Two independent origins of XY sex chromosomes in Asparagus
The relatively young and repeated evolutionary origins of dioecy (separate sexes) in flowering plants enable investigation of molecular dynamics occurring at the earliest stages of sex chromosome evolution. With two independently young origins of dioecy in the genus, Asparagus is a model taxon for studying genetic sex-determination and sex chromosome evolution. Dioecy first evolved in Asparagus [~]3-4 million years ago (Ma) in the ancestor of a now widespread Eurasian clade that includes garden asparagus (Asparagus officinalis), while the second origin occurred in a smaller, geographically restricted, Mediterranean Basin clade including Asparagus horridus. The XY sex chromosomes and sex-determination genes in garden asparagus have been well characterized, but the genetics underlying dioecy in the Mediterranean Basin clade are unknown. We generated new haplotype-resolved reference genomes for garden asparagus and A. horridus, to elucidate the sex chromosomes of A. horridus and explore how dioecy evolved between these two closely related lineages. Analysis of the A. horridus genome revealed an independently evolved XY system derived from different ancestral autosomes (chromosome 3) with different sex-determining genes than documented for garden asparagus (on chromosome 1). We estimate that proto-XY chromosomes evolved around 1-2 Ma in the Mediterranean Basin clade, following an [~]2.1-megabase inversion between the ancestral pair. Recombination suppression and LTR retrotransposon accumulation drove the establishment and expansion of the Y-linked sex-determination region (Y-SDR) that now reaches [~]9.6-megabases in A. horridus. The new garden asparagus genome revealed a Y-SDR that spans [~]1.9-megabases with ten hemizygous genes. Our results evoke hemizygosity as the most probable mechanism responsible for the origin of proto-XY recombination suppression in the Eurasian clade, and that neofunctionalization of one duplicated gene (SOFF) drove the origin of dioecy. These findings support previous inference based on phylogeographic analysis revealing two recent origins of dioecy in Asparagus. Moreover, this work implicates alternative molecular mechanisms for two separate shifts to dioecy in a model taxon important for investigating young sex chromosome evolution. SIGNIFICANCE STATEMENTFlowering plants with separate sexes are ideal systems for investigating genome dynamics underlying the earliest stages of sex chromosome evolution across the tree of life. We use Asparagus as a model to better understand early sex chromosome formation more generally, by investigating how different XY sex chromosomes evolved between two young, closely related clades. Genomic comparisons of garden asparagus and Asparagus horridus (wild related species) revealed distinct evolutionary origins of XY-chromosomes with different sex-determination mechanisms. Whereas the garden asparagus Y-chromosome originally evolved around 3-4 million years ago (Ma), following a small segmental duplication, the Y-chromosome in Asparagus horridus evolved more recently ([~]1-2 Ma) following a large structural inversion between a different chromosome pair. Interestingly, both evolutionary transitions from hermaphroditism to separate sexes occurred as ancestors of garden asparagus and Asparagus horridus independently dispersed northward out of southern Africa.