Asy2/Mer2: an evolutionarily conserved mediator of meiotic recombination, pairing, and global chromosome compaction

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Abstract

Here, Tessé et al. investigated how the complex program of chromosomal events during meiosis (pairing, recombination, and segregation of homologous chromosomes) proceeds in an ordered sequence. Their study now reveals that Mer2 is involved in every step of the DNA-directed meiotic morphogenetic pathway and interhomolog interactions and that Mer2 is highly conserved between fungi, plants, and animals.

Abstract

Meiosis is the cellular program by which a diploid cell gives rise to haploid gametes for sexual reproduction. Meiotic progression depends on tight physical and functional coupling of recombination steps at the DNA level with specific organizational features of meiotic-prophase chromosomes. The present study reveals that every step of this coupling is mediated by a single molecule: Asy2/Mer2. We show that Mer2, identified so far only in budding and fission yeasts, is in fact evolutionarily conserved from fungi (Mer2/Rec15/Asy2/Bad42) to plants (PRD3/PAIR1) and mammals (IHO1). In yeasts, Mer2 mediates assembly of recombination–initiation complexes and double-strand breaks (DSBs). This role is conserved in the fungus Sordaria. However, functional analysis of 13 mer2 mutants and successive localization of Mer2 to axis, synaptonemal complex (SC), and chromatin revealed, in addition, three further important functions. First, after DSB formation, Mer2 is required for pairing by mediating homolog spatial juxtaposition, with implications for crossover (CO) patterning/interference. Second, Mer2 participates in the transfer/maintenance and release of recombination complexes to/from the SC central region. Third, after completion of recombination, potentially dependent on SUMOylation, Mer2 mediates global chromosome compaction and post-recombination chiasma development. Thus, beyond its role as a recombinosome–axis/SC linker molecule, Mer2 has important functions in relation to basic chromosome structure.

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Recombination, Pairing, and Synapsis of Homologs during Meiosis.

Denise Zickler, Nancy Kleckner (2015)

Recombination is a prominent feature of meiosis in which it plays an important role in increasing genetic diversity during inheritance. Additionally, in most organisms, recombination also plays mechanical roles in chromosomal processes, most notably to mediate pairing of homologous chromosomes during prophase and, ultimately, to ensure regular segregation of homologous chromosomes when they separate at the first meiotic division. Recombinational interactions are also subject to important spatial patterning at both early and late stages. Recombination-mediated processes occur in physical and functional linkage with meiotic axial chromosome structure, with interplay in both directions, before, during, and after formation and dissolution of the synaptonemal complex (SC), a highly conserved meiosis-specific structure that links homolog axes along their lengths. These diverse processes also are integrated with recombination-independent interactions between homologous chromosomes, nonhomology-based chromosome couplings/clusterings, and diverse types of chromosome movement. This review provides an overview of these diverse processes and their interrelationships.

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The genetics and molecular biology of the synaptonemal complex.

Scott L Page, R. Hawley (2004)

The synaptonemal complex (SC) is a protein lattice that resembles railroad tracks and connects paired homologous chromosomes in most meiotic systems. The two side rails of the SC, known as lateral elements (LEs), are connected by proteins known as transverse filaments. The LEs are derived from the axial elements of the chromosomes and play important roles in chromosome condensation, pairing, transverse filament assembly, and prohibiting double-strand breaks (DSBs) from entering into recombination pathways that involve sister chromatids. The proteins that make up the transverse filaments of the SC also play a much earlier role in committing a subset of DSBs into a recombination pathway, which results in the production of reciprocal meiotic crossovers. Sites of crossover commitment can be observed as locations where the SC initiates and as immunostaining foci for a set of proteins required for the processing of DSBs to mature crossovers. In most (but not all) organisms it is the establishment of sites marking such crossover-committed DSBs that facilitates completion of synapsis (full-length extension of the SC). The function of the mature full-length SC may involve both the completion of meiotic recombination at the DNA level and the exchange of the axial elements of the two chromatids involved in the crossover. However, the demonstration that the sites of crossover formation are designated prior to SC formation, and the finding that these sites display interference, argues against a role of the mature SC in mediating the process of interference. Finally, in at least some organisms, modifications of the SC alone are sufficient to ensure meiotic chromosome segregation in the complete absence of meiotic recombination.

