Abstract
SummaryThe loss of functional genes from non-recombining sex-specific chromosomes [1, 2], such as the Y chromosomes in mammals [3] or W chromosomes in birds [4], should result in an imbalance of gene products for sex-linked genes [5]. Different chromosome-wide systems that rebalance gene expression are known to operate in organisms with relatively old sex chromosomes [6]; e.g., Drosophila overexpress X-linked genes in males [7], while mammals shut down one of the X chromosomes in females [8]. It is not known how long it takes for a chromosome-wide dosage compensation system to evolve. To shed light on the early evolution of dosage compensation, we constructed a high-density Y-deletion map and used deletion mutants to manipulate gene dose and analyze gene expression in white campion (Silene latifolia), which evolved dioecy and sex chromosomes only 11 million years ago [9]. We demonstrate that immediate dosage compensation can be triggered by deletions in a large portion of the p arm of the Y chromosome. Our results indicate that dosage compensation in S. latifolia does not have to evolve gene by gene because a system to upregulate gene expression is already operating on part of the X chromosome, which likely represents an intermediate step in the evolution of a chromosome-wide dosage compensation system in this species.
Highlights
Y Deletion Mutants and the Deletion Map of S. latifolia Y Chromosome In this study, we used 101 S. latifolia Y-deletion mutants (Table S1), 67 of which have not been described previously
The de novo evolution of sex chromosomes in Silene latifolia (Caryophyllaceae) only 11 million years ago [9] offers a rare opportunity to analyze the early stages of sex chromosome evolution, with actively progressing Y degeneration and evolving dosage compensation (DC) ‘‘caught in action.’’ The previous studies on S. latifolia [12, 13] reported signs of a nascent DC system upregulating X-linked genes with degenerate or partially degenerate Y-linked gametologs—the homologous genes shared between the X and the non-recombining Y chromosomes
It remains unclear whether DC has to evolve gene by gene—independently at each sexlinked gene that lost its Y-linked gametolog or if some form of chromosome- or region-wide DC is already present on S. latifolia sex chromosomes
Summary
Y Deletion Mutants and the Deletion Map of S. latifolia Y Chromosome In this study, we used 101 S. latifolia Y-deletion mutants (Table S1), 67 of which have not been described previously. All these mutants were generated by heavy ion irradiation of pollen grains or dry seeds [14]. As Y-deletion mutants contain Y chromosomes, they are genetically males, but deletions of sex-determining SPF and/or GSF genes altered the presence of stamens and pistils in the flower (Table S1). No deletions outside the Y chromosome were found except one autosomal deletion in linkage group 4 of mutant mut (see below)
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