The role of DNA topoisomerase 1α (AtTOP1α) in regulating arabidopsis meiotic recombination and chromosome segregation

PeerJ. 2024 Aug 28:12:e17864. doi: 10.7717/peerj.17864. eCollection 2024.

Abstract

Meiosis is a critical process in sexual reproduction, and errors during this cell division can significantly impact fertility. Successful meiosis relies on the coordinated action of numerous genes involved in DNA replication, strand breaks, and subsequent rejoining. DNA topoisomerase enzymes play a vital role by regulating DNA topology, alleviating tension during replication and transcription. To elucidate the specific function of DNA topoisomerase 1α ( A t T O P 1 α ) in male reproductive development of Arabidopsis thaliana, we investigated meiotic cell division in Arabidopsis flower buds. Combining cytological and biochemical techniques, we aimed to reveal the novel contribution of A t T O P 1 α to meiosis. Our results demonstrate that the absence of A t T O P 1 α leads to aberrant chromatin behavior during meiotic division. Specifically, the top1α1 mutant displayed altered heterochromatin distribution and clustered centromere signals at early meiotic stages. Additionally, this mutant exhibited disruptions in the distribution of 45s rDNA signals and a reduced frequency of chiasma formation during metaphase I, a crucial stage for genetic exchange. Furthermore, the atm-2×top1α1 double mutant displayed even more severe meiotic defects, including incomplete synapsis, DNA fragmentation, and the presence of polyads. These observations collectively suggest that A t T O P 1 α plays a critical role in ensuring accurate meiotic progression, promoting homologous chromosome crossover formation, and potentially functioning in a shared DNA repair pathway with ATAXIA TELANGIECTASIA MUTATED (ATM) in Arabidopsis microspore mother cells.

Keywords: 45s rDNA; ATM; Centromere; DNA topoisomerase 1α; FISH; Meiosis.

MeSH terms

  • Arabidopsis Proteins* / genetics
  • Arabidopsis Proteins* / metabolism
  • Arabidopsis* / enzymology
  • Arabidopsis* / genetics
  • Chromosome Segregation*
  • DNA Topoisomerases, Type I* / genetics
  • DNA Topoisomerases, Type I* / metabolism
  • Meiosis* / genetics
  • Meiosis* / physiology
  • Mutation
  • Recombination, Genetic

Substances

  • DNA Topoisomerases, Type I
  • Arabidopsis Proteins

Grants and funding

This work was funded by the National Natural Science Foundation of China (No. 31970525), the Advanced Foreign Experts Project (G2023157014L), and the Cultivating Fund Project of Hubei Hongshan Laboratory (2022hspy002). This work was also supported by the Princess Nourah bint Abdulrahman University Researchers Supporting Project number (PNURSP2024R318), and the Deanship of Scientific Research, Vice Presidency for Graduate Studies and Scientific Research, King Faisal University, Saudi Arabia [Project No. KFU241408]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.