Shaw Daniel E, Ross Wynter D, Lambert Alexis V, White Michael A
bioRxiv. 2024 Nov 29:2024.11.26.625488. doi: 10.1101/2024.11.26.625488.
Sex chromosomes often evolve unique patterns of gene expression in spermatogenesis. In many species, sex-linked genes are downregulated during meiosis in response to asynapsis of the heterogametic sex chromosome pair (meiotic sex chromosome inactivation; MSCI). Our understanding of this process has been limited to a handful of species, including mammals, , and Based on findings from these taxa, MSCI has been viewed as likely a conserved process. However, in other groups like teleost fish, our understanding of this process is limited. Teleost fish are a noteworthy group to investigate because sex chromosomes can rapidly evolve between closely related species. Transcriptional profiling of spermatogenesis at the single-cell level is a useful approach to investigate whether MSCI occurs in other species with independently derived sex chromosomes. Here, we investigate whether MSCI occurs in the threespine stickleback fish ( ), which have an X and Y chromosome that evolved less than 26 million years ago. Using single-cell RNA-seq, we found that the X and Y chromosomes do not have a signature of MSCI, maintaining gene expression across meiosis. Using immunofluorescence, we also show the threespine stickleback do not form a condensed sex body around the X and Y, a conserved feature of MSCI in many species. We did not see patterns of gene content evolution documented in other species with MSCI. Y-linked ampliconic gene families were expressed across multiple stages of spermatogenesis, rather than being restricted to post-meiotic stages, like in mammals. Our work shows MSCI does not occur in the threespine stickleback fish and has not shaped the evolution of the Y chromosome. In addition, the absence of MSCI in the threespine stickleback suggests this process may not be a conserved feature of teleost fish and argues for additional investigation in other species.
As male germ cells enter meiosis, the X and Y chromosome of many species undergo a drastic repression of gene expression. In mammals, this process has been shown to be essential for fertility, and the expression of sex-linked genes can lead to meiotic arrest and cell death. This process has only been studied in a handful of organisms, which limits our understanding how conserved MSCI is across the tree of life. Teleost fish are an understudied group with many examples of independently derived sex chromosomes across closely related species. Here, we investigate whether MSCI occurs in the threespine stickleback fish, using single-cell transcriptional profiling. We found gene expression remains active throughout meiosis on the sex chromosomes, indicating MSCI does not occur. This indicates that MSCI is not a conserved feature of all taxa and is not an inevitable outcome of degenerating Y chromosomes.
性染色体在精子发生过程中常常演化出独特的基因表达模式。在许多物种中，性连锁基因在减数分裂期间会因异配子性染色体对的联会失败（减数分裂性染色体失活；MSCI）而下调。我们对这一过程的理解仅限于少数物种，包括哺乳动物、 、以及 。基于这些分类群的研究结果，MSCI被认为可能是一个保守过程。然而，在其他类群如硬骨鱼中，我们对这一过程的理解有限。硬骨鱼是一个值得研究的类群，因为性染色体在亲缘关系相近的物种之间可以迅速演化。在单细胞水平上对精子发生进行转录谱分析是一种有用的方法，可用于研究MSCI是否发生在其他具有独立演化出的性染色体的物种中。在这里，我们研究MSCI是否发生在三刺鱼（ ）中，三刺鱼具有在不到2600万年前演化而来的X和Y染色体。使用单细胞RNA测序技术，我们发现X和Y染色体没有MSCI的特征，在整个减数分裂过程中保持基因表达。通过免疫荧光技术，我们还表明三刺鱼不会在X和Y染色体周围形成浓缩的性体，而这是许多物种中MSCI的一个保守特征。我们没有观察到在其他具有MSCI的物种中记录的基因含量演化模式。Y连锁扩增基因家族在精子发生的多个阶段都有表达，而不是像在哺乳动物中那样仅限于减数分裂后阶段。我们的研究表明，MSCI在三刺鱼中不会发生，并且没有影响Y染色体的演化。此外，三刺鱼中不存在MSCI表明这一过程可能不是硬骨鱼的保守特征，因此需要对其他物种进行进一步研究。
当雄性生殖细胞进入减数分裂时，许多物种的X和Y染色体基因表达会受到剧烈抑制。在哺乳动物中，这一过程已被证明对生育能力至关重要，性连锁基因的表达会导致减数分裂停滞和细胞死亡。这一过程仅在少数生物体中进行了研究，这限制了我们对MSCI在整个生命树中保守程度的理解。硬骨鱼是一个研究较少的类群，在亲缘关系相近的物种中有许多独立演化出的性染色体的例子。在这里，我们使用单细胞转录谱分析来研究MSCI是否发生在三刺鱼中。我们发现性染色体在整个减数分裂过程中基因表达保持活跃，表明MSCI不会发生。这表明MSCI不是所有分类群的保守特征，也不是退化Y染色体的必然结果。
