File_S1.zip from Repurposing of synaptonemal complex proteins for kinetochores in kinetoplastida

Chromosome segregation in eukaryotes is driven by the kinetochore, a macromolecular complex that connects centromeric DNA to microtubules of the spindle apparatus. Kinetochores in well-studied model eukaryotes consist of a core set of proteins that are broadly conserved among distant eukaryotic phyla. By contrast, unicellular flagellates of the class Kinetoplastida have a unique set of 36 kinetochore components. The evolutionary origin and the history of these kinetochores remain unknown. Here, we report evidence of homology between axial element components of the synaptonemal complex and three kinetoplastid kinetochore proteins KKT16-18. The synaptonemal complex is a zipper-like structure that assembles between homologous chromosomes during meiosis to promote recombination. By using sensitive homology detection protocols, we identify divergent orthologues of KKT16-18 in most eukaryotic supergroups, including experimentally established chromosomal axis components, such as Red1 and Rec10 in budding and fission yeast, ASY3-4 in plants and SYCP2-3 in vertebrates. Furthermore, we found 12 recurrent duplications within this ancient eukaryotic SYCP2–3 gene family, providing opportunities for new functional complexes to arise, including KKT16-18 in the kinetoplastid parasite Trypanosoma brucei. We propose the kinetoplastid kinetochore system evolved by repurposing meiotic components of the chromosome synapsis and homologous recombination machinery that were already present in early eukaryotes.真核生物的染色体分离由动粒（kinetochore）驱动，这是一类将着丝粒DNA与纺锤体装置微管相连的大分子复合物。在研究较为深入的模式真核生物中，动粒由一套核心蛋白质组构成，这类蛋白质在远缘真核生物门类中广泛保守。与之形成鲜明对比的是，动质体纲（Kinetoplastida）的单细胞鞭毛虫拥有一套独特的36种动粒组分。此类动粒的进化起源与演化历程至今仍不明晰。本研究报道了联会复合体（synaptonemal complex）轴元件与3种动质体动粒蛋白KKT16-18之间存在同源性的证据。联会复合体是一种拉链状结构，在减数分裂过程中于同源染色体之间组装，以促进同源重组过程。通过采用高灵敏度同源性检测方案，我们在多数真核生物超类群中鉴定出了KKT16-18的趋异直系同源物，其中包括经实验验证的染色体轴元件，如酿酒酵母与裂殖酵母中的Red1和Rec10、植物中的ASY3-4以及脊椎动物中的SYCP2-3。此外，我们在这一古老的真核生物SYCP2-3基因家族中发现了12次反复复制事件，为新型功能复合物的诞生提供了演化契机，其中包括动质体寄生生物布氏锥虫（Trypanosoma brucei）中的KKT16-18。我们提出，动质体动粒系统是通过重塑早期真核生物中已存在的染色体联会与同源重组机制的减数分裂组分演化而来的。