Genetic degeneration of old and young Y chromosomes in the flowering plant Rumex hastatulus

Josh Hough; Jesse D. Hollister; Wei Wang; Spencer C. H. Barrett; Stephen I. Wright

doi:10.1073/pnas.1319227111

New Research In

Edited by James A. Birchler, University of Missouri-Columbia, Columbia, MO, and approved April 18, 2014 (received for review October 11, 2013)

Significance

Evolutionary theory predicts that in dioecious organisms with sex chromosomes, suppressed X-Y recombination should lead to a loss of Y-chromosome gene content and function. However, the extent to which this process occurs in plants, where sex chromosomes evolved relatively recently, is poorly understood. We tested for Y degeneration in Rumex hastatulus, an annual plant that has both XY and XY₁Y₂ sex chromosome systems. We found that Y-linked genes are undergoing degeneration despite their recent origin; they show a faster accumulation of amino acid substitutions, contain more unpreferred changes in codon usage, and are reduced in expression relative to X-linked alleles. Significantly, the magnitude of these effects depended on sex chromosome age, being greater for genes that have been nonrecombining for longer.

Abstract

Heteromorphic sex chromosomes have originated independently in many species, and a common feature of their evolution is the degeneration of the Y chromosome, characterized by a loss of gene content and function. Despite being of broad significance to our understanding of sex chromosome evolution, the genetic changes that occur during the early stages of Y-chromosome degeneration are poorly understood, especially in plants. Here, we investigate sex chromosome evolution in the dioecious plant Rumex hastatulus, in which X and Y chromosomes have evolved relatively recently and occur in two distinct systems: an ancestral XX/XY system and a derived XX/XY₁Y₂ system. This polymorphism provides a unique opportunity to investigate the effect of sex chromosome age on patterns of divergence and gene degeneration within a species. Despite recent suppression of recombination and low X-Y divergence in both systems, we find evidence that Y-linked genes have started to undergo gene loss, causing ∼28% and ∼8% hemizygosity of the ancestral and derived X chromosomes, respectively. Furthermore, genes remaining on Y chromosomes have accumulated more amino acid replacements, contain more unpreferred changes in codon use, and exhibit significantly reduced gene expression compared with their X-linked alleles, with the magnitude of these effects being greatest for older sex-linked genes. Our results provide evidence for reduced selection efficiency and ongoing Y-chromosome degeneration in a flowering plant, and indicate that Y degeneration can occur soon after recombination suppression between sex chromosomes.

Footnotes

↵¹To whom correspondence should be addressed. E-mail: josh.hough{at}utoronto.ca.

Author contributions: J.H., S.C.H.B., and S.I.W. designed research; J.H. and S.I.W. performed research; J.H., J.D.H., and W.W. contributed new reagents/analytic tools; J.H., J.D.H., W.W., and S.I.W. analyzed data; and J.H., J.D.H., S.C.H.B., and S.I.W. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The sequences reported in this paper have been deposited in GenBank's Short Read Archive (SRA) [accession nos. SRP041588 (Rumex hastatulus) and SRP041613 (Rumex bucephalophorus)].
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1319227111/-/DCSupplemental.

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