Centromere positioning orchestrates telomere bouquet formation and the initiation of meiotic differentiation
Abstract Accurate gametogenesis requires the establishment of the telomere bouquet, an evolutionarily conserved, 3D chromosomal arrangement. In this spatial configuration, telomeres temporarily aggregate at the nuclear envelope during meiotic prophase, which facilitates chromosome pairing and recomb...
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Nature Portfolio
2025-01-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-025-56049-9 |
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| author | Alberto Jiménez-Martín Alberto Pineda-Santaella Rebeca Martín-García Rodrigo Esteban-Villafañe Alix Matarrese Jesús Pinto-Cruz Sergio Camacho-Cabañas Daniel León-Periñán Antonia Terrizzano Rafael R. Daga Sigurd Braun Alfonso Fernández-Álvarez |
| author_facet | Alberto Jiménez-Martín Alberto Pineda-Santaella Rebeca Martín-García Rodrigo Esteban-Villafañe Alix Matarrese Jesús Pinto-Cruz Sergio Camacho-Cabañas Daniel León-Periñán Antonia Terrizzano Rafael R. Daga Sigurd Braun Alfonso Fernández-Álvarez |
| author_sort | Alberto Jiménez-Martín |
| collection | DOAJ |
| description | Abstract Accurate gametogenesis requires the establishment of the telomere bouquet, an evolutionarily conserved, 3D chromosomal arrangement. In this spatial configuration, telomeres temporarily aggregate at the nuclear envelope during meiotic prophase, which facilitates chromosome pairing and recombination. The mechanisms governing the assembly of the telomere bouquet remain largely unexplored, primarily due to the challenges in visualizing and manipulating the bouquet. Here, using Schizosaccharomyces pombe as a model system to elucidate telomere bouquet function, we reveal that centromeres, traditionally perceived as playing a passive role in the chromosomal reorganization necessary for bouquet assembly, play a key role in the initiation of telomere bouquet formation. We demonstrate that centromeres are capable to induce telomere mobilization, which is sufficient to trigger the first stages of bouquet assembly and the meiotic transcription program in mitotic cells. This discovery highlights the finely tuned control exerted over long-distance heterochromatic regions and underscores a pivotal step in the mechanism of eukaryotic telomere bouquet formation and meiotic transcriptional rewiring. |
| format | Article |
| id | doaj-art-67a994edf65b49cb8548155e82e27272 |
| institution | Kabale University |
| issn | 2041-1723 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-67a994edf65b49cb8548155e82e272722025-01-26T12:41:55ZengNature PortfolioNature Communications2041-17232025-01-0116111910.1038/s41467-025-56049-9Centromere positioning orchestrates telomere bouquet formation and the initiation of meiotic differentiationAlberto Jiménez-Martín0Alberto Pineda-Santaella1Rebeca Martín-García2Rodrigo Esteban-Villafañe3Alix Matarrese4Jesús Pinto-Cruz5Sergio Camacho-Cabañas6Daniel León-Periñán7Antonia Terrizzano8Rafael R. Daga9Sigurd Braun10Alfonso Fernández-Álvarez11Instituto de Biología Funcional y Genómica, Zacarías González 2Instituto de Biología Funcional y Genómica, Zacarías González 2Instituto de Biología Funcional y Genómica, Zacarías González 2Instituto de Biología Funcional y Genómica, Zacarías González 2Instituto de Biología Funcional y Genómica, Zacarías González 2Instituto de Biología Funcional y Genómica, Zacarías González 2Instituto de Biología Funcional y Genómica, Zacarías González 2Max-Delbrück-Centrum für Molekulare Medizin, Berlin Institute for Medical Systems Biology (BIMSB)Biology of Centrosomes and Genetic Instability Team, Curie Institute, PSL Research University, CNRS, UMR144, 12 rue LhomondCentro Andaluz de Biología del Desarrollo, Universidad Pablo de Olavide, Departamento de Biología Molecular e Ingeniería Bioquímica, Ctra. de Utrera km. 1BioMedical Center (BMC), Division of Physiological Chemistry, Faculty of Medicine, LMU MunichInstituto de Biología Funcional y Genómica, Zacarías González 2Abstract Accurate gametogenesis requires the establishment of the telomere bouquet, an evolutionarily conserved, 3D chromosomal arrangement. In this spatial configuration, telomeres temporarily aggregate at the nuclear envelope during meiotic prophase, which facilitates chromosome pairing and recombination. The mechanisms governing the assembly of the telomere bouquet remain largely unexplored, primarily due to the challenges in visualizing and manipulating the bouquet. Here, using Schizosaccharomyces pombe as a model system to elucidate telomere bouquet function, we reveal that centromeres, traditionally perceived as playing a passive role in the chromosomal reorganization necessary for bouquet assembly, play a key role in the initiation of telomere bouquet formation. We demonstrate that centromeres are capable to induce telomere mobilization, which is sufficient to trigger the first stages of bouquet assembly and the meiotic transcription program in mitotic cells. This discovery highlights the finely tuned control exerted over long-distance heterochromatic regions and underscores a pivotal step in the mechanism of eukaryotic telomere bouquet formation and meiotic transcriptional rewiring.https://doi.org/10.1038/s41467-025-56049-9 |
| spellingShingle | Alberto Jiménez-Martín Alberto Pineda-Santaella Rebeca Martín-García Rodrigo Esteban-Villafañe Alix Matarrese Jesús Pinto-Cruz Sergio Camacho-Cabañas Daniel León-Periñán Antonia Terrizzano Rafael R. Daga Sigurd Braun Alfonso Fernández-Álvarez Centromere positioning orchestrates telomere bouquet formation and the initiation of meiotic differentiation Nature Communications |
| title | Centromere positioning orchestrates telomere bouquet formation and the initiation of meiotic differentiation |
| title_full | Centromere positioning orchestrates telomere bouquet formation and the initiation of meiotic differentiation |
| title_fullStr | Centromere positioning orchestrates telomere bouquet formation and the initiation of meiotic differentiation |
| title_full_unstemmed | Centromere positioning orchestrates telomere bouquet formation and the initiation of meiotic differentiation |
| title_short | Centromere positioning orchestrates telomere bouquet formation and the initiation of meiotic differentiation |
| title_sort | centromere positioning orchestrates telomere bouquet formation and the initiation of meiotic differentiation |
| url | https://doi.org/10.1038/s41467-025-56049-9 |
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