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Meiotic Recombination: The Essence of Heredity.

Neil Hunter (2015)

The study of homologous recombination has its historical roots in meiosis. In this context, recombination occurs as a programmed event that culminates in the formation of crossovers, which are essential for accurate chromosome segregation and create new combinations of parental alleles. Thus, meiotic recombination underlies both the independent assortment of parental chromosomes and genetic linkage. This review highlights the features of meiotic recombination that distinguish it from recombinational repair in somatic cells, and how the molecular processes of meiotic recombination are embedded and interdependent with the chromosome structures that characterize meiotic prophase. A more in-depth review presents our understanding of how crossover and noncrossover pathways of meiotic recombination are differentiated and regulated. The final section of this review summarizes the studies that have defined defective recombination as a leading cause of pregnancy loss and congenital disease in humans.

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Author and article information

Journal

Journal ID (nlm-ta): Genes Dev

Journal ID (iso-abbrev): Genes Dev

Journal ID (hwp): genesdev

Journal ID (pmc): genesdev

Journal ID (publisher-id): GAD

Title: Genes & Development

Publisher: Cold Spring Harbor Laboratory Press

ISSN (Print): 0890-9369

ISSN (Electronic): 1549-5477

Publication date (Print): 15 September 2017

Volume: 31

Issue: 18

Pages: 1880-1893

Affiliations

[1 ]Institute for Integrative Biology of the Cell (I2BC), Centre National de la Recherche Scientifique (CNRS), Commissariat Energie Atomique (CEA), Université Paris-Sud, Université Paris-Saclay, 91198 Gif-sur-Yvette, France;

[2 ]Centre de Biologie du Développement (CBD), Centre de Biologie Intégrative (CBI) Université de Toulouse, CNRS, 31062 Toulouse, France;

[3 ]Key Laboratory of Microbial Technology, School of Life Sciences, Shandong University, Jinan, Shandong 250100, China;

[4 ]UMR 3215, U934, Institut National de la Santé et de la Recherche Médicale (INSERM), Institut Curie, 75005 Paris, France;

[5 ]Department of Molecular and Cellular Biology, Harvard University, Cambridge, Massachusetts 02138, USA

Author notes

[6]

These authors contributed equally to this work.

Corresponding authors: denise.zickler@ 123456i2bc.paris-saclay.fr , eric.espagne@ 123456i2bc.paris-saclay.fr

Article

Medline ID: 8711660

DOI: 10.1101/gad.304543.117

PMC ID: 5695089

PubMed ID: 29021238

SO-VID: 1eed6088-50ae-489c-9f4e-1d661b11c59d

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This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genesdev.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.

History

Date received : 11 July 2017

Date accepted : 15 September 2017

Page count

Pages: 14

Funding

Funded by: Centre National de la Recherche Scientifique , open-funder-registry 10.13039/501100004794;

Funded by: National Institutes of Health , open-funder-registry 10.13039/100000002;

Award ID: RO1 GM 044794

Funded by: CNRS , open-funder-registry 10.13039/501100004794;

Funded by: National Natural Science Foundation of China , open-funder-registry 10.13039/501100001809;

Award ID: 31671293

Funded by: Shandong Provincial Natural Science Foundation, China

Award ID: JQ201605

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Asy2/Mer2: an evolutionarily conserved mediator of meiotic recombination, pairing, and global chromosome compaction

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Most cited references 44

Recombination, Pairing, and Synapsis of Homologs during Meiosis.

The genetics and molecular biology of the synaptonemal complex.

Meiotic Recombination: The Essence of Heredity.

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