Chromosome fusion enhances dependency on Rif1 for entanglement resolution during meiosis in S. pombe

Chromosome fusion represents a major form of karyotype evolution. However, it remains unclear how cells adapt to drastic changes in chromosomal organisation and overcome the topological challenges imposed by fusion to ensure accurate segregation, genome stability, and genome function. Here, we report that in the fission yeast Schizosaccharomyces pombe, nascently fused chromosomes exhibit elevated entanglements during meiosis due to the accumulation of recombination intermediates, which are eventually resolved in late anaphase I with high fidelity. Notably, loss of the conserved replication/repair factor Rif1 increases the frequency of these entanglements, revealing a meiotic role for Rif1 in promoting efficient resolution of recombination-derived DNA bridges, particularly in the context of chromosome fusion. Moreover, the delayed mid-region nuclear envelope breakdown observed in anaphase I appears to provide an extended time window and stable intranuclear environment for resolution, thereby ensuring faithful segregation of the fused chromosomes. Together, our findings uncover a heightened dependence of cells with altered karyotypes on DNA repair machinery and suggest that adaptive regulation of entanglement resolution safeguards genome integrity during karyotype evolution.