Rapid Y degeneration and dosage compensation in plant sex chromosomes

Abstract

The nonrecombining regions of animal Y chromosomes are known to undergo genetic degeneration, but previous work has failed to reveal large-scale gene degeneration on plant Y chromosomes. Here, we uncover rapid and extensive degeneration of Y-linked genes in a plant species, Silene latifolia, that evolved sex chromosomes de novo in the last 10 million years. Previous transcriptome-based studies of this species missed unexpressed, degenerate Y-linked genes. To identify sex-linked genes, regardless of their expression, we sequenced male and female genomes of S. latifolia and integrated the genomic contigs with a high-density genetic map. This revealed that 45% of Y-linked genes are not expressed, and 23% are interrupted by premature stop codons. This contrasts with X-linked genes, in which only 1.3% of genes contained stop codons and 4.3% of genes were not expressed in males. Loss of functional Y-linked genes is partly compensated for by gene-specific up-regulation of X-linked genes. Our results demonstrate that the rate of genetic degeneration of Y-linked genes in S. latifolia is as fast as in animals, and that the evolutionary trajectories of sex chromosomes are similar in the two kingdoms.

Keywords: Y degeneration; dosage compensation; gene expression; plants; sex chromosome evolution.

Fig. 1.

Synonymous divergence between homologous X- and Y-linked genes plotted against position in the genetic map of the X chromosome. The PAR extends to the right of this plot, from 64 to 114 cM. The curve is a fourth-order polynomial fitted to the data. Mapped X-linked genes with no homologous reconstructed Y-linked copy are shown as open circles on the horizontal axis. Data points corresponding to genes that were mapped in previous studies (22, 38) are represented by crossed circles and labeled with gene names used previously. Gray rectangles at the top signify approximate locations of the evolutionary strata, as defined in ref. .

Fig. 2.

Distribution of relative transcript abundance in S. latifolia males and females. (A) Relative male (m) versus female (f) expression for autosomal genes with known positions in the genetic map (1,657 genes). (B) Expression of Y-linked genes in males normalized by expression of X-linked gametologs in females (866 genes). (C) Expression of X-linked genes in males relative to females (848 genes). The curve shows the kernel-smoothed density function.

Fig. 3.

Probability density histograms of relative transcript abundance for X-linked genes in S. latifolia males and females (mX/fXX). The data are partitioned according to transcript abundance for Y-linked genes in S. latifolia males (mY) compared with S. vulgaris (Sv) (A–D) and quartiles for synonymous divergence (dS) between homologous X- and Y-linked genes (E–H). (A) Genes with mY/Sv ≥ 0.667 (176 genes); (B) 0.667 > mY/Sv ≥ 0.256 (201 genes); (C): 0.256 > mY/Sv ≥ 0.0001 (250 genes); and (D): mY = 0 (233 genes). (E) Includes the genes with dS ≤ 0.038 (225 genes); (F) 0.038 < dS ≤ 0.0602 (218 genes); (G) 0.0602 < dS ≤ 0.0975 (212 genes); and (H) dS > 0.0975 (216 genes). The curve shows the kernel-smoothed density function.

Fig. 4.

Relative transcript abundance in males and females for genes with known genetic positions on S. latifolia X chromosome. Expression ratios are shown for sex-linked genes with detectable expression (>0) (black points) or no expression (colored points) of the Y gametolog in males. Colors denote Gaussian mixed-model clusters based on mX/fXX expression ratios. Red and green points correspond to putatively dosage compensated and noncompensated genes, respectively. Blue points denote genes falling in the small cluster with high mX/fXX expression ratio. Dotted lines mark the null expectation for complete dosage compensation [log₂(mX/fXX) = 0] and no compensation [log₂(mX/fXX) = −1].