Divergence of X and Y Chromosomes in Asparagus

An elegant model for the conversion of an autosomal pair in a hermaphroditic species to a sex chromosome in a dioecious species was formalized by Deborah and Brian Charlesworth in 1978. Briefly, the conversion from autosome to sex chromosome could require just two loci linked perfectly in non-recombination on a young Y chromosome: one locus must dominantly suppress female (pistil) organogenesis, while another locus must promote the formation of male (anther) organogenesis, but this model has never had strong genic support in any dioecious species. Garden asparagus (Asparagus officinalis) is an ideal system to test this question, given that the X and Y sex chromosomes are evolutionarily young and cytologically homomorphic. Leveraging a doubled haploid YY individual and a doubled haploid mapping population, we generated a chromosome-level genome assembly using Illumina, PacBio, and Bionano optical maps and identified a 1Mb region of non-recombination on the Y chromosome that is largely missing from the X. Several independent male-to-hermaphrodite mutants (gamma irradiation, spontaneous SNP) implicate a single gene SOFF (Suppressor of Female Function) on the Y chromosome as being responsible for female suppression. While only 12 gene annotations are in this non-recombining region, there exists Tapetum Development and Function 1, a gene with an Arabidopsis knockout phenotype very similar to Asparagus females. With an additional PacBio and optical map genome assembly for a sibling XX female, we have compared the structure of the X and Y chromosomes and identified ~130kb of X-specific sequence, including several X-specific genes. This is the strongest evidence to date for the Charlesworth’s “two gene” model.