Data from: The telomere bouquet is a hub where meiotic double-strand breaks, synapsis, and stable homolog juxtaposition are coordinated in the zebrafish, Danio rerio

Meiosis is a cellular program that generates haploid gametes for sexual reproduction. While chromosome events that contribute to reducing ploidy (homologous chromosome pairing, synapsis, and recombination) are well conserved, their execution varies across species and even between sexes of the same species. The telomere bouquet is a conserved feature of meiosis that was first described nearly a century ago, yet its role is still debated. Here we took advantage of the prominent telomere bouquet in zebrafish, Danio rerio, and super-resolution microscopy to show that axis morphogenesis, synapsis, and the formation of double-strand breaks (DSBs) all take place within the immediate vicinity of telomeres. We established a coherent timeline of events and tested the dependence of each event on the formation of Spo11-induced DSBs. First, we found that the axis protein Sycp3 loads adjacent to telomeres and extends inward, suggesting a specific feature common to all telomeres seeds the development of the axis. Second, we found that newly formed axes near telomeres engage in presynaptic co-alignment by a mechanism that depends on DSBs, even when stable juxtaposition of homologous chromosomes at interstitial regions is not yet evident. Third, we were surprised to discover that ~30% of telomeres in early prophase I engage in associations between two or more chromosome ends and these interactions decrease in later stages. Finally, while pairing and synapsis were disrupted in both spo11 males and females, their reproductive phenotypes were starkly different; spo11 mutant males failed to produce sperm while females produced offspring with severe developmental defects. Our results support zebrafish as an important vertebrate model for meiosis with implications for differences in fertility and genetically derived birth defects in males and females.

减数分裂（Meiosis）是一类为有性生殖生成单倍体配子的细胞程序。尽管介导染色体倍性降低的染色体事件——同源染色体配对、联会与重组——均高度保守，但其执行过程在不同物种间乃至同一物种的不同性别间均存在差异。端粒花束（telomere bouquet）是减数分裂的一类保守特征，该结构于近一个世纪前首次被报道，但其具体功能至今仍存在争议。本研究借助斑马鱼（Danio rerio）体内显著的端粒花束结构与超分辨率显微镜技术，证实轴形态发生、联会以及双链断裂（double-strand breaks, DSBs）的形成均发生于端粒的紧邻区域。我们构建了一套连贯的事件时间线，并检验了各事件对Spo11诱导的双链断裂形成的依赖性。其一，我们发现轴蛋白Sycp3在端粒附近加载并向内延伸，提示所有端粒共有的一类特定特征介导了染色体轴的发育。其二，我们发现端粒附近新形成的染色体轴通过依赖于双链断裂的机制完成联会前共对齐，即便此时同源染色体在间隙区域的稳定并置尚未显现。其三，我们意外发现，减数分裂I早期约30%的端粒会发生两个或多个染色体末端之间的关联，且这类相互作用在后续发育阶段逐渐减少。最后，尽管spo11突变体的雌雄个体均出现配对与联会异常，但其生殖表型却存在显著差异：spo11突变雄性无法产生精子，而雌性则可产下具有严重发育缺陷的后代。本研究结果确立斑马鱼作为减数分裂研究的重要脊椎动物模型，其研究发现可为雌雄个体生育力差异以及遗传性出生缺陷的遗传机制提供新的启示。