Immediate Dosage Compensation Is Triggered by the Deletion of Y-Linked Genes in Silene latifolia

The 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.