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SCF^Cdc4 ubiquitin ligase regulates synaptonemal complex formation during meiosis.

ABSTRACT: Homologous chromosomes pair with each other during meiosis, culminating in the formation of the synaptonemal complex (SC), which is coupled with meiotic recombination. In this study, we showed that a meiosis-specific depletion mutant of a cullin (Cdc53) in the SCF (Skp-Cullin-F-box) ubiquitin ligase, which plays a critical role in cell cycle regulation during mitosis, is deficient in SC formation. However, the mutant is proficient in forming crossovers, indicating the uncoupling of meiotic recombination with SC formation in the mutant. Furthermore, the deletion of the PCH2 gene encoding a meiosis-specific AAA+ ATPase suppresses SC-assembly defects induced by CDC53 depletion. On the other hand, the pch2 cdc53 double mutant is defective in meiotic crossover formation, suggesting the assembly of SC with unrepaired DNA double-strand breaks. A temperature-sensitive mutant of CDC4, which encodes an F-box protein of SCF, shows meiotic defects similar to those of the CDC53-depletion mutant. These results suggest that SCF^Cdc4, probably SCF^Cdc4-dependent protein ubiquitylation, regulates and collaborates with Pch2 in SC assembly and meiotic recombination.

SUBMITTER: Zhu Z

PROVIDER: S-EPMC7756916 | biostudies-literature | 2021 Feb

REPOSITORIES: biostudies-literature

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SCF<sup>Cdc4</sup> ubiquitin ligase regulates synaptonemal complex formation during meiosis.

Zhu Zhihui Z Bani Ismail Mohammad M Shinohara Miki M Shinohara Akira A

Life science alliance 20201208 2

Homologous chromosomes pair with each other during meiosis, culminating in the formation of the synaptonemal complex (SC), which is coupled with meiotic recombination. In this study, we showed that a meiosis-specific depletion mutant of a cullin (Cdc53) in the SCF (Skp-Cullin-F-box) ubiquitin ligase, which plays a critical role in cell cycle regulation during mitosis, is deficient in SC formation. However, the mutant is proficient in forming crossovers, indicating the uncoupling of meiotic recom ...[more]

PMID: 33293336

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Project description:The intimate synapsis of homologous chromosome pairs (homologs) by synaptonemal complexes (SCs) is an essential feature of meiosis. In many organisms, synapsis and homologous recombination are interdependent: recombination promotes SC formation and SCs are required for crossing-over. Moreover, several studies indicate that initiation of SC assembly occurs at sites where crossovers will subsequently form. However, recent analyses in budding yeast and fruit fly imply a special role for centromeres in the initiation of SC formation. In addition, in budding yeast, persistent SC-dependent centromere-association facilitates the disjunction of chromosomes that have failed to become connected by crossovers. Here, we examine the interplay between SCs, recombination, and centromeres in a mammal. In mouse spermatocytes, centromeres do not serve as SC initiation sites and are invariably the last regions to synapse. However, centromeres are refractory to de-synapsis during diplonema and remain associated by short SC fragments. Since SC-dependent centromere association is lost before diakinesis, a direct role in homolog segregation seems unlikely. However, post-SC disassembly, we find evidence of inter-centromeric connections that could play a more direct role in promoting homolog biorientation and disjunction. A second class of persistent SC fragments is shown to be crossover-dependent. Super-resolution structured-illumination microscopy (SIM) reveals that these structures initially connect separate homolog axes and progressively diminish as chiasmata form. Thus, DNA crossing-over (which occurs during pachynema) and axis remodeling appear to be temporally distinct aspects of chiasma formation. SIM analysis of the synapsis and crossover-defective mutant Sycp1?/? implies that SCs prevent unregulated fusion of homolog axes. We propose that SC fragments retained during diplonema stabilize nascent bivalents and help orchestrate local chromosome reorganization that promotes centromere and chiasma function.

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SCF^Cdc4 ubiquitin ligase regulates synaptonemal complex formation during meiosis.

Publications

SCF<sup>Cdc4</sup> ubiquitin ligase regulates synaptonemal complex formation during meiosis.

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Dataset Information

SCFCdc4 ubiquitin ligase regulates synaptonemal complex formation during meiosis.

Publications

SCF<sup>Cdc4</sup> ubiquitin ligase regulates synaptonemal complex formation during meiosis.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

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SCF^Cdc4 ubiquitin ligase regulates synaptonemal complex formation during meiosis.