Abstract
The eukaryotic structural maintenance of chromosomes (SMC) proteins are involved in key processes of chromosome structure and dynamics. SMC1β was identified as a component of the meiotic cohesin complex in vertebrates, which aids in keeping sister chromatids together prior to segregation in meiosis II and is involved in association of homologous chromosomes in meiosis I. The role of SMC1β in meiosis has primarily been studied in mice, where mutant male and female mice are infertile due to germ cell arrest at pachytene and metaphase II stages, respectively. Here, we investigate the function of zebrafish Smc1b to understand the role of this protein more broadly in vertebrates. We found that zebrafish smc1b is necessary for fertility and has important roles in meiosis, yet has no other apparent roles in development. Therefore, smc1b functions primarily in meiosis in both fish and mammals. In zebrafish, we showed that smc1b mutant spermatocytes initiated telomere clustering in leptotene, but failed to complete this process and progress into zygotene. Furthermore, mutant spermatocytes displayed a complete failure of synapsis between homologous chromosomes and homolog pairing only occurred at chromosome ends. Interestingly, meiotic DNA double strand breaks occurred in the absence of Smc1b despite failed pairing and synapsis. Overall, our findings point to an essential role of Smc1b in the leptotene to zygotene transition during zebrafish spermatogenesis. In addition, ovarian follicles failed to form in smc1b mutants, suggesting an essential role in female meiosis as well. Our results indicate that there are some key differences in Smc1b requirement in meiosis among vertebrates: while Smc1b is not required for homolog pairing and synapsis in mice, it is essential for these processes in zebrafish.
Highlights
Germ cells are unique since only they can undergo meiosis and contribute to the generation by producing haploid gametes
We found that most mouse and human structural maintenance of chromosomes (SMC) proteins are evolutionary closer to each other than to those of zebrafish
We demonstrate that the meiotic cohesin complex protein Smc1b is necessary for meiosis and fertility in zebrafish
Summary
Germ cells are unique since only they can undergo meiosis and contribute to the generation by producing haploid gametes. Meiosis is a specialized cell division where DNA replicates once but chromosomes go through two rounds of segregation (Bolcun-Filas and Handel, 2018). The first meiotic division (meiosis-I) segregates homologous chromosome pairs whereas the second division (meiosis-II) is more similar to mitotic divisions, separating sister chromatids. To accomplish the unique segregation in meiosis-I, homologous chromosomes (each of which consists of two sister chromatids) must find each other, pair, and undergo synapsis. Telomeres attach to the nuclear envelope during the leptotene stage via a meiotic-specific protein complex. This complex interacts with a protein chain that spans the nuclear envelope and interacts with the cytoskeleton to drive chromosome movements (Burke, 2018). The telomeres cluster at one side of the nucleus, forming the “bouquet.” This process of chromosome movement and clustering is thought to be essential for homologous chromosomes to find each other and pair
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