Heteromorphic XY chromosomes with pericentromeric recombination suppression in Hippophae (Elaeagnaceae)

Among the relatively few flowering plants with strongly heteromorphic XY chromosomes are dioecious species of Hippophae (Elaeagnaceae). To understand the evolution of these sex chromosomes, we generated haplotype-resolved genomes for H. rhamnoides and H. tibetana, carried out ancestral karyotype reconstruction using Elaeagnus mollis (with bisexual flowers) as the outgroup, inferred the location of the sex-linked regions (SLRs), and used transcriptome data to test for dosage compensation. In H. rhamnoides, the X chromosome is 30% larger than the Y and in H. tibetana 15%, a difference primarily due to the accumulation of repetitive sequences on the X and extensive gene loss on the Y in H. rhamnoides. Both sex chromosome pairs have an older (S1, 6.3-7.6 million years ago (Ma)) and a younger stratum (S2, 1.9-2.5 Ma), the latter with more species-specific inversions. The SLRs coincide with the pericentromere regions, which already in the ancestor of Hippophae were greatly enlarged by the insertion of another chromosome. Dosage compensation occurs primarily in floral tissues and mainly through downregulation of female X-specific genes, balancing expression between the sexes in floral tissues. These results add to the growing evidence for SLRs often evolving in pericentromeric regions, which are prone to extensive rearrangements and have low recombination frequencies.