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Reference - PMID:39833200 - Centromere positioning orchestrates telomere bouquet formation and the initiation of meiotic differentiation.

Reference summary

PubMed ID
PMID:39833200
Title
Centromere positioning orchestrates telomere bouquet formation and the initiation of meiotic differentiation.
Authors
Jiménez-Martín A, Pineda-Santaella A, Martín-García R, Esteban-Villafañe R, Matarrese A, Pinto-Cruz J, Camacho-Cabañas S, León-Periñán D, Terrizzano A, Daga RR, Braun S, Fernández-Álvarez A
Citation
Nat Commun 2025 Jan 20;16(1):837
Publication year
2025
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.

Annotation

GO biological process

GO:0072766 - centromere clustering at the mitotic interphase nuclear envelope

Genes:

GO:1990571 - meiotic centromere clustering

Genes:

GO:0045141 - meiotic telomere clustering

Genes:

GO:0110045 - negative regulation of cell cycle switching, mitotic to meiotic cell cycle

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GO cellular component

GO:0035974 - meiotic spindle pole body

Genes:

GO:0005637 - nuclear inner membrane

Genes:

Multi-locus phenotype

FYPO:0008009 - abnormal interphase mitotic telomere clustering during vegetative growth

Genes:

Genotypes:

FYPO:0006800 - decreased centromere clustering at nuclear periphery during mitotic interphase

Genes:

Genotypes:

FYPO:0003803 - decreased protein localization to telomere

Genes:

Genotypes:

FYPO:0000584 - decreased sporulation frequency

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Genotypes:

FYPO:0001355 - decreased vegetative cell population growth

Genes:

Genotypes:

FYPO:0002173 - increased level of meiotic gene mRNA during vegetative growth

Genes:

Genotypes:

FYPO:0004656 - increased protein localization to telomere during vegetative growth

Genes:

Genotypes:

FYPO:0005917 - increased subtelomeric heterochromatin RNA level

Genes:

Genotypes:

FYPO:0002061 - inviable vegetative cell population

Genes:

Genotypes:

FYPO:0000964 - normal growth on thiabendazole

Genes:

Genotypes:

FYPO:0007269 - normal interphase mitotic telomere clustering during vegetative growth

Genes:

Genotypes:

FYPO:0007281 - normal level of meiotic gene mRNA during vegetative growth

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Genotypes:

FYPO:0005602 - normal subtelomeric heterochromatin RNA level

Genes:

Genotypes:

FYPO:0004924 - normal telomere tethering at nuclear periphery during vegetative growth

Genes:

Genotypes:

FYPO:0003840 - sensitive to carbendazim

Genes:

Genotypes:

FYPO:0000091 - sensitive to thiabendazole

Genes:

Genotypes:

Single locus phenotype

FYPO:0008009 - abnormal interphase mitotic telomere clustering during vegetative growth

Genes:

Genotypes:

FYPO:0006800 - decreased centromere clustering at nuclear periphery during mitotic interphase

Genes:

Genotypes:

FYPO:0005917 - increased subtelomeric heterochromatin RNA level

Genes:

Genotypes: