Abstract
Meiotic recombination is essential for faithful segregation of homologous chromosomes during gametogenesis. The progression of recombination is associated with dynamic changes in meiotic chromatin structures. However, whether Sycp2, a key structural component of meiotic chromatin, is required for the initiation of meiotic recombination is still unclear in vertebrates. Here, we describe that Sycp2 is required for assembly of the synaptonemal complex and early meiotic events in zebrafish spermatocytes. Our genetic screening by N-ethyl-N-nitrosourea mutagenesis revealed that ietsugu (its), a mutant zebrafish line with an aberrant splice site in the sycp2 gene, showed a defect during meiotic prophase I. The its mutation appeared to be a hypomorphic mutation compared to sycp2 knockout mutations generated by TALEN mutagenesis. Taking advantage of these sycp2 hypomorphic and knockout mutant lines, we demonstrated that Sycp2 is required for the assembly of the synaptonemal complex that is initiated in the vicinity of telomeres in wild-type zebrafish spermatocytes. Accordingly, homologous pairing, the foci of the meiotic recombinases Dmc1/Rad51 and RPA, and γH2AX signals were largely diminished in sycp2 knockout spermatocytes. Taken together, our data indicate that Sycp2 plays a critical role in not only the assembly of the synaptonemal complex, but also early meiotic recombination and homologous pairing, in vertebrates.
Highlights
Meiotic recombination plays a key role in the faithful segregation of homologous chromosomes in the gametogenesis of most sexually reproducing organisms
Zebrafish Sycp2 is essential for synaptonemal complex (SC) assembly and early meiotic recombination that the SC components SYCP2 and SYCP3 form antiparallel heterotetramers that resemble the coiled-coil tetramer structure of budding yeast Red1 [19]
Zebrafish Sycp2 is essential for SC assembly and early meiotic recombination spermatocyte chromosomal spreads were immunostained with antibodies against the SC components Sycp3, Sycp2 and Sycp1 (Fig 3 and S6 Fig)
Summary
Meiotic recombination plays a key role in the faithful segregation of homologous chromosomes in the gametogenesis of most sexually reproducing organisms. The key challenge of meiotic recombination is coordination between the processing of recombinant molecules and changes in chromosomal organization to ensure homologous pairing and the formation of at least one crossover per homologous pair. This process is initiated with programmed DNA double-strand breaks (DSBs) catalyzed by the meiotic endonuclease SPO11. Observations in budding yeast and in Caenorhabditis elegans suggest that axial elements are required for DSB formation. In C. elegans, RNAi-mediated knockdown of the axis component HTP-3 attenuates the formation of foci of the recombinase RAD-51 to the same level as that in spo-11 null mutants, suggesting that no detectable DSBs are formed in the absence of HTP-3 [7]
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