Artificial chromosome reorganization reveals high plasticity of the budding and fission yeast genomes
Abstract Background The genome of a eukaryotic cell is usually organized on a set of chromosomes. Recently, karyotype engineering has been applied to various organisms, but whether and to what extent a naturally evolved genome can resist or tolerate massive artificial manipulations remains unexplore...
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2025-07-01
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| Online Access: | https://doi.org/10.1186/s13059-025-03689-1 |
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| author | Xueting Zhu Shaochun Liu Tiantian Ye Xin Gu Feiyu Pu Zhen Zhou Zhi-Jing Wu Jin-Qiu Zhou |
| author_facet | Xueting Zhu Shaochun Liu Tiantian Ye Xin Gu Feiyu Pu Zhen Zhou Zhi-Jing Wu Jin-Qiu Zhou |
| author_sort | Xueting Zhu |
| collection | DOAJ |
| description | Abstract Background The genome of a eukaryotic cell is usually organized on a set of chromosomes. Recently, karyotype engineering has been applied to various organisms, but whether and to what extent a naturally evolved genome can resist or tolerate massive artificial manipulations remains unexplored. Results Using unicellular yeast models of both Saccharomyces cerevisiae and Schizosaccharomyces pombe, we deliberately construct dozens of single-chromosome strains with different chromosome architectures. Three S. cerevisiae strains have the individual chromosomes fused into a single chromosome, but with the individual chromosomes in different orders. Eighteen S. cerevisiae strains have a single chromosome but with different centromeric sequences. Fifteen S. cerevisiae strains have a single chromosome with the centromere at different distances relative to the telomeres. Two S. pombe strains have a single, circular chromosome, and three strains have a single, linear chromosome with the centromere at different distances relative to the telomeres. All of these single-chromosome strains are viable, but the strains with an acrocentric or a telocentric chromosome have abnormal cell morphologies, and grow more slowly than those with a metacentric or sub-metacentric chromosome, and show increased genome instability with chromosome segregation abnormalities or genome diploidization. Conclusion The functional genomes of both the evolutionarily distant yeasts S. cerevisiae and S. pombe are highly tolerant of diversified genome organizations. The phenotypic abnormalities and increased genome instability of the acrocentric/telocentric single-chromosome yeasts suggest that yeasts with metacentric chromosomes have an evolutionary advantage. |
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| institution | DOAJ |
| issn | 1474-760X |
| language | English |
| publishDate | 2025-07-01 |
| publisher | BMC |
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| series | Genome Biology |
| spelling | doaj-art-50de72906d4e49ab857f49fdeb7421692025-08-20T03:05:29ZengBMCGenome Biology1474-760X2025-07-0126112810.1186/s13059-025-03689-1Artificial chromosome reorganization reveals high plasticity of the budding and fission yeast genomesXueting Zhu0Shaochun Liu1Tiantian Ye2Xin Gu3Feiyu Pu4Zhen Zhou5Zhi-Jing Wu6Jin-Qiu Zhou7Key Laboratory of RNA Innovation-Science and Engineering, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of SciencesKey Laboratory of RNA Innovation-Science and Engineering, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of SciencesKey Laboratory of RNA Innovation-Science and Engineering, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of SciencesKey Laboratory of RNA Innovation-Science and Engineering, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of SciencesInterdisciplinary Research Center On Biology and Chemistry, Shanghai Institute of Organic Chemistry, Chinese Academy of Sciences, University of Chinese Academy of SciencesInterdisciplinary Research Center On Biology and Chemistry, Shanghai Institute of Organic Chemistry, Chinese Academy of Sciences, University of Chinese Academy of SciencesKey Laboratory of Systems Health Science of Zhejiang Province, School of Life Science, Hangzhou Institute for Advanced Study, University of Chinese Academy of SciencesKey Laboratory of RNA Innovation-Science and Engineering, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of SciencesAbstract Background The genome of a eukaryotic cell is usually organized on a set of chromosomes. Recently, karyotype engineering has been applied to various organisms, but whether and to what extent a naturally evolved genome can resist or tolerate massive artificial manipulations remains unexplored. Results Using unicellular yeast models of both Saccharomyces cerevisiae and Schizosaccharomyces pombe, we deliberately construct dozens of single-chromosome strains with different chromosome architectures. Three S. cerevisiae strains have the individual chromosomes fused into a single chromosome, but with the individual chromosomes in different orders. Eighteen S. cerevisiae strains have a single chromosome but with different centromeric sequences. Fifteen S. cerevisiae strains have a single chromosome with the centromere at different distances relative to the telomeres. Two S. pombe strains have a single, circular chromosome, and three strains have a single, linear chromosome with the centromere at different distances relative to the telomeres. All of these single-chromosome strains are viable, but the strains with an acrocentric or a telocentric chromosome have abnormal cell morphologies, and grow more slowly than those with a metacentric or sub-metacentric chromosome, and show increased genome instability with chromosome segregation abnormalities or genome diploidization. Conclusion The functional genomes of both the evolutionarily distant yeasts S. cerevisiae and S. pombe are highly tolerant of diversified genome organizations. The phenotypic abnormalities and increased genome instability of the acrocentric/telocentric single-chromosome yeasts suggest that yeasts with metacentric chromosomes have an evolutionary advantage.https://doi.org/10.1186/s13059-025-03689-1Chromosome engineeringSingle-chromosome yeastGenome plasticityTelocentric chromosome |
| spellingShingle | Xueting Zhu Shaochun Liu Tiantian Ye Xin Gu Feiyu Pu Zhen Zhou Zhi-Jing Wu Jin-Qiu Zhou Artificial chromosome reorganization reveals high plasticity of the budding and fission yeast genomes Genome Biology Chromosome engineering Single-chromosome yeast Genome plasticity Telocentric chromosome |
| title | Artificial chromosome reorganization reveals high plasticity of the budding and fission yeast genomes |
| title_full | Artificial chromosome reorganization reveals high plasticity of the budding and fission yeast genomes |
| title_fullStr | Artificial chromosome reorganization reveals high plasticity of the budding and fission yeast genomes |
| title_full_unstemmed | Artificial chromosome reorganization reveals high plasticity of the budding and fission yeast genomes |
| title_short | Artificial chromosome reorganization reveals high plasticity of the budding and fission yeast genomes |
| title_sort | artificial chromosome reorganization reveals high plasticity of the budding and fission yeast genomes |
| topic | Chromosome engineering Single-chromosome yeast Genome plasticity Telocentric chromosome |
| url | https://doi.org/10.1186/s13059-025-03689-1 |
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