Two Y-chromosome-encoded genes determine sex in kiwifruit

Two Y-chromosome-encoded genes determine sex in kiwifruit
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DOI:
10.1038/s41477-019-0489-6
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发表时间:
2019-08-01
期刊:
影响因子:
18
通讯作者:
Tao, Ryutaro
Tao, Ryutaro
中科院分区:
生物学1区
文献类型:
--
作者:
Akagi, Takashi;Pilkington, Sarah M.;Tao, Ryutaro

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雌雄个体的存在,在多个开花植物谱系中独立进化(1-3)。虽然关于雌雄异株进化的理论模型,如“两突变”模型,已经很好地建立起来(4,5),但对决定性别的特定基因及其进化历史知之甚少(3)。猕猴桃是一种雌雄异株的植物,是世界上主要的食用树种。在猕猴桃中,我们先前确定了一个Y编码的性别决定因子候选基因作为女性化(SuF)的抑制因子,名为害羞女孩(SyGI)(6)。在这里,我们确定了第二个Y编码的性别决定簇,我们将其命名为Friendly Boy(FrBy),它在绒毡层细胞中表现出强表达。拟南芥和烟草中的基因编辑和互补分析表明,FrBy独立于SyGI维持雄性(M)功能,并且这些功能在被子植物物种中是保守的。我们进一步表征了Y染色体(MSY)的小(< 1兆碱基对(Mb))男性特异性区域的基因组结构,该区域仅包含两个分别在发育中的雌核发育期和雄核发育期广泛表达的基因:SyGI和FrBy。对天然雌雄同体猕猴桃的基因组重新测序显示,该个体在遗传上是男性,但携带Y染色体部分缺失,包括SyGI。此外,FrBy在雌性猕猴桃中的表达导致雌雄同体植物。这些结果清楚地表明,Y-编码的SyGI和FrBy作为猕猴桃中的SuF和M因子分别独立地起作用,并且不仅提供了对导致双因子性别决定系统的进化路径的深入了解,而且还提供了雌雄异株物种的新育种方法。
Dioecy, the presence of male and female individuals, has evolved independently in multiple flowering plant lineages(1-3). Although theoretical models for the evolution of dioecy, such as the 'two-mutations' model, are well established(4,5), little is known about the specific genes determining sex and their evolutionary history(3). Kiwifruit, a major tree crop consumed worldwide, is a dioecious species. In kiwifruit we previously identified a Y-encoded sex-determinant candidate gene acting as the suppressor of feminization (SuF), named Shy Girl (SyGI)(6). Here, we identify a second Y-encoded sex-determinant that we named Friendly Boy (FrBy), which exhibits strong expression in tapetal cells. Gene-editing and complementation analyses in Arabidopsis thaliana and Nicotiana tabacum indicated that FrBy acts for the maintenance of male (M) functions, independently of SyGI, and that these functions are conserved across angiosperm species. We further characterized the genomic architecture of the small (< 1 megabase pairs (Mb)) male-specific region of the Y chromosome (MSY), which harbours only two genes expressed extensively in developing gynoecia and androecia, respectively: SyGI and FrBy. Re-sequencing of the genome of a natural hermaphrodite kiwifruit revealed that this individual is genetically male but carries deletion(s) of parts of the Y chromosome, including SyGI. Additionally, expression of FrBy in female kiwifruit resulted in hermaphrodite plants. These results clearly indicate that Y-encoded SyGI and FrBy act independently as the SuF and M factors in kiwifruit, respectively, and provide insight into not only the evolutionary path leading to a two-factor sex-determination system, but also a new breeding approach for dioecious species.