Sequencing the Mouse Y Chromosome Reveals Convergent Gene Acquisition and Amplification on Both Sex Chromosomes

Soh, Y. Q. Shirleen; Alföldi, Jessica; Pyntikova, Tatyana; Brown, Laura G.; Graves, Tina; Minx, Patrick; Fulton, Robert S.; Kremitzki, Colin; Koutseva, Natalia; Mueller, Jacob L.; Rozen, Steve; Hughes, Jennifer F.; Owens, Elaine; Womack, James E.; Murphy, William J.; Cao, Qing; Jong, Pieter J. de; Warren, Wesley C.; Wilson, Richard K.; Skaletsky, Helen; Page, David C.

doi:10.1016/j.cell.2014.09.052

Cited by 301 publications

(414 citation statements)

References 102 publications

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“…A recent report in mouse also suggests that amplification of Y-linked ampliconic genes is driven by the gene amplification of the gametologous X-linked gene pairs to restore an optimal sex ratio (36). However, in great apes, ampliconic regions on the Y and X are of different origin (37,38), suggesting that a mechanism to adjust sex ratio may not involve correlated amplification between gametologous gene pairs.…”

Section: Discussionmentioning

confidence: 99%

Extreme selective sweeps independently targeted the X chromosomes of the great apes

Nam¹,

Dutheil

Schierup

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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The unique inheritance pattern of the X chromosome exposes it to natural selection in a way that is different from that of the autosomes, potentially resulting in accelerated evolution. We perform a comparative analysis of X chromosome polymorphism in 10 great ape species, including humans. In most species, we identify striking megabase-wide regions, where nucleotide diversity is less than 20% of the chromosomal average. Such regions are found exclusively on the X chromosome. The regions overlap partially among species, suggesting that the underlying targets are partly shared among species. The regions have higher proportions of singleton SNPs, higher levels of population differentiation, and a higher nonsynonymous-to-synonymous substitution ratio than the rest of the X chromosome. We show that the extent to which diversity is reduced is incompatible with direct selection or the action of background selection and soft selective sweeps alone, and therefore, we suggest that very strong selective sweeps have independently targeted these specific regions in several species. The only genomic feature that we can identify as strongly associated with loss of diversity is the location of testis-expressed ampliconic genes, which also have reduced diversity around them. We hypothesize that these genes may be responsible for selective sweeps in the form of meiotic drive caused by an intragenomic conflict in male meiosis. X-chromosome evolution | great apes | selective sweeps | ampliconic genes | meiotic drive

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Section: Discussionmentioning

confidence: 99%

Extreme selective sweeps independently targeted the X chromosomes of the great apes

Nam¹,

Dutheil

Schierup

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…However, in other respects, the Anopheles and Drosophila Y are much more similar. More than one-third of the human Y chromosome and 99.9% of the mouse Y is euchromatic (56,62), whereas Drosophila and Anopheles Y chromosomes are entirely heterochromatic. Although relatively few in number, some ancestral X-Y gene pairs have been conserved throughout mammalian evolution because of their vital role as dosage-sensitive regulators of global gene expression (6,7).…”

Section: Discussionmentioning

confidence: 99%

Radical remodeling of the Y chromosome in a recent radiation of malaria mosquitoes

Hall

Papathanos

Sharma

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

100

152

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Y chromosomes control essential male functions in many species, including sex determination and fertility. However, because of obstacles posed by repeat-rich heterochromatin, knowledge of Y chromosome sequences is limited to a handful of model organisms, constraining our understanding of Y biology across the tree of life. Here, we leverage long single-molecule sequencing to determine the content and structure of the nonrecombining Y chromosome of the primary African malaria mosquito, Anopheles gambiae. We find that the An. gambiae Y consists almost entirely of a few massively amplified, tandemly arrayed repeats, some of which can recombine with similar repeats on the X chromosome. Sex-specific genome resequencing in a recent species radiation, the An. gambiae complex, revealed rapid sequence turnover within An. gambiae and among species. Exploiting 52 sex-specific An. gambiae RNA-Seq datasets representing all developmental stages, we identified a small repertoire of Y-linked genes that lack X gametologs and are not Y-linked in any other species except An. gambiae, with the notable exception of YG2, a candidate male-determining gene. YG2 is the only gene conserved and exclusive to the Y in all species examined, yet sequence similarity to YG2 is not detectable in the genome of a more distant mosquito relative, suggesting rapid evolution of Y chromosome genes in this highly dynamic genus of malaria vectors. The extensive characterization of the An. gambiae Y provides a long-awaited foundation for studying male mosquito biology, and will inform novel mosquito control strategies based on the manipulation of Y chromosomes.

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“…However, analysis of map positions of these genes revealed no such physical overlap or proximity. We also investigated the distribution of miRNA genes among regions of the mouse X chromosome reported to be most highly conserved (the XCR region) (Graves et al, 1995) or more recently added during evolution (the XAR and New regions) (Graves et al, 1995;Soh et al, 2014). We found that all three types of miRNA loci are located predominantly in the more recently added regions of the X chromosome, with a preponderance (∼80%) of Type I miRNA genes mapping within the XAR region, whereas Type II and III miRNA genes were equally distributed among the XAR and New regions.…”

Section: Discussionmentioning

confidence: 99%

Escape of X-linked miRNA genes from meiotic sex chromosome inactivation

et al. 2015

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Past studies have indicated that transcription of all X-linked genes is repressed by meiotic sex chromosome inactivation (MSCI) during the meiotic phase of spermatogenesis in mammals. However, more recent studies have shown an increase in steady-state levels of certain X-linked miRNAs in pachytene spermatocytes, suggesting that either synthesis of these miRNAs increases or that degradation of these miRNAs decreases dramatically in these cells. To distinguish between these possibilities, we performed RNA-FISH to detect nascent transcripts from multiple miRNA genes in various spermatogenic cell types. Our results show definitively that Type I X-linked miRNA genes are subject to MSCI, as are all or most X-linked mRNA genes, whereas Type II and III X-linked miRNA genes escape MSCI by continuing ongoing, active transcription in primary spermatocytes. We corroborated these results by co-localization of RNA-FISH signals with both a corresponding DNA-FISH signal and an immunofluorescence signal for RNA polymerase II. We also found that X-linked miRNA genes that escape MSCI locate non-randomly to the periphery of the XY body, whereas genes that are subject to MSCI remain located within the XY body in pachytene spermatocytes, suggesting that the mechanism of escape of X-linked miRNA genes from MSCI involves their relocation to a position outside of the repressive chromatin domain associated with the XY body. The fact that Type II and III X-linked miRNA genes escape MSCI suggests an immediacy of function of the encoded miRNAs specifically required during the meiotic stages of spermatogenesis.

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Sequencing the Mouse Y Chromosome Reveals Convergent Gene Acquisition and Amplification on Both Sex Chromosomes

Cited by 301 publications

References 102 publications

Extreme selective sweeps independently targeted the X chromosomes of the great apes

Extreme selective sweeps independently targeted the X chromosomes of the great apes

Radical remodeling of the Y chromosome in a recent radiation of malaria mosquitoes

Escape of X-linked miRNA genes from meiotic sex chromosome inactivation

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