Identification of the master sex determining gene in Northern pike (Esox lucius) reveals restricted sex chromosome differentiation
Identification of the master sex determining gene in Northern pike (Esox lucius) reveals restricted sex chromosome differentiation
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DOI：
10.1371/journal.pgen.1008013
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发表时间：
2019-02
期刊：
影响因子：
4.5
通讯作者：
Qiaowei Pan;Romain Feron;Ayaka Yano;R. Guyomard;E. Jouanno;E. Vigouroux;M. Wen;Jean-Mickaël Busnel-Jean-Mickaël-B
中科院分区：
文献类型：
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作者：
Qiaowei Pan;Romain Feron;Ayaka Yano;R. Guyomard;E. Jouanno;E. Vigouroux;M. Wen;Jean-Mickaël Busnel-Jean-Mickaël-B
硬骨鱼由于其性别决定机制的快速进化，为研究性染色体的形成和驱动新的性别决定基因(MSD)的诞生提供了极好的机会。然而，性染色体和它们所蕴含的MSD基因之间的进化相互作用还相当未被探索。我们利用基因组和表达证据，并通过功能丧失和功能获得实验，鉴定了北方狗鱼(Esox Lucius)中MSD基因的抗苗勒氏激素(AMH)的雄性特异性重复。通过对家系进行RAD测序，我们确定了连锁群(LG)24为性染色体，并将其定位在其亚端粒区域。此外，我们证明了这种MSD起源于常染色体AMH基因的一个古老的重复，该基因随后被移位到LG24。利用性别特异性的混合基因组测序和使用纳米孔长阅读组装的新的男性基因组序列，我们还表征了X和Y染色体的分化，揭示了包含MSD基因的小的男性特异性插入和重组减少的有限区域。我们的研究描述了野生硬骨鱼种群中一对含有旧MSD基因的性染色体中出人意料的有限分化水平，强调了AMH途径中的基因在性别决定中的关键作用，以及基因复制作为驱动这一分支中性染色体周转的机制的重要性。作者摘要与哺乳动物和鸟类形成鲜明对比的是，硬骨鱼具有主要同态的性染色体，并显示出高度多样性的性别决定基因。然而，种群水平的性染色体和主要性别决定基因的知识只适用于模式物种日本青竹。在这里，我们鉴定并提供了一个古老的抗苗勒氏激素的复制品，它是转化生长因子-β家族的成员，是北方狗狗的雄性主宰性别决定基因。我们发现，这个被命名为Amhby(Y染色体特异的反缪勒激素Paralog b)的重复序列被移位到新的性染色体的亚端粒区域，现在Amhby与其常染色体副染色体Amhby显示出强烈的序列差异和实质性的表达模式差异。我们使用纳米孔长阅读器组装了一个雄性基因组序列，并在野生种群的性染色体对中确定了一个有限的分化区域。我们的结果为深入了解性别决定途径中的保守角色、性染色体周转的机制以及硬骨鱼同态性染色体之间分化水平的差异提供了深入的认识。
Teleost fishes, thanks to their rapid evolution of sex determination mechanisms, provide remarkable opportunities to study the formation of sex chromosomes and the mechanisms driving the birth of new master sex determining (MSD) genes. However, the evolutionary interplay between the sex chromosomes and the MSD genes they harbor is rather unexplored. We characterized a male-specific duplicate of the anti-Müllerian hormone (amh) as the MSD gene in Northern Pike (Esox lucius), using genomic and expression evidences as well as by loss-of-function and gain-of-function experiments. Using RAD-Sequencing from a family panel, we identified Linkage Group (LG) 24 as the sex chromosome and positioned the sex locus in its sub-telomeric region. Furthermore, we demonstrated that this MSD originated from an ancient duplication of the autosomal amh gene, which was subsequently translocated to LG24. Using sex-specific pooled genome sequencing and a new male genome sequence assembled using Nanopore long reads, we also characterized the differentiation of the X and Y chromosomes, revealing a small male-specific insertion containing the MSD gene and a limited region with reduced recombination. Our study depicts an unexpected level of limited differentiation within a pair of sex chromosomes harboring an old MSD gene in a wild population of teleost fish, highlights the pivotal role of genes from the amh pathway in sex determination, as well as the importance of gene duplication as a mechanism driving the turnover of sex chromosomes in this clade. Author Summary In stark contrast to mammals and birds, teleosts have predominantly homomorphic sex chromosomes and display a high diversity of sex determining genes. Yet, population level knowledge of both the sex chromosome and the master sex determining gene is only available for the Japanese medaka, a model species. Here we identified and provided functional proofs of an old duplicate of anti-Müllerian hormone (Amh), a member of the Tgf-β family, as the male master sex determining gene in the Northern pike, Esox lucius. We found that this duplicate, named amhby (Y-chromosome-specific anti-Müllerian hormone paralog b), was translocated to the sub-telomeric region of the new sex chromosome, and now amhby shows strong sequence divergence as well as substantial expression pattern differences from its autosomal paralog, amha. We assembled a male genome sequence using Nanopore long reads and identified a restricted region of differentiation within the sex chromosome pair in a wild population. Our results provide insight on the conserved players in sex determination pathways, the mechanisms of sex chromosome turnover, and the diversity of levels of differentiation between homomorphic sex chromosomes in teleosts.