Dynamics of recombination, X inactivation and centromere proteins during stick insect spermatogenesis

William Toubiana, Zoe Dumas, Marie Delattre, Tanja Schwander
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Abstract

In eukaryotes, the cellular processes contributing to gamete formation form the building blocks of genetic inheritance across generations. While traditionally viewed as conserved across model organisms, emerging studies reveal significant variation among eukaryotes in meiotic and post-meiotic processes. Extending our knowledge to non-model organisms is therefore critical to improve our understanding of the evolutionary origin, significance and subsequent modifications associated with gamete formation. We describe the mechanisms underlying recombination, chromosome segregation, and meiotic sex chromosome inactivation in the stick insect group Timema. Our results reveal that in males, 1) recombination initiates before synapsis, 2) the mechanisms of X inactivation are variable among species and the X remains silenced despite two waves of transcriptional activation in autosomes during spermatogenesis, 3) chromosome segregation is preceded by the recruitment of centromere proteins that either bind locally or longitudinally along the chromosomes. Together, our observations help understand the evolutionary significance of key cellular processes related to spermatogenesis and shed light on the diversity of their underlying mechanisms among species, including Timema.
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粘虫精子发生过程中重组、X 失活和中心粒蛋白的动态变化
在真核生物中,配子形成的细胞过程构成了跨代遗传的基石。虽然传统上认为模式生物之间的配子形成过程是保守的,但新的研究显示,真核生物之间的减数分裂和减数分裂后过程存在显著差异。因此,将我们的知识扩展到非模式生物,对于提高我们对配子形成的进化起源、意义和后续修饰的理解至关重要。我们描述了粘虫类群蒂玛虫的重组、染色体分离和减数分裂性染色体失活的基本机制。我们的研究结果表明,在雄性个体中,1)重组在突触之前就开始了;2)X 失活的机制在不同物种之间存在差异,尽管在精子形成过程中常染色体发生了两波转录激活,但 X 仍然保持沉默;3)染色体分离之前需要招募中心粒蛋白,这些蛋白或沿染色体局部结合,或沿染色体纵向结合。我们的观察结果有助于理解与精子发生有关的关键细胞过程的进化意义,并揭示了包括蒂默马在内的不同物种之间精子发生机制的多样性。
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