Bentz Philip C, Carey Sarah B, Mercati Francesco, Hale Haley, Ricciardi Valentina, Sunseri Francesco, Harkess Alex, Leebens-Mack James H
Department of Plant Biology and The Plant Center, University of Georgia, Athens, GA 30605, USA.
HudsonAlpha Institute for Biotechnology, Huntsville, AL 35806, USA.
Mol Biol Evol. 2026 Feb 2;43(2). doi: 10.1093/molbev/msag003.
The relatively young and repeated evolutionary origins of dioecy (separate sexes) in flowering plants enables the 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 to 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 a different ancestral pair of autosomes with different sex-determining genes than have been characterized for garden asparagus. We estimate that proto-XY chromosomes evolved 1 to 2 Ma in the Mediterranean Basin clade, following a ∼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.
开花植物中雌雄异株（两性分离）相对年轻且多次独立的进化起源，使得研究性染色体进化最早阶段发生的分子动态成为可能。由于雌雄异株有两个独立的年轻起源，芦笋属是研究性别决定遗传学和性染色体进化的模式属。雌雄异株最早于约300万至400万年前在芦笋属中进化产生，其祖先为一个现今广泛分布于欧亚大陆的进化枝，包括园圃芦笋（石刁柏）。第二次起源发生在一个较小的、地理分布受限的地中海盆地进化枝中，包括刺芦笋。园圃芦笋和刺芦笋新的单倍型解析参考基因组，阐明了欧亚大陆和地中海盆地进化枝祖先性染色体起源的不同初始步骤。对刺芦笋基因组的分析揭示了一个XY系统，该系统源自一对不同的常染色体祖先，其性别决定基因与园圃芦笋已鉴定的不同。我们估计，在地中海盆地进化枝中，原XY染色体在约210万个碱基对的倒位之后于100万至200万年前进化产生，该倒位现在区分了X和Y染色体。重组抑制和LTR逆转座子积累推动了Y染色体上雄性特异性区域（MSY）的扩展，在刺芦笋中该区域达到约960万个碱基对。园圃芦笋基因组显示MSY跨越约190万个碱基对。一个重复基因（SOFF）的片段重复和新功能化推动了欧亚进化枝中雌雄异株的起源。这些发现支持了先前基于系统地理学分析得出的推断，即芦笋属中雌雄异株有两个近期起源，并将该属确立为研究性染色体进化的模式。
