Chromosome–nuclear envelope tethering – a process that orchestrates homologue pairing during plant meiosis?

Abstract

During prophase I of meiosis, homologous chromosomes pair, synapse and exchange their genetic material through reciprocal homologous recombination, a phenomenon essential for faithful chromosome segregation. Partial sequence identity between non-homologous and heterologous chromosomes can also lead to recombination (ectopic recombination), a highly deleterious process that rapidly compromises genome integrity. To avoid ectopic exchange, homology recognition must be extended from the narrow position of a crossover-competent double-strand break to the entire chromosome. Here, we review advances on chromosome behaviour during meiotic prophase I in higher plants, by integrating centromere- and telomere dynamics driven by cytoskeletal motor proteins, into the processes of homologue pairing, synapsis and recombination. Centromere–centromere associations and the gathering of telomeres at the onset of meiosis at opposite nuclear poles create a spatially organised and restricted nuclear state in which homologous DNA interactions are favoured but ectopic interactions also occur. The release and dispersion of centromeres from the nuclear periphery increases the motility of chromosome arms, allowing meiosis-specific movements that disrupt ectopic interactions. Subsequent expansion of interstitial synapsis from numerous homologous interactions further corrects ectopic interactions. Movement and organisation of chromosomes, thus, evolved to facilitate the pairing process, and can be modulated by distinct stages of chromatin associations at the nuclear envelope and their collective release.

Rewiring Meiosis for Crop Improvement

“…How centromeres function during meiosis in plants is still poorly understood but a number of studies have described the essential role of early centromere associations in homologous chromosome recognition, pairing, and subsequent synapsis during meiosis (reviewed in Da Ines and White, 2015 ; Sepsi and Schwarzacher, 2020 ). Remarkably, early centromere associations seem not directly mediated by DSB formation and recombination but rather by local chromatin homology, although stabilization of centromere pairing appears to be partially dependent on recombination initiation ( Da Ines et al, 2012 ; Da Ines and White, 2015 ; Sepsi and Schwarzacher, 2020 ). Centromere association requires active centromeres and the presence of functional CENH3 variants ( Zhang et al, 2013 ).…”

The Arabidopsis HOP2 Gene Has a Role in Preventing illegitimate Exchanges between Nonhomologous Chromosomes

“…Another intriguing possibility is that HOP2 impacts chromosome movements during prophase I. Sepsi and Schwarzacher (2020) reviewed the literature on chromosome-nuclear envelope tethering in plants and proposed that nuclear envelope bridge complexes control chromosome tethering to the nuclear envelope and subsequent chromosome movement during prophase I. They further consider that chromosome movement, as prophase I progresses, could serve to disrupt ectopic nonhomologous DSB repair intermediates prior to the commitment of the type of DSB repair intermediates that could produce a CO outcome.…”

Participation of Multifunctional RNA in Replication, Recombination and Regulation of Endogenous Plant Pararetroviruses (EPRVs)

“…This ssDNA is essential for repair and can become quite long reaching 2–10 kb when less homologous ectopic sequences are involved ( Chung et al, 2010 ). This leads to higher fidelity in one way, as it prevents recombination within short DNA repeats next to the break, and can lead to homology recognition over a larger DNA segment that avoids recombination between homologous chromosomes in polyploids ( Sepsi and Schwarzacher, 2020 ). On the other hand, involvement of longer ssDNA in the homology search and slower repair kinetics ( Chung et al, 2010 ) enhance recombination with sequences located further away from the break or with external sources such as viral DNA sequences.…”