Chromosome–Nuclear Envelope Tethering – a Process That Orchestrates Homologue Pairing During Plant Meiosis? Adél Sepsi1,2,* and Trude Schwarzacher3,4

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Chromosome–Nuclear Envelope Tethering – a Process That Orchestrates Homologue Pairing During Plant Meiosis? Adél Sepsi1,2,* and Trude Schwarzacher3,4 © 2020. Published by The Company of Biologists Ltd | Journal of Cell Science (2020) 133, jcs243667. doi:10.1242/jcs.243667 REVIEW Chromosome–nuclear envelope tethering – a process that orchestrates homologue pairing during plant meiosis? Adél Sepsi1,2,* and Trude Schwarzacher3,4 ABSTRACT genome integrity from one generation to another relies on accurate During prophase I of meiosis, homologous chromosomes pair, homologous partner identification. synapse and exchange their genetic material through reciprocal In higher plants, hundreds of genome-wide double-strand breaks homologous recombination, a phenomenon essential for faithful (DSBs) (see Glossary) initiate meiotic recombination within a single chromosome segregation. Partial sequence identity between non- nucleus (Choi et al., 2013; Kurzbauer et al., 2012; Pawlowski et al., homologous and heterologous chromosomes can also lead to 2003). Interactions between homologous chromosomes follow recombination (ectopic recombination), a highly deleterious process recombination initiation (Bozza and Pawlowski, 2008; Hunter and that rapidly compromises genome integrity. To avoid ectopic Kleckner, 2001; Schwarzacher, 1997), suggesting an extremely quick exchange, homology recognition must be extended from the narrow and efficient activation of the homology recognition process. Moreover, – position of a crossover-competent double-strand break to the entire in allopolyploid species (see Glossary) such as the hexaploid wheat chromosome. Here, we review advances on chromosome behaviour Triticum aestivum (2n=6x=42, in which x indicates the number of – during meiotic prophase I in higher plants, by integrating centromere- haploid genomes) each homologous chromosome pair has not only and telomere dynamics driven by cytoskeletal motor proteins, into the one but often several highly similar, i.e. homoeologous (see Glossary), processes of homologue pairing, synapsis and recombination. but not strictly homologous, chromosomes (e.g. AA BB DD Centromere–centromere associations and the gathering of chromosomes in wheat), with whom genetic exchange must be telomeres at the onset of meiosis at opposite nuclear poles create a avoided. How homologous chromosomes recognize each other is not spatially organised and restricted nuclear state in which homologous entirely clear yet but the paradox between the complexityof the process DNA interactions are favoured but ectopic interactions also occur. (Renkawitz et al., 2014) and the short time taken for pairing (see The release and dispersion of centromeres from the nuclear Glossary) (Barzel and Kupiec, 2008) suggests that an elaborate but periphery increases the motility of chromosome arms, allowing reliable mechanism controlling spatial organisation of chromosomes meiosis-specific movements that disrupt ectopic interactions. and chromatin proximity has a significant role. Subsequent expansion of interstitial synapsis from numerous Although meiotic recombination underlies genetic diversity, the homologous interactions further corrects ectopic interactions. introduction of genome-wide DSBs is highly hazardous for the cell Movement and organisation of chromosomes, thus, evolved to and the activation of a programmed repair mechanism is mandatory facilitate the pairing process, and can be modulated by distinct for its survival. In contrast to somatic repair, meiotic recombination stages of chromatin associations at the nuclear envelope and their utilises homologous chromosomes rather than sister chromatids to collective release. repair DSBs. Recombination is initiated by nucleolytic degradation of the 5′-termini of the broken DNAs (strand resection). The KEY WORDS: Meiosis, Chromatin dynamics, Centromere associations, resulting single-stranded DNA (ssDNA) then attracts recombinases Synaptonemal complex, Recombination RAD51 and DMC1 that form nucleofilaments (see Glossary) and catalyse search and invasion into an intact homologous double- Introduction stranded DNA (dsDNA) sequence located within a partner Accurate chromosome inheritance from the diploid parental cell chromosome (Pradillo et al., 2014). Current models of meiotic nucleus into haploid gametes depends on the intimate juxtaposition recombination propose that DNA sequences involved in homology and recombination of paternal and maternal homologous searches are determined by strand resection, which typically chromosomes (see Glossary) during meiosis. As recombination generates 2–10 kb ssDNA, depending on the type of repair through crossovers (see Glossary) involves the reciprocal exchange (Cannavo et al., 2019; Mimitou and Symington, 2008). During of genetic information between two chromosomes, conservation of non-allelic recombination, the resulting ssDNA is longer and repair kinetics are much slower (Chung et al., 2010), indicating that 1Department of Plant Cell Biology, Centre for Agricultural Research, 2462, homology recognition can be extended locally to a larger DNA Martonvásár, Brunszvik u. 2, Hungary. 