Abstract
The origin and early evolution of sex chromosomes have been hypothesized to involve the linkage of factors with antagonistic effects on male and female function. Garden asparagus (Asparagus officinalis) is an ideal species to investigate this hypothesis, as the X and Y chromosomes are cytologically homomorphic and evolved from an ancestral autosome pair in association with a shift from hermaphroditism to dioecy. Mutagenesis screens paired with single-molecule fluorescence in situ hybridization directly implicate Y-specific genes that respectively suppress female (pistil) development and are necessary for male (anther) development. Comparison of contiguous X and Y chromosome assemblies shows that hemizygosity underlies the loss of recombination between the genes suppressing female organogenesis (SUPPRESSOR OF FEMALE FUNCTION) and promoting male function (TAPETAL DEVELOPMENT AND FUNCTION1 [aspTDF1]). We also experimentally demonstrate the function of aspTDF1. These findings provide direct evidence that sex chromosomes can function through linkage of two sex determination genes.
Highlights
Beginning with Nettie Stevens’ (Stevens, 1905) elegant explanation of male and female mealworm gamete differences involving “sex chromosomes”, sex chromosomes have been characterized in dioecious species across all major eukaryotic lineages
One model developed over time by both Westergaard (Westergaard, 1958; Charlesworth, 2018) and Charlesworth and Charlesworth (Charlesworth and Charlesworth, 1978) hypothesizes that a sex chromosome could evolve from an autosomal pair via mutations in two perfectly linked sexually antagonistic genes in a non-recombining region of a proto-Y chromosome: one gene that promotes anther development, and another that suppresses female organ development
Sequencing of a YY “supermale” garden asparagus genome revealed the existence of a nearly one megabase non-recombining, male specific sex determination region (SDR) on the Y chromosome with only thirteen gene models (Harkess et al, 2017), two of which we identify here as the master sex determination genes (Figure 1A)
Summary
Beginning with Nettie Stevens’ (Stevens, 1905) elegant explanation of male and female mealworm gamete differences involving “sex chromosomes”, sex chromosomes have been characterized in dioecious species (with separate male and female sexes) across all major eukaryotic lineages. One model developed over time by both Westergaard (Westergaard, 1958; Charlesworth, 2018) and Charlesworth and Charlesworth (Charlesworth and Charlesworth, 1978) hypothesizes that a sex chromosome could evolve from an autosomal pair via mutations in two perfectly linked sexually antagonistic genes in a non-recombining region of a proto-Y chromosome: one gene that promotes anther development, and another that suppresses female organ development Westergaard supported his two-gene model with genetic data from papaya (Carica papaya) (Storey, 1953), and his own work in Silene (formerly Melandrium) (Westergaard, 1953, 1958). Comparisons of the X and Y chromosomes, and single-molecule in situ data support two Y-specific genes as being sufficient for sex determination in garden asparagus
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