Joint control of meiotic crossover patterning by the synaptonemal complex and HEI10 dosage

Nature Communications, Год журнала: 2022, Номер 13(1)

Опубликована: Окт. 12, 2022

Abstract Meiotic crossovers are limited in number and prevented from occurring close to each other by crossover interference. In many species, is subject sexual dimorphism, a lower associated with shorter chromosome axes lengths. How this patterning imposed remains poorly understood. Here, we show that overexpression of the Arabidopsis pro-crossover protein HEI10 increases but maintains some interference dimorphism. Disrupting synaptonemal complex mutating ZYP1 also leads an increase but, contrast, abolishes disrupts link between axis length crossovers. Crucially, combining zyp1 mutation massive unprecedented These observations support can be predicted by, recently proposed model which diffusion along drives coarsening process leading well-spaced crossover-promoting foci, providing mechanism for patterning.

Язык: Английский

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Chromosome architecture and homologous recombination in meiosis

Frontiers in Cell and Developmental Biology, Год журнала: 2023, Номер 10

Опубликована: Янв. 6, 2023

Meiocytes organize higher-order chromosome structures comprising arrays of chromatin loops organized at their bases by linear axes. As meiotic prophase progresses, the axes homologous chromosomes align and synapse along lengths to form ladder-like called synaptonemal complexes (SCs). The entire process recombination, from initiation

Язык: Английский

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Coarsening dynamics can explain meiotic crossover patterning in both the presence and absence of the synaptonemal complex

eLife, Год журнала: 2023, Номер 12

Опубликована: Фев. 27, 2023

The shuffling of genetic material facilitated by meiotic crossovers is a critical driver variation. Therefore, the number and positions crossover events must be carefully controlled. In Arabidopsis, an obligate repression nearby on each chromosome pair are abolished in mutants that lack synaptonemal complex (SC), conserved protein scaffold. We use mathematical modelling quantitative super-resolution microscopy to explore mechanistically explain pattering Arabidopsis lines with full, incomplete, or synapsis. For zyp1 mutants, which SC, we develop coarsening model precursors globally compete for limited pool pro-crossover factor HEI10, dynamic HEI10 exchange mediated through nucleoplasm. demonstrate this capable quantitatively reproducing predicting experimental patterning foci intensity data. Additionally, find combining both SC- nucleoplasm-mediated can wild-type pch2 display partial Together, our results reveal regulation SC-defective likely acts same underlying mechanism, differing only spatial compartments diffuses.

Язык: Английский

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The regulation of meiotic crossover distribution: a coarse solution to a century-old mystery?

Biochemical Society Transactions, Год журнала: 2023, Номер 51(3), С. 1179 - 1190

Опубликована: Май 5, 2023

Meiotic crossovers, which are exchanges of genetic material between homologous chromosomes, more evenly and distantly spaced along chromosomes than expected by chance. This is because the occurrence one crossover reduces likelihood nearby events — a conserved intriguing phenomenon called interference. Although interference was first described over century ago, mechanism allowing coordination fate potential sites half chromosome away remains elusive. In this review, we discuss recently published evidence supporting new model for patterning, coined coarsening model, point out missing pieces that still needed to complete fascinating puzzle.

Язык: Английский

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Meiotic recombination dynamics in plants with repeat-based holocentromeres shed light on the primary drivers of crossover patterning

Nature Plants, Год журнала: 2024, Номер 10(3), С. 423 - 438

Опубликована: Фев. 9, 2024

Abstract Centromeres strongly affect (epi)genomic architecture and meiotic recombination dynamics, influencing the overall distribution frequency of crossovers. Here we show how is regulated distributed in holocentric plant Rhynchospora breviuscula , a species with diffused centromeres. Combining immunocytochemistry, chromatin analysis high-throughput single-pollen sequencing, discovered that crossover distally biased, sharp contrast to hundreds centromeric units features. Remarkably, found crossovers were abolished inside but not their proximity, indicating absence canonical centromere effect. We further propose telomere-led synapsis homologues feature best explains observed landscape. Our results hint at primary influence mechanistic features pairing rather than organization determining biased R. whereas centromeres (epi)genetic properties only positioning locally.

