The Origin and Evolution of Dioecy and Sex Chromosomes in Asparagus

Sex chromosomes have evolved multiple, independent times in the flowering plants, making them ideal systems to study both young and old sex chromosome pairs. Garden asparagus (Asparagus officinalis) is a dioecious vegetable crop species with a recently evolved, homomorphic sex chromosome pair which makes it ideal for studying the earliest events in sex chromosome evolution. Sex determination has been genetically mapped to a small (<2Mb) non-recombining region on the proto-Y chromosome that actively differentiates males (XY) from females (XX). Regardless of sex, all floral buds initiate as hermaphrodites, but anthers will degenerate in female flowers during tapetum development, whereas pistil development will arrest later in male flowers. This temporal separation of sterility events suggests that at least two sex determination genes are linked in the non-recombining region on the Y (Charlesworth & Charlesworth, 1978), but a two-gene hypothesis for sex determination has never been definitively tested in plants. We have identified two independent male-to-hermaphrodite mutants that implicate a single gene on the Y chromosome as responsible for dominantly interrupting pistil development. Anther development is not affected in these mutants. To identify the gene(s) responsible for anther sterility in females, we have assessed gene expression in male and female spears profiles and identified known anther development genes exhibiting male-biased expression. A small subset of genes exhibiting male-baised expression have also been identified as sex-linked. These results support the two-gene hypothesis of Charlesworth & Charlesworth by identifying a female suppressor that does not influence flower development.