Evolution of heteromorphic XY chromosomes in sea buckthorn via chromosomal fusion followed by inversions and tissue-specific dosage compensation

Abstract Recombination suppression is crucial for the evolution of sex chromosomes, but remains poorly understood. Two recent models explaining recombination suppression start with the occurrence of a chance inversion that includes a sex-determining gene and that becomes established either because it shelters recessive deleterious mutations or instead because dosage compensation stabilizes the inversion. We assembled the male and female genomes of the sea buckthorn (Hippophae rhamnoides), a shrub with large X and small Y chromosomes, and compared them to the chromosomes of a relative with bisexual flowers representing the ancestral condition. The sex-determining region of 13-15 Mb is located inside the fusion site of two ancestral chromosomes and coincides with a large inversion, while an adjacent younger stratum includes four inversions, and an even younger stratum two inversions. Using de novo transcriptome data from five tissues, we quantified tissue-specific gene expression and found that dosage compensation is mainly achieved through the upregulation of X-specific genes in males. Few genes with sex-biased expression were found in the three strata. These data fit with models that focus on sequential inversions and dosage compensation and poorly match the classic model of an increasing accumulation of sexually antagonistic genes leading to recombination suppression.