Genomic imprinting mediates dosage compensation in a young plant XY system.: An article peer-reviewed and recommended by Peer Community In Evolutionary Biology (PCI Evol Biol)

This preprint has been reviewed and recommended by Peer Community In Evolutionary Biology (http://dx.doi.org/10.24072/pci.evolbiol.100044). Sex chromosomes have repeatedly evolved from a pair of autosomes. Consequently, X and Y chromosomes initially have similar gene content, but ongoing Y degeneration leads to reduced Y gene expression and eventual Y gene loss. The resulting imbalance in gene expression between Y genes and the rest of the genome is expected to reduce male fitness, especially when protein networks have components from both autosomes and sex chromosomes. A diverse set of dosage compensating mechanisms that alleviates these negative effects has been described in animals. However, the early steps in the evolution of dosage compensation remain unknown and dosage compensation is poorly understood in plants. Here we show a novel dosage compensation mechanism in the evolutionarily young XY sex determination system of the plant Silene latifolia. Genomic imprinting results in higher expression from the maternal X chromosome in both males and females. This compensates for reduced Y expression in males but results in X overexpression in females and may be detrimental. It could represent a transient early stage in the evolution of dosage compensation. Our finding has striking resemblance to the first stage proposed by Ohno for the evolution of X inactivation in mammals

Rapid De Novo Evolution of X Chromosome Dosage Compensation in Silene latifolia, a Plant with Young Sex Chromosomes

Evidence for dosage compensation in Silene latifolia, a plant with 10-million-year-old sex chromosomes, reveals that dosage compensation can evolve rapidly in young XY systems and is not an animal-specific phenomenon

Genomic imprinting mediates dosage compensation in a young plant XY system

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Genomic imprinting mediates dosage compensation in a young plant XY system

ISSN:2055-026XISSN:2055-027

Distribution of the ratio between the expression of the single X in males and the two X copies in females (Xmale/2Xfemale) for all sex-linked contigs.

<p>Different categories of sex-linked contigs are shown: Y/X ratio below 0.5 (379 contigs), Y/X ratio between 0.5 and 1 (656 contigs), Y/X ratio between 1 and 1.5 (315 contigs), Y/X ratio above 1.5 (195 contigs). Medians are indicated in the colour corresponding to each Y/X ratio category. When the contigs with high Xmale/2Xfemale ratios are removed as in <a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1001308#pbio-1001308-g003" target="_blank">Figure 3</a> (see text for explanations) the medians remain unaltered except for the category Y/X<0.5 where it changes to 0.76 but is still significantly different from 0.5 (Wilcoxon test, <i>p</i><10⁻¹⁶). Total X read numbers were summed at sex-linked SNP locations in each contig and normalized for each individual separately, then averaged among males and females to get the Xmale/2Xfemale ratio.</p

Distribution of Y/X expression ratios in <i>S. latifolia</i> males for the 1,736 sex-linked contigs.

<p>Total Y and X read numbers were summed at sex-linked SNP locations for each contig and normalized for each male separately, then averaged across males to obtain the Y/X ratio. The median is shown in red.</p

Expression levels of sex-linked contigs in both sexes for different Y/X expression ratio categories.

<p>Total read numbers were summed at sex-linked SNP locations and normalized for each individual and contig separately; medians for all contigs and individuals of the same sex were then obtained. Contigs with Y/X expression ratios above 1.5 were excluded, as well as contigs with Xmale/2Xfemale ratios above 2 (see text for explanations), which reduces the dataset to 1,346 sex-linked contigs. XX females, median expression level of both X-linked alleles in females; X males, median expression level of the single X-linked allele in males; Y males, median expression level of the Y-linked allele in males; XY males, median expression level of the X-linked plus Y-linked alleles in males. To compare different Y/X expression ratio categories, medians were normalized using the XX expression levels in females. Sample sizes are: 0–0.25, 110; 0.25–0.5, 269; 0.5–0.75, 315; 0.75–1, 341; 1–1.5, 315. Note that we do not have any contig with Y/X = 0 as our method did not allow us to detect such contigs (see <a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1001308#s4" target="_blank">Material and Methods</a>). Error bars indicate 95% confidence intervals.</p

Identifying new sex-linked genes through BAC sequencing in the dioecious plant Silene latifolia

Background Silene latifolia represents one of the best-studied plant sex chromosome systems. A new approach using RNA-seq data has recently identified hundreds of new sex-linked genes in this species. However, this approach is expected to miss genes that are either not expressed or are expressed at low levels in the tissue(s) used for RNA-seq. Therefore other independent approaches are needed to discover such sex-linked genes. Results Here we used 10 well-characterized S. latifolia sex-linked genes and their homologs in Silene vulgaris, a species without sex chromosomes, to screen BAC libraries of both species. We isolated and sequenced 4 Mb of BAC clones of S. latifolia X and Y and S. vulgaris genomic regions, which yielded 59 new sex-linked genes (with S. vulgaris homologs for some of them). We assembled sequences that we believe represent the tip of the Xq arm. These sequences are clearly not pseudoautosomal, so we infer that the S. latifolia X has a single pseudoautosomal region (PAR) on the Xp arm. The estimated mean gene density in X BACs is 2.2 times lower than that in S. vulgaris BACs, agreeing with the genome size difference between these species. Gene density was estimated to be extremely low in the Y BAC clones. We compared our BAC-located genes with the sex-linked genes identified in previous RNA-seq studies, and found that about half of them (those with low expression in flower buds) were not identified as sex-linked in previous RNA-seq studies. We compiled a set of ~70 validated X/Y genes and X-hemizygous genes (without Y copies) from the literature, and used these genes to show that X-hemizygous genes have a higher probability of being undetected by the RNA-seq approach, compared with X/Y genes; we used this to estimate that about 30 % of our BAC-located genes must be X-hemizygous. The estimate is similar when we use BAC-located genes that have S. vulgaris homologs, which excludes genes that were gained by the X chromosome. Conclusions Our BAC sequencing identified 59 new sex-linked genes, and our analysis of these BAC-located genes, in combination with RNA-seq data suggests that gene losses from the S. latifolia Y chromosome could be as high as 30 %, higher than previous estimates of 10-20 %