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.sex chromosome evolution | Y degeneration | gene expression | dosage compensation | plants

Extremely low nucleotide diversity in the X-linked region of papaya caused by a strong selective sweep

“…Because X-linked regions spend a higher proportion of time in females, compared with autosomal genes, a higher mutation rate in males than females results in a lower mutation rate for the X than the autosomes [32, 33]. It is not known whether papaya has a sex difference in mutation rate, as is observed for some genes in another plant, S. latifolia [34]. Ideally, an Hudson–Kreitman–Aguadé (HKA) test should be done to establish whether the diversity for X-linked genes is significantly lower than expected, after taking account of mutation rate differences between different loci or genome regions [35].…”

“…However, this explanation can be excluded because an implausibly large mutation rate difference between PAR and X-linked genes would be required to account for the 12-fold diversity difference (or a more than 16-fold difference, taking account of the difference in N e ). Mutation rate differences in [34] are detectable only in the older stratum genes, implying that, in papaya, any such difference is likely to be minor. Taken together, therefore, the low nucleotide diversity in the X-linked region suggests a strong selective sweep caused by the spread of a beneficial mutation in the region.…”

Dosage compensation of the sex chromosomes and autosomes

“…Complete dosage compensation by upregulation of the male X chromosome evolved independently in Drosophila melanogaster and in a mosquito Anopheles stephensi [99], while in another insect, Heliconius butterfly, there is only partial dosage compensation [100]. In a plant ( Silene latifola ) with newly evolved sex chromosomes no global dosage compensation between sexes was detected in one study [101], while two others showed increased X expression [102, 103], further demonstrating the difficulty of reaching a consensus. In C. elegans an initial study that showed absence of X upregulation [83] was subsequently shown to be flawed because it did not take into account the progressive accumulation of germ cells in which the X chromosome is silenced [84].…”

Sequence diversity patterns suggesting balancing selection in partially sex‐linked genes of the plant Silene latifolia are not generated by demographic history or gene flow

“…; Papadopulos et al . ). Although the mechanism by which new strata form is not yet certain, new sex‐linked regions in some organisms have formed without events such as sex chromosome–autosome translocations adding new regions onto the sex chromosomes (e.g.…”