Two independent origins of XY sex chromosomes in Asparagus

Abstract

The relatively young and repeated evolutionary origins of dioecy (separate sexes) in flowering plants enables the investigation of molecular dynamics occurring at the earliest stages of sex chromosome evolution. With two independently young origins of dioecy, Asparagus is a model genus for studying the genetics of sex-determination and sex chromosome evolution. Dioecy first evolved in Asparagus ∼3 to 4 million years ago (Ma) in the ancestor of a now widespread Eurasian clade including garden asparagus (Asparagus officinalis). A second origin occurred in a smaller, geographically restricted, Mediterranean Basin clade, including Asparagus horridus. New haplotype-resolved reference genomes for garden asparagus and A. horridus, elucidate contrasting first steps in the origin of the sex chromosomes of the Eurasian and Mediterranean Basin clade ancestors. Analysis of the A. horridus genome revealed an XY system derived from a different ancestral pair of autosomes with different sex-determining genes than have been characterized for garden asparagus. We estimate that proto-XY chromosomes evolved 1 to 2 Ma in the Mediterranean Basin clade, following a ∼2.1-megabase inversion that now distinguishes the X and Y chromosomes. Recombination suppression and LTR retrotransposon accumulation drove the expansion of the male-specific region on the Y (MSY) that reaches ∼9.6-megabases in A. horridus. The garden asparagus genome revealed an MSY spanning ∼1.9-megabases. A segmental duplication and neofunctionalization of one duplicated gene (SOFF) drove the origin of dioecy in the Eurasian clade. These findings support previous inference based on phylogeographic analysis revealing two recent origins of dioecy in Asparagus and establish the genus as a model for investigating sex chromosome evolution.