Chromosome Organization in Early Meiotic Prophase

Abstract

One of the most fascinating aspects of meiosis is the extensive reorganization of the genome at the prophase of the first meiotic division (prophase I). The first steps of this reorganization are observed with the establishment of an axis structure, that connects sister chromatids, from which emanate arrays of chromatin loops. This axis structure, called the axial element, consists of various proteins, such as cohesins, HORMA-domain proteins, and axial element proteins. In many organisms, axial elements are required to set the stage for efficient sister chromatid cohesion and meiotic recombination, necessary for the recognition of the homologous chromosomes. Here, we review the different actors involved in axial element formation in Saccharomyces cerevisiae and in mouse. We describe the current knowledge of their localization pattern during prophase I, their functional interdependence, their role in sister chromatid cohesion, loop axis formation, homolog pairing before meiotic recombination, and recombination. We also address further challenges that need to be resolved, to fully understand the interplay between the chromosome structure and the different molecular steps that take place in early prophase I, which lead to the successful outcome of meiosis I.

Meiotic Chromosome Dynamics in Zebrafish

“…Meiotic chromosomes are organized in a special higher-order structure that consists of chromatin loops anchored along proteinaceous axes (Zickler and Kleckner, 2015). The meiotic chromosome axis comprises meiosis-specific cohesin complexes, components of the SC, and HORMA-domain proteins (Figure 3; Grey and de Massy, 2021). In zebrafish, nearly all chromosome structures studied to date appear to originate from telomeres in the bouquet, including several cohesin proteins (Rad21l1, Smc3, Smc1β), the SC proteins (Sycp1, Sycp2, Sycp3), and Hormad1 Chromosomes joined by this tripartite structure are considered "synapsed."…”

“…In addition, as homologs pair, meiotic chromosomes are organized in the nucleus in a way that telomeres are held transiently together near the nuclear envelope in the bouquet configuration. Mechanisms supporting meiotic pairing and recombination have been extensively studied using a number of different model organisms that include yeasts and fungi, protists, plants, and animals (Klutstein and Cooper, 2014;Kleckner, 2015, 2016;Loidl, 2016;Hughes et al, 2018;Grey and de Massy, 2021). Nevertheless, meiosis in fish groups, which occupy more than half of vertebrate species, remains largely unknown.…”

Epigenetic Dysregulation of Mammalian Male Meiosis Caused by Interference of Recombination and Synapsis

“…In organism such as yeast, plants, and mammals, recombination is initiated during leptotene with the induction of hundreds of DNA double strand breaks (DSBs). This requires the action of the SPO11–TOP6BL transesterase and a number of accessory proteins, including the members of the MRN complex (composed by MRE11, RAD51, and NBS1 in mammals), which contributes to the processing of DSBs, and the RMM complex (REC114, MEI4, and IHO1 in mammals), which associate with the SC and promote DSBs [ 10 , 11 ]. Subsequently, a DNA damage response (DDR) is triggered, activating the homologous recombination repair pathway.…”

Meiotic Behavior of Achiasmate Sex Chromosomes in the African Pygmy Mouse Mus mattheyi Offers New Insights into the Evolution of Sex Chromosome Pairing and Segregation in Mammals

“…Concomitantly, homologous chromosomes undergo recombination. This is a DNA repair process that initiates at the beginning of meiosis with the endogenous production and processing of hundreds of DNA double strand breaks (DSBs) by SPO11 (a topoisomerase-like protein) and a number of associated proteins, including the MRN (MRE11-RAD51-NBS1) and RMM (REC114-MER2-MEI4) complexes [ 4 , 5 ]. The production of DSBs triggers a DNA repair response through the homologous recombination pathway.…”