2BME Budapest University of Technology segment. Local homology exists between non-allelic regions, and Economics, Department of Applied Biotechnology and Food Science (ABÉT), especially in allopolyploids. To avoid non-allelic recombination 1111, Budapest, Mu˝ egyetem rkp. 3-9., Hungary. 3University of Leicester, Department of Genetics and Genome Biology, University Road, Leicester LE1 7RH, and the resulting major rearrangements of the chromosome, it is UK. 4Key Laboratory of Plant Resources Conservation and Sustainable Utilization/ essential to broaden homology recognition from the site of a Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical crossover-competent DSB and apply a control mechanism based on Garden, Chinese Academy of Sciences, Guangzhou 510650, China. entire chromosomes. For example, in the allotetraploid oilseed rape *Author for correspondence ([email protected]; [email protected]) Brassica napus, homologous genomes are sorted and homologues recognise each other during the repair process that follows DSB A.S., 0000-0003-4473-5490; T.S., 0000-0001-8310-5489 formation (Cifuentes et al., 2010; Howell et al., 2008). Crossovers This is an Open Access article distributed under the terms of the Creative Commons Attribution are formed between chromosomal regions with the closest sequence License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed. homology; however, when lacking a homologous partner, Journal of Cell Science 1 REVIEW Journal of Cell Science (2020) 133, jcs243667. doi:10.1242/jcs.243667 recombination is promoted between homoeologues (Grandont et al., Glossary 2014). This can be explained by the presence of a nuclear Allopolyploid species: species with more than one non-identical recognition system, in which recombination intermediates with chromosome set (genome), resulting from hybridisation between two or the highest level of homology are favoured over the weakest more different species followed by genome duplication. recombination intermediates. Axial elements: a meiosis-specific protein structure established along each chromosome during leptotene whereby the chromatin is organised in Here, we summarise the current understanding of meiotic an array of loops with connected and co-oriented sister chromatids. chromatin dynamics in plants, by connecting recent cytological Chiasma/chismata: cytological manifestation of crossovers. and molecular information, to explore and advance our Chromosome pairing: the side-by-side alignment of homologous understanding of the role of meiotic chromosome behaviour in chromosomes prior to initiation of synapsis. homologous pairing. Several recent reviews have highlighted the Crossover: site of homologous reciprocal recombination. Diplotene: fourth sub-stage of meiotic prophase I, homologous possible function of early, non-homologous centromere chromosomes separate except at sites of chiasmata. The synaptonemal associations in meiosis (da Ines and White, 2015) and the complex dissolves. different pairing strategies observed in other eukaryotes (Loidl, Double-strand break (DSB): universally the initial step in the process of 2016; Zickler and Kleckner, 2015), as well as the movement of meiotic recombination, involving a self-imposed DNA-damage event that is meiotic chromosomes directed by nuclear envelope-associated catalysed by the evolutionarily conserved protein Spo11. Endoreduplication: replication of the nuclear genome without subsequent proteins (Zeng et al., 2018). The present Review adds to these cell division, leading to a nucleus with a duplicated diploid chromosome set. studies by examining telomere and centromere-led chromatin Homoeologue/homoeologous: partially homologous chromosomes, dynamics in relation to formation of the synaptonemal complex usually indicating some ancestral sequence homology. (SC) (see Glossary) and meiotic recombination. Building on our Homologue/homologous chromosomes: have the same genetic own research in wheat and barley (Schwarzacher, 1997; Sepsi et al., information and order of genes, showing only allelic variation. 2017, 2018) as well as other studies of plants, we argue that specific Leptotene: first sub-stage of meiotic prophase I, i.e. the period from appearance of the first elongated axial element stretches along the chromatin steps of synapsis (see Glossary) progression are modulated by the until their elongation, forming the continuous
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