The asparagus genome sheds light on the origin and evolution of a young Y chromosome

Abstract

Sex chromosomes evolved from autosomes many times across the eukaryote phylogeny. Several models have been proposed to explain this transition, some involving male and female sterility mutations linked in a region of suppressed recombination between X and Y (or Z/W, U/V) chromosomes. Comparative and experimental analysis of a reference genome assembly for a double haploid YY male garden asparagus (Asparagus officinalis L.) individual implicates separate but linked genes as responsible for sex determination. Dioecy has evolved recently within Asparagus and sex chromosomes are cytogenetically identical with the Y, harboring a megabase segment that is missing from the X. We show that deletion of this entire region results in a male-to-female conversion, whereas loss of a single suppressor of female development drives male-to-hermaphrodite conversion. A single copy anther-specific gene with a male sterile Arabidopsis knockout phenotype is also in the Y-specific region, supporting a two-gene model for sex chromosome evolution.

Fig. 1

Genome assembly and identification of the sex-linked region. a The distribution of full-length Gypsy and Copia-class retroelements and genes along the ten Asparagus officinalis pseudomolecules in 1 Mb bins. b The alignment of the optical map against the assembled sequence contigs across the non-recombining region of the Y chromosome. Gray bars connecting the two indicate optical map BspQI nick sites that align. Red bars indicate putative boundaries for the non-recombining region on the Y chromosome. Seven gene models within the contiguously assembled region are numbered with red dots above the sequence assembly. Six additional hemizygous gene models were placed in this recombination bin but are in contigs that could not be anchored onto the optical map (Table 1)

Fig. 2

Mutations in sex determination genes on the Y. a Read alignment coverage (read counts) across the SOFF and aspTDF1 gene models for an XY male (K323), a sibling XX female related to the YY assembled genome, and the gamma-irradiated G033 genotype. b Flowers from a spontaneous male-to-hermaphrodite mutant compared to wild-type male and female flowers (Line3). A frameshift mutation was found in the SOFF CDS sequence (Supplementary Note 1)

Fig. 3

miRNA expression variation across sexes and tissues. a Developmental profile of conserved and novel miRNAs (n=106) identified in garden asparagus. Novel miRNAs have identifiers starting miR8000 and above. The miRNAs are clustered to display tissue-type preferences. An asterisk marks where the cluster plot is split and continued. b miRNAs showing preferential expression patterns between XY male (M) and XX female (F) asparagus spears from three genotypes (8A, 8B, and 10) included in this study. The miRNAs displaying preferential expression (> =2 fold) in at least two spear genotypes are represented here. Higher values highlighted in red indicate enrichment in male spears, and green cells indicate female-biased expression

Fig. 4

Polyploidy and the evolution of sex determination genes. a Synteny dotplot between chromosome Y and chromosome 5. b Gene tree of homologous SOFF gene contigs identified in hermaphroditic A. virgatus and a male and female accession of A. cochinchinensis. The gene and species tree were manually reconciled to identify speciation nodes versus gene duplication nodes

Fig. 5

Mapping whole genome duplication events. Phylogeny with mapping of whole genome duplication events (WGDs) inferred in this work or previous publications: (1, 2) ρ and σ; (3, 4, 5) Zingiberales α, β, and ϒ; (6) palm WGD; (7, 8) Asparagales α and β supported by synteny analyses and gene trees; (9) Agavoideae bimodal karyotype WGD; (10) Orchidaceae WGD; (11) τ; (12, 13) Spirodella α and β; (14, 15) Acorus WGDs inferred from K_s plots; (16) possible early monocot WGD; (17, 18, 19) α, β, and γ hexaploidy event^,; (20) Solanales hexaploidy event; (21) Angiosperm ξ^,. All relationships other than the node joining the two Alismatales species, Spirodella polyrhiza and Zostera marina are supported with bootstrap support values > 95%. Branch coloring represents the number of gene trees analyzed in this study that support WGDs in the ancestors of at least two terminal taxa