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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 in the genus,Asparagusis a model taxon for studying genetic sex-determination and sex chromosome evolution. Dioecy first evolved inAsparagus~3-4 million years ago (Ma) in the ancestor of a now widespread Eurasian clade that includes garden asparagus (Asparagus officinalis), while the second origin occurred in a smaller, geographically restricted, Mediterranean Basin clade includingAsparagus horridus. The XY sex chromosomes and sex-determination genes in garden asparagus have been well characterized, but the genetics underlying dioecy in the Mediterranean Basin clade are unknown. We generated new haplotype-resolved reference genomes for garden asparagus andA. horridus, to elucidate the sex chromosomes ofA. horridusand explore how dioecy evolved between these two closely related lineages. Analysis of theA. horridusgenome revealed an independently evolved XY system derived from different ancestral autosomes (chromosome 3) with different sex-determining genes than documented for garden asparagus (on chromosome 1). We estimate that proto-XY chromosomes evolved around 1-2 Ma in the Mediterranean Basin clade, following an ~2.1-megabase inversion between the ancestral pair. Recombination suppression and LTR retrotransposon accumulation drove the establishment and expansion of the Y-linked sex-determination region (Y-SDR) that now reaches ~9.6-megabases inA. horridus. The new garden asparagus genome revealed a Y-SDR that spans ~1.9-megabases with ten hemizygous genes. Our results evoke hemizygosity as the most probable mechanism responsible for the origin of proto-XY recombination suppression in the Eurasian clade, and that neofunctionalization of one duplicated gene (SOFF) drove the origin of dioecy. These findings support previous inference based on phylogeographic analysis revealing two recent origins of dioecy inAsparagus. Moreover, this work implicates alternative molecular mechanisms for two separate shifts to dioecy in a model taxon important for investigating young sex chromosome evolution.
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Bursts of Rapid Diversification, Dispersals Out of Southern Africa, and Two Origins of Dioecy Punctuate the Evolution of Asparagus
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.
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- Award ID(s):
- 2110875
- PAR ID:
- 10549577
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Genome Biology and Evolution
- Volume:
- 16
- Issue:
- 10
- ISSN:
- 1759-6653
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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