Single-chromosome fission yeast models reveal the configuration robustness of a functional genome

• Published in: Cell reports (Cambridge) Vol. 40; no. 8; p. 111237
• Main Authors: Gu, Xin, Ye, Tiantian, Zhang, Xiao-Ran, Nie, Lingyun, Wang, Huan, Li, Wei, Lu, Rui, Fu, Chuanhai, Du, Li-Lin, Zhou, Jin-Qiu
• Format: Journal Article
• Language: English
• Published: Elsevier Inc 23.08.2022
• Subjects: 3D genome organization; gene expression; meiosis; reproductive isolation; Schizosaccharomyces pombe; single chromosome; speciation; meiosis; 3D genome organization; CP: Molecular biology; Schizosaccharomyces pombe; single chromosome; reproductive isolation; gene expression; speciation
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2022.111237

In eukaryotic organisms, genetic information is usually carried on multiple chromosomes. Whether and how the number and configuration of chromosomes affect organismal fitness and speciation remain unclear. Here, we have successfully established several single-chromosome fission yeast Schizosaccharomyces pombe strains, in which the three natural chromosomes have been fused into one giant chromosome in different orders. Chromosome fusions accompanied by the deletions of telomeres and centromeres result in the loss of chromosomal interactions and a drastic change of global chromosome organization, but alter gene expression marginally. The single-chromosome strains display little defects in cell morphology, mitosis, genotoxin sensitivity, and meiosis. Crosses between a wild-type strain and a single-chromosome strain or between two single-chromosome strains with different fusion orders suffer defective meiosis and poor spore viability. We conclude that eukaryotic genomes are robust against dramatic chromosomal reconfiguration, and stochastic changes in chromosome number and genome organization during evolution underlie reproductive isolation and speciation. [Display omitted] •S. pombe can tolerate the fusion of its chromosomes into one chromosome•The 3D structure change of the genome has no significant effect on gene expression•Chromosome fusions cause few defects in cell morphology and growth•Chromosome number and genome organization affect meiosis and natural speciation Gu et al. fuse three native chromosomes of the fission yeast Schizosaccharomyces pombe into one giant chromosome in different orders. They characterize these single-chromosome strains in terms of genome 3D structure, transcriptome, mitosis, and meiosis.