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Abstract The relatively young and repeated evolutionary origins of dioecy (separate sexes) in flowering plants enable 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 ∼3-4 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 different ancestral autosomes with different sex-determining genes than have been characterized for garden asparagus. We estimate that proto-XY chromosomes evolved 1-2 Ma in the Mediterranean Basin clade, following an ∼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. 

Abstract The genus Asparagus arose ∼9 to 15 million years ago (Ma), and transitions from hermaphroditism to dioecy (separate sexes) occurred ∼3 to 4 Ma. Roughly 27% of extant Asparagus species are dioecious, while the remaining are bisexual with monoclinous flowers. As such, Asparagus is an ideal model taxon for studying the early stages of dioecy and sex chromosome evolution in plants. Until now, however, understanding of diversification and shifts from hermaphroditism to dioecy in Asparagus has been hampered by the lack of robust species tree estimates for the genus. In this study, a genus-wide phylogenomic analysis including 1,726 nuclear loci and comprehensive species sampling supports two independent origins of dioecy in Asparagus—first in a widely distributed Eurasian clade and then in a clade restricted to the Mediterranean Basin. Modeling of ancestral biogeography indicates that both dioecy origins were associated with range expansion out of southern Africa. Our findings also reveal several bursts of diversification across the phylogeny, including an initial radiation in southern Africa that gave rise to 12 major clades in the genus, and more recent radiations that have resulted in paraphyly and polyphyly among closely related species, as expected given active speciation processes. Lastly, we report that the geographic origin of domesticated garden asparagus (Asparagus officinalis L.) was likely in western Asia near the Mediterranean Sea. The presented phylogenomic framework for Asparagus is foundational for ongoing genomic investigations of diversification and functional trait evolution in the genus and contributes to its utility for understanding the origin and early evolution of dioecy and sex chromosomes. 