Язык: Английский

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ASYNAPSIS3 has diverse dosage-dependent effects on meiotic crossover formation in Brassica napus

The Plant Cell, Год журнала: 2024, Номер 36(9), С. 3838 - 3856

Опубликована: Июль 24, 2024

Abstract Crossovers create genetic diversity and are required for equal chromosome segregation during meiosis. Crossover number distribution highly regulated by different mechanisms that not yet fully understood, including crossover interference. The axis is crucial formation. Here, we explore the function of protein ASYNAPSIS3. To this end, use allotetraploid species Brassica napus; due to its polyploid nature, system allows a fine-grained dissection dosage meiotic regulators. simultaneous mutation all 4 ASY3 alleles results in defective synapsis drastic reduction crossovers, which largely rescued presence only one functional allele. Crucially, while class I crossovers mutants with 2 comparable wild type, significantly increased allele, indicating reducing increases Moreover, on each bivalent 1 allele follow random distribution, compromised These reveal distinct dosage-dependent effects formation provide insights into role patterning recombination.

Язык: Английский

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Dynamic molecular architecture of the synaptonemal complex

Science Advances, Год журнала: 2025, Номер 11(4)

Опубликована: Янв. 22, 2025

During meiosis, pairing between homologous chromosomes is stabilized by the assembly of synaptonemal complex (SC). The SC ensures formation crossovers and regulates their distribution. However, how crossover remains elusive. We isolated an unusual mutation in Caenorhabditis elegans that disrupts interference but not assembly. This alters unique C terminal domain essential protein, SYP-4, a likely ortholog vertebrate protein SIX6OS1. use three-dimensional stochastic optical reconstruction microscopy (3D-STORM) to interrogate molecular architecture from wild-type mutant C. animals. Using probabilistic mapping approach analyze super-resolution image data, we detect changes organization animals coincide with designation. also found our syp-4 perturbs architecture. Our findings add growing evidence active material whose contributes chromosome-wide regulation.

Язык: Английский

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Distinct and interdependent functions of three RING proteins regulate recombination during mammalian meiosis

Proceedings of the National Academy of Sciences, Год журнала: 2025, Номер 122(2)

Опубликована: Янв. 6, 2025

During meiosis, each pair of homologous chromosomes becomes connected by at least one crossover, as required for accurate segregation, and adjacent crossovers are widely separated thereby limiting total numbers. In coarsening models, this crossover patterning results from nascent recombination sites competing to accrue a pro-crossover RING-domain protein (COR) that diffuses between synapsed chromosomes. Here, we delineate the localization dynamics three mammalian CORs in mouse determine their interdependencies. RNF212, HEI10, newest member RNF212B show divergent spatiotemporal along chromosomes, including profound differences spermatocytes oocytes, not easily reconciled elementary models. Contrasting mutant phenotypes genetic requirements indicate RNF212B, HEI10 play distinct but interdependent functions regulating meiotic coordinating events prophase-I integrating signals DNA breaks, homolog synapsis, cell-cycle, incipient sites.

Язык: Английский

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The synaptonemal complex aligns meiotic chromosomes by wetting

Science Advances, Год журнала: 2025, Номер 11(9)

Опубликована: Фев. 26, 2025

During meiosis, the parental chromosomes are drawn together to enable exchange of genetic information. Chromosomes aligned through assembly a conserved interface, synaptonemal complex, composed central region that forms between two parallel chromosomal backbones called axes. Here, we identify axis-central interface in C. elegans , containing positive patch on axis component HIM-3 and negative C terminus protein SYP-5. Crucially, canonical ultrastructure complex is altered upon weakening this using charge-reversal mutations. We developed thermodynamic model recapitulates our experimental observations, indicating liquid-like can assemble by wetting axes without active energy consumption. More broadly, data show condensation drives tightly regulated nuclear reorganization during sexual reproduction.

Язык: Английский

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Crossover patterning in plants

Plant Reproduction, Год журнала: 2022, Номер 36(1), С. 55 - 72

Опубликована: Июль 14, 2022

Abstract Key message Chromatin state, and dynamic loading of pro-crossover protein HEI10 at recombination intermediates shape meiotic chromosome patterning in plants. Meiosis is the basis sexual reproduction, its basic progression conserved across eukaryote kingdoms. A key feature meiosis formation crossovers which result reciprocal exchange segments maternal paternal chromosomes. This generates chromosomes with new combinations alleles, increasing efficiency both natural artificial selection. Crossovers also form a physical link between homologous metaphase I critical for accurate segregation fertility. The along length highly regulated process, our current understanding regulation forms focus this review. At global scale, crossover plants largely governed by classically observed phenomena interference, homeostasis obligatory regulate total number their relative spacing. molecular actors behind these have long remained obscure, but recent studies implicate ZYP1 as players coordination. In addition to broad forces, wealth has highlighted how genomic epigenomic features chromosomal local scales, revealing that are primarily located open chromatin associated gene promoters terminators low nucleosome occupancy.

Язык: Английский

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