Topoisomerase 1 alpha is required for synchronous spermatogenesis in Physcomitrium patens

DNA topoisomerase 1 (TOP1) plays general roles in DNA replication and transcription by regulating DNA topology in land plants and metazoans. TOP1 is also involved in specific developmental events; however, whether TOP1 plays a conserved developmental role among multicellular organisms is unknown. Here, we investigated the developmental roles of TOP1 in the moss Physcomitrium (Physcomitrella) patens with gene targeting, microscopy, 3D image segmentation and crossing experiments. We discovered that the disruption of TOP1 alpha, but not its paralogue TOP1 beta, leads to a defect in fertilisation and subsequent sporophyte formation in P. patens. In the top1 alpha mutant, the egg cell was functional for fertilisation, while sperm cells were fewer and infertile with disordered structures. We observed that the nuclei volume of wild-type sperm cells synchronously decreases during antheridium development, indicating chromatin condensation towards the compact sperm head. By contrast, the top1 alpha mutant exhibited attenuated cell divisions and asynchronous and defective contraction of the nuclei of sperm cells throughout spermatogenesis. These results indicate that TOP1 alpha is involved in cell division and chromatin condensation during spermatogenesis in P. patens. Our results suggest that the regulation of DNA topology by TOP1 plays a key role in spermatogenesis in both land plants and metazoans.

Automated summary

This study investigated the developmental roles of TOP1 in the moss Physcomitrium patens. The results showed that TOP1 alpha is involved in fertilization and sporophyte formation, while TOP1 beta does not have this role. In the top1 alpha mutant, the number of sperm cells is reduced and they exhibit abnormal structures. The study also found that TOP1 alpha is involved in cell division and chromatin condensation during spermatogenesis.