Abstract
Intragenomic conflicts arise when a genetic element favours its own transmission to the detriment of others. Conflicts over sex chromosome transmission are expected to have influenced genome structure, gene regulation, and speciation. In the mouse, the existence of an intragenomic conflict between X- and Y-linked multicopy genes has long been suggested but never demonstrated. The Y-encoded multicopy gene Sly has been shown to have a predominant role in the epigenetic repression of post meiotic sex chromatin (PMSC) and, as such, represses X and Y genes, among which are its X-linked homologs Slx and Slxl1. Here, we produced mice that are deficient for both Sly and Slx/Slxl1 and observed that Slx/Slxl1 has an opposite role to that of Sly, in that it stimulates XY gene expression in spermatids. Slx/Slxl1 deficiency rescues the sperm differentiation defects and near sterility caused by Sly deficiency and vice versa. Slx/Slxl1 deficiency also causes a sex ratio distortion towards the production of male offspring that is corrected by Sly deficiency. All in all, our data show that Slx/Slxl1 and Sly have antagonistic effects during sperm differentiation and are involved in a postmeiotic intragenomic conflict that causes segregation distortion and male sterility. This is undoubtedly what drove the massive gene amplification on the mouse X and Y chromosomes. It may also be at the basis of cases of F1 male hybrid sterility where the balance between Slx/Slxl1 and Sly copy number, and therefore expression, is disrupted. To the best of our knowledge, our work is the first demonstration of a competition occurring between X and Y related genes in mammals. It also provides a biological basis for the concept that intragenomic conflict is an important evolutionary force which impacts on gene expression, genome structure, and speciation.
Highlights
Transmission distorters (TDs), known as segregation distorters or meiotic drivers, are genetic elements that are transmitted to the generation with a higher frequency than the expected 1:1 Mendelian inheritance ratio
We believe that the conflict in which Slx/Slxl1 and Sly are involved led to the amplification of X and Y genes and may have played an important role in mouse speciation
This study has shown that Slx/Slxl1 are indispensable for normal sperm differentiation, and that Slx/Slxl1 deficiency leads to the deregulation of a number of autosomal genes [28]
Summary
Transmission distorters (TDs), known as segregation distorters or meiotic drivers, are genetic elements that are transmitted to the generation with a higher frequency than the expected 1:1 Mendelian inheritance ratio. The non-recombining region of the heteromorphic sex chromosomes is the largest genomic example of recombination suppression [4], with the consequent potential for TDs to arise and distort the population sex ratio. In Drosophila, the X- and Y-encoded multicopy genes Stellate and Suppressor of Stellate are believed to illustrate the genomic conflict theory since deletions of Su(Ste) locus lead to a derepression of Stellate associated with a distorted sex ratio towards an excess of females; but to date it remains unclear whether or not Stellate is a transmission distorter [7,8]. Intragenomic conflicts over sex chromosome transmission are predicted to have influenced genome structure, gene expression and speciation [2,3]. Sex ratio segregation distortion may be more frequent than observed as the distortion is often masked by the presence of a suppressor in wild-type (WT) populations [2,9,10,11,12,13,14,15]
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