Abstract
During early meiotic prophase, homologous chromosomes are connected along their entire lengths by a proteinaceous tripartite structure known as the synaptonemal complex (SC). Although the components that comprise the SC are predominantly studied in this canonical ribbon-like structure, they can also polymerize into repeated structures known as polycomplexes. We find that in Drosophila oocytes, the ability of SC components to assemble into canonical tripartite SC requires the E3 ubiquitin ligase Seven in absentia (Sina). In sina mutant oocytes, SC components assemble into large rod-like polycomplexes instead of proper SC. Thus, the wild-type Sina protein inhibits the polymerization of SC components, including those of the lateral element, into polycomplexes. These polycomplexes persist into meiotic stages when canonical SC has been disassembled, indicating that Sina also plays a role in controlling SC disassembly. Polycomplexes induced by loss-of-function sina mutations associate with centromeres, sites of double-strand breaks, and cohesins. Perhaps as a consequence of these associations, centromere clustering is defective and crossing over is reduced. These results suggest that while features of the polycomplexes can be recognized as SC by other components of the meiotic nucleus, polycomplexes nonetheless fail to execute core functions of canonical SC.
Highlights
The faithful segregation of chromosomes away from their homologs at the first meiotic division is the physical basis for Mendelian inheritance
Mistakes that occur during meiotic chromosome segregation can lead to fetal death or various disorders in offspring, proper chromosome segregation is crucial
Crossovers form only in the presence of a large proteinaceous structure called the synaptonemal complex (SC), which forms between homologs during early meiosis
Summary
The faithful segregation of chromosomes away from their homologs at the first meiotic division is the physical basis for Mendelian inheritance. Chromosome segregation is achieved by recombination between paired homologs, a process that results in chiasmata and in the production of gametes bearing recombined chromosomes. Both the maintenance of homolog pairing and crossing over depend on the production of doublestrand breaks (DSBs) in the context of the synaptonemal complex (SC). Electron dense lines, referred to as the lateral elements (LEs), associate along each of the homologous chromosomes. The structure between the LEs is called the central region, and the electron-dense line that runs down the center of the central region is referred to as the central element. While the amino acid sequences of SC proteins evolve rapidly between even closely related species [15], the basic tripartite structure of the SC is maintained from yeast to humans, indicating the SC’s structure is crucial for its function in meiosis [5]
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