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

Summary 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.