aphids

Jaquiéry

Peccoud

Ouisse

et al. 2018

Genome Biology and Evolution

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“…This questions whether prior trends ascribed to sexual antagonism might not have an alternative explanation, possibly related to the commonly reported faster evolution of reproduction-related genes [ 55 – 57 ] and hemizygosity of the X. Against such a hypothesis is the recent finding that in mammals any faster sequence evolution of X-linked genes is not owing to hemizygosity, but can be accounted for in terms of GC-bias and low expression [ 58 ]. No matter what the explanation, that the trends are seen after controlling for expression maxima suggests that the enrichment of reproduction-related genes is not simply explained by our maximal expression hypothesis, but neither is it necessarily owing to sex specificity per se.…”

Section: Discussionmentioning

confidence: 99%

The Constrained Maximal Expression Level Owing to Haploidy Shapes Gene Content on the Mammalian X Chromosome

et al. 2015

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X chromosomes are unusual in many regards, not least of which is their nonrandom gene content. The causes of this bias are commonly discussed in the context of sexual antagonism and the avoidance of activity in the male germline. Here, we examine the notion that, at least in some taxa, functionally biased gene content may more profoundly be shaped by limits imposed on gene expression owing to haploid expression of the X chromosome. Notably, if the X, as in primates, is transcribed at rates comparable to the ancestral rate (per promoter) prior to the X chromosome formation, then the X is not a tolerable environment for genes with very high maximal net levels of expression, owing to transcriptional traffic jams. We test this hypothesis using The Encyclopedia of DNA Elements (ENCODE) and data from the Functional Annotation of the Mammalian Genome (FANTOM5) project. As predicted, the maximal expression of human X-linked genes is much lower than that of genes on autosomes: on average, maximal expression is three times lower on the X chromosome than on autosomes. Similarly, autosome-to-X retroposition events are associated with lower maximal expression of retrogenes on the X than seen for X-to-autosome retrogenes on autosomes. Also as expected, X-linked genes have a lesser degree of increase in gene expression than autosomal ones (compared to the human/Chimpanzee common ancestor) if highly expressed, but not if lowly expressed. The traffic jam model also explains the known lower breadth of expression for genes on the X (and the Z of birds), as genes with broad expression are, on average, those with high maximal expression. As then further predicted, highly expressed tissue-specific genes are also rare on the X and broadly expressed genes on the X tend to be lowly expressed, both indicating that the trend is shaped by the maximal expression level not the breadth of expression per se. Importantly, a limit to the maximal expression level explains biased tissue of expression profiles of X-linked genes. Tissues whose tissue-specific genes are very highly expressed (e.g., secretory tissues, tissues abundant in structural proteins) are also tissues in which gene expression is relatively rare on the X chromosome. These trends cannot be fully accounted for in terms of alternative models of biased expression. In conclusion, the notion that it is hard for genes on the Therian X to be highly expressed, owing to transcriptional traffic jams, provides a simple yet robustly supported rationale of many peculiar features of X’s gene content, gene expression, and evolution.

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“…Possible reasons for this observation were discussed in depth in [ 4 ]. Furthermore, the mean level of gene expression is similar for the X and autosomes, and the GC content at third coding positions is somewhat higher for the X [ 12 ], so that a lower level of X chromosome gene expression or GC content cannot contribute to the Drosophila Faster-X effect, in contrast to the situation in mammals [ 13 ].…”

Section: Discussionmentioning

confidence: 99%

The effects of sex-biased gene expression and X-linkage on rates of adaptive protein sequence evolution inDrosophila

2015

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A faster rate of adaptive evolution of X-linked genes compared with autosomal genes may be caused by the fixation of new recessive or partially recessive advantageous mutations (the Faster-X effect). This effect is expected to be largest for mutations that affect only male fitness and absent for mutations that affect only female fitness. We tested these predictions in Drosophila melanogaster by using genes with different levels of sex-biased expression and by estimating the extent of adaptive evolution of non-synonymous mutations from polymorphism and divergence data. We detected both a Faster-X effect and an effect of male-biased gene expression. There was no evidence for a strong association between the two effects—modest levels of male-biased gene expression increased the rate of adaptive evolution on both the autosomes and the X chromosome, but a Faster-X effect occurred for both unbiased genes and female-biased genes. The rate of genetic recombination did not influence the magnitude of the Faster-X effect, ruling out the possibility that it reflects less Hill–Robertson interference for X-linked genes.

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Gene expression, chromosome heterogeneity and the fast-X effect in mammals

Cited by 18 publications

References 16 publications

Disentangling the Causes for Faster-X Evolution in Aphids

Disentangling the Causes for Faster-X Evolution in Aphids

The Constrained Maximal Expression Level Owing to Haploidy Shapes Gene Content on the Mammalian X Chromosome

The effects of sex-biased gene expression and X-linkage on rates of adaptive protein sequence evolution inDrosophila

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