Chromosomal Gene Movements Reflect the Recent Origin and Biology of Therian Sex Chromosomes

Abstract

Mammalian sex chromosomes stem from ancestral autosomes and have substantially differentiated. It was shown that X-linked genes have generated duplicate intronless gene copies (retrogenes) on autosomes due to this differentiation. However, the precise driving forces for this out-of-X gene “movement” and its evolutionary onset are not known. Based on expression analyses of male germ-cell populations, we here substantiate and extend the hypothesis that autosomal retrogenes functionally compensate for the silencing of their X-linked housekeeping parental genes during, but also after, male meiotic sex chromosome inactivation (MSCI). Thus, sexually antagonistic forces have not played a major role for the selective fixation of X-derived gene copies in mammals. Our dating analyses reveal that although retrogenes were produced ever since the common mammalian ancestor, selectively driven retrogene export from the X only started later, on the placental mammal (eutherian) and marsupial (metatherian) lineages, respectively. Together, these observations suggest that chromosome-wide MSCI emerged close to the eutherian–marsupial split approximately 180 million years ago. Given that MSCI probably reflects the spread of the recombination barrier between the X and Y, crucial for their differentiation, our data imply that these chromosomes became more widely differentiated only late in the therian ancestor, well after the divergence of the monotreme lineage. Thus, our study also provides strong independent support for the recent notion that our sex chromosomes emerged, not in the common ancestor of all mammals, but rather in the therian ancestor, and therefore are much younger than previously thought.

Pollen-Specific Activation of Arabidopsis Retrogenes Is Associated with Global Transcriptional Reprogramming

“…Since retrotransposon reverse transcriptases favor specific sequences in combination with transcript folding (Ohshima, 2013), it is possible that such structures exist also in transcripts of some protein genes. Similar to other plant and animal studies (Marques et al, 2005;Potrzebowski et al, 2008;Sakai et al, 2011), we have confirmed that parents are generally strongly and ubiquitously transcribed, indicating that higher amounts of transcript may increase the probability of retroposition. Although produced by the retrotransposon amplification machinery, they are located in gene-rich chromosome arms in Arabidopsis and thus fundamentally differ in their genomic distribution from repetitive elements.…”

“…Second, we observed many nonretrogene genes with pollen-specific transcription. The second model proposes spermatocyte-specific transcriptional reprogramming by global chromatin changes and transcriptional activation of retrogenes and their subsequent functionalization specific to spermatocytes (Marques et al, 2005;Potrzebowski et al, 2008). In plants, pollen has been identified as the hotspot of chromatin reprogramming (Slotkin et al, 2009;Ibarra et al, 2012;Hoffmann and Palmgren, 2013), and we have shown that pollen upregulated genes are depleted from transcription-permissive chromatin marks in somatic tissues.…”

Recent de novo origin of human protein-coding genes

“…There are many examples in the literature of new genes with functionality in brain and testis (Burki and Kaessmann 2004;Emerson et al 2004;Begun et al 2007;Potrzebowski et al 2008;Rosso et al 2008;Zhou et al 2008). One of the novel genes is expressed in male reproductive tissue and one was identified in brain tissues, but they were also identified in many other tissues (Table 1) and there is no statistical trend.…”

Extensive Structural Renovation of Retrogenes in the Evolution of the Populus Genome

“…For example, the meiotic sex chromosome inactivation may be responsible for driving male genes out of the X chromosome in mammals, and sexual antagonisms may enhance the fixation probability of new male genes into autosomes in Drosophila (Rice, 1984;Sturgill et al, 2007). The origination of meiotic sex chromosome inactivation and the male retrogene movement were found to be associated (Potrzebowski et al, 2008). The genetic control of sex determination and related genetic processes were a consequence of a long evolutionary process in which a pair of sex chromosomes was completely developed.…”