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Stage-resolved genome architecture maps throughout meiotic prophase link regional variations in chromosome organization with homolog alignment (Hi-C, Cut&Tag, RNA-seq)

ABSTRACT: During meiosis, chromosomes undergo extensive changes in structure and intranuclear positioning. How these chromosome organization changes occur and how they influence meiosis-specific chromosome events are not fully understood. Using Hi-C, we characterized chromosome architecture throughout mouse spermatogenesis at high temporal resolution. Our study revealed an intimate link between chromosome organization features and homolog pairing and alignment. We found that the meiotic chromosomes progressively reshape from TAD-like domains into linearly arranged loop arrays during prophase I. The transcriptionally active and inactive genomic regions exhibit distinct dynamics of loop growth, resulting in alternating domains consisting of shorter and longer chromosome loops. Such a domanial organization along meiotic chromosome axes is tightly correlated with the strength and precision of inter-homolog alignment. We further showed that a significant fraction of chromosomes near chromosome ends exhibit elevated inter-chromosomal association upon entering zygotene stage, while also exhibiting a higher degree of inter-homolog alignment. Using a mouse model defective in LINC complex component SUN1, we demonstrated that the prominent alignment of chromosome ends is dependent on the association of telomeres with the mechano-transducing LINC complex, but not the tethering of telomeres to the nuclear periphery. Taken together, our results suggest the 3D chromosome organization may provide a structural framework for the regulation of meiotic chromosome processes in higher eukaryotes.

ORGANISM(S): Mus musculus

PROVIDER: GSE155967 | GEO | 2021/08/25

REPOSITORIES: GEO

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Stage-resolved genome architecture maps throughout meiotic prophase link regional variations in chromosome organization with homolog alignment

Project description:During meiosis, chromosomes undergo extensive changes in structure and intranuclear positioning. How these chromosome organization changes occur and how they influence meiosis-specific chromosome events are not fully understood. Using Hi-C, we characterized chromosome architecture throughout mouse spermatogenesis at high temporal resolution. Our study revealed an intimate link between chromosome organization features and homolog pairing and alignment. We found that the meiotic chromosomes progressively reshape from TAD-like domains into linearly arranged loop arrays during prophase I. The transcriptionally active and inactive genomic regions exhibit distinct dynamics of loop growth, resulting in alternating domains consisting of shorter and longer chromosome loops. Such a domanial organization along meiotic chromosome axes is tightly correlated with the strength and precision of inter-homolog alignment. We further showed that a significant fraction of chromosomes near chromosome ends exhibit elevated inter-chromosomal association upon entering zygotene stage, while also exhibiting a higher degree of inter-homolog alignment. Using a mouse model defective in LINC complex component SUN1, we demonstrated that the prominent alignment of chromosome ends is dependent on the association of telomeres with the mechano-transducing LINC complex, but not the tethering of telomeres to the nuclear periphery. Taken together, our results suggest the 3D chromosome organization may provide a structural framework for the regulation of meiotic chromosome processes in higher eukaryotes.

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Dynamic Reorganization of the Genome Shapes the Recombination Landscape in Meiotic Prophase

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Project description:Chromosomes pair and synapse with their homologous partners to segregate correctly at meiosis I. Association of telomeres with the LINC (Linker of Nucleoskeleton and Cytoskeleton) complex enables telomere-led chromosome movements and telomere bouquet formation, facilitating precise pairwise alignment of homologs. Here, we identify a direct interaction between SUN1 and Speedy A (SPDYA) and determine the crystal structure of human SUN1-SPDYA-CDK2 ternary complex. Analysis of meiosis prophase I process in SPDYA-binding-deficient SUN1 mutant mice reveals that the SUN1-SPDYA interaction is required for the telomere-LINC complex connection and the assembly of a ring-shaped telomere supramolecular architecture at the nuclear envelope, which is critical for efficient homologous pairing and synapsis. Overall, our results provide structural insights into meiotic telomere structure that is essential for meiotic prophase progression.

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SWR1-independent association of H2A.Z to the LINC complex promotes meiotic chromosome motion

Project description:The H2A.Z histone variant is deposited into chromatin by the SWR1 complex affecting multiple aspects of meiosis. Here we describe a SWR1-independent localization of H2A.Z at meiotic telomeres and the centrosome. We demonstrate that H2A.Z colocalizes and interacts with Mps3, the SUN component of the LINC complex that spans the nuclear envelope and links meiotic telomeres to the cytoskeleton promoting meiotic chromosome movement. H2A.Z also interacts with the meiosis-specific Ndj1 protein that anchors telomeres to the nuclear periphery via Mps3. Telomeric localization of H2A.Z depends on Ndj1 and the N-terminal domain of Mps3. Although telomeric attachment to the nuclear envelope is maintained in the absence of H2A.Z, the distribution of Mps3 is altered. The velocity of chromosome movement during meiotic prophase I is reduced in the htz1? mutant lacking H2A.Z, but it is unaffected in swr1? cells. We reveal that H2A.Z is an additional LINC-associated factor that contributes to promote telomere-driven chromosome motion critical for error-free gametogenesis.

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Stage-resolved genome architecture maps throughout meiotic prophase link regional variations in chromosome organization with homolog alignment

Project description:Stage-resolved genome architecture maps throughout meiotic prophase link regional variations in chromosome organization with homolog alignment

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