File  Contents Ahor_pb32m_HAP1_v1.0.chrY_regions.bed.gz  Y chromosome nonrecombining region coordinatesAhor_pb32m_HAP1_v1.0.EDTA.TEanno.gff3.gz  All TE annotations by EDTAAhor_pb32m_HAP1_v1.0.EDTA.TEintact.fa.gz  Intact TE sequences by EDTAAhor_pb32m_HAP1_v1.0.EDTA.TEintact.gff3.gz  Intact TE annotations by EDTAAhor_pb32m_HAP1_v1.0.entap_results.tsv  Reciprocal functional gene annotations by EnTAPAhor_pb32m_HAP1_v1.0.fa.gz  Haplotype assembly fasta fileAhor_pb32m_HAP1_v1.0.ISOFORMS.bed.gz  Filtered gene annotations - all isoformsAhor_pb32m_HAP1_v1.0.ISOFORMS.CDS.fa.gz  Filtered gene annotations (protein coding nucleotides) - all isoformsAhor_pb32m_HAP1_v1.0.ISOFORMS.gff3.gz  Filtered gene annotations - all isoformsAhor_pb32m_HAP1_v1.0.ISOFORMS.peptides.fa.gz  Filtered gene annotations (protein sequences) - all isoformsAhor_pb32m_HAP1_v1.0.PRIMARY.bed.gz  Filtered gene annotations - longest isoforms onlyAhor_pb32m_HAP1_v1.0.PRIMARY.CDS.fa.gz  Filtered gene annotations (protein coding nucleotides) - longest isoforms onlyAhor_pb32m_HAP1_v1.0.PRIMARY.gff3.gz  Filtered gene annotations - longest isoforms onlyAhor_pb32m_HAP1_v1.0.PRIMARY.peptides.fa.gz  Filtered gene annotations (protein sequences) - longest isoforms onlyAhor_pb32m_HAP1_v1.0.RM.TE.gff.gz  All TE annotations by RepeatMaskerAhor_pb32m_HAP2_v1.0.chrX_regions.bed.gz  X chromosome nonrecombining region coordinatesAhor_pb32m_HAP2_v1.0.EDTA.TEanno.gff3.gz  All TE annotations by EDTAAhor_pb32m_HAP2_v1.0.EDTA.TEintact.fa.gz  Intact TE sequences by EDTAAhor_pb32m_HAP2_v1.0.EDTA.TEintact.gff3.gz  Intact TE annotations by EDTAAhor_pb32m_HAP2_v1.0.entap_results.tsv  Reciprocal functional gene annotations by EnTAPAhor_pb32m_HAP2_v1.0.fa.gz  Haplotype assembly fasta fileAhor_pb32m_HAP2_v1.0.ISOFORMS.bed.gz  Filtered gene annotations - all isoformsAhor_pb32m_HAP2_v1.0.ISOFORMS.CDS.fa.gz  Filtered gene annotations (protein coding nucleotides) - all isoformsAhor_pb32m_HAP2_v1.0.ISOFORMS.gff3.gz  Filtered gene annotations - all isoformsAhor_pb32m_HAP2_v1.0.ISOFORMS.peptides.fa.gz  Filtered gene annotations (protein sequences) - all isoformsAhor_pb32m_HAP2_v1.0.PRIMARY.bed.gz  Filtered gene annotations - longest isoforms onlyAhor_pb32m_HAP2_v1.0.PRIMARY.CDS.fa.gz  Filtered gene annotations (protein coding nucleotides) - longest isoforms onlyAhor_pb32m_HAP2_v1.0.PRIMARY.gff3.gz  Filtered gene annotations - longest isoforms onlyAhor_pb32m_HAP2_v1.0.PRIMARY.peptides.fa.gz  Filtered gene annotations (protein sequences) - longest isoforms onlyAhor_pb32m_HAP2_v1.0.RM.TE.gff.gz  All TE annotations by RepeatMaskerAoff_pb81m_HAP1_v1.0.chrX_regions.bed.gz  X chromosome nonrecombining region coordinatesAoff_pb81m_HAP1_v1.0.EDTA.TEanno.gff3.gz  All TE annotations by EDTAAoff_pb81m_HAP1_v1.0.EDTA.TEintact.fa.gz  Intact TE sequences by EDTAAoff_pb81m_HAP1_v1.0.EDTA.TEintact.gff3.gz  Intact TE annotations by EDTAAoff_pb81m_HAP1_v1.0.entap_results.tsv  Reciprocal functional gene annotations by EnTAPAoff_pb81m_HAP1_v1.0.fa.gz  Haplotype assembly fasta fileAoff_pb81m_HAP1_v1.0.ISOFORMS.bed.gz  Filtered gene annotations - all isoformsAoff_pb81m_HAP1_v1.0.ISOFORMS.CDS.fa.gz  Filtered gene annotations (protein coding nucleotides) - all isoformsAoff_pb81m_HAP1_v1.0.ISOFORMS.gff3.gz  Filtered gene annotations - all isoformsAoff_pb81m_HAP1_v1.0.ISOFORMS.peptides.fa.gz  Filtered gene annotations (protein sequences) - all isoformsAoff_pb81m_HAP1_v1.0.PRIMARY.bed.gz  Filtered gene annotations - longest isoforms onlyAoff_pb81m_HAP1_v1.0.PRIMARY.CDS.fa.gz  Filtered gene annotations (protein coding nucleotides) - longest isoforms onlyAoff_pb81m_HAP1_v1.0.PRIMARY.gff3.gz  Filtered gene annotations - longest isoforms onlyAoff_pb81m_HAP1_v1.0.PRIMARY.peptides.fa.gz  Filtered gene annotations (protein sequences) - longest isoforms onlyAoff_pb81m_HAP1_v1.0.RM.TE.gff.gz  All TE annotations by RepeatMaskerAoff_pb81m_HAP2_v1.0.chrY_regions.bed.gz  Y chromosome nonrecombining region coordinatesAoff_pb81m_HAP2_v1.0.EDTA.TEanno.gff3.gz  All TE annotations by EDTAAoff_pb81m_HAP2_v1.0.EDTA.TEintact.fa.gz  Intact TE sequences by EDTAAoff_pb81m_HAP2_v1.0.EDTA.TEintact.gff3.gz  Intact TE annotations by EDTAAoff_pb81m_HAP2_v1.0.entap_results.tsv  Reciprocal functional gene annotations by EnTAPAoff_pb81m_HAP2_v1.0.fa.gz  Haplotype assembly fasta fileAoff_pb81m_HAP2_v1.0.ISOFORMS.bed.gz  Filtered gene annotations - all isoformsAoff_pb81m_HAP2_v1.0.ISOFORMS.CDS.fa.gz  Filtered gene annotations (protein coding nucleotides) - all isoformsAoff_pb81m_HAP2_v1.0.ISOFORMS.gff3.gz  Filtered gene annotations - all isoformsAoff_pb81m_HAP2_v1.0.ISOFORMS.peptides.fa.gz  Filtered gene annotations (protein sequences) - all isoformsAoff_pb81m_HAP2_v1.0.PRIMARY.bed.gz  Filtered gene annotations - longest isoforms onlyAoff_pb81m_HAP2_v1.0.PRIMARY.CDS.fa.gz  Filtered gene annotations (protein coding nucleotides) - longest isoforms onlyAoff_pb81m_HAP2_v1.0.PRIMARY.gff3.gz  Filtered gene annotations - longest isoforms onlyAoff_pb81m_HAP2_v1.0.PRIMARY.peptides.fa.gz  Filtered gene annotations (protein sequences) - longest isoforms onlyAoff_pb81m_HAP2_v1.0.RM.TE.gff.gz  All TE annotations by RepeatMaskerAhorridus_MSY_CODEML.zip  CODEML M2a output for 11 MSY genes with evidence of positive selection in Asparagus horridus 

Sex chromosomes have evolved hundreds of times across the flowering plant tree of life; their recent origins in some members of this clade can shed light on the early consequences of suppressed recombination, a crucial step in sex chromosome evolution. Amborella trichopoda, the sole species of a lineage that is sister to all other extant flowering plants, is dioecious with a young ZW sex determination system. Here we present a haplotype-resolved genome assembly, including highly contiguous assemblies of the Z and W chromosomes. We identify a ~3-megabase sex-determination region (SDR) captured in two strata that includes a ~300-kilobase inversion that is enriched with repetitive sequences and contains a homologue of the Arabidopsis METHYLTHIOADENOSINE NUCLEOSIDASE (MTN1-2) genes, which are known to be involved in fertility. However, the remainder of the SDR does not show patterns typically found in non-recombining SDRs, such as repeat accumulation and gene loss. These findings are consistent with the hypothesis that dioecy is derived in Amborella and the sex chromosome pair has not significantly degenerated. 

Dataset and result files from phylogenomic analysis and ancestral biogeography estimation across the genus Asparagus using the Asparagaceae1726 bait set.  Contents of this version replaces Quartet_Sampling.zip in the previous version. Contents: Quartet_Sampling_FINAL.zip = input dataset and final results from Quartet Sampling (i.e., 1000 quartet replicates sampled per node)